Received: 31 May 2021 Revised: 17 August 2021 Accepted: 27 August 2021

DOI: 10.1111/ppl.13545

MINIREVIEW Physiologia Plantarum

The ACC deaminase-producing plant growth-promoting

bacteria: Influences of bacterial strains and ACC deaminase
activities in plant tolerance to abiotic stress

Aung Htay Naing1 | The-Thiri Maung2 | Chang Kil Kim1

1
Department of Horticulture, Kyungpook
National University, Daegu, Korea
2
Department of Food Science and Technology,
Kongju National University, Yesan, Korea
Correspondence
Chang Kil Kim, Department of Horticulture,
Kyungpook National University, Daegu 41566,
Korea.
Email: ckkim@knu.ac.kr
Funding information
The National Research Foundation of Korea
(NRF) grant (MSIT), Grant/Award Number:
2021R1A2C2008951
Edited by B. Huang
Abstract
Global climate change results in frequent occurrences and/or long durations of abi-
otic stress. Field grown plants are affected by abiotic stress, and they modulate ethyl-
ene in response to abiotic stress exposure and use it as a signaling molecule in stress
tolerance mechanisms. However, frequent occurrences and/or long durations of
stress conditions can cause plants to induce ethylene levels higher than their thresh-
olds, resulting in a reduction of plant growth and crop productivity. The use of plant
growth-promoting bacteria (PGPB) that produce 1-aminocyclopropane-1-carboxylate
(ACC) deaminase has increased in various plant species to ameliorate the deleterious
effects of stress-induced ethylene and promote plant growth despite abiotic stress
conditions. Unfortunately, there are restrictions that limit the use of ACC deaminase-
producing PGPB to protect plants from abiotic stresses. This review describes how
abiotic stress induces ethylene and how stress-induced ethylene adversely affects
plant growth. In addition, this review emphasizes the importance of the compatibility
of PGPB strains and specific host plants and ACC deaminase activities in the reduc-
tion of stress ethylene and the promotion of plant growth, based on the research
published in the last 10 years. Moreover, due to the restrictions in PGPB use, this
review highlights the potential generation of transgenic plants expressing the AcdS
gene that encodes the ACC deaminase enzyme as a substitute for PGPB in the future
to support and uplift agricultural sustainability and food security globally.

1 | I N T RO DU CT I O N Ethylene is derived from methionine, which is converted into

Abiotic stresses, such as drought, salinity, flooding, heat, and heavy
metals, have become more severe and adversely affect plant growth
and crop productivity worldwide, approximately 70% yield losses in
major food crops (Mantri et al., 2012). Global climate change directly
or indirectly affects the severity of abiotic stresses and results in an
increase of uncultivable land area (i.e., salinity soil and heavy metal-
contaminated soil), and this may cause a steady decline in available
cultivable land area in the future. Furthermore, the world's population
is expected to reach 10 billion by 2070 (Goswami et al., 2016;
Shahbaz & Ashraf, 2013), creating a threat to global food security and
making it necessary to facilitate improved crop production to cope.
S-adenosyl-L-methionine (SAM) by the SAM synthetase, and SAM is
then converted to 1-aminocyclopropane-1-carboxylic acid (ACC) by
the ACC synthetase, and ACC is finally converted to ethylene by the
ACC oxidase (Yang and Hoffman, 1984). It is regarded as an important
regulator of many plant developmental and physiological processes,
such as seed germination, senescence, stress signaling, and root elon-
gation (Masood et al., 2012; Nazar et al., 2014; Pierik et al., 2006). In
abiotic stress conditions, plants modulate ethylene to activate signal-
ing pathways and protect them from the deleterious effects of
stressors. However, when abiotic stress is more severe, ethylene is
produced in plant tissues and the levels could be greater than the
acceptable threshold limits. This can cause inhibition of root and shoot

Physiologia Plantarum. 2021;1–21. wileyonlinelibrary.com/journal/ppl © 2021 Scandinavian Plant Physiology Society. 1

2 NAING ET AL.
Physiologia Plantarum

proliferation and enhancement of leaf senescence, thereby hindering

C2 H4
plant growth and development (Singh et al., 2015). Therefore, stress-
induced ethylene (ethylene stress) needs to be reduced to sustain
C 2H 4
crop productivity against stress. Of several strategies attempted for C2H4
this purpose, the use of plant growth-promoting bacteria (PGPB) with
ACC deaminase (ACCD) activity to reduce stress-induced ethylene
has recently been improved. As ACCD is contained in the PGPB, it
breaks down the immediate precursor of ethylene ACC to
C2H4 C2H4
α-ketobutyrate and ammonia, resulting in a decrease in ethylene levels
in plants and ameliorating the adverse effects of ethylene on plant
growth (Glick, 2014; Glick et al., 2007; Honma & Shimomura, 1978;
Singh et al., 2015). In addition, PGPB can improve plant growth and
development during stress through rhizospheric, endophytic, and sym-
biotic interactions with plants (Glick, 2014; Khalid et al., 2004;
Martinez-Viveros et al., 2010; Zahir et al., 2004). Recently, many
researchers have isolated several ACCD-producing bacterial strains
Methionine
hionine
from different rhizosphere zones and plant species for the inoculation
flooding
floodi
of agricultural crops, and they found a wide distribution of bacterial SAM synthase

strains and a variation of ACCD activities in the bacteria. When using

the bacteria as an inoculum, their growth-promoting effects are
dependent on their survival in the soil, compatibility with the crop on
which they are inoculated, interactions with the indigenous microflora
in the soil, and the stability of ACCD activities under abiotic stress. In
response to these restrictions, plant biologists have cloned AcdS
encoding the ACCD enzyme from PGPBs and genetically engineered
AcdS-containing transgenic plants as an alternative approach. This has
also proven that transgenic plants expressing AcdS reduce ethylene
levels and can tolerate various abiotic stresses (Grichko &
Glick, 2001a, 2001b; Robison et al., 2001; Sergeeva et al., 2006;
Farwell et al., 2007; Zhang et al., 2008). This review describes how
abiotic stresses induce ethylene and how this adversely affects plant
growth, and the importance of the compatibility of PGPB strains and
host plants as well as ACCD activities in ethylene reduction and plant
growth promotion in abiotic stress conditions were discussed. In addi-
tion, current progress for the use of the AcdS gene in plant biotech-
nology has also been highlighted.
2 | A B I O T I C ST R E S S E S —I N D U C E D
ETHYLENE PRODUCTION AND ITS ADVERSE
E F F E C T S ON P L A N T G R O W T H
The ethylene biosynthesis pathway and its involvement in plant devel-
opment and physiological processes has been described in the Intro-
duction section (Figures 1 and 2). Generally, ethylene is synthesized
during fruit ripening, flower opening, and leaf senescence. However,
abiotic stress-induced ethylene production in plants has also been
documented (Dubois et al., 2017; Savada et al., 2017; Skirycz
et al., 2011; Thao et al., 2015; Zhang et al., 2016). Plants are sessile,
and this means that their survival can be threatened by abiotic stress.
In response to abiotic stresses, plants induce so-called stress ethylene,
via, complex molecular response mechanisms. In this case, two ethyl-
ene synthesis peaks were observed, with a small amount in the first
SAM
ACS
ACC
F I G U R E 1 Ethylene production in plants under flooding
conditions. ACC is accumulated in the roots and is transported
through the xylem to the leaves. It is then oxidized and high levels of
ethylene are produced in the leaves, which causes leaf epinasty and
abscission. ACC, 1-aminocyclopropane-1-carboxylic acid; ACS, ACC
synthetase; C2H4, ethylene; SAM, S-adenosyl-L-methionine
peak and a large amount in the second peak (Glick et al., 2007).
Although stress-induced ethylene synthesis usually starts within 10–
30 min, its decline starts several hours after reaching its peak point
(Yang and Hoffman, 1984). Plants utilize the ethylene induced in the
first peak to transcriptionally regulate the genes that encode the plant
defensive and protective proteins, leading to sustained growth against
abiotic stresses (Desbrosses et al., 2009; Robison, Griffith,
et al., 2001; VanLoon et al., 2006). However, the ethylene induced in
the second peak can exceed the threshold level considered optimal
for plant tissue growth and development (Glick, 2014; Singh
et al., 2015). It can instead have detrimental effects on plant growth
and development, such as the inhibition of root elongation, chloro-
phyll destruction, and leaf senescence and defoliation (Glick
et al., 2007; Singh et al., 2015).
In waterlogged or flooding conditions, as plant roots suffer from
hypoxia, the regulation of ACC synthesis genes (ACS) in the roots
starts 3–12 h after the initiation of waterlogging (Grichko &
Glick, 2001a, 2001b; Shiono et al., 2008; Vanderstraeten & Van Der
Straeten, 2017). However, ACC cannot be converted into ethylene
because of an inadequate supply of molecular oxygen, which is
required for the oxidation and conversion of ACC to ethylene. As
ACC is transported through the xylem to the shoots, the expression
NAING ET AL. 3
Physiologia Plantarum

F I G U R E 2 Mode of ACCD-
producing PGPB in amelioration of
the deleterious effect of stress
ethylene under abiotic stress.
Under abiotic stress, when plants
are inoculated with ACCD-
producing PGPB, the bacteria
received stress-induced ACC from
the plants and induced ACC
deaminase enzymes, which in turn
hydrolyze excess ACC in plant
tissues to ammonia and
α-ketobutyrate and ameliorate
deleterious effects of stress
ethylene. ACC,
1-aminocyclopropane-1-carboxylic
acid; IAA, indole-3-acetic acid;
SAM, S-adenosyl-L-methionine.
This image is modified from the
original image of Glick (2014)

of the ACO genes is promoted, and high levels of ethylene are pro-
duced, which causes leaf epinasty and abscission (Figure 1;
Bradford & Yang, 1980; Grichko & Glick, 2001a, 2001b; Glick, 2014;
Vanderstraeten & Van Der Straeten, 2017). The association between
flooding or waterlogging and faster rates of ethylene production has
previously been observed in various plant species (Beltrano
et al., 1999; Chen et al., 2002; English et al., 1995; Morgan
et al., 1990; Sharp, 2002), and the enhanced ethylene concentration
caused alterations of the plasma membrane integrity, accumulation of
ABA, and a breakdown of cytokinins, which negatively affects plant
growth and development. Similarly, the enhancement of ethylene pro-
duction in plants subjected to heat stress has also been observed
(Mitcham & McDonald, 1993). The results were in agreement with
Antunes and Sfakiotakis (2000), who speculated that heat stress had a
prominent effect on ethylene biosynthesis in kiwi fruits. Heat stress-
enhanced ethylene production and its subsequent negative effects on
leaf senescence, seed set, seed size, and crop yield have also been
reported in wheat, soybean, and sunflower (De la Haba et al., 2014;
Djanaguiraman & Prasad, 2010; Hays et al., 2007), whereas applica-
tion of the ethylene inhibitor 1-MCP reduced or postponed leaf
senescence in heat stress conditions (Djanaguiraman & Prasad, 2010).
This demonstrates how heat stress-induced ethylene adversely affects
crop physiology and yield.
Drought stress has also been associated with enhanced levels of
ethylene in several plant species (Balota et al., 2004; Graves &
Gladon, 1985; Mayak et al., 2004a; Sharp, 2002). However, when the
ethylene biosynthesis gene was knocked out in maize, drought stress-
induced ethylene production was found to be lower in the mutant
than in the wild type, and drought-induced senescence in the older
leaves of the mutant was also inhibited (Young et al., 2004). A similar
finding was further confirmed by Habben et al. (2014), who found that
downregulating the ethylene biosynthetic pathway improved the grain
yield of maize under drought stress conditions. Shi et al. (2015) also
confirmed the adverse effects of ethylene on maize in drought stress
using the overexpression of the ethylene inhibitory gene ARGOS, and
they reported that the transgenic plants had a greater grain yield than
the nontransgenic plants in both the drought stress and well-watered
conditions (Shi et al., 2015). In addition, the application of ethylene inhib-
itors also supports the negative effect of stress-induced ethylene on
plant growth because they reduced yield loss by reducing ethylene pro-
duction and improved tolerance to stress conditions, such as drought,
heat, and a combination of both (Hays et al., 2007; Huberman
et al., 2014; Kawakami et al., 2010, 2013).
Similarly, metal-induced ethylene synthesis has been documented
in various tissues of several plant species, whereas ethylene synthesis
is associated with the transcriptional regulation of ethylene-related
genes (reviewed in Keunen et al., 2016). The synthesis of ethylene
under metal stress has two main causes: (1) metal toxicity often leads
to nutrient deficiency (Cuypers et al., 2009; Lynch & Brown, 1997),
which in turn is related to alterations in ethylene biosynthesis and sig-
naling (Iqbal et al., 2013); and (2) metal stress generates reactive oxy-
gen species (ROS) and induces an oxidative challenge in plants, which
4 NAING ET AL.
Physiologia Plantarum
might trigger ethylene for ROS signaling (Mersmann et al., 2010;
Montero-Palmero et al., 2014). The induced ethylene at higher levels
negatively affects root and leaf development (Arteca & Arteca, 2007;
Schellingen et al., 2015). Conversely, Ciardi et al. (1997) and Zhang
and Huang (2010) claimed that low temperature-induced ethylene
regulates freezing tolerance in tomato and tobacco, but Shi
et al. (2012) opposed this statement because low temperature-
enhanced ethylene production suppresses the expression of cold-
regulated genes and does not regulate freezing tolerance. This was
proven by Zhao et al. (2014) using ethylene inhibitors and enhancers,
whereas the inhibition of ethylene biosynthesis by ethylene inhibitors
enhanced freezing tolerance, and exogenous applications of ethylene
reduced cold acclimation-induced freezing tolerance. This suggests
that the adverse or beneficial effects of low temperature-induced eth-
ylene on plant growth vary depending on plant species (i.e., cold-
sensitive or cold-insensitive) and the amount of ethylene induced by
the stress. Variation in the salinity-induced ethylene production rates
has been found to depend on the growth stages of the plants and
plant species (Arbona et al., 2005; Bar et al., 1998; Botella
et al., 2000). Nadeem et al. (2010) summarized the results of previous
studies that reported ethylene production at different developmental
stages under salinity stress. Ethylene production was positively associ-
ated with salt concentrations, and salt-induced ethylene production neg-
atively affected seed germination and growth in lettuce cultivars
(Lactuca sativa L.; Alvarez et al., 2003). In addition, salt stress-induced
ethylene significantly shortened the shelf life of tomato (Mizrahi, 1982)
and inhibited the seedling growth of alfalfa (Li et al., 1995). Overall, this
section has identified that stress ethylene production is induced in
various plants in response to various abiotic stresses, and the stress
ethylene adversely affects plant growth and development. Despite
several approaches that can ameliorate the adverse effects of ethyl-
ene stress on plant growth, ACCD-producing PGPBs have been
widely utilized as more environmentally friendly and economically
cost-effective approaches.
3 | MODE OF ACCD-PRODUCING PGPB IN
ETHYLENE AMELIORATION AND PLANT
G RO WTH P R OM O TI ON
The bacterial enzyme ACCD is a type of pyridoxal 5-phosphate (PLP)-
dependent polymeric enzyme belonging to the tryptophan synthase
family, with a subunit molecular mass of approximately 35–42 kDa
(Ali & Glick, 2021; Honma & Shimomura, 1978). It was first discovered
in the Pseudomonas sp. strain ACP and its modulatory effects on the
ethylene levels in plants via, the breakdown of ACC into ammonia and
α-ketobutyrate have been documented (Honma & Shimomura, 1978).
The presence of ACCD in all three domains of life, eukarya, bacteria,
and archaea, has been reported, despite being majorly present in dif-
ferent species of bacteria and in some fungi (Nascimento et al., 2014;
Singh, Shelke, et al., 2015). Its presence in some plant species such as
Arabidopsis, poplar, and tomato plants has also been documented
(McDonnell et al., 2009; Plett et al., 2009). The induction of ACCD is
a complex and slow process, and its enzyme activity in many bacterial
species varies depending on pH and temperature, and the highest
activity levels are found with a pH of 8.0–8.5 and temperatures of
30
C (Glick et al., 1998; Zhao et al., 2003). In addition, as ACCD is a
type of inducible enzyme, its substrate ACC, with a minimum level of
100 nM (in Pseudomonas sp. strain ACP and Pseudomonas putida
GR12-2) is required for the induction of ACCD (Jacobson et al., 1994;
Walsh et al., 1981). Under abiotic stress conditions, ACC is induced
and is converted to ethylene, and stress-induced ethylene inhibits
auxin response factors. When the plants were inoculated with ACCD-
producing bacteria, the bacteria synthesized indole-3-acetic acid (IAA)
due to the presence of tryptophan and other small molecules in the
plant root exudates. The IAA synthesized in the bacteria, together
with endogenous plant IAA, can regulate several phases of plant
growth and development and can also induce the transcription of the
plant enzyme ACC synthase (ACS), which catalyzes the formation of
ACC (Tsakelova et al., 2006). In this case, the bacteria use the ACC
synthesized in plant tissues to induce the ACCD enzyme, and the
ACCD enzyme finally hydrolyzes excess ACC to ammonia and
α-ketobutyrate (Figure 2). The hydrolysis of ACC modulated the
stress-induced ACC levels inside the plants and reduced the amount
of ACC outside the roots (rhizosphere environment) under abiotic
stress conditions, through the exudation of more ACC into the rhizo-
sphere. This led to a reduction in ethylene production and promoted
water and nutrient uptake and plant growth by modification of the
root architecture and the root uptake system (Glick, 2014; Glick
et al., 1998, 2007; Timmusk et al., 2011).
Although ACCD can hydrolyze ACC, its hydrolyzing power is
dependent on its activities. For example, high ACCD activity is effec-
tive in modulating stress-induced ethylene for a wide range of plant
species, while low activity is effective for some specific plant species,
or they are not able to sufficiently lower the overproduction of ethyl-
ene levels in plants (Glick, 2005). By measuring the concentrations of
α-ketobutyrate, ACCD activities in different bacterial strains are
largely different (Glick, 2005). In addition, the compatibility of bacte-
rial strains and host plants also influences plant growth. Therefore, an
appropriate choice of bacterial strains with high ACCD activity is nec-
essary for the targeted plant species. In the following section, we dis-
cuss the interactions of ACCD-producing bacteria and host plants
that have been encountered in previous studies and the influence of
the ACCD present in the bacteria for the modulation of stress ethyl-
ene levels in different abiotic stress conditions.
4 | DI STRIBUTI ON OF THE A C D S G E N E I N
B A C TE R I A A N D P L A N T S
AcdS, which encodes ACCD activity, has been observed in a wide
range of bacterial strains (Belimov et al., 2001; Hontzeas et al., 2004;
Timmusk et al., 2011; Tak et al., 2013) and in a few plant species such
as Arabidopsis, poplar, and tomato (McDonnell et al., 2009; Plett
et al., 2009). The expression levels of the AcdS gene in bacteria were
found to be controlled by the presence or absence of oxygen, the
TABLE 1 Abiotic stress tolerance and growth responses of host plants after inoculation with ACC deaminase producing PGPB strains

Host plant ACCD producing PGPB strains Growth response against abiotic stress Stress tolerance References
NAING ET AL.

Alfafa Bacillus megaterium NMp082 Increased nodulation, shoot, and primary root growth Salt stress Chinnaswamy
et al. (2018)
Pseudomonas aeruginosa (LJL-5) Enhanced plant biomass, SPAD, and P contents Saline-Alkali stress Liu et al. (2019)
Enterobacter aerogenes (LJL-13) Induced activity of antioxidant enzymes (SOD, POD, and CAT) and
accumulation of antioxidants
Removed harmful substances
Increase in crude protein but decrease in fiber content
Argentine screwbean Lysinibacillus fusiformis Promoted germination and early growth Salt stress Sgroy et al. (2009)
Bacillus subtilis
Brevibacterium halotolerans
Bacillus licheniformis
Bacillus pumilus
Achromobacter xylosoxidans
Pseudomonas putida
Black gram and Pea Ochrobactrum pseudogrignonense RJ12 Increased seed germination percentage, root and shoot length, and dry Drought stress Saikia et al. (2018)
Pseudomonas sp. RJ15 weight
B. subtilis RJ46 Elevated ROS scavenging enzymes and cellular osmolytes
Higher chlorophyll content, relative water content, and root recovery
intention
Camelina P. putida UW4 Less decline in root length and weight Salt stress Heydarian
Pseudomonas migulae 8R6 Enhanced root system development et al. (2016)
Pseudomonas fluoresces YsS6 Increased shoot length
P. migulae 8R6M (mutant) Better seed production and seed quality
Pseudomonas fluorescens YsS6 (mutant) Higher levels of seed oil production
Chickpea P. putida MTCC5279 (RA) Modulated membrane integrity, osmolyte accumulation (proline, glycine Drought stress Tiwari et al. (2016)
betaine), reactive oxygen species (ROS) scavenging ability, and stress-
responsive gene expressions
B. subtilis BERA 71 Enhanced synthesis of photosynthetic pigments Salt stress Abd_Allah
Reduced ROS level and lipid peroxidation et al. (2018)
Increased activities of ROS scavenging antioxidants (superoxide dismutase,
peroxidase, catalase, and glutathione reductase)
Increased levels of nonenzymatic antioxidants (ascorbic acid and glutathione)
and phenol contents
Decreased sodium accumulation
Enhanced nitrogen, potassium, calcium, and magnesium content
Improved membrane stability
Common bean Aneurinibacillus aneurinilyticus strain AIOA1 Enhanced seed germination, root and shoot length, fresh and dry weight of Salt stress Gupta and
Paenibacillus sp. SG_AIOA2 root and shoot, relative water content, chlorophyll, and carotenoid Pandey (2020)
content
Physiologia Plantarum

Increase in osmoprotectants (proline and total sugars)

Increased activities of antioxidative defensive enzymes (POD, SOD, and
CAT) and phenolics content for scavenging salt-induced ROS
5

(Continues)
 6

TABLE 1 (Continued)

Host plant ACCD producing PGPB strains Growth response against abiotic stress Stress tolerance References
Edible birdsfoot Variovorax paradoxus 5C-2 Improved nodulation, root growth, and uptake of nutrients (N, P, Ca, Mg, Na, Heavy metal stress Safronova
trefoil Mn, Zn, and Pb) et al. (2012)
Clustered birdsfoot
trefoil
Ciliate medick
Physiologia Plantarum

French bean A. aneurinilyticus ACC02 Increased plant growth in terms of length, fresh and dry weight of root/ Salt and drought stress Gupta and
Paenibacillus sp. ACC06 shoot biomass Pandey (2019)
Guinea grass B. licheniformis Higher shoot and root length, leaf area, and dry matter Salt and drought stress Tiwari et al. (2018)
B. subtilis Conservation of plant water content
Decrease in electrolyte leakage
Maintaining chlorophyll content under drought stress
Enhanced proline, total soluble sugar, total soluble protein content, and total
phenol
Increase in cellulose, hemicellulose, and decrease in lignin contents of cell
walls
Improvement of total reducing sugar and ethanol yield
Holy basil A. xylosoxidans Fd2 Reduced ethylene production Waterlogging stress Barnawal et al. (2012)
Serratia ureilytica Bac5 Higher chlorophyll concentration
Herbaspirillum seropedicae Oci9 Lower lipid peroxidation (MDA concentration)
Ochrobactrum rhizosphaerae Oci13 Lower proline concentration
Increased foliar nutrient uptake (N, P, and K+)
Maximum waterlogging tolerant, growth, and herb yield induced by A.
xylosoxidans
Jujube Pseudomonas lini Increased plant height, shoot and root dry matter, and relative water content Drought stress Zhang et al. (2020)
Serratia plymuthica Decreased malondialdehyde and abscisic acid (ABA) levels
Enhanced antioxidant enzyme activities
Madagasar periwinkle A. xylosoxidans AMU54 Maximum germination percentage, vigor index, plant height, root dry weight, Salt stress Karthikeyan
and anmalicine content et al. (2012)
Increase in antioxidative enzyme (SOD and CAT)
Maize Bacillus amyloliquefaciens SQR9 Enhanced chlorophyll content, total soluble sugar content, decreased cell Salt stress Chen et al. (2016)
destruction, improved peroxidase/catalase activity and glutathione
content for scavenging ROS, reduced Na+ level, and decreased Na+
toxicity
Bacillus aryabhattai NBRI YN4.4 (MTCC Increased photosynthetic pigments and soluble sugar Alkalinity stress Dixit et al. (2020)
7755T) Decreased proline level
Marsh dock P. putida WT Reduced flood responses such as an increased leaf elongation and shoot Water logging stress Ravanbakhsh
fresh weight et al. (2017)
Mini carnation cut P. fluorescens YsS6 (wild type) Delay in flower senescence Salt stress Ali et al. (2012)
flowers P. migulae 8R6 (wild type)
Mung bean B. subtilis Enhanced germination, root and shoot length Salt stress Patel et al. (2015)
B. megaterium
NAING ET AL.
TABLE 1 (Continued)

Host plant ACCD producing PGPB strains Growth response against abiotic stress Stress tolerance References
NAING ET AL.

Pea Arthrobacter protophormiae (SA3) Increase in fresh weight Salt stress Barnawal et al. (2014)
(Synergistic effect with Rhizobium Significant improvement in nodulation
leguminosarum (R) and Glomus mosseae (G)) Higher chlorophyll level in combination with R and G
Lower oxidative damage to lipids
Increase in proline concentration
Minimum Na+ content along with G
Improved P and K+
V. paradoxus 5C-2 Increased K uptake and K flow from root to shoot Salt stress Wang et al. (2016)
Decreased Na flow and increased Na deposition in root zone
Increased shoot K+/Na+ ratio
Decreased stomatal resistance and xylem balancing pressure
Improved photosynthetic efficiency and maximal electron transport rate
Pepper Bulkhorderia cepacia Proliferation of root system Drought and salt stress Maxton et al. (2018)
Citrobacter feurendii Increase in plant biomass
Serratia marcescens Sustained high chlorophyll “a” concentration
Decreased proline concentration
Potato Bacillus sp. (SR-2-1/1) Increase in relative leaf water content Salt stress Tahir et al. (2019)
Bacillus sp. (SR-2-1) Decrease in electrolyte leakage and antioxidant enzyme activity
Decrease in Na+ whereas increase in K+, Ca+2, K+/Na+, and Ca+2/Na+ in
plant
Enhanced auxin production in roots
Increased plant biomass, number of tubers per plant, and tuber weight
Rapeseed Sinorhizobium mellilote Increase in shoot and root elongation, dry weight, stem diameter, leaf Salt stress Saghafi et al. (2019)
Sinorhizobium mellilote numbers, and relative water content
Rhizobium legominozaroum bv. phaseoli Improved nutrient uptakes (N, P, and K) and chlorophyll (SPAD value)
Rhizobium legominozaroum bv. phaseoli
Red pepper Pseudomonas frederiksbergensis OB139 Significantly increased plant growth Salt stress Samaddar et al. (2019)
Pseudomonas vancouverensis OB155 Enhanced catalase activity leading to neutralization of hydrogen peroxide
ions
Lower malondialdehyde (MDA) content
Increased photosynthetic pigment contents
Red Thorn B. subtilis BERA 71 Enhanced osmoprotectants production Salt stress Hashem et al. (2016)
Reduced lipid peroxidation
Modulated osmoregulatory system (glycine betaine, proline, and phenols)
and antioxidant enzyme system
Rice Alcaligenes sp. SB1.ACC2 Higher plant growth parameters Salt stress Bal et al. (2013)
Bacillus sp. SB1.ACC3 Longest roots and shoots; highest root fresh weight, and dry weight by
Ochrobactrum sp. SB2.ACC2 Alcaligenes sp.
P. fluorescens REN1 Increased root elongation Flooding stress Etesami et al. (2014)
Physiologia Plantarum

Pseudomonas stutzeri A1501 Promoted plant height, root length, root fresh weight, and dry weight Salt and heavy metal Han et al. (2015)
stress
7

(Continues)
 8

TABLE 1 (Continued)

Host plant ACCD producing PGPB strains
Streptomyces sp. GMKU 336
Growth response against abiotic stress Stress tolerance References
Increased plant growth, chlorophyll, proline, K+, Ca+, and water contents Salt stress Jaemsaeng
Decreased ethylene, reactive oxygen species (ROS), Na+, and Na+/K+ ratio et al. (2018)
Down-regulation of genes in ethylene pathway, ACO1 and EREBP1
Up-regulation of acdS encoding ACCD in-vivo, osmotic balance (BADH1),
Na + tansporters (NHX1 and SOS1), calmodulin (Cam1-1), and antioxidant
Physiologia Plantarum

enzymes (CuZn-OD1 and CATb)

Down-regulation of gene in a signaling cascade, MAPK5
Enterobacter sp. S2 Enhanced amylase, protease, total sugar content, and total protein content Cadmium (Cd) stress Mitra et al. (2018)
Decreased protease activity
Stimulation of antioxidant proteins
Increase in chlorophyll a, b, and total chlorophyll content
Enhanced SOD, catalase activity, and proline content
Reduced MDA content
Decreased Cd uptake
E. aerogenes K6 Increased α-amylase activity Cadmium (Cd) stress Pramanik, Mitra,
Reduced degradation of proteins and maintained protein homeostasis via, et al. (2018)
active proteases
Increased chlorophyll content
Enhanced active antioxidant enzymes
Reduced ethylene content and Cd uptake
Enterobacter sp. K2 Enhanced growth characters including seed germination, root and shoot Cadmium (Cd) stress Pramanik, Soumik,
length, root and shoot biomass, seedling vigor index, and chlorophyll et al. (2018)
content
Enterobacter sp. P23 Increased germination, seedling vigor index (SVI), root length, root fresh Salt stress Sarkar, Ghosh,
(99.38% similar to weight, root dry weight, lateral branching of the roots, and chlorophyll et al. (2018)
Enterobacter ludwigii strain EN119) contents
Increased antioxidant enzymes, MDA, proline, total protein, IAA, and total
sugar
Burkholderia sp. P50 Increased germination, root and shoot length, root and shoot weight, and Salt stress Sarkar, Pramanik,
SVI et al. (2018)
Enhanced IAA, amylase, protease, total auxin, and chlorophyll
Decrease in ROS scavenging antioxidant enzymes (SOD and CAT) and lipid
peroxidation
Safflower Bacillus cereus Increased plant growth Salt stress Hemida and
B. aerius Enhanced ascorbate-glutathione redox cycle Reyad (2018)
Slender glasswort Bacillus sp. Improved seed germination and seedling biomass CO2, temperature, and Mesa-Marín
Enhanced seed nitrogen content and consequent increase in seedling vigor salt stress et al. (2019)
Soybean B. cereus SA1 Improved plant biomass, chlorophyll content and fluorescence Heat stress Khan et al. (2020b)
Reduced abscisic acid and increased salicylic acid
Higher levels of ascorbic acid peroxidase, superoxide dismutase, and
glutathione
Increased amino acid contents
NAING ET AL.
TABLE 1 (Continued)

Host plant ACCD producing PGPB strains Growth response against abiotic stress Stress tolerance References
NAING ET AL.

Increased heat shock protein (HSP) expression

Overexpression of stress-responsive GMLAX3 and GmAKT2
Decrease in ROS
Alteration of auxin and abscisic acid stimuli
Enhancement of potassium gradients
Switchgrass Pseudomonas grimontii Bc09 High expression of HSP70 and HMA2 genes Cadmium (Cd) stress Begum et al. (2019)
Pantoea vagans So23 Reduced Cd accumulation
Pseudomonas veronii E02 Increased IAA production and biomass
P. fluorescens Oj24
Tomato P. fluorescens YsS6 Higher chlorophyll contents, fresh and dry biomass, greater number of Salt stress Ali et al. (2014)
P. migulae 8R6 flowers and buds
Pseudomonas spp. OFT2 and OFT 5 Promotion of plant growth, leaf water contents, photosynthetic Salt stress Win et al. (2018)
performance, and ionic balance
No reduction in shoot uptake of Na
Improvement in shoot uptake of macronutrients (P, K, and Mg) and
micronutrients (Mn, Fe, Cu, and Zn)
Leclercia adecarboxylata MO1 Increased growth attributes Salt stress Kang et al. (2019)
Improvement of glucose, fructose, citric acid, malic acid, serine, glycine,
methionine, threonine, and proline
Noticeably lower level of endogenous abscisic acid (ABA) level
Pseudomonas sp. UW4 (wild type) UW4 strain Salt stress Orozco-Mosqueda
Pseudomonas sp. (OxtreS, trehalose over- Increased plant root, shoot length, total dry weight, and chlorophyll content et al. (2019)
expressing strain) OxtreS strain
Greater improvement in root length than UW4 strain
Similar beneficial effect on shoot length, total dry weight, and chlorophyll
content as wild type
B. cereus SA1 (in co-application Improved biomass and chlorophyll fluorescence Heat stress Khan et al. (2020a)
with humic acid [HA]) Reduced abscisic acid and improved salicylic acid
Increased ascorbate peroxidase (APX) and SOD
Decreased glutathione (GSH)
Higher iron, phosphorus, and potassium uptake
Increased relative expression of SIWRKY33b and autophagy related (SIATG5)
genes
Reduced SIWRKY33b and SIATG5 expression
Upregulated heat stress-responsive transcription factor (SIHsfA1a) and high-
affinity potassium transporter (SIHKT1)
B. cereus Promoted growth of shoot, root length, leaf surface area, fresh and dry Heat stress Mukhtar et al. (2020)
weight
Reduced extracellular polymeric substances (EPS) production
Physiologia Plantarum

Wheat P. putida (W2) Enhanced germination percentage, rate, and index Salt stress Nadeem et al. (2013)
Enterobacter cloacae (W6) Increased growth and yield parameters
Serratia ficaria (W10)
9

(Continues)
 (Continued)
10

TABLE 1

Host plant ACCD producing PGPB strains Growth response against abiotic stress Stress tolerance References
P. fluorescens (W17) Improved nutrient balance (low sodium and high nitrogen, phosphorus, and
potassium contents)
B. cereus strain Y5 Improved growth Salt stress Khan et al. (2017)
Bacillus sp. Y14
B. subtilis strain Y16
Physiologia Plantarum

Halophilic strains Increased yield Alkalinity stress Torbaghan

Virgibacillus sp. (H1) et al. (2017)
Virgibacillus pantothenticus (H7)
Alkaliphilic strains
Bacillus clausii (A1 and A7)
Haloalkaliphilic strains
Virgibacillus marismortui (HA1)
Alkalibacillus haloalkaliphilus (HA6)
Klebsiella isolates (8LJA and 27IJA) Significant increase in plant biomass content and root SOD activity Salt stress Acuña et al. (2019)
Kocuria rhizophila (14ASP) Higher fresh and dry root masses, shoot length, number of leaves, relative Salt stress Afridi et al. (2019)
Cronobacter sakazakii (OF115) water contents, K+/Na+ ratios, chlorophyll contents, and antioxidant
activities
V. paradoxus RAA3 Improved plant growth, foliar nutrient concentrations, and antioxidant Water stress Chandra et al. (2019)
Pseudomonas spp. DPC12, DPB13, DPB15, properties
DPB16
Achromobacter spp. PSA7, PSB8
Ochrobactrum anthropic DPC9
Pseudomonas sp. Enhanced seed germination percent, shoot length, fresh and dry weigh, Salt stress Damodaran
Agromyces tropicus seedling vigor I and II (Lysinibacillus sp. being the most effective isolate) et al. (2019)
L. fusiformis Higher root length, fresh and dry weight (L. fusiformis)
Bacillus flexus
Lysinibacillus sp.
Bacillus tequilensis
B. licheniformis
Pseudomonas mendocina
B. licheniformis
Velvet bean Bacillus sp. Improved plant growth Drought stress Saleem et al. (2018)
Enterobacter sp. Higher isoprene emission
NAING ET AL.
NAING ET AL.
presence of its substrate ACC, leucine responsive regulatory protein
(LRP; Li & Glick, 2001; Cheng et al., 2008), nitrogen-fixing regulator
(nifA; Nukui et al., 2006), and ACCD regulatory genes (acdR; Cheng
et al., 2008; Duan et al., 2009; Li & Glick, 2001), depending on the
bacterial strain. Isolation of AcdS genes from different bacterial strains
and plant species was performed, and their introduction to commer-
cially important plants via, metabolic genetic engineering provides
benefits for the reduction of stress-induced ethylene. This alterna-
tively helps crops that are not compatible with direct inoculations of
ACCD-producing bacteria to reduce ethylene. Consequently, the cur-
rent progress in the use of the AcdS gene in plant biotechnology for
the amelioration of stress ethylene in plants is highlighted.
5 | I M P O R TA N CE O F T HE C O M P A T I BI L I T Y
O F B A C T E R I A L ST R A I N S A N D H O S T P L A N T S ,
AS WELL AS ACCD ACTIVITIES IN THE
P R O M O TI O N OF P L A N T G R O W T H U ND E R
A B I O T I C ST R E S S
As described above, ACCD can ameliorate the deleterious effects of
stress-induced ethylene and promote plant growth under abiotic
stress via, the breakdown of the ethylene precursor ACC into ammo-
nia and α-ketobutyrate. Consequently, inoculating plants with ACCD-
producing bacteria in different abiotic stress conditions has received
more attention and has shown noticeable results. Previous review
articles described the roles of the ACCD-producing PGPBs in plant
growth promotion in normal or stress conditions. However, most of
the previous reviews did not discuss how the PGPB strains and their
ACCD activities influenced the promotion of the host plant growth
and how the PGPBs' functions were changed under abiotic stress. In
this section, we focus on the issues that have been lacking in most
previous reviews using the facts described in the research reports
published during the past 10 years.
During the past 10 years, several PGPB strains with different
ACCD activities have been inoculated into various plants to promote
plant growth and crop yields under various abiotic stress conditions
(such as flooding, drought, heavy metals, salinity, heat, and alkalinity).
Table 1 summarizes the positive roles of PGPBs in plant growth pro-
motion during abiotic stresses via, the amelioration of the deleterious
effects of stress-induced ethylene, elevation of antioxidant activities,
and transcriptional activation of the stress-responsive genes. Begum
et al. (2019) observed that two bacterial strains (Pseudomonas veronii
and Pseudomonas grimontii) affected the growth of switchgrass differ-
ently in normal and cadmium (Cd) stress conditions, with better plant
growth in the Cd stress conditions with the P. grimontii and in normal
conditions with the P. veronii. This was linked to the higher production
of IAA in these strains. The amount of IAA produced in the P. grimontii
was higher than that in the P. veronii in Cd stress conditions, which
were opposite to those observed under normal conditions. In a study
by Afridi et al. (2019), ACCD activity was found to be elevated in
Cronobacter sakazakii (OF115) and reduced in Kocuria rhizophila
(14ASP) in salt stress conditions, when compared to normal growth
11
Physiologia Plantarum
conditions. Whereas, OF115 with high ACCD activity levels resulted
in higher salt tolerance for wheat plants. The two strains used in the
study by Afridi et al. (2019) were halotolerant (salt tolerant). However,
the mechanisms for the reduction or elevation of the ACCD activity in
the strains with the same salt stress is still unknown. The authors did
not discuss possible reasons for this. This could be due to changes in
the environment because expression of the AcdS gene that induces
ACCD activity in bacteria can be controlled by variable environments
(Li & Glick, 2001; Singh, Jha, & Jha, 2015). This could also be due to
changes in the pH and temperature, because the highest activity
levels were seen with a pH 8.0–8.5 and temperature of 30
C (Glick
et al., 1998; Zhao et al., 2003). Another possible reason is that the
degree of stress tolerance for strains like 14ASP and OF115 might be
different, in which 14ASP itself might be less tolerant to high salt
stress (15% NaCl) when compared to OF115. Thus, they might be
inactive to produce ACCD activity, which resulted in the production
of lower ACCD activity for stress tolerance. Previous studies have
reported that the ACCD-producing halotolerant bacteria (Bacillus, Azo-
tobacter, Microbacterium, Pseudomonas, and Serratia) survived in salt
stress conditions ranging from 2 to 11% NaCl (Barra et al., 2016;
Singh & Jha, 2016), but their tolerances to high salt concentrations of
15% were not investigated. Depending on the salt level and the type
of bacterial strain, variation in the bacterial survival rate has been
observed (Naz et al., 2009; Sgroy et al., 2009; Trabelsi et al., 2009).
Unfortunately, those authors did not investigate the variations in
ACCD activity in bacteria (Bacillus, Azotobacter, Microbacterium, Pseu-
domonas, and Serratia) under salt stress (Table 2).
Khan et al. (2017) also observed a wide variation in ACCD activity
(85–399 nmol α-ketobutyrate mg1 h1) in halotolerant Bacilius spp.
isolated from wheat plant rhizospheres. Interestingly, despite the
presence of ACCD activity, some bacteria did not improve plant
growth in normal or salt stress conditions, and more interestingly,
some bacteria negatively affected plant growth, compared to the non-
inoculated plants. In addition, the promotion of plant growth by the
bacteria in stress conditions was not linked to the presence of higher
or lower ACCD activity levels. For example, the isolate Y22, induced
the highest ACCD activity level (399.33 nmol α-ketobutyrate
mg1 h1) and the IAA concentration negatively affected plant growth
in stress conditions. In a study by Penrose and Glick (2003), bacteria
with ACCD activity levels of higher than 300–400 nmol
α-ketobutyrate mg1 h1 did not improve or inhibit plant growth,
whereas ACCD (20 nmol α-ketobutyrate mg1 h1) was found to be
sufficient for the amelioration of stress-induced ethylene. The nega-
tive effects of high ACCD levels on plant growth could be that it will
break down most of the ACC induced in the plant tissues and produce
ammonia levels higher than 0.1 mM, which lowers root/shoot ratios
and causes leaf chlorosis (Britto & Kronzucker, 2002). It has been
suggested that high ACCD activity levels are not always important for
the promotion of plant growth, irrespective of whether there are nor-
mal or stress conditions. Another explanation for the negative effects
on wheat growth by Y22 could be the overproduction of auxins (IAA)
(Spaepen et al., 2007). Alternatively, isolate Y22 itself is likely harmful
to wheat plant growth. The authors also claimed that 28% of the
12 NAING ET AL.
Physiologia Plantarum

TABLE 2 AcdS-overexpressing plants that reduced ethylene production and improved plant growth against abiotic stress

AcdS expressing
Source of AcdS gene transgenic plants Growth responses References
Pseudomonas sp. 6G5 Tomato Reduced ethylene production and promoted shelf- Klee et al. (1991)
life of tomato fruits
Pseudomonas sp. 6G5 Tomato, tobacco, and Reduced ethylene production and delayed Klee and Kishore (1992)
petunia senescence in plant tissues
Pseudomonas Tomato Reduced ethylene production and delayed fruit Reed et al. (1995)
chlororaphis ripening
Enterobacter cloacae Tomato Higher uptake of metal and less deleterious effect of Grichko et al. (2000)
UW4 metals-induced ethylene
E. cloacae UW4 Tomato Reduced the deleterious effects of root hypoxia and Grichko and Glick (2001a,
maintained plant growth against flooding stress. 2001b)
E. cloacae CAL2 Canola Higher uptake of arsenic content and reduced Nie et al. (2002)
deleterious effect of the stress-induced ethylene
and sustained plant growth against arsenic stress
(35 s only)
Pseudomonas putida Canola Higher uptake of Nickle content and reduced Stearns et al. (2005)
UW4 deleterious effect of the stress-induced ethylene
and sustained plant growth against Nickle stress
P. putida UW4 Canola Reduced deleterious effect of salt-induced ethylene Sergeeva et al. (2006)
and promoted plant growth against salt stress
P. putida UW4 Canola Promoted plant growth against flooding Farwell et al. (2007)
Pseudomonas veronii-KJ Arabidopsis Increased tolerance to waterlogging and salt stress Jung et al. (2018)
conditions
Trichoderma asperellum Arabidopsis Improved plant growth against salt stress Zhang et al. (2015)
P. putida Garden petunia Improved plant growth against heavy metal stress Zhang et al. (2008)
P. putida UW4 Gold-of-pleasure Increased seed production, better seed quality, and Heydarian et al. (2016)
higher levels of seed oil production under salt
stress

bacteria isolated from the wheat rhizosphere were harmful to wheat
plant growth. On the other hand, the negative effects observed in the
plants inoculated with the isolate (Y22) might be due to the incompat-
ibility of the isolate and host plants but were not due to higher ACCD
levels. This was proven with two isolates (i.e., Y3 and Y14) that have
similar ACCD activities (339.0 and 338.3 nmol α-ketobutyrate
mg1 h1,), but the Y3 inhibited and the Y14 improved plant growth.
Consideration of the appropriate choice of Bacilius strains for the
selected host plants is likely to be more important. In fact, several
Bacilius spp. such as Bacillus amyloliquefaciens, Bacillus megaterium
NMp082, Bacillus cereus, Bacillus aerius, and Bacillus subtilis BERA
71, had promoted growth of various plant species, such as alfalfa,
potato, maize, chickpea, soybean, safflower, tomato, and red thorn,
under salt and heat stress conditions (Abd_Allah et al., 2018; Chen
et al., 2016; Chinnaswamy et al., 2018; Hashem et al., 2016;
Hemida & Reyad, 2018; Khan et al., 2020a, 2020b; Mukhtar
et al., 2020; Tahir et al., 2019). Nevertheless, according to the findings
observed in the study by Khan et al. (2017), ACCD-producing Bacillus
species that are compatible with host plants should be screened for
wheat plant growth promotion in normal or stress conditions.
Acuña et al. (2019) claimed that some of the ACCD-producing
rhizobacteria that were isolated from the plant Parastrephia
quadrangularis contained a wide range of ACCD activities
(830–3320 nmol α-ketobutyrate mg1 h1). In contrast to a study by
Khan et al. (2017), the inoculation of the wheat seedlings with Klebsi-
ella isolates (8LJA and 27IJA) showed salt tolerance (from 2.5 to 7.5%
NaCl), although the activities contained in the isolates were higher
than those observed in the bacteria of Khan et al. (2017). Therefore, it
was again supposed that the negative effects were not likely to be
mainly associated with the ACCD activity levels, but could probably
be due to incompatibility of the bacterial strain and the wheat host
used. Occurrence of the incompatibility between the bacterial strains
and the host plants relies on a set of adaptation mechanisms by both
the bacterial strains (metabolic abilities, root colonization capacity,
regulation of genetic determinants involved in plant-growth-
promoting properties) and the host plants (pattern of exuded com-
pounds, properties of root surface, sensitivity to bacterial phytohor-
mones; Drogue et al., 2012).The importance of the compatibility
between the bacterial strains and the wheat host plants has been
reported using the different bacterial strains P. putida, Enterobacter
cloacae, Serratia ficaria, and Pseudomonas fluorescens (Nadeem
et al., 2013), whereas Pseudomonas spp. showed an improved perfor-
mance, regardless of the ACCD activity levels. In addition to the
importance of the bacterial strains, Acuña et al. (2019) also proved the
NAING ET AL.
requirement for higher ACCD activity levels to tolerate salt stress in
wheat seedlings when using two Klebsiella isolates (27IJA and 8LJA)
as the inoculum, which have the lowest and highest activity levels,
respectively. It is likely that if the compatibility of the bacterial stains
and host plants worked appropriately, the strain with the highest
activity level would make the plants more tolerant to stress than the
strain with the lowest level.
Barnawal et al. (2012) also observed the distribution of various
bacterial strains with varying ACCD activities (Fd2 [Achromobacter
xylosoxidans with 525.53 nmol mg1 protein h1], Bac5 [Serratia
1 1
ureilytica with 193.72 nmol mg protein h ], Oci9 [Herbaspirillum
seropedicae with 868.96 nmol mg1 protein h1], and Oci13
[Ochrobactrum rhizosphaerae with 403.27 nmol mg1 protein h1]) in
the rhizosphere of the waterlogged Ocimum plants. Despite the better
growth of plants inoculated with the bacterial strains, the strain Fd2
(A. xylosoxidans) with moderate levels of ACCD activity resulted in
maximum waterlogging tolerance of Ocimum sanctum, indicating again
the importance of the interactions between the bacterial strains and
the host plant.
In a study by Torbaghan et al. (2017), different groups of bacterial
strains (halophilic, alkaliphilic, and haloalkaliphilic strains) were found
to improve the growth of the wheat plants under salinity and alkalinity
stresses, when compared to noninoculated plants. However, the
plants inoculated with haloalkaliphilic strains had higher yields when
compared to the other strains due to better root growth systems,
which alleviates the detrimental effects of the stress. This is not sur-
prising as haloalkaliphilic strains have the ability to tolerate both salin-
ity and alkalinity stress. The bacterial strain Lysinibacillus sp. may also
be a member of the haloalkaliphilic group, as among several bacterial
strains isolated, it was observed to provide the best growth perfor-
mance under saline or saline-alkali stress conditions (Damodaran
et al., 2019). However, the authors did not reveal the reason why the
strain performed better than the other strains in stress conditions.
Such tolerance has also been observed in alfalfa and maize (Dixit
et al., 2020; Liu et al., 2019). Dixit et al. (2020) claimed that there was
more improvement of the alkali tolerance in maize plants by Bacillus
sp. NBRI YN4.4 than by other strains (Alcaligenes sp. NBRI NB2.5 and
Bacillus sp. NBRI YE1.3) and this was due to its maximum survivability
at pH 11. In fact, most PGPB did not effectively induce ACCD at pH
levels higher than 8.0–8.5, but Bacillus sp. NBRI YN4.4 survived well
at pH 11 compared to the other strains (Alcaligenes sp. NBRI NB2.5
and Bacillus sp. NBRI YE1.3). It seemed that the former strain is more
tolerant to high alkalinity than the latter strains, which will result in a
tolerance of the plants to alkaline conditions. It was suggested that
hyper-tolerant strains could be screened to help plants tolerate
extreme environments.
Similarly to wheat, the screening and characterization of bacterial
strains is a prerequisite for plant growth promotion in rice. In a study
by Etesami et al. (2014), not all isolates that survived inside the roots
of rice plants produced both IAA and ACCD activity. Generally, such
bacterial strains were not highly effective at promoting plant growth
under stress conditions, when compared to the strains that did pro-
duce both IAA and ACCD activity. Furthermore, they also found that
13
Physiologia Plantarum
the isolate REN1 (P. fluorescens) that produced IAA (<15 μg ml1) and
the highest ACCD activity levels (0.73 μmol of α-ketobutyrate
mg1 h1), exhibited the best results for root elongation in flooding
conditions. A similar finding was also reported by Misra et al. (2017),
as about half of the isolated strains showed ACCD activity. Of these,
only some strains resulted in the seed germination of a salt-sensitive
rice variety in saline conditions. Interestingly, although the bacteria
were salt-tolerant types and produced ACCD, none of the isolates
corresponded equally in mitigating salinity stress. Therefore, the inter-
actions between the bacteria and host plants should be investigated
to gain a better understanding of the mechanisms. In addition,
unequal mitigation of the stress by the bacteria could be due to the
differences in salinity tolerance of the bacterial strains or the varia-
tions of the original ACCD activity present in the bacteria.
Previous studies reported that although heavy metal-tolerant bac-
terial strains survive in metal-contaminated rice rhizosphere zones,
the presence of ACCD activity in the bacteria and their effects on the
growth of rice seedlings in heavy metal stress conditions varied (Mitra
et al., 2018; Pramanik, Mitra, et al., 2018; Pramanik, Soumik,
et al., 2018). Whereas, the isolates (S2, K6, and K2) with the highest
ACCD activity and IAA levels exhibited cadmium tolerance to rice in
their respective studies (Mitra et al., 2018; Pramanik, Mitra,
et al., 2018; Pramanik, Soumik, et al., 2018). The importance of ACCD
activity for rice plant growth in salt and heavy metal stress conditions
was previously confirmed by Han et al. (2015) using Pseudomonas
stutzeri A1501 (wild type) and A1815 (negative for ACCD activity).
While the A1501 strain significantly improved plant growth, signifi-
cant differences were not observed between mutant A1815 treated
plants and the controls. Similarly, Jaemsaeng et al. (2018) and Sarkar,
Ghosh, et al. (2018) and Sarkar, Pramanik, et al. (2018) also proved the
importance of ACCD activity for rice plant growth promotion in salt
stress conditions using an acds gene mutant strain and a high ACCD-
producing strain. Moreover, among the many bacterial strains tested,
the strains Streptomyces sp. GMKU 336, Enterobacter sp., and Bur-
kholderia sp. were shown to have a greater promoting effect on rice
seedling growth in salt stress conditions in their respective studies
(Jaemsaeng et al., 2018; Sarkar, Ghosh, et al., 2018; Sarkar, Pramanik,
et al. (2018)), supporting the importance of bacterial strains as well in
this regard. Overall, the improvement of plant growth by the ACCD-
producing bacteria in abiotic stress conditions was due to the amelio-
ration of the deleterious effects of the stress ethylene by ACCD via,
the downregulation of ethylene-related genes and the upregulation of
antioxidant related genes, as well as the interactions of the bacterial
strains and host plants.
As observed for the above crops, a significant influence of the
ACCD and bacterial strain on tomato host plant growth has also been
reported (Ali et al., 2014; Kang et al., 2019; Mayak et al., 2004b;
Orozco-Mosqueda et al., 2019; Win et al., 2018). Mayak et al. (2004b)
observed that the PGPB (Achromobacter piechaudii) with ACCD activ-
ity significantly increased the fresh and dry weights of tomato seed-
lings grown under the salt stress conditions. Ali et al. (2014) proved
that ACCD activity had a positive role in plant growth in salt stress
conditions using the bacterial stains P. fluorescens YsS6 (ACCD;
14
Physiologia Plantarum
12.5 mmol of α-ketobutyrate mg1 h1), Pseudomonas migulae 8R6
(ACCD; 10.9 mmol of α-ketobutyrate mg1 h1), and their ACCD defi-
cient mutants (ACCD; 0.11 mmol of α-ketobutyrate mg1 h1 and
0.03 mmol of α-ketobutyrate mg1 h1), respectively. However, they
did not compare the differential roles of the bacterial strains
(P. fluorescens and P. migulae) in plant growth, while a significant influ-
ence of Pseudomonas spp. strains (OFT2 and OFT5) on tomato plant
growth under salt stress was reported by Win et al. (2018). A knock-
out of the AcdS gene in the bacterial strains indicated that ACCD was
directly responsible for plant growth under stress conditions. This was
further confirmed by Orozco-Mosqueda et al. (2019), whereas knock-
outs of the AcdS gene in Pseudomonas sp. UW4 reduced the tolerance
of tomato plants to salt stress when compared to the wild type, which
was consistent with the results observed in the study by Ali
et al. (2014). The knockout of the AcdS gene in P. putida UW4, Pseu-
domonas lini, and Serratia plymuthica was also performed by
Ravanbakhsh et al. (2017) and Zhang et al. (2020), and observed no
reduction in the amount of stress-induced ethylene released in Rumex
palustris and jujube seedlings in flooding and drought stress. Similarly,
carnation cut flowers and Camelina sativa plants inoculated with the
acds-deficient bacteria P. migulae 8R6 and Pseudomonas fluoresces
YsS6 did not promote flower longevity and plant growth in salt stress
conditions, whereas wild-type strain inoculations did promote flower
longevity and plant growth (Ali et al., 2012; Heydarian et al., 2016).
This demonstrated that the amount of ethylene released in the plants
could be related to the ACCD produced by the wild strains in stress
conditions.
Maxton et al. (2018) reported that some bacteria such as Serratia
marcescens, Citrobacter feurendii, and Bulkhorderia cepacia, could pro-
tect pepper plants from both salt and drought stress, despite the max-
imal efficacy of Burkholderia cepacia with high ACCD activity on stress
tolerance. Such bacterial strains were also observed in the rhizosphere
zone of Panicum maximum by Tiwari et al. (2018) and in garlic by
Gupta and Pandey (2019). However, the distribution of ACCD-
producing bacteria is different in the rhizosphere, and mainly depends
on the plant species present. When P. maximum and French bean
were inoculated with the ACCD-producing bacterial strains, plant
growth was promoted under salt and drought stress conditions. How-
ever, depending on the presence of ACCD activity in the strains and
compatibility of the bacterial strain and host plants, plant growth pro-
motion against stress also varied. Typically, the strain ACC06
(Paenibacillus sp.) has high ACCD activity levels, and when inoculated
with French bean it promoted plant growth under salt and drought
stress conditions (Gupta & Pandey, 2019). It seemed that the pres-
ence of high ACCD in the bacteria was able to protect the crops from
multiple stresses, which might be because high ACCD activity levels
hydrolyzed large amounts of ACC that was induced by multiple
stresses. Thus, the use of such bacterial strains as inoculums could
have more benefits for plant growth than the application of bacteria
that can tolerate only a single stress. These findings further supported
the theory that the negative effect of the high ACCD-producing bac-
teria on wheat plant growth in salt stress conditions was due to the
incompatibility of the bacterial strain and host plant.
NAING ET AL.
Zhang et al. (2020) reported the dominant distribution of Pseudo-
monas spp. (six out of eight isolates) in the rhizosphere zone of jujube
seedlings, whereas even in the same genus, the presence of the ACCD
activity varied depending on the species. For example, the ACCD
activity in the strain P. lini was higher than that of the other five Pseu-
domonas spp. and its inoculation to the jujube seedlings effectively
improved drought stress tolerance. The group of pulse crops such as
velvet bean or chickpea inoculated with the bacterial strains
(Enterobacter spp. (HS9), and Bacillus spp. (G9)) or P. putida improved
drought stress (Saleem et al., 2018; Tiwari et al., 2016). Similarly, peas
inoculated with Variovorax paradoxus 5C-2 also improved salt stress
tolerance (Wang et al., 2016). However, most of these studies did not
investigate the compatibility of bacterial strains and host plants.
5.1 | Consortium effect of bacterial strains on
plant growth
As described above, there have been several reports describing the
positive roles of ACCD-producing bacteria in plant tolerance to vari-
ous abiotic stresses, regardless of the incompatibility of the bacterial
strains and host plants and the influence of the ACCD activity present
in the bacteria. However, in most reports comparing the effects of the
single inoculation and mixed inoculation of the bacterial strains on
plant growth against abiotic stress, a mixed inoculation strategy was
found to be better for plant growth than a single inoculation strategy.
For example, in the studies of Gupta and Pandey (2019, 2020), mixed
inoculations of Aneurinibacillus aneurinilyticus and Paenibacillus
sp. were better for the growth of French bean and common bean
plants in normal or stress conditions than a single inoculation. Such
consortium effects on drought stress tolerance were also observed in
other pulse crops such as black gram and pea, which were inoculated
with a combination of Ochrobactrum pseudogrignonense
RJ12 + Pseudomonas sp. RJ15 + B. subtilis RJ46 (Saikia et al., 2018).
Similarly, mung beans inoculated with B. subtilis + B. megaterium
(Patel et al., 2015) and red pepper inoculated with Pseudomonas
frederiksbergensis OB139 + Pseudomonas vancouverensis OB155
(Samaddar et al., 2019) also exhibited more tolerance to salt stress
than a single inoculation. Similarly, mixed inoculations of such bacteria
like Arthrobacter protophormiae with other beneficial microbes such as
Rhizobium leguminosarum have synergistic effects on pea plant growth
(Barnawal et al., 2014). This could also be due to the ability of Rhizo-
bium strains to promote plant growth. Saghafi et al. (2019) demon-
strated the plant growth-promoting role of Rhizobium strains such as
R29 (Sinorhizobium mellilote), R103 (Sinorhizobium mellilote), R281 (Rhi-
zobium legominozaroum bv. phaseoli), and R307 (Rhizobium
legominozaroum bv. phaseoli) in canola seedlings under salt stress. It
seemed that the interactions between the strains and the host plants
were compatible, and the constituent strains also worked in a syner-
gistic and coordinated manner for plant growth promotion and stress
tolerance. Recently, Santoyo et al. (2021) also highlighted benefits of
using different bacterial consortia on plant growth stimulation. Due to
the consortium effects, a mixed application strategy can be used as an
NAING ET AL.
alternative approach to effectively promote plant growth against abi-
otic stresses that cannot be achieved with a single inoculation. How-
ever, selecting bacterial strains that interact well with each other as
well as being compatible with the host plants is necessary.
6 | G EN E R A TI O N O F TR A N SGE N I C
P L A N T S O V ER E X P RE S S I N G A C D S G E N E
Despite the sustained growth of plants inoculated with ACCD-
producing bacteria against abiotic stresses via, the amelioration of
stress ethylene in plant tissues, there are still some restrictions in the
appropriate use of the bacteria due to differences in their survival
rates in the soil, the incompatibility with the crops on which they are
inoculated, variation of the ACCD activities under abiotic stress, and
the ability to interact with indigenous microflora in soil and environ-
mental factors (Martinez-Viveros et al., 2010). In addition, the modes
of action of PGPB are diverse and not all bacteria possess the same
mechanisms. These disadvantages limit the application of the PGPB.
Consequently, there has been great interest in cloning AcdS genes
encoding the ACCD enzyme from bacteria and transferring them to
plants via, metabolic genetic engineering as an alternative approach to
ameliorate the deleterious effects of stress ethylene in plants. The
first successful development of an AcdS gene (from Pseudomonas sp.
6G)-expressed in transgenic plants was in tomato by Klee
et al. (1991). The overexpression of the AcdS gene significantly
reduced ethylene production (up to 90%) and promoted the shelf-life
of the transgenic tomato compared to the wild type. In 1992, Klee
and Kishore (1992) developed transgenic petunia, tobacco, and
tomato expressing the AcdS gene and investigated the ability of the
AcdS gene to delay flower longevity and/or the fruit ripening process,
which is controlled by ethylene synthesis. As expected, they observed
a significant reduction in ethylene production (up to 77%) in all plant
tissues and delayed flower senescence and/or fruit ripening in the
transgenic plants. These results were further supported by Reed
et al. (1995) using two tomato transgenic lines expressing the AcdS
gene (from Pseudomonas chlororaphis), in which the transgenic lines
showed a significant reduction in ethylene production and delayed
fruit ripening compared to the wild type. A few years later, Grichko
et al. (2000) transferred the AcdS gene (from E. cloacae UW4) to
tomato plants using different promoters, such as the 35S CaMV pro-
moter, rol-D promoter, and the PRB-1b promoter, and the transgenic
lines exhibited increased tolerance to heavy metal stress compared to
the wild type. However, the ability of the transgenic lines to produce
ACCD activity and metal uptake differed depending on the promoters
used. In addition, when the transgenic tomato lines were subjected to
flooding stress, they showed some increased tolerance to flooding
stress and were less susceptible to the deleterious effects of root hyp-
oxia on plant growth, when compared to the wild-type plants. How-
ever, of these lines, the line with the rol-D promoter showed the
greatest tolerance to stress (Grichko & Glick, 2001a, 2001b). More-
over, when the transgenic lines with the 35S CaMV promoter were
infected with Verticillium, they induced ACCD activity in the leaf
15
Physiologia Plantarum
tissues and exhibited resistance to the phyto-pathogen (Robison,
Shah, et al., 2001). Similarly, transgenic canola plants were produced
by the overexpression of the AcdS genes (from E. cloacae CAL2) and
their tolerance to arsenic stress was determined (Nie et al., 2002). In
the arsenic stress conditions, the transgenic canola plants exhibited
higher uptake of arsenic, less deleterious effects of stress-induced
ethylene, and improved plant growth, when compared with the wild-
type plants (Nie et al., 2002). As investigated for the transgenic
tomato, Stearns et al. (2005) and Sergeeva et al. (2006) also generated
transgenic canola expressing the AcdS (from P. putida UW4) by placing
it under the control of different promoters (35S CAMV, rol-D, and
PRB-1b). When the transgenic lines were tested for nickel and salt
stress tolerance, the transgenic lines with the rol-D promoter showed
higher accumulations of nickel and less deleterious effects of the
metal and salt stress, when compared to the wild-type plants
(Sergeeva et al., 2006; Stearns et al., 2005). The most promising role
of the rol-D promoter in the expression of the AcdS gene was further
reported in transgenic camelina by Heydarian et al. (2016), with a
decreased decline in root length and weight, increased seed produc-
tion, better seed quality, and higher levels of seed oil production
under salt stress, when compared to the transgenic lines with 35S
CAMV and prb-1b promoters. The prb-1b promoter exhibited lower
ACCD activity in both the transgenic tomato, camelina, and canola
plants than the 35S CaMV and rolD promoters (Grichko et al., 2005;
Heydarian et al., 2016; Robison, Shah, et al., 2001; Sergeeva
et al., 2006). This trend of lower expression of the AcdS gene with the
prb-1b promoter, irrespective of the stressed or unstressed condi-
tions, indicates that the prb-1b promoter is not suitable for the
expression of the AcdS gene. In addition, the transgenic canola plants
not only tolerated the flooding stress but also absorbed high levels of
nickel from the soil, when compared to the wild type, suggesting that
they could be used for phytoremediation to reduce metal contamina-
tion in the soil (Farwell et al., 2006, 2007). Lei et al. (1996) generated
transgenic Petunia hybrida expressing AcdS and reported a significant
reduction in the ACC content in pollen. However, they did not test
the tolerance of the transgenic lines to abiotic stress. In subsequent
studies, a greater tolerance of the transgenic petunia co-expressing
AcdS and iaaM genes to heavy metal stress was reported by Zhang
et al. (2008), and the transgenic plants showed faster growth with
larger biomass and a more extensive root system, and a greater accu-
mulation of the heavy metals than the wild-type plants. Recently, Jung
et al. (2018) and Zhang et al. (2015) also observed improved growth
and development of transgenic Arabidopsis expressing AcdS (from
P. veronii-KJ and Trichoderma asperellum) in water-logged and salt
stress conditions, compared to the wild type. However, high levels of
stress tolerance were associated with high expression levels of the
AcdS gene in the transgenic lines (Jung et al., 2018).
Despite several reports describing the AcdS genes from bacteria
that encode their ACCD activity, there have only been a few studies
that have reported the ACCD activities of AcdS genes from plants
such as poplar, tomato, and Arabidopsis (McDonnell et al., 2009; Plett
et al., 2009). Downregulation of the endogenous AcdS gene in Ara-
bidopsis distinctly decreased ACCD activity (approximately 70%)
16
Physiologia Plantarum
compared to the wild type, displaying an increased sensitivity to ethyl-
ene production (McDonnell et al., 2009). However, their significance
in ameliorating the deleterious effects of ethylene stress are not well
known. Therefore, further research is required to confirm their poten-
tial applications in plant biotechnology to reduce the deleterious
effects of stress ethylene and improve stress tolerance. Taken
together, overexpression of the bacterial AcdS in many plant species
has indicated that it results in an enhancement of ACCD activity,
which reduces the deleterious effects of stress ethylene in stress con-
ditions and improves the quality traits of the fresh horticultural crops.
Thus, transgenic technology will help to reduce the deleterious effects
of stress ethylene on plant species that are recalcitrant to do so via,
direct inoculation of ACCD-producing bacteria.
7 | CONCLUSION AND FUTURE
PERSPECTIVE
Global climate change is increasing, and its effects continue to impact
the severity of abiotic stress conditions such as flooding, salinity, heat,
and drought. Plants grown in the field are often affected by one or
more abiotic stress conditions, and plants modulate ethylene in
response and use it as a signaling molecule in stress tolerance mecha-
nisms. However, the duration and frequency of the stress can cause
the overproduction of ethylene in plant tissues and consequently
cause a reduction in plant growth and crop yield productivity. As the
human population continues to increase, there is an ongoing threat
for the future of global food security. To cope with this issue, ACCD-
producing PGPBs have been widely used in the agricultural produc-
tion of major crops (such as pulses, wheat, and rice) and other horti-
cultural crops, due to their positive effects on plant growth promotion
and crop productivity in abiotic stress conditions. It is recommended
to use a mixed application of two or more PGPB rather than using a
single PGPB because the consortium effects are able to provide better
plant growth and crop productivity under multiple stresses. Consider-
ing the positive impact of PGPBs in terms of crop productivity when
faced with abiotic stress conditions and their eco-friendliness, the
exploitation of PGPBs in the agricultural industry should be encour-
aged, to reduce the use of inorganic fertilizers and chemicals, and to
reduce cultivation costs and the disruption of ecosystems. However,
unfortunately, the compatibility of PGPBs and host plants, the ACCD
activities in the PGPBs, and the synergistic effects among the PGPBs
are crucial for plant growth and crop yields in abiotic stress conditions.
Therefore, careful screening of the appropriate PGPBs that have high
ACCD activity, have compatibility with specific host plants, as well as
synergistic effects are necessary. In fact, this screening contains multi-
ple tasks such as the isolation and characterization of several bacteria
and an investigation of their compatibility and synergy with targeted
host plants. As an alternative approach, the generation of transgenic
plants expressing the AcdS gene may be more popular in the future as
a substitute for PGPBs to continue to support and uplift agricultural
sustainability and food security globally.
NAING ET AL.
ACKNOWLEDG MENT
This work was supported by the National Research Foundation of
Korea(NRF) grant funded by the Korea government (MSIT) (No.
2021R1A2C2008951).
AUTHOR CONTRIBU TIONS
Aung Htay Naing designed the contents for this review. Aung Htay
Naing and The-Thiri Maung collected the literature. The-Thiri Maung
summarized the results and made the tables. Aung Htay Naing wrote
the manuscript. Aung Htay Naing and The-Thiri Maung revised the
manuscript. Chang Kil Kim supervised the project.
DATA AVAILABILITY STAT EMEN T
Data sharing is not applicable to this article as no new data were cre-
ated or analyzed in this study.
OR CID
Aung Htay Naing https://orcid.org/0000-0002-3048-2667
RE FE RE NCE S
Abd_Allah, E.F., Alqarawi, A.A., Hashem, A., Radhakrishnan, R.,
Al-Huqail, A.A., Al-Otibi, F.O.N. et al. (2018) Endophytic bacterium
Bacillus subtilis (BERA 71) improves salt tolerance in chickpea plants by
regulating the plant defense mechanisms. Journal of Plant Interactions,
13, 37–44.
Acuña, J.J., Campos, M., De, M., Mora, L., Jaisi, D.P. & Jorquera, M.A.
(2019) ACCD-producing rhizobacteria from an Andean Altiplano
native plant (Parastrephia quadrangularis) and their potential to allevi-
ate salt stress in wheat seedlings. Applied Soil Ecology, 136, 184–190.
Afridi, M.S., Amna, S., Mahmood, T., Salam, A., Mukhtar, T., Mahmood, S.
et al. (2019) Induction of tolerance to salinity in wheat genotypes by
plant growth promoting endophytes: involvement of ACC deaminase
and antioxidant enzymes. Plant Physiology and Biochemistry, 139,
569–577.
Ali, S., Charles, T.C. & Glick, B.R. (2012) Delay of flower senescence by
bacterial endophytes expressing 1-aminocyclopropane-1-carboxylate
deaminase. Journal of Applied Microbiology, 113, 1139–1144.
Ali, S., Charles, T.C. & Glick, B.R. (2014) Amelioration of high salinity stress
damage by plant growth-promoting bacterial endophytes that contain
ACC deaminase. Plant Physiology and Biochemistry, 80, 160–167.
Ali, S. & Glick, B.R. (2021) The biochemistry and molecular biology of the
enzyme ACC deaminase. In: Hurst, C. (Ed.) Microbes: the foundation
stone of the biosphere. Switzerland: Springer, pp. 365–390.
Alvarez, I., Tomaro, M.L. & Benavides, M.P. (2003) Changes in polyamines,
proline and ethylene in sunflower calluses treated with NaCl. Plant
Cell, Tissue and Organ Culture, 74, 51–59.
Antunes, M.D.C. & Sfakiotakis, E.M. (2000) Effect of high temperature
stress on ethylene biosynthesis, respiration and ripening of ’Hayward’
kiwifruit. Postharvest Biology and Technology, 20, 251–259.
Arbona, V., Marco, A.J., Iglesias, D.J., Lo  pez-Climent, M.F., Talon, M. &
Go mez-Cadenas, A. (2005) Carbohydrate depletion in roots and leaves
of salt-stressed potted Citrus clementina L. Plant Growth Regulation, 46,
153–160.
Arteca, R.N. & Arteca, J.M. (2007) Heavy-metal-induced ethylene produc-
tion in Arabidopsis thaliana. Journal of Plant Physiology, 164, 1480–
1488.
Bal, H.B., Nayak, L., Das, S. & Adhya, T.K. (2013) Isolation of ACC deami-
nase producing PGPR from rice rhizosphere and evaluating their plant
growth promoting activity under salt stress. Plant and Soil, 355,
1011e4.
NAING ET AL.
Balota, M., Cristescu, S., Payne, W.A., Hekkert, S.T.L., Laarhoven, L.J.J. &
Harren, F.J.M. (2004) Ethylene production of two wheat cultivars
exposed to desiccation, heat, and paraquat-induced oxidation. Crop
Science, 44, 812–818.
Bar, Y., Apelbaum, A., Kafkafi, U. & Goren, R. (1998) Ethylene association
with chloride stress in citrus plants. Scientia Horticulturae, 73, 99–109.
Barnawal, D., Bharti, N., Maji, D., Chanotiya, C.S. & Kalra, A. (2012)
1-Aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing
rhizobacteria protect Ocimum sanctum plants during waterlogging
stress via reduced ethylene generation. Plant Physiology and Biochemis-
try, 58, 227–235.
Barnawal, D., Bharti, N., Maji, D., Chanotiya, C.S. & Kalra, A. (2014) ACC
deaminase-containing Arthrobacter protophormiae induces NaCl stress
tolerance through reduced ACC oxidase activity and ethylene produc-
tion resulting in improved nodulation and mycorrhization in Pisum sat-
ivum. Journal of Plant Physiology, 171, 884–894.
Barra, P.J., Inostrozab, N.G., Acunab, J.J., Morab, M.L., Crowley, D.E. &
Jorquerab, M.A. (2016) Formulation of bacterial consortia from avo-
cado (Perseaamericana Mill.) and their effect on growth, biomass and
superoxide dismutase activity of wheat seedlings under salt stress.
Applied Soil Ecology, 102, 80–91.
Begum, N., Hu, Z., Cai, Q. & Lou, L. (2019) Influence of PGPB inoculation
on HSP70 and HMA3 gene expression in switchgrass under cadmium
stress. Plants, 8, 504.
Belimov, A.A., Safronova, V.I., Sergeyeva, T.A., Egorova, T.N.,
Matveyeva, V.A., Tsyganov, V.E. et al. (2001) Characterization of plant
growth promoting rhizobacteria isolated from polluted soils and con-
taining 1-aminocyclopropane-1-carboxylate deaminase. Canadian Jour-
nal of Microbiology, 47, 642–652.
Beltrano, J., Ronco, M.G. & Montaldi, E.R. (1999) Drought stress syndrome
in wheat is provoked by ethylene evolution imbalance and reversed by
rewatering, aminoethoxyvinylglycine, or sodium benzoate. Journal of
Plant Growth Regulation, 18, 59–64.
Botella, M.A., Del Amor, F., Amoro  s, A., Serrano, M., Martínez, V. &
Cerdá, A. (2000) Polyamine, ethylene and other physico-chemical
parameters in tomato (Lycopersicon esculentum) fruits as affected by
salinity. Physiologia Plantarum, 109, 428–434.
Bradford, K.J. & Yang, S.F. (1980) Xylem transport of
1-aminocyclopropane1-carboxylic acid, an ethylene precursor, in
waterlogged tomato plants. Plant Physiology, 65, 322–326.
Britto, D.T. & Kronzucker, H.J. (2002) NHþ 4 toxicity in higher plants: a criti-
cal review. Journal of Plant Physiology, 159, 567–584.
Chandra, D., Srivastava, R., Gupta, V.V.S.R., Franco, C.M.M. & Sharma, A.K.
(2019) Evaluation of ACC-deaminase-producing rhizobacteria to allevi-
ate water-stress impacts in wheat (Triticum aestivum L.) plants. Cana-
dian Journal of Microbiology, 65, 387–403.
Chen, H., Qualls, R.G. & Miller, G.C. (2002) Adaptive response of Ledidium
latifolium to soil flooding: biomass allocation, adventitious rooting, aer-
enchyma formation and ethylene production. Environmental and Exper-
imental Botany, 48, 119–128.
Chen, L., Liu, Y., Wu, G., Veronican, N.K., Shen, Q., Zhang, N. et al. (2016)
Induced maize salt tolerance by rhizosphere inoculation of Bacillus
amyloliquefaciens SQR9. Physiologia Plantarum, 158, 34–44.
Cheng, Z., Duncker, B.P., Mc Conkey, B.J. & Glick, B.R. (2008) Transcrip-
tional regulation of ACC deaminase gene expression in Pseudomonas
putida UW4. Canadian Journal of Microbiology, 54, 128–136.
Chinnaswamy, A., Coba de la Peña, T., Stoll, A., de la Peña Rojo, D.,
Bravo, J., Rinco  n, A. et al. (2018) A nodule endophytic Bacillus meg-
aterium strain isolated from Medicago polymorpha enhances growth,
promotes nodulation by Ensifer medicae and alleviates salt stress in
alfalfa plants. The Annals of Applied Biology, 172, 295–308.
Ciardi, J.A., Deikman, J. & Orzolek, M.D. (1997) Increased ethylene synthe-
sis enhances chilling tolerance in tomato. Physiologia Plantarum, 101,
333–340.
17
Physiologia Plantarum
Cuypers, A., Smeets, K. & Vangronsveld, J. (2009) Heavy metal stress in
plants. In: Hirt, H. (Ed.) Plant stress biology. From genomics to systems
biology. Wiley-VCH: Weinheim, pp. 161–178.
Damodaran, T., Mishra, V.K., Jha, S.K., Pankaj, U., Gupta, G. & Gopal, R.
(2019) Identification of rhizosphere bacterial diversity with promising
salt tolerance, PGP traits and their exploitation for seed germination
enhancement in sodic soil. Agricultural Research, 8, 36–43.
De la Haba, P., De la Mata, L., Molina, E. & Agüera, E. (2014) High temper-
ature promotes early senescence in primary leaves of sunflower
(Helianthus annuus L.) plants. Can. J. Plant Science, 94, 659–669.
Desbrosses, G., Contesto, C., Varoquaux, F., Galland, M. & Touraine, B.
(2009) PGPR-Arabidopsis interaction is an useful system to study sig-
naling pathways involved in plant developmental control. Plant Signal-
ing & Behavior, 4, 321–323.
Dixit, V.K., Misra, S., Mishra, S.K., Joshi, N. & Chauhan, P.S. (2020) Charac-
terization of plant growth-promoting alkalotolerant Alcaligenes and
Bacillus strains for mitigating the alkaline stress in Zea mays. Antonie
Van Leeuwenhoek, 113, 889–905.
Djanaguiraman, M. & Prasad, P.V.V. (2010) Ethylene production under
high temperature stress causes premature leaf senescence in soybean.
Functional Plant Biology, 37, 1071–1084.
Drogue, B., Doré, H., Borland, S., Wisniewski-Dyé, F. & Prigent-
Combaret, C. (2012) Which specificity in cooperation between
phytostimulating rhizobacteria and plants? Research in Microbiology,
163, 500–510.
Duan, J., Muller, K.M., Charles, T.C., Vesely, S. & Glick, B.R. (2009)
1-Aminocyclopropane-1-carboxylate (ACC) deaminase genes in
Rhizobia from southern Saskatchewan. Microbial Ecology, 57, 423–436.
Dubois, M., Claeys, H., Van den Broeck, L. & Inzé, D. (2017) Time of day
determines Arabidopsis transcriptome and growth dynamics under
mild drought. Plant, Cell & Environment, 40, 180–189.
English, P.J., Lycett, G.W., Roberts, J.A. & Jackson, M.B. (1995) Increased
1-aminocyclopropane-1-carboxylic acid oxidase activity in shoots of
flooded tomato plants raises ethylene production to physiologically
active levels. Plant Physiology, 109, 1435–1440.
Etesami, H., Hosseini, H.M. & Alikhani, H.A. (2014) Bacterial biosynthesis
of 1-aminocyclopropane-1-caboxylate (ACC) deaminase, a useful trait
to elongation and endophytic colonization of the roots of rice under
constant flooded conditions. Physiology and Molecular Biology of Plants,
20, 425–434.
Farwell, A.J., Vesely, S., Nero, V., Rodriguez, H., McCormack, K., Shah, S.
et al. (2007) Tolerance of transgenic canola plants (Brassica napus)
amended with plant growth-promoting bacteria to flooding stress at
a metal contaminated field site. Environmental Pollution, 147,
540–545.
Farwell, A.J., Vesely, S., Nero, V., Rodriguez, H., Shah, S., Dixon, D.G. et al.
(2006) The use of transgenic canola (Brassica napus) and plant growth-
promoting bacteria to enhance plant biomass at a nickel-contaminated
field site. Plant and Soil, 288, 309–318.
Glick, B.R. (2005) Modulation of plant ethylene levels by the bacterial
enzyme ACC deaminase. FEMS Microbiology Letters, 251, 1–7.
Glick, B.R. (2014) Bacteria with ACC deaminase can promote plant growth
and help to feed the world. Microbiological Research, 169, 30–39.
Glick, B.R., Penrose, D.M. & Li, J. (1998) A model for the lowering of plant
ethylene concentrations by plant growth promoting bacteria. Journal
of Theoretical Biology, 190, 63–68.
Glick, B.R., Todorovic, B., Czarny, J., Cheng, Z., Duan, J. & McConkey, B.
(2007) Promotion of plant growth by bacterial ACC deaminase. Critical
Reviews in Plant Sciences, 26, 227–242.
Goswami, D., Janki, N. & Pinakin, C. (2016) Portraying mechanics of plant
growth promoting rhizobacteria (PGPR): a review. Cogent Food & Agri-
culture, 2, 1127500.
Graves, W.R. & Gladon, R.J. (1985) Water stress, endogenous ethylene
and Ficus benjamina leaf abscission. HortScience, 20, 273–275.
18
Physiologia Plantarum
Grichko, V.P., Filby, B. & Glick, B.R. (2000) Increased ability of transgenic
plants expressing the bacterial enzyme ACC deaminase to accumulate
Cd, Co, Cu, Ni, Pb, and Zn. Journal of Biotechnology, 81, 45–53.
Grichko, V.P. & Glick, B.R. (2001a) Flooding tolerance of transgenic tomato
plants expressing the bacterial enzyme ACC deaminase controlled by
the 35S, rolD or PRB-1b promoter. Plant Physiology and Biochemistry,
39, 19–25.
Grichko, V.P. & Glick, B.R. (2001b) Amelioration of flooding stress by ACC
deaminase-containing plant growth-promoting bacteria. Plant Physiol-
ogy and Biochemistry, 39, 11–17.
Grichko, V.P., Glick, B.R., Grishko, V.I. & Pauls, K.P. (2005) Evaluation of
tomato plants with constitutive, root-specific, and stress-induced ACC
deaminase gene expression. Russian Journal of Plant Physiology, 52,
359–364.
Gupta, S. & Pandey, S. (2019) ACC deaminase producing bacteria with
multifarious plant growth promoting traits alleviates salinity stress in
French bean (Phaseolus vulgaris) plants. Frontiers in Microbiology, 10,
1506.
Gupta, S. & Pandey, S. (2020) Enhanced salinity tolerance in the common
bean (Phaseolus vulgaris) plants using twin ACC deaminase producing
rhizobacterial inoculation. Rhizosphere, 16, 100241.
Habben, J.E., Bao, X.M., Bate, N.J., De Bruin, J.L., Dolan, D., Hasegawa, D.
et al. (2014) Transgenic alteration of ethylene biosynthesis increases
grain yield in maize under field drought-stress conditions. Plant Bio-
technology Journal, 12, 685–693.
Han, Y., Wang, R., Yang, Z., Zhan, Y., Ma, Y., Ping, S. et al. (2015)
1-aminocyclopropane-1-carboxylate deaminase from Pseudomonas
stutzeri A1501 facilitates the growth of rice in the presence of salt or
heavy metals. Journal of Microbiology and Biotechnology, 25, 1119–
1128.
Hashem, A., Abd_sAllah, E.F., Alqarawi, A.A., Al-Huqail, A.A. & Shah, M.A.
(2016) Induction of osmoregulation and modulation of salt stress in
Acacia gerrardii Benth. By arbuscular mycorrhizal fungi and Bacillus
subtilis (BERA 71). BioMed Research International, 2016, 6294098.
Hays, D.B., Do, J.H., Mason, R.E., Morgan, G. & Finlayson, S.A. (2007) Heat
stress induced ethylene production in developing wheat grains induces
kernel abortion and increased maturation in a susceptible cultivar.
Plant Science, 172, 1113–1123.
Hemida, K.A. & Reyad, A.M.M. (2018) Improvement salt tolerance of saf-
flower plants by endophytic bacteria. Journal of Horticulture and Plant
Research, 5, 38–56.
Heydarian, Z., Yu, M., Gruber, M., Glick, B.R., Zhou, R. & Hegedus, D.D.
(2016) Inoculation of soil with plant growth promoting bacteria pro-
ducing 1-Aminocyclopropane-1-Carboxylate Deaminase or expression
of the corresponding acdS gene in transgenic plants increases salinity
tolerance in Camelina sativa. Frontiers in Microbiology, 7, 1966.
Honma, M. & Shimomura, T. (1978) Metabolism of 1-aminocyclopropane-
1-carboxylic acid. Agricultural and Biological Chemistry, 43, 1825–1831.
Hontzeas N., Zoidakis J., Glick B.R., & Abu-Omar M.M. (2004) Expression
and characterization of 1-aminocyclopropane-1-carboxylate deami-
nase from the rhizobacterium Pseudomonas putida UW4: a key
enzyme in bacterial plant growth promotion. Biochimica et Biophysica
Acta (BBA) - Proteins and Proteomics, 1703(1), 11–19. https://doi.org/
10.1016/j.bbapap.2004.09.015
Huberman, M., Riov, J., Goldschmidt, E.E., Apelbaum, A. & Goren, R.
(2014) The novel ethylene antagonist, 3-cyclopropyl-1-enyl-propanoic
acid sodium salt (CPAS), increases grain yield in wheat by delaying leaf
senescence. Plant Growth Regulation, 73, 249–255.
Iqbal, N., Trivellini, A., Masood, A., Ferrante, A. & Khan, N.A. (2013)
Current understanding on ethylene signaling in plants: the influ-
ence of nutrient availability. Plant Physiology and Biochemistry, 73,
128–138.
Jacobson, C.B., Pasternak, J.J. & Glick, B.R. (1994) Partial purification and
characterization of 1-aminocyclopropane-1-carboxylate deaminase
NAING ET AL.
from the plant growth promoting rhizobacterium Pseudomonas putida
GR12-2. Canadian Journal of Microbiology, 40, 1019–1025.
Jaemsaeng, R., Jantasuriyarat, C. & Thamchaipenet, A. (2018) Molecular
interaction of 1-aminocyclopropane-1-carboxylate deaminase
(ACCD)-producing endophytic Streptomyces sp. GMKU 336 towards
salt-stress resistance of Oryza sativa L. cv. KDML105. Scientific
Reports, 8, 1–50.
Jung, H., Ali, S., Kim, J.Y. & Kim, W.C. (2018) Transgenic Arabidopsis
expressing acdS gene of Pseudomonas veronii-KJ alleviate the adverse
effects of salt and water-logging stress. Plant Breeding and Biotechnol-
ogy, 6, 221–232.
Kang, S.M., Shahzad, R., Bilal, S., Khan, A.L., Park, Y.G., Lee, K.E. et al.
(2019) Indole-3-acetic-acid and ACC deaminase producing Leclercia
adecarboxylata MO1 improves Solanum lycopersicum L. growth and
salinity stress tolerance by endogenous secondary metabolites regula-
tion. BMC Microbiology, 19, 1–14.
Karthikeyan, B., Joe, M.M., Islam, M.R. & Sa, T. (2012) ACC deaminase
containing diazotrophic endophytic bacteria ameliorate salt stress in
Catharanthus roseus through reduced ethylene levels and induction of
antioxidative defense systems. Symbiosis, 56, 77–86.
Kawakami, E.M., Oosterhuis, D.M. & Snider, J. (2013) High temperature
and the ethylene antagonist 1-methylcyclopropene alter ethylene evo-
lution patterns, antioxidant responses, and boll growth in Gossypium
hirsutum. American Journal of Plant Sciences, 4, 1400–1408.
Kawakami, E.M., Oosterhuis, D.M. & Snider, J.L. (2010) Physiological
effects of 1-methylcyclopropene on well-watered and water-stressed
cotton plants. Journal of Plant Growth Regulation, 29, 280–288.
Keunen, E., Schellingen, K., Vangronsveld, J. & Cuypers, A. (2016) Ethylene
and metal stress: small molecule, big impact. Frontiers in Plant Science,
7, 23.
Khalid, A., Arshad, M. & Zahir, Z.A. (2004) Screening plant growth promot-
ing rhizobacteria for improving growth and yield of wheat. Journal of
Applied Microbiology, 96, 473–480.
Khan, M.A., Asaf, S., Khan, A.L., Jan, R., Kang, S.-M., Kim, K.-M. et al.
(2020a) Extending thermotolerance to tomato seedlings by inoculation
with SA1 isolate of Bacillus cereus and comparison with exogenous
humic acid application. PLoS One, 5, e0232228.
Khan, M.A., Asaf, S., Khan, A.L., Jan, R., Kang, S.-M., Kim, K.-M. et al.
(2020b) Thermotolerance effect of plant growth-promoting Bacillus
cereus SA1 on soybean during heat stress. BMC Microbiology, 20, 175.
Khan, M.Y., Zahir, Z.A., Asghar, H.N. & Waraich, E.A. (2017) Preliminary
investigations on selection of synergistic halo tolerant plant growth
promoting rhizobacteria for inducing salinity tolerance in wheat.
Pakistan Journal of Botany, 49, 1541–1551.
Klee, H.J., Hayford, M.B., Kretzmer, K.A., Barry, G.F. & Kishore, G.M.
(1991) Control of ethylene synthesis by expression of a bacterial
enzyme in transgenic tomato plants. Plant Cell, 3, 1187–1193.
Klee, H.J. & Kishore, G.M. (1992) Control of fruit ripening and senescence
in plants, U.S. patent no. 5702933.
Lei, C.H., Lindstrom, J.T. & Woodson, W.R. (1996) Reduction of
1-aminocyclopropane-1-carboxylic acid (ACC) in pollen by expression
of ACC deaminase in transgenic Petunias. Plant Physiology, 111, 149.
Li, J. & Glick, B.R. (2001) Transcriptional regulation of the Enterobacter
cloaceae UW4 1-aminocyclopropane-1-carboxylate (ACC) deaminase
gene (AcdS). Canadian Journal of Microbiology, 47, 259–267.
Li, Y., Gupta, G., Joshi, J.M. & Slyumbano, A.K. (1995) Effect of methanol
on soybean photosynthesis and chlorophyll. Journal of Plant Nutrition,
18, 1875–1880.
Liu, J., Tang, L., Gao, H., Zhang, M. & Guo, C. (2019) Enhancement of
alfalfa yield and quality by plant growth-promoting rhizobacteria under
saline-alkali conditions. Journal of the Science of Food and Agriculture,
99, 281–289.
Lynch, J. & Brown, K.M. (1997) Ethylene and plant responses to nutritional
stress. Physiologia Plantarum, 100, 613–619.
NAING ET AL.
Mantri, N., Patade, V., Penna, S., Ford, R. & Pang, E. (2012) Abiotic stress
responses in plants: present and future. In: Ahmad, P. & Prasad, M.
(Eds.) Abiotic stress responses in plants. New York, NY: Springer.
https://doi.org/10.1007/978-1-4614-0634-1_1
Martinez-Viveros, O., Jorquera, M.A., Crowley, D.E., Gajardo, G. &
Mora, M.L. (2010) Mechanisms and practical considerations involved
in plant growth promotion by rhizobacteria. Journal of Soil Science and
Plant Nutrition, 10, 293–319.
Masood, A., Iqbal, N. & Khan, N.A. (2012) Role of ethylene in alleviation of
cadmium-induced photosynthetic capacity inhibition by sulphur in
mustard. Plant, Cell & Environment, 35, 524–533.
Maxton, A., Singh, P. & Masih, S.A. (2018) ACC deaminase-producing bac-
teria mediated drought and salt tolerance in Capsicum annuum. Journal
of Plant Nutrition, 41, 574–583.
Mayak, S., Tirosh, T. & Glick, B.R. (2004a) Plant growth-promoting bacteria
that confer resistance to water stress in tomato and pepper. Plant Sci-
ence, 166, 525–530.
Mayak, S., Tirosh, T. & Glick, B.R. (2004b) Plant growth-promoting bacteria
that confer resistance in tomato to salt stress. Plant Physiology and Bio-
chemistry, 42, 565–572.
McDonnell, L., Plett, J.M., Andersson-Gunnerås, S., Kozela, C.,
Dugardeyn, J., Van Der Straeten, D. et al. (2009) Ethylene levels are
regulated by a plant encoded 1-aminocyclopropane-1-carboxylic acid
deaminase. Physiologia Plantarum, 136, 94–109.
Mersmann, S., Bourdais, G., Rietz, S. & Robatzek, S. (2010) Ethylene signal-
ing regulates accumulation of the FLS2 receptor and is required for
the oxidative burst contributing to plant immunity. Plant Physiology,
154, 391–400.
Mesa-Marín, J., Perez-Romero, J.-A., Naranjo, E., Bernabeu-Meana,
Pajuelo, E., Rodriguez-Llorente, I. & Redondo-G'omez, S. (2019) Effect
of plant growth-promoting rhizobacteria on Salicornia ramosissima
seed germination under salinity, CO2 and temperature stress. Agron-
omy, 9, 655.
Misra, S., Dixit, V.K., Khan, M.H., Mishra, S.K., Dviwedi, G., Yadav, S. et al.
(2017) Exploitation of agro-climatic environment for selection of
1-aminocyclopropane-1-carboxylic acid (ACC) deaminase producing
salt tolerant indigenous plant growth promoting rhizobacteria. Microbi-
ological Research, 205, 25–34.
Mitcham, E.J. & McDonald, R.E. (1993) Effects of quarantine heat treat-
ment on mango fruit physiology. Acta Horticulturae, 343, 361–366.
Mitra, S., Pramanik, K., Sarkar, A., Ghosh, P.K., Soren, T. & Maiti, T.K.
(2018) Bioaccumulation of cadmium by Enterobacter sp. and enhance-
ment of rice seedling growth under cadmium stress. Ecotoxicology and
Environmental Safety, 156, 183–196.
Mizrahi, Y. (1982) Effect of salinity on tomato fruit ripening. Plant Physiol-
ogy, 69, 966–970.
Montero-Palmero, M.B., Martín-Barranco, A., Escobar, C. & Hernández, L.
E. (2014) Early transcriptional responses to mercury: a role for ethyl-
ene in mercuryinduced stress. The New Phytologist, 201, 116–130.
Morgan, P.W., He, C.J., De Greef, J.A. & De Proft, M.P. (1990) Does water
deficit stress promote ethylene synthesis by intact plants? Plant Physi-
ology, 94, 1616–1624.
Mukhtar, T., Smith, D., Sultan, T., Seleiman, M.F., Alsadon, A.A., Ali, S. et al.
(2020) Mitigation of heat stress in Solanum lycopersicum L. by ACC-
deaminase and exopolysaccharide producing Bacillus cereus: effects on
biochemical profiling. Sustainability, 12, 2159.
Nadeem, S., Zahir, Z., Naveed, M. & Nawaz, S. (2013) Mitigation of
salinity-induced negative impact on the growth and yield of wheat by
plant growth-promoting rhizobacteria in naturally saline conditions.
Annals of Microbiology, 63, 225–232.
Nadeem, S.M., Zahir, A.Z., Naveed, M. & Ashraf, M. (2010) Microbial ACC-
deaminase: prospects and applications for inducing salt tolerance in
plants. Critical Reviews in Plant Sciences, 29, 360–393.
Nascimento, F.X., Rossi, M.J., Soares, C.R.F.S., McConkey, B.J. & Glick, B.R.
(2014) New insights in to 1-aminocyclopropane-1-carboxylate (ACC)
19
Physiologia Plantarum
deaminase phylogeny, evolution and ecological significance. PLoS One,
9, e99168.
Naz, I., Bano, A. & Hassan T.U. (2009) Morphological, biochemical and
molecular characterization of rhizobia from halophytes of Khewra Salt
Range and Attock. Pakistan Journal of Botany, 41, 3159–3168.
Nazar, R., Khan, M.I.R., Iqbal, N., Masood, A. & Khan, N.A. (2014) Involve-
ment of ethylene in reversal of salt-inhibited photosynthesis by sulfur
in mustard. Physiologia Plantarum, 152, 331–344.
Nie, L., Shah, S., Rashid, A., Burd, G.I., Dixon, D.G. & Glick, B.R. (2002)
Phytoremediation of arsenate contaminated soil by transgenic canola
and the plant growth-promoting bacterium Entero-bacter cloacae
CAL2. Plant Physiology and Biochemistry, 40, 355–361.
Nukui, N., Minamisawa, K., Ayabe, S.I. & Aoki, T. (2006) Expression of the
1-aminocyclopropane-1-carboxylic acid deaminase gene requires sym-
biotic nitrogen-fixing regulator gene nifA2 in Mesorhizobium loti
MAFF303099. Applied and Environmental Microbiology, 72, 4964–
4969.
Orozco-Mosqueda, M., Duan, J., DiBernardo, M., Zetter, E., Campos-
Garcia, J., Glick, B.R. et al. (2019) The production of ACC deaminase
and trehalose by the plant growth promoting bacterium Pseudomonas
sp. UW4 synergistically protect tomato plants against salt stress. Fron-
tiers in Microbiology, 10, 1392.
Patel, R.R., Patel, D.D., Thakor, P., Patel, B. & Thakkar, V.R. (2015) Allevia-
tion of salt stress in germination of Vigna radiata L. by two halotolerant
Bacilli sp. isolated from saline habitats of Gujarat. Plant Growth Regula-
tion, 76, 51–60.
Penrose, D.M. & Glick, B.R. (2003) Methods for isolating and characteriz-
ing ACC deaminase-containing plant growth-promoting rhizobacteria.
Physiologia Plantarum, 118, 10–15.
Pierik, R., Tholen, D., Poorter, H., Visser, E.J. & Voesenek, L.A.C.J. (2006)
The Janus face of ethylene: growth inhibition and stimulation. Trends
in Plant Science, 11, 176–183.
Plett, J.M., McDonnell, L. & Regan, S. (2009) Plant encoded
1-aminocyclopropane-1-carboxylic acid deaminase activity implicated
in different aspects of plant development. Plant Signaling & Behavior, 4,
1186–1189.
Pramanik, K., Mitra, S., Sarkar, A. & Maiti, T.K. (2018) Alleviation of phyto-
toxic effects of cadmium on rice seedlings by cadmium resistant PGPR
strain Enterobacter aerogenes MCC 3092. J. Hazardous Materials, 351,
317–329.
Pramanik, K., Soumik, M., Anumita, S., Tithi, S. & Tushar, K.M. (2018) Char-
acterization of a Cd2+-resistant plant growth promoting
rhizobacterium (Enterobacter sp.) and its effects on rice seedling
growth promotion under Cd2+-stress in vitro. Agriculture and Natural
Resources, 52, 215–221.
Ravanbakhsh, M., Sasidharan, R., Voesenek, L.A., Kowalchuk, G.A. &
Jousset, A. (2017) ACC deaminase-producing rhizosphere bacteria
modulate plant responses to flooding. Journal of Ecology, 105,
979–986.
Reed, A.J., Magin, K.M., Anderson, J.S., Austin, G.D., Rangwala, T.,
Linde, D.C. et al. (1995) Delayed ripening tomato plants expressing the
enzyme 1-aminocyclopropane-1-carboxylic acid deaminase. 1. Molecu-
lar characterization, enzyme expression, and fruit ripening traits. Jour-
nal of Agricultural and Food Chemistry, 43, 1954–1962.
Robison, M.M., Griffith, M., Pauls, K.P. & Glick, B.R. (2001) Dural role of
ethylene in susceptibility of tomato to Verticillium wilt. Journal of Phy-
topathology, 149, 385–388.
Robison, M.M., Shah, S., Tamot, B., Pauls, K.P., Moffatt, B.A. & Glick, B.R.
(2001) Reduced symptoms of Verticillium wilt in transgenic tomato
expressing a bacterial ACC deaminase. Molecular Plant Pathology, 2,
135–145.
Safronova, V.I., Piluzza, G., Zinovkina, N.Y., Kimeklis, A.K., Belimov, A.A. &
Bullitta, S. (2012) Relationships between pasture legumes,
rhizobacteria and nodule bacteria in heavy metal polluted mine waste
of SW Sardinia. Symbiosis, 58, 149–159.
20
Physiologia Plantarum
Saghafi, D., Ghorbanpour, M., Shirafkan Ajirloo, H. & Asgari Lajayer, B.
(2019) Enhancement of growth and salt tolerance in Brassica napus
L. seedlings by halotolerant Rhizobium strains containing ACC deami-
nase activity. Plant Physiology Reports, 24, 225–235.
Saikia, J., Sarma, R.K., Dhandia, R., Yadav, A., Bharali, R., Gupta, V.K. et al.
(2018) Alleviation of drought stress in pulse crops with ACC deami-
nase producing rhizobacteria isolated from acidic soil of Northeast
India. Scientific Reports, 8, 3560.
Saleem, A.R., Brunetti, C., Khalid, A., Della Rocca, G., Raio, A., Emiliani, G.
et al. (2018) Drought response of Mucuna pruriens (L.) DC. Inoculated
with ACC deaminase and IAA producing rhizobacteria. PLoS One, 13,
e0191218.
Samaddar, S., Chatterjee, P., Choudhury, A.R., Ahmed, S. & Sa, T. (2019)
Interactions between Pseudomonas spp. and their role in improving
the red pepper plant growth under salinity stress. Microbiological
Research, 219, 66–73.
Santoyo, G., Guzman-Guzman, P., Parra-Cota, F.I., de los Santos-
Villalobos, S., Orozco-Mosqueda, M.C. & Glick, B.R. (2021) Plant
growth stimulation by microbial consortia. Agron., 11, 219.
Sarkar, A., Ghosh, P.K., Pramanik, K., Mitra, S., Soren, T., Pandey, S. et al.
(2018) A halotolerant Enterobacter sp. displaying ACC deaminase
activity promotes rice seedling growth under salt stress. Research in
Microbiology, 169, 20–32.
Sarkar, A., Pramanik, K., Mitra, S., Soren, T. & Maiti, T.K. (2018) Enhance-
ment of growth and salt tolerance of rice seedlings by ACC
deaminase-producing Burkholderia sp. MTCC 12259. Journal of Plant
Physiology, 231, 434–442.
Savada, R.P., Ozga, J.A., Jayasinghege, C.P., Waduthanthri, K.D. &
Reinecke, D.M. (2017) Heat stress differentially modifies ethylene bio-
synthesis and signaling in pea floral and fruit tissues. Plant Molecular
Biology, 95, 313–331.
Schellingen, K., Van Der Straeten, D., Remans, T., Loix, C.,
Vangronsveld, J. & Cuypers, A. (2015) Ethylene biosynthesis is
involved in the early oxidative challenge induced by moderate Cd
exposure in Arabidopsis thaliana. Environmental and Experimental Bot-
any, 117, 1–11.
Sergeeva, E., Shah, S. & Glick, B.R. (2006) Growth of transgenic canola
(Brassica napus cv. Westar) expressing a bacterial
1-aminocyclopropane- 1-carboxylate (ACC) deaminase gene on high
concentrations of salt. World J. Microbial Biotechnology, 22, 277–282.
Sgroy, V., Cassan, F., Masciarelli, O., Del-Papa, M.F., Lagares, A. & Luna, V.
(2009) Isolation and characterization of endophytic plant growth-
promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria
associated to the halophyte Prosopis strombulifera. Applied Microbiology
and Biotechnology, 85, 371–381.
Shahbaz, M. & Ashraf, M. (2013) Improving salinity tolerance in cereals.
Critical Reviews in Plant Sciences, 32, 237–249.
Sharp, R.E. (2002) Interaction with ethylene: changing views on the role of
abscisic acid in root and shoot growth responses to water stress. Plant,
Cell & Environment, 25, 211–222.
Shi, J., Habben, J.E., Archibald, R.L., Drummond, B.J., Chamberlin, M.A.,
Williams, R.W. et al. (2015) Overexpression of ARGOS genes modifies
plant sensitivity to ethylene, leading to improved drought tolerance in
both Arabidopsis and maize. Plant Physiology, 169, 266–282.
Shi, Y.T., Tian, S.W., Hou, L.Y., Huang, X.Z., Zhang, X.Y., Guo, H.W. et al.
(2012) Ethylene signaling negatively regulates freezing tolerance by
repressing expression of CBF and type-A ARR genes in Arabidopsis.
Plant Cell, 24, 2578–2595.
Shiono, K., Takahashi, H., Colmer, T.D. & Nakazono, M. (2008) Role of eth-
ylene in acclimations to promote oxygen transport in roots of plants in
waterlogged soils. Plant Science, 175, 52–58.
Singh, R.P., Jha, P. & Jha, P.N. (2015) The plant-growth-promoting bacte-
rium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat
(Triticum aestivum) under salt stress. Journal of Plant Physiology, 184,
57–67.
NAING ET AL.
Singh, R.P. & Jha, P.N. (2016) A halotolerant bacterium Bacillus
licheniformis HSW-16 augments induced systemic tolerance to salt
stress in wheat plant (Triticum aestivum). Frontiers in Plant Science, 7,
1890.
Singh, R.P., Shelke, G.M., Kumar, A. & Jha, P.N. (2015) Biochemistry and
genetics of ACC deaminase: a weapon to “stress ethylene” produced
in plants. Frontiers in Microbiology, 6, 937.
Skirycz, A., Claeys, H., De Bodt, S., Oikawa, A., Shinoda, S.,
Andriankaja, M. et al. (2011) Pause-and-stop: the effects of osmotic
stress on cell proliferation during early leaf development in Ara-
bidopsis and a role for ethylene signaling in cell cycle arrest. The
Plant Cell, 23, 1876–1888.
Spaepen, S., Vanderleyden, J. & Remans, R. (2007) Indole-3-acetic acid in
microbial and microorganism-plant signaling. FEMS Microbiology
Reviews, 31, 425–448.
Stearns, J.C., Saleh, S., Greenberg, B.M., Dixon, D.G. & Glick, B.R. (2005)
Tolerance of transgenic canola expressing 1-aminocyclopropane-
1-carboxylic acid deaminase to growth inhibition by nickel. Plant Physi-
ology and Biochemistry, 43, 701–708.
Tahir, M., Ahmad, I., Shahid, M., Shah, G.M., Farooq, A.B.U., Akram, M.
et al. (2019) Regulation of antioxidant production, ion uptake and pro-
ductivity in potato (Solanum tuberosum L.) plant inoculated with
growth promoting salt tolerant Bacillus strains. Ecotoxicology and Envi-
ronmental Safety, 178, 33–42.
Tak, H.I., Ahmad, F. & Babalola, O.O. (2013) Advances in the application of
plant growth-promoting rhizobacteria in phytoremediation of heavy
metals. Reviews of Environmental Contamination and Toxicology, 223,
33–52.
Thao, N.P., Khan, M.I.R., Thu, N.B.A., Hoang, X.L.T., Asgher, M., Khan, N.A.
et al. (2015) Role of ethylene and its cross talk with other signaling
molecules in plant responses to heavy metal stress. Plant Physiology,
169, 73–84.
Timmusk, S., Paalme, V., Pavlicek, T., Bergquist, J., Vangala, A., Danilas, T.
et al. (2011) Bacterial distribution in the rhizosphere of wild barley
under contrasting microclimates. PLoS One, 6, e17968.
Tiwari, G., Duraivadivel, P., Sharma, S. & Hariprasad, P. (2018)
1-Aminocyclopropane-1-carboxylic acid deaminase producing benefi-
cial rhizobacteria ameliorate the biomass characters of Panicum maxi-
mum Jacq. By mitigating drought and salt stress. Scientific Reports, 8,
17513.
Tiwari, S., Lata, C., Chauhan, P.S. & Nautiyal, C.S. (2016) Pseudomonas
putida attunes morphophysiological, biochemical and molecular
responses in Cicer arietinum L. during drought stress and recovery.
Plant Physiology and Biochemistry, 99, 108–117.
Torbaghan, M.E., Lakzian, A., Astaraei, A.R., Fotovat, A. & Besharati, H.
(2017) Salt and alkali stresses reduction in wheat by plant growth pro-
moting haloalkaliphilic bacteria. Journal of Soil Science and Plant Nutri-
tion, 17, 1058–1087.
Trabelsi, D., Mengoni, A., Aouani, M.E., Mhamdi, R. & Bazzicalupo, M.
(2009) Genetic diversity and salt tolerance of bacterial communities
from two Tunisian soils. Annales de Microbiologie, 59, 25–32.
Tsakelova, E.A., Klimova, S.Y., Cherdyntseva, T.A. & Netrusov, A.I. (2006)
Microbial producers of plant growth stimulators and their practical
use: a review. Applied Biochemistry and Microbiology, 42, 117–126.
Vanderstraeten, L. & Van Der Straeten, D. (2017) Accumulation and trans-
port of 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: cur-
rent status, considerations for future research and agronomic
applications. Frontiers in Plant Science, 8, 38.
VanLoon, L.C., Geraats, B.P.J. & Linthorst, H.J.M. (2006) Ethylene as a
modulator of disease resistance in plants. Trends in Plant Science, 11,
184–191.
Walsh, C., Pascal, R.A., Johnston, M., Raines, R., Dikshit, D., Krantz, A. et al.
(1981) Mechanistic studies on the pyridoxal phosphate enzyme
1-aminocyclopropane-1-carboxylate deaminase from Pseudomonas sp.
Biochemistry, 20, 7509–7519.
NAING ET AL.
Wang, Q., Dodd, I.C., Belimov, A.A. & Jiang, F. (2016) Rhizosphere bacteria
containing 1-aminocyclopropane-1-carboxylate deaminase increase
growth and photosynthesis of pea plants under salt stress by limiting
Na+ accumulation. Functional Plant Biology, 43, 161–172.
Win, K.T., Fukuyo, T., Keiki, O. & Ohwaki, Y. (2018) The ACC deaminase
expressing endophyte Pseudomonas spp. enhances NaCl stress toler-
ance by reducing stress-related ethylene production, resulting in
improved growth, photosynthetic performance, and ionic balance in
tomato plants. Plant Physiology and Biochemistry, 127, 599–607.
Yang, S.F. & Hoffman, N.E. (1984) Ethylene biosynthesis and its regulation
in higher-plants. Annual Review of Plant Physiology, 35, 155–189.
Young, T.E., Meeley, R.B. & Gallie, D.R. (2004) ACC synthase expression
regulates leaf performance and drought tolerance in maize. The Plant
Journal, 40, 813–825.
Zahir, Z.A., Arshad, M. & Frankenberger, W.T., Jr. (2004) Plant growth pro-
moting rhizobacteria: applications and perspectives in agriculture.
Advances in Agronomy, 81, 97–168.
Zhang, F., Zhang, J., Chen, L., Shi, X., Lui, Z. & Li, C. (2015) Heterologous
expression of ACC deaminase from Trichoderma asperellum improves
the growth performance of Arabidopsis thaliana under normal and salt
stress conditions. Plant Physiology and Biochemistry, 94, 41–47.
Zhang, M., Smith, J.A.C., Harberd, N.P. & Jiang, C. (2016) The regulatory
roles of ethylene and reactive oxygen species (ROS) in plant salt stress
responses. Plant Molecular Biology, 91, 651–659.
Zhang, M., Yang, L., Hao, R., Bai, X., Wang, Y. & Yu, X. (2020) Drought-
tolerant plant growth-promoting rhizobacteria isolated from jujube
(Ziziphus jujuba) and their potential to enhance drought tolerance. Plant
and Soil, 452, 423–440.
21
Physiologia Plantarum
Zhang, Y., Zhao, L., Wang, Y., Yang, B. & Chen, S. (2008) Enhancement
of heavy metal accumulation by tissue specific coexpression of
iaaM and ACC deaminase genes in plants. Chemosphere, 72,
564–571.
Zhang, Z. & Huang, R. (2010) Enhanced tolerance to freezing in tobacco
and tomato overexpressing transcription factor TERF2/LeERF2 is
modulated by ethylene biosynthesis. Plant Molecular Biology, 73,
241–249.
Zhao, M., Liu, W., Xia, X., Wang, T. & Zhang, W.H. (2014) Cold
acclimation-induced freezing tolerance of Medicago truncatula seed-
lings is negatively regulated by ethylene. Physiologia Plantarum, 152,
115–129.
Zhao, Z., Chen, H., Li, K., Du, W., He, S. & Liu, H.W. (2003) Reaction
of 1-amino-2-methylenecyclopropane-1-carboxylate with 1-
aminocyclopropane-1-carboxylate deaminase: analysis and mecha-
nistic implications. Biochemistry, 42, 2089–2103.
How to cite this article: Naing, A.H., Maung, T.-T., Kim, C.K.
(2021) The ACC deaminase-producing plant
growth-promoting bacteria: Influences of bacterial strains and
ACC deaminase activities in plant tolerance to abiotic stress.
Physiologia Plantarum, 1–21. Available from: https://doi.org/
10.1111/ppl.13545