Ecotoxicology and Environmental Safety 158 (2018) 131–138

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Ecotoxicology and Environmental Safety

journal homepage: www.elsevier.com/locate/ecoenv

Review

Bioherbicides: Current knowledge on weed control mechanism T

a,⁎ b b,⁎
Ramalingam Radhakrishnan , Abdulaziz A. Alqarawi , Elsayed Fathi Abd_Allah
a
Department of Biotechnology, Yeungnam University, Gyeongsan 38541, Republic of Korea
b
Plant Production Department, College of Food and Agricultural Sciences, King Saud University, P.O. Box. 2460, Riyadh 11451, Saudi Arabia

A R T I C LE I N FO A B S T R A C T

Keywords: Weed control is a challenging event during crop cultivation. Integrated management, including the application
Plant extracts of bioherbicides, is an emerging method for weed control in sustainable agriculture. Plant extracts, allelo-
Bacteria chemicals and some microbes are utilized as bioherbicides to control weed populations. Bioherbicides based on
Fungi plants and microbes inhibit the germination and growth of weeds; however,few studies conducted in weed
Weed control
physiology. This review ascribes the current knowledge of the physiological changes in weeds that occur during
Metabolites
the exposure to bioherbicides. Plant extracts or metabolites are absorbed by weed seeds, which initiates damage
to the cell membrane, DNA, mitosis, amylase activity and other biochemical processes and delays or inhibits seed
germination. The growth of weeds is also retarded due to low rates of root-cell division, nutrient uptake, pho-
tosynthetic pigment synthesis, and plant growth hormone synthesis, while the productions of reactive oxygen
species (ROS) and stress-mediated hormones increase, including irregular antioxidant activity. However, lytic
enzymes and toxic substances secreted from microbes degrade the weed seed coat and utilize the endosperm for
survival, which inhibits seed germination. The microbes grow through the intercellular spaces to reach the root
core, and the deposition of toxins in the cells affects cell division and cellular functions. Some of the metabolites
of deleterious microbes cause disease, necrosis and chlorosis,which inhibit the germination and growth of weed
seeds by suppressing photosynthesis and gibberellin activities and enhancing ROS, abscisic acid and ethylene.
This review explains the effects of bioherbicides (derived from plants and microbes) on weed-plant physiology to
elucidate their modes of action.

1. Introduction
Weed (a plant considered undesirable in a particular situation) po-
pulations in agricultural fields are a major cause of crop yield reduc-
tion. The individual controlling measures cannot provide the expected
outcome of weed control so the integrated weed management by crop
rotation, tillage before sowing and mechanical weeding can reduce
weed populations (Marshall et al., 2003; Chikowo et al., 2009;
Koocheki et al., 2009). In addition, several chemical herbicides are
applied to control weed growth. For example, glyphosate, dicamba and
2,4-dichlorophenoxyacetic acid (2,4-D) have been sprayed to control
weed germination and growth, but the long-term use of chemical her-
bicides does not effectively control weeds due to the development of
resistant weed germplasms (Green and Owen, 2011). Moreover, che-
mical herbicides also contaminate the water and land, which leads to
numerous hazardous effects in living organisms, including humans
(Radosevich et al., 1997). The increase of herbicide-resistant weeds
reduces crop productivity and new environmentally friendly methods
are required to control weeds (Duke, 2012). The global interest
inorganic farming supports alternative methods that do not use che-
mical herbicides for weed control and prevent herbicide-resistant weed
development. Recently, biological agents have been added to integrated
weed management strategies (Cordeau et al., 2016).
Bioherbicides are products that naturally originate from either
living organisms or their natural metabolites that are used to control
weed populations without degrading the environment (Hoagland et al.,
2007; Bailey, 2014). Bioherbicides are categorized as host-specific and
non-host specific to control weeds. Hoagland et al. (2007) reviewed and
documented several species of bacteria and fungi to show their host-
specific or non-specific bioherbicide activities in susceptible weed po-
pulations. The target specificity and rapid environmental degradation
of bioherbicide products warrant more attention to the development of
commercial products that are alternatives to chemical herbicides
(Cordeau et al., 2016). Bioherbicides were first introduced in com-
mercial markets in 1980 and farmers in the USA, Canada, Ukraine and
Europe were the only users of the products (Charudattan, 2001; Bailey,
2014; Cordeau et al., 2016). The utilization of bioherbicides instead of
chemicals is becoming popular in other countries. Although several

⁎
Corresponding authors.
E-mail addresses: ramradhakrish@gmail.com (R. Radhakrishnan), eabdallah@ksu.edu.sa (E.F. Abd_Allah).

https://doi.org/10.1016/j.ecoenv.2018.04.018
Received 7 November 2017; Received in revised form 3 April 2018; Accepted 7 April 2018
Available online 24 April 2018
0147-6513/ © 2018 Elsevier Inc. All rights reserved.
R. Radhakrishnan et al.
microbes and plant products have been tested in the laboratory and
have been successfully field trialed, only a few (9 fungi, 3 bacteria and 1
plant extract) of them are commercially available in current markets
(Cordeau et al., 2016). Crop plants also produce allelochemicals, which
naturally prevent the growth of weeds. For example, tomatine and to-
matidine of tomato plants reduce the growth of weeds, pathogenic fungi
and some crop plants (Hoagland, 2009). Recently, the metagenomics
technique was used to isolate bioherbicide compounds by extracting
DNA fragments obtained from the soil and cloning the genes in vectors
to produce phytotoxic compounds (Kao-Kniffin et al., 2013).
Several studies have revealed that plant extracts, bacteria, fungi and
other products effectively control the germination and growth of weed
seeds (Ghosheh, 2005; Cavalieri and Caporali, 2010; Motlagh, 2011;
Harding and Raizada, 2015; Dharsini et al., 2017), but few studies have
been conducted to identify the mode of action and physiological
changes in weeds. This review provides the mode of action of biological
agents and their products on weed control and physiological changes in
weeds but does not discuss the positive or negative effects of bio-
herbicides on crop plants.
2. Plant-based bioherbicide on physiological changes in weed
populations
Plants secrete various metabolites in their environment, including
water-soluble organic acids, alcohols, aldehydes, ketones, lactones,
fatty acids, polyacetylenes, quinones, phenolics, cinnamic acid, cou-
marins, flavonoids, tannins, terpenoids and steroids (Soltys et al.,
2013), which inhibit weed seed germination and growth (Dayan et al.,
2000). Some plant extracts specific to weed control prevent weed po-
pulations and do not damage crop plants (Mendes et al., 2014). The
plant extract compounds are specific to weeds and might be attributed
to the existence of a specific receptor in weeds (Hosni et al., 2013). For
that reason, plant-based bioherbicides could be a natural method to
control weed populations. Several plant extracts have been applied to
inhibit weed growth (Table 1; Fig. 1). For example, Lee et al. (2015)
used a seed extract from burcucumber plants to control weeds and re-
vealed that the weed control efficiency is dependent on the con-
centration of the extract. A higher concentration of seed extracts more
effectivity inhibits seed germination than a lower concentration. Al-
though several reports have proven that those chemicals inhibit weed
growth, very few studies have recorded the effects of allelochemicals on
weed metabolism.
2.1. Seed germination and seedling growth
The essential oils of some plants can exhibit the weed herbicidal
activity. Essential oils cause damage to DNA, some biochemical pro-
cesses, mitosis and meristematic cells in seedling growth (Vaughn,
1991; Romagni et al., 2000; Zanellato et al., 2009). Fatty acids (pe-
largonic acid) have a wide range of bioherbicide activities that can
disturb cell membranes and result in the loss of cellular functioning
(Lederer et al., 2004). The effect of the phytotoxic nature of plant ex-
tracts on germination varies with the size and seed coat permeability of
the weed seed (Hanley and Whiting, 2005; Dayan, 2006). The phenolic
compounds of herbal extracts reduce the amylase activity in weeds,-
which delays the seed germination due to the slow starch hydrolysis
process (Hegab et al., 2008).
The bioherbicide effects of plant extracts have been proven by
anatomical changes in seedlings, including an increase in lipid globules,
a decrease in mitochondria and the destruction of mitochondrial and
nuclei membranes (Nishida et al., 2005). Allelochemicals affect primary
root surfaces more than hypocotyls due to thin cuticle layers, which
allows the transport of more phytotoxic compounds into the root cells
(Bessire et al., 2007; Yoshimura et al., 2011). As a result, the cell cycle
and division are altered and the membrane and cellular ultrastructure
are damaged, all of which can inhibit root growth (Yoshimura et al.,
132
Ecotoxicology and Environmental Safety 158 (2018) 131–138
2011; Yang et al., 2011; Soltys et al., 2011; Chowhan et al., 2013; Grana
et al., 2013). Phytotoxic compounds reduce the cell size of metaxylem
in roots, which might inhibit cell elongation due to changes in auxin,
ethylene and cytokinins (Anese et al., 2015). Plant hormones sy-
nergistically regulate cell elongation, differentiation of vascular tissues
and lateral root growth (Aloni et al., 2006; Stepanova et al., 2007;
Grana et al., 2013). The role of auxin is well known for root growth and
development; the alteration in cellular processes reflects the dis-
turbance of enzyme activities that are involved in auxin biosynthesis
(Prasad and Subhashini, 1994; Rahman et al., 2001).
2.2. Photosynthesis
Plant extracts alter protein metabolism via abnormal up or down
regulation of proteins. Specifically, the chlorophyll a/b binding protein
is decreased by two-fold, which leads to the suppression of chlorophyll
synthesis and affects photosynthesis. However, the biosynthesis of an-
other important nuclear-encoded chloroplast protein, i.e., oxygen-
evolving enhancer protein 1 (OEE1), is decreased under the influence of
plant-based bioherbicides (Lee et al., 2015). OEE1 plays a vital role in
the release of oxygen by splitting water, promotes thioredoxin activity
and protects the tetra-manganese cluster and ionic content (Seidier,
1996; Weng and Xu, 2003; Heide et al., 2004). It has been suggested
that the reduction of OEE1 affects gas and nutrient exchange in weeds.
In addition, the concentration of Mg is reduced when plant extracts are
used for treatment, which might reduce the synthesis of chlorophyll
because Mg is a central element of chlorophyll and is involved in carbon
fixation and many biochemical reactions (Shaul, 2002). The synthesis
rate of other important photosynthetic pigments, carotenoids, is re-
duced, which can increase photooxidation. Carotenoids are able to
scavenge reactive oxygen species (ROS) to protect the plants from
photooxidation (Siefermann-Harms, 1987). Photosynthesis-inhibiting
herbicides reduce the photochemical quenching coefficient, electron
transport and carbohydrate synthesis (Sousa et al., 2014; Powles and
Yu, 2010).
2.3. Plant hormones
Plant hormones are signaling molecules, it involved in several me-
tabolic pathways that regulate plant growth and development.
Gibberellin (GA) is a plant hormone that triggers shoot growth
(Radhakrishnan et al., 2013). The application of a burcucumber seed
extract and their phenolic allelochemical (2-linoleoyl glycerol) inhibits
the gibberellin pathway and stimulates the accumulation of abscisic
acid (ABA), jasmonic acid (JA) and salicylic acid (SA) (Lee et al., 2015).
Higher accumulation of ABA is triggered by ethylene synthesis due to
the cleavage of xanthophyll (Hansen and Grossmann, 2000). ABA
causes stomatal closure, low photosynthetic rates and ROS production,
which reduces growth and initiates senescence (Grossmann, 2003). JA
accumulation also induces stomatal closure and senescence, which re-
duces photosynthesis (Creelman and Mullet, 1997). In addition, an in-
crease of SA production reduces the electron transport and stomatal
closure, which inhibits photosynthesis (Janda et al., 2012).
2.4. Nutrient uptake
Plant-based bioherbicides limit weed growth by deregulating nu-
trient uptake, photosynthesis and membrane permeability (Duke et al.,
2000). The absorption of nutrients (Ca, K, Mg, and Fe) in weeds is re-
duced by allelochemicals due to changes in the structure and function
of cellular membranes (Franche et al., 2009; Hussain and Reigosa,
2014). Ca plays a vital role in cell signaling and protein activities
(White and Broadley, 2003). The reduction of Ca inhibits root growth
and induces senescence (Himelblau and Amasino, 2001). Decreases in
K, Mg and Fe results in chlorosis because those elements are involved in
chloroplast functions (Christin et al., 2009). The higher accumulation of
R. Radhakrishnan et al. Ecotoxicology and Environmental Safety 158 (2018) 131–138

Table 1
Effect of plant based bioherbicides on weed physiology.
Plant extract Bioherbicide stimulant Mode of action in weeds References

Aglaia odorata Lour
Ammi visnaga (L.) Lam.
Artemisia absinthium L
Artemisia scoparia Waldst et Kit.
Artemisia vulgaris L.
Beta vulgaris L. var. Cicla
Brassica napus
Canavalia ensiformis
Chrysanthemum coronarium
Cinnamomum zeylanicum L.
Cymbopogon citratus ( DC) Stapf
Drimys brasiliensisMiers
Echinochloa colona
Echinochloa colona L.
Eucalyptus citriodoraHook.
Eucalyptus tereticornis
Eucalyptus cladocalyx
Lavandula spp.
Limnanthes alba
Mentha spicata L. subsp. spicata
Mentha x piperita L
Nepeta meyeri Benth
Ocimum basilicum L.
Origanum vulgare L
Parthenium hysterophorus L.
Pinus halepensisMiller
Salvia officinalis L.
Sicyos angulatus L
(Burcumumber)
Sinapis alba
Sonchus oleraceus L.
Sonchus oleraceus L.
Syzygium aromaticum (L.)
Merrill and Perry
Thymbra spicata L. subsp. spicata
Leaf extract (rocaglaol) Inhibit weed growth Kato-Noguchi et al.
(2016)
Plant extract (Khellin and Visnagin) Inhibit seed germination and seedling growth, photosynthesis, cell Travaini et al. (2016)
division, and cell death and induce membrane destabilization.
Essential oil Inhibit seed germination and seedling growth Fouad et al. (2015)
Essential oil (Mono terphenes, Inhibit weed growth and cellular respiration, and while, increase Kaur et al. (2010)
sesquiterpenes, aromatic and aliphatic electrolytic leakage, membrane disruption, chlorosis, necrosis and wilt
compounds)
Essential oil Inhibit seed germination and seedling growth Onen et al. (2002)
Water extract (eight phenolic aglycones) Inhibit seed germination, vigour and seedling growth, biomass, total Hegab et al. (2008)
phenol, phenolic glycoside, amylase activity, DNA, and RNA, and while
increase aglycones
Se-seed meals Inhibit seed germination and seedling emergence Banuelos, 2010
Leaf and seed extract (chlorogenic acid, Inhibit weed growth and biomass Mendes and Rezende
p-Anisic acid, naringin and rutin) (2014)
Essential oil Inhibit seed germination and seedling growth Hosni et al. (2013)
Essential oil Inhibit seed germination Cavalieri1 and Caporali
(2010)
Essential oil Inhibit seed germination and seedling growth Fouad et al. (2015)
Root extract (drimane sesquiterpenes) Inhibit seed germination, seedling growth and cell division of metaxylem Anese et al. (2015)
in roots
Shoot extract (Tricin) Inhibition of seed germination and seedling growth Gomaa and
AbdElgawad (2012)
Tricin Inhibit seed germination, seedling growth, amylase activity, total soluble Hegab et al. (2013)
sugar, CAT, POX, POL and SOD, and while increase starch, polyphenols,
glutathione and ascorbate
Oil Inhibit respiration, loss of membrane integrity, chlorosis and necrosis, Batish et al. (2007)
wilting and plant death
Oil (α-Pinene and 1,8-cineole) Inhibit seedling growth and seedling vigor respiration and pigments Kaur et al. (2011)
synthesis
Essential oil Inhibit seed germination and seedling growth Fouad et al. (2015)
Essential oil Inhibit seed germination Cavalieri1 and Caporali
(2010)
Activated seed meal (Isothiocyanate) Inhibit seed germination, seedling growth and biomass Intanon et al. (2014)
Essential oil Inhibit seed germination and seedling growth Onen et al. (2002)
Essential oil Inhibit seed germination Cavalieri1 and Caporali
(2010)
Essential oil (4aα,7α,7aβ-nepetalactone.) Inhibit seed germination, increase lipid peroxidation, H2O2, CAT and Mutlu et al. (2011)
decrease SOD
Essential oil Inhibit seed germination and seedling growth Onen et al. (2002)
Essential oil Inhibit seed germination and seedling growth Fouad et al. (2015)
Ethylacetate and methanolic crude Inhibit seed germination, growth and vigour Pati and Chowdhury
extracts (2015)
Spore Inhibit seed germination, growth and vigour Amri et al. (2013)
Essential oil Inhibit seed germination and seedling growth Onen et al. (2002)
Seed extract (2-linoleoyl glycerol) Inhibit seed germination, seedling growth, pigments, chlorophyll a/b Lee et al. (2015)
binding protein, oxygen evolving enhancer protein 1, GA, Ca, Fe, Mg, K,
S and Mo and increase ABA, JA, SA, Cu, Zn and Na
Se-seed meals Inhibit seed germination and seedling emergence Banuelos and Bradley
(2010)
Plant powder Inhibit seed germination, seedling growth, reduce soil pH, enhance the Hassan et al. (2014)
soluble salts, electrical conductivity, organic matter, CaCO3, nutritional
elements and total phenolics in soil
Aqueous extract (phenols, alkaloids, Inhibit seed germination and seedling growth Gomaa et al. (2014)
flavonoids, tannins and saponins)
Essential oil (eugenol) Inhibit seed germination, seedling growth, chlorophyll, respiration Ahuja et al. (2015)
Essential oil Inhibit seed germination and seedling growth Onen et al. (2002)

elements, including Na, Cu and Zn, which reflects a nutritional im-
balance and low rates of protein, carbohydrate and chlorophyll synth-
esis (Neel et al., 2002; Xing et al., 2010). Higher accumulation of Na in
plants disturbs the uptake of nutrients and water (Radhakrishnan and
Lee, 2013, 2014). Mo is a micronutrient that is required for several
enzyme activities, including xanthine dehydrogenase, nitrate reductase,
sulfite oxidase and aldehyde oxidase. Those enzymes are involved in
purine catabolism, nitrogen assimilation and fixation, ureide bio-
synthesis, ABA biosynthesis, and catabolism of sulfur-containing amino
acids (Mendel and Haensch, 2002; Williams and Frausto-da-Silva, 2002;
Lee et al., 2015).
2.5. Reactive oxygen species (ROS) and antioxidants
The plant extract (cinnamic acid) produces ROS in cucumber species
and not fig leaf gourd shows the action of bioherbicides might be
species specific. The accumulation of ROS is an indicator of plant stress,
which leads to lipid peroxidation of the membrane and electrolyte re-
lease from the cells (Mittler, 2002). The allelopathic effects of plant
extracts on weeds enhance the superoxide (O2-), hydrogen peroxide
(H2O2) and hydroxyl radicals, which results in damage to DNA, proteins
and cellular membranes (Duke et al., 2002; Ding et al., 2007; Tigre
et al., 2012). Electrolytic leakage induces endonucleases, proteases and
programmed cell death,which inhibits weed growth (Demidchik et al.,

133
R. Radhakrishnan et al.
Fig. 1. Effect of bioherbicides (plant extract or microbes) on weed control.
2014) and causes necrosis (Travaini et al., 2016). The peroxidation of
lipids and irregular activities of ROS scavenging enzymes, such as
catalase (CAT), peroxidase (POX) and superoxide dismutase (SOD) in
weeds, indicate the toxicity of plant extracts (Mutlu et al., 2011). CAT
and POX enzymes detoxify H2O2 into H2O and O2, and while the SOD
enzyme scavenges O2. Generally, under stress conditions, these en-
zymes help to remove excess H2O2 and O2. The application of plant
extracts on weeds triggers CAT and POX activity and suppresses SOD
activity in weeds, which reflects the increased accumulation of H2O2,
but O2 production cannot be controlled by the autoimmunity process of
weeds (Mutlu et al., 2011). In addition, the presence of phenolic com-
pounds in the plant extract reduces cell division and retards weed
growth (Li et al., 2010).
3. Influence of microbial herbicides on the growth and physiology
of weeds
Microorganisms that promote plant growth have been identified
from various environmental soil samples, plants and other sources and
are applied to enhance crop productivity. Several groups of bacteria
and fungi are commercialized as biofertilizers due to their positive re-
lationship with plant growth. Some bacteria suppress plant growth by
various mechanisms. For example, the production of hydrogen cyanide,
indoleacetic acid (IAA), ammonia, dimethyl disulfide, hydrocinnamic
acid, toxic volatile compounds and other plant growth inhibiting me-
tabolites from bacterial or fungal cells retard plant growth (Astrom and
Gerhardson, 1989; Egamberdieva, 2009; Kim and Rhee, 2012; Popovic
et al., 2013; Park et al., 2015). The usage of those microorganism
groups in agriculture can prevent weed populations and can protect the
environment (Boyette and Hoagland, 2015). The prolonged use of
chemical herbicides generates herbicide-resistant weed populations,
but microbial association limits the resistance and controls different
weed species (Omer et al., 2010). The genera Alternaria, Bacillus,
Chondrostereum, Colletorichum, Curvularia, Dactylaria, Diaporthe, Drech-
slera, Enterobacter, Epicoccum, Exserohilum, Fusarium, Gloeocercospora,
Microsphaeropsis, Mycoleptodiscus, Myrothecium, Phoma,Phomopsis, Plec-
tosporium, Pseudolagarobasidium, Pseudomonas, Puccinia, Pyricularia,
Pythium, Sclerotinia, Serratia, Stagonospora, Streptomycetes, Tricho-
derma,Verticillium and Xanthomonas have been recorded as bioherbi-
cidal agents that inhibit seed germination and the growth of weeds
(Table 2).
134
Ecotoxicology and Environmental Safety 158 (2018) 131–138
3.1. Germination and growth of weed seeds
Deleterious bacteria and fungi limit weed populations by causing
disease or inhibiting seed germination and growth of weed plants.
Bailey et al. (2011) attempted to determine the model pathway of mi-
crobial infection to control weed growth and suggested that Phoma
macrostoma colonizes and enters the root hairs of a host and growing in
the intercellular spaces to reach the root core. The proliferation of
mycelium infects the vascular trachea to prevent the supply of food and
nutrition. The phytotoxin α,β-dehydrocurvularin inhibits mitosis in
root tip cells and halts seedling growth (Jiang et al., 2008). Fungal
pectinase penetrates the cell wall of the host by rupturing the poly-
saccharide layers and enlarging the pores in the wall and releases
several signaling and toxic molecules in infected plant cells (Bowling
et al., 2010). The extracellular lipases of fungi utilize the lipids and
proteins in the endosperm of weed seeds for growth (Thomas et al.,
1999). In addition, Enterobacter sp. I-3 secretes high concentrations of
IAA and transfers it to weeds during their association,resulting in en-
hanced plant endogenous IAA and aminocyclopropane-1-carboxylate
(ACC) synthase, which stimulates an increase of ethylene biosynthesis
and causes a reduction in weed growth (Kende, 1993; Park et al., 2015).
A disease-causing fungus, Alternaria alternate, produces tenuazonic acid
and isotenuazonic acid to induce disease in weeds and inhibits the
germination of Striga hermonthica and Echinochloa sp. seeds (Qiang
et al., 2008; Motlagh, 2012). Extracellular and hydrophilic phytotoxins,
such as N2-β-D-glucopyranoside, trans−4-amino-D-proline and agly-
cone of ascaulitoxin,are synthesized from a plant pathogenic fungus,
Ascochyta caulina,which damage the plants and increase their mortality
(Netland et al., 2001). Similarly, Cercospora sp. produces cercosporin
and beticolin to inhibit weed growth and spread disease (Moran, 2005;
Tessmann et al., 2008). Other bioherbicidal compounds,including α,β-
dehydrocurvularin, 24-kDa protein (Nep1), trichothecene, β−1,4-exo-
glucanase, β−1,4-endoglucanase, glucosidase, xylanase and pectinase,
3-nitro-1,2-benzenedi-carboxylic acid (3-nitrophthalic acid), macro-
cidins, diethyl 7-hydroxytrideca-2,5,8,11-tetraenedioate, cyclo-(Pro-
Phe) and organic acids, are produced from bacteria and fungi to control
the germination and growth of weed seeds (Table 2).
3.2. Weed plant metabolism
The activities of chloroplasts, a prime organelle that converts solar
energy to plant available form of chemical energy, are affected in weeds
during the interaction between deleterious microorganisms (Hoagland
et al., 2013). The macrocidin-producing Phoma sp. degrades carotenoid
production and leads to enhanced phytone production and reduced
theβ-carotene to lutein ratio, which inhibits chlorophyll synthesis and
reduces the rate of photosynthetic gas exchange (Dankov et al., 2009;
Hubbard et al., 2015). A decrease in β-carotene reflects damage to the
photosystem II (PSII) reaction centers (Ladygin, 2003). Necrosis and
chlorosis in weeds are symptoms of pathogenic infections caused by
pigment degradation by chlorophyllase activity and affect ATP synth-
esis, Mg2+-ATPase activity and chlorophyll A fluorescence (Jiang et al.,
2008). Pathogen-induced oxidative stress in weeds generates ROS and
misleads antioxidants, including POX (Ahn et al., 2005), and affects
regular cellular processes. Recently, the bioherbicide characteristics of
microorganism-induced plant metabolism were studied by
Radhakrishnan et al. (2016), who reported that Enterobacteria sp. I-3
inoculation inhibits the germination of weed seeds and plant growth by
suppressing the synthesis of chlorophyll, gibberellins (GA12, GA19, GA20
and GA8), amino acids (aspartic acid, glutamic acid, glycine, threonine,
alanine, serine, leucine, isoleucine and tyrosine) and stimulating the
accumulation of ABA. GAs play a major role in seed germination and
stem and leaf growth, including flower formation (Achard and
Genschik, 2009). Similarly, ion transport, stomatal opening and other
physiological processes are regulated by several amino acids (Rai,
2002). However, microbial proteins induce necrosis and enhance
R. Radhakrishnan et al.
Table 2
Effect of microbial bioherbicides on weed physiology.
Microbes
Alternaria alternata
Alternaria cassiae
Alternaria crassa
Alternaria destruens
Ascochyta caulina (P. Karst)
Bacillus cereus
Cercospora piaropi
Chondrostereum purpureum
Colletorichum coccodes(Wallr.)
Colletotrichum gloeosporioides
Colletotrichum graminicola
Colletotrichum truncatum
Curvularia eragrostidis Isolate QZ-
2000
Dactylaria higginsii
Diaporthe sp.
Drechslera avenacea(Curtis ex
Cooke) Shoem
Drechslera gigantea
Enterobacter sp. I-3
Epicoccum purpurascens
Exserohilum monoceras
Exserohilum longirostratum
Exserohilum rostratum
Fusarium equiseti
Fusarium oxysporum
Fusarium tumidum
Gloeocercospora sorghi
Microsphaeropsis amaranthi
Mycoleptodiscus terrestris
Myrothecium roridum
Myrothecium verrucaria
Phoma commelinicola
Phoma herbarum
Phoma macrostoma
Phoma macrostoma
Phomopsis amaranthicola
Phomopsis convolvulus
Plectosporium tabacinum
Pseudolagarobasidium acaciicola
Pseudomonas fluorescens
Pseudomonas trivialis
Puccinia romagnoliana
Pyricularia setariae
Pythium spp.
Sclerotinia minor
Serratia marcescens
Serratia plymuthica
Stagonospora convolvuli
Streptomycetes isolates.
Trichoderma virens
Verticillium dahliae
Xanthomonas campestris
Ecotoxicology and Environmental Safety 158 (2018) 131–138
Bioherbicide stimulant Mode of action in weeds References
Spore and culture Leaf blight disease and inhibit seed germination Masangkay et al. (1999) and
Motlagh (2012)
Spore Increase mortality of weed growth and cause disease Pitelli and Amorim (2003)
Spore Control weed growth Stewart-Wade et al. (1998)
Spore Cause disease and damage the weeds Cook et al. (2009)
Spore (N2-β-D-glucopyranoside, Inhibit growth and induce disease Netland et al. (2001)
trans−4-amino-D-proline and aglycone of
ascaulitoxin)
Culture extract Inhibit seed germination and growth Carvalho et al. (2007)
Spore and culture (cercosporin and Inhibit growth, induce disease Moran (2005) and Tessmann et al.
beticolin) (2008)
Spore Reduce shoot growth Bourdot et al. (2006)
Spore Induce disease and POD activity Ahn et al. (2005)
Spore High rate of mortality, dry weight reduction and reduce Boyette et al. (2010) and Bowling
plant growth, anthracnose lesions in stems, et al. (2010)
polysaccharides changes in cell wall
Spore Reduce weed biomass Mitchell et al. (2008)
Spore High rate of mortality and dry weight reduction Boyette and Hoagland (2010)
Spore and culture (α,β-dehydrocurvularin) Inhibit seed germination, biomass, chlorophyll, Zhu and Qiang (2004) and Jiang
photophosphorylation, Mg2+ ATPase, mitosis of root et al. (2008)
tips, increase necrosis, mortality
Spore Induce disease and reduce growth Kadir et al. (2000a), (2000b)
Spore Disease induction Souza et al. (2017)
Spore Disease induction and necrosis Hetherington et al. (2002)
Spore Increase disease and mortality Peng and Boyetchko (2006)
Culture (IAA) Inhibit seed germination, growth, synthesis of GAs, Asp, Park et al. (2015) and
Glu, Gly, Thr, Ala, Ser, Leu, Iso, Tyr and increase ABA Radhakrishnan et al. (2016)
Spore Inhibit seed germination and disease induction Motlagh (2011)
Spore Disease induction Zhang and Watson (1997)
Spore Disease induction Chandramohan and Charudattan
(2001)
Spore Increase disease and mortality Peng and Boyetchko (2006)
Spore Inhibit seed germination and disease induction Motlagh (2011)
Spore (24-kDa protein (Nep1)) Disease induction, necrosis, ethylene production, inhibit Thomas et al. (1999), Jennings
seed germination and infect seed testa and endosperm et al., 2000 and Ray and
Vijayachandran (2013)
Spore (trichothecene) Induce disease and reduce shoot growth Morin et al. (2000) and Bourdot
et al. (2006)
Spore Reduce weed growth and biomass Mitchell et al. (2008) and Motlagh
and Javadzadeh (2011)
Spore Inhibit seed germination, growth and induce disease Shabana et al. (2010)
Spore Reduce shoot biomass Shearer and Jackson (2006)
Spore and culture (β−1,4-exoglucanase, Inhibit seed germination, growth and disease Lee et al. (2008) and Piyaboon et al.
β−1,4-endoglucanase, glucosidase, (2016)
xylanase and pectinase)
Spore Inhibit weed growth, chlorophyll and induce disease Weaver et al. (2009) and Hoagland
et al. (2013)
Spore Mortality, disease induction and dry weight reduction Boyette et al. (2015)
Spore and culture (3-nitro−1,2-benzenedi- Inhibit weed growth Schnick and Boland (2004) and
carboxylic acid (3-nitrophthalic acid)) Vikrant et al. (2006)
Spore Inhibit weed growth and disturb root cells Bailey et al. (2011)
Spore and culture (macrocidins) Inhibit growth, chlorosis, photosynthesis, carotenoid Hubbard et al. (2015)
biosynthesis
Spore Inhibit weed growth, increase disease and mortality rate Ortiz-Ribbing and Williams (2006)
Spore Inhibit weed growth, increase disease and mortality rate Vogelgsang et al. (1998)
Spore Induce disease Chung et al. (1998)
Spore Increase disease and mortality Kotze et al. (2015)
Spore Reduce root growth Caldwell et al. (2012)
Spore Inhibit weed growth Mejri et al. (2012)
Spore Increase disease and mortality Gupta et al. (2002)
Spore Increase disease and mortality Peng and Boyetchko (2006)
Culture Reduce weed emergence and increase weed seedling Hoagland et al. (2008)
mortality
Spore Inhibit weed growth Abu-Dieyeh et al. (2010)
Culture Inhibit weed growth Juan et al. (2015)
Culture Inhibit weed growth Weissmann et al. (2003)
Spore Induce necrosis and disease Pfirter et al. (1999)
Culture (diethyl 7-hydroxytrideca-2, 5, 8, Inhibit seed germination and growth Dhanasekaran et al. (2010) and
11-tetraenedioate) Dharsini et al. (2017)
Spore Inhibit weed growth Heraux et al. (2005)
Spore Disease induction and reduction of weed growth Skipp et al. (2013)
Culture (cyclo-(Pro-Phe) and organic acids) Inhibit weed growth, increase mortality Mingzhi et al. (2007) and Boyette
Hoagland (2015)
135
R. Radhakrishnan et al.
ethylene biosynthesis in weeds (Jennings et al., 2000).
4. Conclusions
Although very few studies have been conducted to elucidate weed
physiology during bioherbicide treatments, several studies have high-
lighted significant metabolic processes, such as those related to pho-
tosynthesis, antioxidants, nutrients and hormones. Both plant-derived
and microbial bioherbicides suppress weed populations by secreting
toxic metabolites or affecting regular cellular functions. Cell division,
pigment synthesis, nutrient uptake and plant growth promoting reg-
ulators are all inhibited, while the irregular activation of antioxidants,
stress-mediated hormones and other metabolites control the germina-
tion and growth of weed seeds. Thus, this review suggests that more
bio-molecular studies are required in weeds to determine the biological
interaction mechanism of weed control.
Acknowledgments
The authors would like to extend their sincere appreciation to the
Deanship of Scientific Research at King Saud University for its funding
this research group (No: RG-1435-014).
Conflicts of interest
The authors have no conflicts of interest to declare.
Author contributions
RR, AAA and EFA involved in research article collections and wrote
and revised the article together. All the authors approved the final
version of this manuscript.
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