Plant Stress 6 (2022) 100110

Contents lists available at ScienceDirect

Plant Stress
journal homepage: www.sciencedirect.com/journal/plant-stress

The hunt for beneficial fungi for tomato crop improvement – Advantages
and perspectives☆
Abhay K. Pandey a, b, *, Abhishek Kumar c, K. Dinesh d, Richa Varshney e, Pranab Dutta f
a
World Vegetable Center, South Asia, ICRISAT Campus, Patancheru, Hyderabad 502324, TS, India
b
Department of Mycology & Microbiology, Tea Research Association, North Bengal Regional R & Center, Nagrakata 735225, Jalpaiguri, West Bengal, India
c
Department of Plant Pathology, Chaudhary Charan Singh Haryana Agricultural University, Hisar 125004, Haryana, India
d
Department of Plant Pathology, Dr. YSR Horticultural University, College of Horticulture, Anantharajupeta 516105, Andhra Pradesh, India
e
ICAR-National Bureau of Agricultural Insect Resources, HA Farm Post, Bellary Road, P. Bag No. 2491, Bengaluru, Karnataka 560024, India
f
School of Crop Protection, College of Post-graduate Studies in Agricultural Sciences, Central Agricultural University (Imphal), Umiam 793103, Meghalaya, India

A R T I C L E I N F O A B S T R A C T

Keywords: Beneficial fungi with antagonistic and entomopathogenic properties have shown promising effect in the bio­
Fungal antagonists, Entomopathogenic fungi, logical control of diseases and pests in a variety of commercially significant crops, including tomato, in recent
Growth promotion, Biological control years. Despite the fact that such treatments are environmentally safe, their risk on non-target species in tomato
Eco-friendly approach
fields remains unknown. Beneficial fungi that have been commercialised for field use have had little effects on
the population of arthropod pests and the incidence of diseases in tomato fields due to various reasons. The use of
fungal antagonists and entomopathogenic fungi-based products for the management of diseases and pests of
tomato crop has been done all over the world. The investigated reports, however, are scattered throughout the
research papers, so they need to be compiled and discussed. Therefore, efficiency of antagonistic and entomo­
pathogenic fungi against important pests and pathogens of tomato crop, as well as their practical use as bio­
fungicides and bioinsecticides to reduce the use of synthetic pesticides, are discussed in this review paper.
Besides, plant growth promotion activity of beneficial fungi, their appropriateness as an alternative of synthetic
pesticides, and future prospects are also discussed.

1. Introduction
Among the vegetables, tomato, Solanum lycopersicum L. occupies an
important place and is grown worldwide for its edible fruits. The crop is
cultivated for many other purposes, like its use in salad preparation and
for several industrial purposes in the preparation of tomato-based
products (Islam et al., 2013). According to a recent report, at a global
level, the total tomato production was 182 MT (million tonnes).
Worldwide, China is the largest tomato producer, producing 61.5% MT
annually. India is the second largest producer producing 19.4 MT fol­
lowed by the United State of America with 12.6 MT, Turkey with 12.2
MT, and Egypt with 6.6 MT. Nutritionally, it is a rich source of various
types of vitamins including vitamin C (17%), comprising <1% each of
protein and fat and 4% carbohydrates (FAO, 2018). However, tomato
production is inhibited by numerous abiotic and biotic factors, which
detrimentally reduce the quality, quantity, and its productivity (Sain
and Pandey, 2016).
In biotic factors, insect pests and diseases that affect tomato crop
causes significant loss in production as well as quality attributes (Sain
and Pandey, 2016; Pandey et al., 2021; Sarr et al., 2021). For the miti­
gation of insect pests and diseases, farmers rely on the use of synthetic
fungicides and insecticides (Mizubutiet al., 2007). However, regular use
of synthetic pesticides causes residue problems in the vegetables along
with fungicide resistance/insect tolerance, therefore, their application
should be limited (Stangarlin et al., 2011; Guedes et al., 2019) and de­
mands a substitute for pest and disease management. Additionally, small
farmers growing tomatoes do not use protective gear during the spraying
of synthetic pesticides, and they do not know how to dilute the chem­
icals, making their own safety at risk (Damalas and Koutrobous, 2015).
Thus, the requirements of alternative pest management options have

This article is part of a special issue entitled: “Induced Systemic Response in Plants against Biotic Stress” published at the journal Plant Stress.
☆

* Corresponding author at: Department of Mycology & Microbiology, Tea Research Association, North Bengal Regional R & D Center, Nagrakata 735225, Jal­
paiguri, West Bengal, India.
E-mail address: abhaykumarpandey.ku@gmail.com (A.K. Pandey).

https://doi.org/10.1016/j.stress.2022.100110
Received 19 June 2022; Received in revised form 1 August 2022; Accepted 5 August 2022
Available online 6 August 2022
2667-064X/© 2022 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
A.K. Pandey et al. Plant Stress 6 (2022) 100110

become more stringent, especially for chemical residues found on fresh Table 1
vegetables (European Commission, 2012). Pests and diseases of tomato crop and their economic impacts.
Therefore, a microbial biocontrol agent-based approach to managing Biotic Causal organisms Yield References
tomato pests and diseases is ecologically safe and capable of hindering stresses loss
or defeating pathogen populations (Chow et al., 2018), making it a (%)
suitable alternative strategy. Among microbial agents, beneficial fungi, Diseases
or fungal biocontrol agents (FBCAs), may present both Damping off Pythium aphanidermatum 30-60 Al-Hussini et al. (2019),
growth-promoting and antagonistic/entomopathogenic qualities, mak­ (Edson) Fitzp Michel-Aceves et al.
(2019)
ing them useful for promoting plant growth as well as controlling pests Fusarium Fusarium oxysporum f. sp. 20-80 Maurya et al. (2019),
and diseases (Kareem and Matloob, 2019). Beneficial fungi are more wilt lycopersici Synder & Hansen Ashraf et al. (2020)
likely to establish and be effective when adapted to the soil than exotic Early blight Alternaria solani Sorauer or 30-60 Kokaeva et al. (2018);
microorganisms. In fact, native microbes are already adapted to local A. alternata (Fr.) Keissl. Hussain et al. (2019)
Late blight Phytophthora infestans 20-50 Mazumdar et al. (2021),
conditions, including climate and edaphic conditions (Gómez et al.,
(Mont.) de Bary Zhang et al. (2003)
2016). Besides FBCAs, other microbes such as viruses and bacteria as Septoria leaf Septoria lycopersici Speg. 10-40 Mattos et al. (2020)
well as nematodes have also been deployed for disease and pest man­ spot
agement of tomatoes. For examples, Acinetobacter calcoaceticus, Bacillus Insect pests
siamensis, and Pseudomonas fluorescens have been used for control of Tobacco Spodoptera litura Fab. 40-80 Monobrullah et al.
caterpillar (2007), Bano and
Fusarium wilt (Khalil et al., 2021; Vignesh et al., 2021), SNPV (a simple Muqarab (2017)
nucleopolyhedrovirus) has been used against African bollworm, Heli­ Pod borer Helicoverpa armigera Hubner 20-60 Amin et al. (2017)
coverpa armigera Hubner (Lepidoptera: Noctuidae) (Singh and Singh, Herald and Tayde
2011), and entomopathogenic nematodes including Steinernema feltiae, (2018)
Tomato leaf Tuta absoluta Meyrick 40-100 Alam et al. (2019)
Steinernema carpocapsae, and Heterorhabditis bacteriophora have been
miner
used to control tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Spider mite Tetranychus urticae Koch. 40-90 Rakha et al. (2017)
Gelechiidae) (Batalla-Carrera et al., 2010). Whitefly Trialeurodes vaporariorum 30-100 Lefeuvre et al. (2010),
Using beneficial fungi also decreases the problems of pesticide risks Westwood, Bemisia tabaci Iftikhar et al. (2021)
in tomatoes (Arshi et al., 2021; Elnahal et al., 2022). In order to improve Gennadius

tomato plant defenses by incorporating systemic resistance inducing

fungi, it is necessary to understand the host responses and mechanisms
towards a particular disease. At present, there is no review on use of Table 2
beneficial fungi (FBCAs) for management of diseases and insect pests in Biocontrol efficacy of fungal antagonists against major tomato phytopathogens.
tomato crop. Due to tomato’s global relevance as a fresh and processed Fungal agents Target disease Control Reference
crop, there is a great deal of interest in improving tomato crop that is Trichoderma harzianum Fusarium solani 100% Kareem and
free of pests and diseases. Therefore, this review captures the latest in­ Matloob (2019)
terventions carried out on the use of FBCAs for pest and disease man­ T. harzianum (Th), + Pythium 57.2% Elshahawy and
agement of tomatoes and reviews the advantages and perspectives on T. asperellum (Ta), + aphanidermatum Mohamedy
T. virens (Tvs1), + (2019)
this issue. We also discuss the compatibility of insecticides and fungi­
T. virens (Tvs2) +
cides with FBCAs during field applications. Besides, frontier research T. virens (Tvs3)
areas for the innovative use of beneficial fungi as antagonistic and Trichoderma asperellum P. aphanidermatum 60% Kumhar et al.
entomopathogenic agents are summarized. (2022)
T. viride Fusarium oxysporum f. 83.56% Jamil et al. (2021)
T. harzianum sp. lycopersici 75.29%
2. Major insect pests and diseases of tomato crop and their A. niger 71.84%
economic significance T. harzianum (Pusa Fusarium oxysporum f. 99.5% Dubey et al.
5SD) + Vitavax sp. lycopersici (2020)
During the cropping period, i.e., from sowing to harvesting, tomato power
Xylaria feejeensis, Fusarium oxysporum 75% Brooks et al.
plants are attacked by many insect pests and diseases. Under favourable
SRNE2BP Alternaria solani 87% (2022)
conditions these insect pests and diseases cause potential yield loss to Aspergillus tubingensis Botrytis cinerea 33% Zhao et al. (2018)
the tomato production (Iqbal et al., 2019). The major diseases of to­ strain QF05
matoes include root rots and foliar diseases. The damping-off incited by Acrophialophora Rhizactonia solani 40% Daroodi et al.
jodhpurensis (2021)
Pythium aphanidermatum and wilt by Fusarium oxysporum f. sp. lycopersici
Penicillium sp. Colletotrichum coccodes 85% Hassine et al.
and Rhizoctonia solani, are prevalent root rot diseases, while Septoria leaf Gliocladium catenulatum 85% (2022)
spot by Septoria lycopersici, early blight by Alternaria solani or Piriformospora indica Verticillium dahliae 68% Fakhro et al.
A. alternata, and late blight by Phytophthora infestans are the prevalent (2010)
foliar diseases of tomato crop caused by fungi (Agrios, 2005). Besides, Trichoderma harzianum Septoria lycopersici 100% Sain and Pandey
(2016)
bacterial wilt due to Ralstonia solanacearum, bacterial leaf spot caused by
Xanthomonas perforans and tomato yellow leaf curl disease caused by
TYLCV (Tomato Yellow leaf curl virus) are also major diseases of tomato worldwide. These insect pests collectively have been reported to cause
but negligible FBCAs were used against these diseases (Abdulridha et al., 40-100% yield loss of tomato production under favourable conditions
2020). Therefore, in this review we only discuss potential yield loss of (Alam et al., 2019). Tuta absoluta, for instance, globally has become a
major yield limiting fungal diseases. These diseases have been found to major threat to tomato production in just a few years. Today, it is
cause collectively 30-100% yield loss in tomato production in various considered the most invasive pest of tomato crop in countries across the
countries (Table 1). Mediterranean Basin, including Egypt, Bangladesh, Tunisia, Algeria,
As far as insect pests are concerned, Tobacco caterpillar, Spodoptera Libya, Morocco, and others (Haque, 2015). Tuta absoluta is one of the
litura Fab. (Lepidoptera: Noctuidae), pod borer, Helicoverpa armigera most important oligophagous pests of tomatoes in Bangladesh. This
Hub. (Lepidoptera: Noctuidae), whitefly, Trialeurodes vaporariorum causes 50-100% loss in yield production along with fruit quality in
Westwood, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) and leaf greenhouses and fields. A pest can damage plants by eating their various
miner, Tuta absoluta are prevalent insect pests of tomato crop

2
A.K. Pandey et al. Plant Stress 6 (2022) 100110

Table 3
Mode of action of FBCAs against major fungal pathogens of tomato crop.
Fungal agents Target disease Mechanism Reference

Trichoderma harzianum-T10 Alternaria solani
Trichoderma harzianum Fusarium oxysporum f.sp.
lycopersici
Clonostachys rosea IK726 Fusarium oxysporum f. sp. radicis-
lycopersici (Forl)
T. viride and Glomus spp. R. solani
T. atroviride and Fusarium oxysporum f.sp.
T. longibrachiatum lycopersici
Aspergillus tubingensis F. solani
T. hamatum 382 Xanthomonas euvesicatoria
F. oxysporum Fo47 (Non- Fusarium oxysporum f.sp.
pathogenic) lycopersici Fol8
Piriformospora indica Verticillium dahliae
Piriformospora indica F. oxysporum f. sp. lycopersici
Trichoderma viride Fusarium oxysporum and
Rhizoctonia solani
T. virens Soil borne pathogens
Upregulated of genes involved in auxin, ethylene and lignin pathways, and Pr-1 and Selim (2015)
Pr-5
Upregulation of salicylic acid (SA) or methyl jasmonate (MeJA), PR proteins, Zehra et al. (2017)
proline
Induction of SA and JA/ETH signalling pathways and PR-1a gene Kamou et al. (2020)
Total phenols content, defence enzymes like peroxidase, poly phenol oxidase Aboelmagd et al. (2021)
enzymes. PR proteins such as β-1,3 glucanase and chitinase
β-1,3-glucanase (PR-2) Sallam et al. (2019)
Glucose oxidase (GOD), by catalysing the oxidation of β-D-glucose into gluconic Kriaa et al. (2015)
acid and H2O2
JA- and SA-regulated, defence genes (41) including extensin and extensin-like Martinez-Medina et al.
protein genes. (2017)
ISR (unknown pathway) Olivain et al. (2006)
Increased production of antioxidants in roots and shoots Fakhro et al. (2010)
Increased production of antioxidants in roots and shoots Sarma et al. (2011)
Defensin genes (DF1 and DF2) Hafez et al. (2013)
Glycoside hydrolases and other related transporters Moran-Diez et al. (2015)

parts such as stems, leaves, buds, unripe & ripe fruits, as well as by
entering through the wounds made by the pest. In India, T. absoluta first
appeared infesting tomato fields in Maharashtra, and has since spread to
neighbouring states such as Gujarat (Ballal et al., 2016), Karnataka and
Tamil Nadu (Buragohain et al., 2021), Telangana and Andhra Pradesh
(Kumari et al., 2015). There is little way to envisage the exact route of
spread within India, but some possible causes include unrestricted
movement of agricultural commodities across states and wind currents
that disperse pests (Shashank et al., 2016). To reduce the use of synthetic
pesticides, tomato growers are eager to explore alternative options. This
has led to an increased interest in the use of formulated products of
beneficial fungi to combat pests and diseases of tomato crops because of
their effectiveness and eco-friendliness. Therefore, the present review
focuses on the efficacy of antagonistic and entomopathogenic fungi
(EPFs) against major insect pests and diseases of tomato crop.
3. Beneficial fungi for control of major diseases of tomato
Beneficial fungi having biological control attributes are increasingly
gaining importance due to the several benefits they provide to the plant
system as well as to the environment. Many species of fungi are recog­
nised as FBCAs with abroad range of bioactivity, which in turn reduces
the uses of synthetic pesticides in agriculture, thus providing advantages
to both human health and environment (Suarez-Lopez et al., 2022).
Food manufacturers are increasingly looking for ways to lower their
pesticide and fertilizer usage in order to produce safer foods. To do this,
FBCAs are being examined for use and understanding (Mugala et al.,
2022). Aside from direct effects on phytopathogenic agents, these
beneficial microbes may also produce antimicrobial, insecticidal, or
biostimulating metabolites. To date, the applications of fungal bioagents
to tomatoes has generally hiked significantly (Kabdwal et al., 2019). In
this context we have highlighted potential efficacy of various beneficial
fungi and underlying mechanisms accountable for their efficacy.
3.1. Direct suppression of the fungal phytopathogens
It is well known that tomato plant is prone to many diseases starting
from the seedling stage, in this stage it is highly prone to damping-off
and root rot. In particular, many species of the genus Trichoderma are
known to prevent plants against fungal soil-borne and foliar pathogens
(Alizadeh et al., 2020). Through mechanisms such as mycoparasitism,
competition, antibiosis, and induced systemic resistance (ISR), Tricho­
derma species control plant pathogens (Ghorbanpour et al., 2018).
Trichoderma harzianum, a potential FBCA can be able to suppress the
pathogen F. solani completely (100%) and can enhance the seed
germination upto 100% (Kareem and Matloob, 2019). Trichoderma iso­
lates can also suppress chromistan pathogen, P. aphanidermatum indi­
vidually or in the form of consortia. Various species of Trichoderma such
as T. harzianum, T. asperellum, and T. virens have been found efficient in
suppressing growth of P. aphanidermatum in the field when used as a
consortium by decreasing 57.2% root rot incidence over control
(Elshahawy and Mohamedy, 2019). Upon treating nursery beds with
T. asperellum there was 10.93% seedling mortality due to damping off
which was significantly lower than the control (26.98%) (Kumhar et al.,
2022). Direct mycoparasitism by coiling and disintegration of pathogen
hyphae has been considered the main antagonism mechanism of Tri­
choderma spp. They also produce various lytic enzymes capable of
degrading hyphal as well as resting structures. Trichoderma spp. are also
reported to produce various antifungal constituents viz., endo-chitinase,
trichodermin, β-1,3-glucanase, and β-glucosidase (Sain and Pandey,
2018).
Fusarium wilt of tomato causes heavy yield loss and becoming severe
year by year due to increase in the quantity of primary inoculum in the
fields because their resting chlamydospores escape various management
practices like chemicals. To some extent this issue can be tackled in a
sustainable way by using FBCAs which can even suppress chlamydo­
spores as well as mycelium (Jamil et al., 2021). FBCAs also reduce the
amount of inoculum production in plants by activating various defence
related pathways against pathogens. This could be a long-term option
for mitigation of this pathogen. In a study, A. niger, T. harzianum, and
T. viride evaluated against wilt pathogen were able to suppress pathogen
by 83.56%, 75.29% and 71.84%, respectively (Jamil et al., 2021).
Sometimes FBCAs have given sound results when they become a
component of an integrated disease management (IDM) system than
alone. In an experiment conducted by Dubey et al. (2020), soil appli­
cation and seedling root dip in a suspension of T. harzianum resulted
highest fruit number, shoot length, and weight along with the minimum
wilt incidence (0.5%) over control where 100% disease incidence was
reported (Dubey et al., 2020). Trichoderma harzianum also exhibited
potential antagonistic activity and disease controlling properties against
A. solani by various mechanisms (Sain and Pandey, 2016).
In another study, Xylaria feejeensis, an endophytic fungus recovered
from a mangrove tree was found effective against F. oxysporum and
A. solani (Brooks et al., 2022) with 60-75% antagonistic activity against
F. oxysporum and 56% to 87% antagonistic activity against A. solani. In
addition, soil treated with 10% concentration of this antagonist not only

3
A.K. Pandey et al.
reduced Fusarium wilt with 55.55% disease severity over control
(91.66%) but also encouraged growth of tomato plants in field condi­
tions (Brooks et al., 2022). They also identified 12 secondary metabo­
lites in this antagonist and found that especially mellein derivatives
were major components in X. feejeensis crude extract. It was concluded
that these compounds might be attributed for wilt controlling properties
(Brooks et al., 2022). In another study, Azadi et al. (2016) reported that
B. bassiana isolates TS7 and TS12 were found effective against
damping-off by induced systemic resistance and also produced peroxi­
dases (POX) and phenylalanine ammonia-lyase (PAL) enzymes along
with increase in plant growth attributes.
Another beneficial fungus, Acrophialophora jodhpurensis (syn. Chae­
tomium jodhpurense) controlled 60% wilt in tomato caused by R. solani
compared to control (Daroodi et al., 2021). Many studies reported that
Acrophialophora sp. can produce useful enzymes and also play an
important role in cellulose degradation. Production of pectinases, cel­
lulases, xylanases, β-mannanase, and some other antifungal compounds
were reported. Investigators found disintegration of mycelia due to this
antagonist in scanning electron microscopy (Fig. 1., Daroodi et al. 2021)
due to antifungal compounds produced by this antagonist. Besides,
comparing hyphal cells of the dual cultured pathogen with controls,
Daroodi et al. (2021) noticed changes in nucleus, cell membrane, cell
wall, nuclear membrane, parenthesome, septum, mitochondria, septal
pore, and cytoplasm (Fig. 2). Hassine et al. (2022) showed that cell-free
culture filtrates and organic extracts of Gliocladium spp. and Penicillium
sp. had antifungal efficacy against Colletotrichum coccodes, which causes
tomato anthracnose fruit rot. They found that isolate CH6 from Penicil­
lium sp. and Gc1 from G. catenulatum were the most active agents in
suppressing mycelial growth of pathogen and anthracnose severity.
Extracts of these both fungi were able to reduce the disease severity up
to 85% under in vivo conditions. They also examined if these treatments
had caused a significant morphological change in pathogen mycelium,
primarily a decrease in colony melanisation. Besides, some Aspergillus
species including A. tubingensis have also been found to be reduced grey
mould of tomato incited by Botrytis cinerea, which is a highly damaging
disease worldwide. Although Acrophialophora, Penicillium, and Asper­
gillus have been reported efficient against important pathogens of to­
mato and possess active metabolites, however, their commercialization
needs attention, as some species of Aspergillus cause human diseases like
aspergillosis (Zhao et al., 2018). Therefore, before recommendation and
commercialization of such beneficial fungal agents, toxicity tests are
required.
3.2. Induction of systemic resistance
To protect themselves from biotic stress, plants have a variety of
Fig. 1. Images showing effect of an antagonist, Acrophialophora jodhpurensis on disintegration in mycelial structure of R. solani under scanning electron microscopy
(SEM), R. solani hyphae in control (A) and the SEM of R. solani hyphae in dual culture with A. jodhpurensis (B) (Daroodi et al., 2021).
4
Plant Stress 6 (2022) 100110
effective constitutive and inductive resistance mechanisms. Plants show
a variety of protective responses in response to pathogen invasion,
including alteration in cell wall composition, antimicrobial secondary
metabolites stimulation and synthesis, including phytoalexins, stimula­
tion of defense-related genes, and formation of ROS (reactive oxygen
species) (Lehmann et al., 2015). Secondary metabolites like phenolic
compounds facilitate defense by providing mechanical strength and
stiffness to the cell wall, thus preventing pathogens from entering the
cell. Because tomato is susceptible to a variety of biotic stresses such as
bacteria, fungi, and viruses, chemical management has become a source
of concern in recent years, and there is a gap in chemical management of
plant viruses, biotic and abiotic induction of host plant defence mech­
anisms may be the best alternative management strategy (Meena et al.,
2022).
Different types of FBCAs have been shown to be effective in inducing
a defence response in plants (Fig. 3). Disease resistance can be induced
by a variety of eukaryotic fungi from the Hypocreales, Glomerales, and
Oomycete families, with the fungus Trichoderma being the most signif­
icant genus (Rey et al., 2017). Trichoderma species are well known for
their capacity to induce defence responses in a wide range of host sys­
tems. Trichoderma also includes a diverse range of plant
growth-promoting fungi that have been shown to protect plants from
soil-borne fungal diseases (Alizadeh et al., 2020). Trichoderma-induced
systemic resistance (TISR), which includes the salicylic acid (SA)
signaling pathway but is mostly based on increased Jasmonic acid
(JA)-dependent responses to diseases caused by necrotrophic pathogens,
is generated by biopriming plants with Trichoderma. Besides, various
plant hormones such as ethylene, salicylic acid, jasmonic acid, and
abscisic acid are required by defensive signalling networks for optimal
TISR development (Martnez-Medina et al., 2013). Tomato roots treated
with T. harzianum isolate changed the relative expression levels of eight
genes implicated in auxin, ethylene, and lignin processes in tomato
leaves (Martnez-Medina et al., 2013; Meena et al., 2022).
Furthermore, the expression levels of several PR-protein genes, such
as Pr-1 and Pr-5, were increased, implying that T. harzianum induced
systemic defence mechanisms (Selim, 2015). The use of bioagents like
Trichoderma to control F. oxysporum is an effective wilt disease man­
agement method (Sain and Pandey, 2016). The use of chemical inducers
in combination with beneficial fungi, on the other hand, is an intriguing
method because the combined treatment effectively boosts the plant
defence system against the pathogen causing wilt disease. In this regard,
Houssien et al. (2010) found that combining T. harzianum with salicylic
acid (SA) considerably improved plant defence against the wilt path­
ogen. Juber et al. (2014) investigated the effect of T. viride and chemical
compounds ASM (Acibenzolar-S-methyl) against Fusarium wilt of to­
mato and discovered that combining FBCA with chemical inducers led in
A.K. Pandey et al. Plant Stress 6 (2022) 100110

Fig. 2. Images showing effect of an antagonist, Acrophialophora jodhpurensis on disintegration in cell structure of R. solani under transmission electron microscopy
(TEM), R. solani in control (A & B) and the TEM of R. solani in dual culture with A. jodhpurensis (C & B) (Daroodi et al. 2021). N = nucleus; CW = cell wall; CM = cell
membrane; P = parenthesome; S = septum; SP = septal pore; M = mitochondria; and V = vacuole

Fig. 3. Three-way system plant-pathogen-antagonist interaction, how Trichoderma species can modulate the molecular signaling in the challenge between the
ascomycete pathogens, Fusarium and Alternaria and the host plant tomato.

a decrease in percent disease incidence as well as an increase in plant dry
weights. In a similar study, Zehra et al. (2017) found that T. harzianum,
alone or in combination with SA or methyl jasmonate (MeJA), could
activate the phenylpropanoid pathway and accumulate total phenolics.
This antagonist was also found to activate activities of PR proteins and
various defense-related enzymes, which were found to be highest at 72
hours, providing better protection against Fusarium wilt (Zehra et al.,
2017). Besides, they also found that tomato plants challenged with
F. oxysporum f.sp. lycopersici and treated synergistically with
T. harzianum and chemical elicitors (SA and MeJA) showed enhanced
level of antioxidant enzymes such as superoxide dismutase, scorbate
peroxidase, guaiacol peroxidase, catalase (except in SA treatment) and
ascorbate peroxidase (except in SA treatment). Some MAMP receptors,
such as endopolygalacturonase, cellulases, xylanases, ceratoplatanins,
peptaibols, and swollenin can also be stimulated by the genus Tricho­
derma (Shoresh and Harman, 2008).

5
A.K. Pandey et al.
In another study, Kamou et al. (2020) discovered that a fungal bio­
agent, Clonostachys rosea IK726, can endophytically colonise and trigger
systemic defence responses via the SA and JA/ETH signaling pathways
by activation of the SA-related PR-1a gene, offering protection to the
host from the early growth stages (Kamou et al., 2020). Induced resis­
tance in plants may occur as a result of various phenolic compounds
accumulation and the activation of various defence related enzymes
such as chitinases, β-1,3-glucanases, peroxidases, and polyphenol oxi­
dases, as well as other key enzymes in the isoflavonoid and phenyl­
propanoid pathways, which may play an important role in disease
control and pathogenic attack resistance in plants. In comparison to
control, both T. viride and Glomus spp. were able to increase overall
phenol content, as well as defence enzymes such as polyphenol oxidase,
peroxidase, and chitinase enzymes in the leaves of tomato plants. The
creation of PR proteins such as chitinase and β-1,3 glucanase aids in the
degradation of pathogenic mycelia’s lytic activity, and therefore their
concentrations rise (Aboelmagd and colleagues, 2021). Among PR pro­
teins, β-1,3-glucanase (PR-2) is one of the most significant, as it inhibits
the growth of various plant pathogens directly. In light of this, Sallam
et al. (2019) tested T. atroviride and T. longibrachiatum for their ability to
induce β-1,3-glucanase (PR-2) and discovered that these two Tricho­
derma species can considerably induce PR-2 and suppress the wilt
pathogen. A. tubingensis, which produces glucose oxidase (GOD) by
catalysing the oxidation of d-glucose into gluconic acid and H2O2, has
become popular and frequently employed as an antimicrobial agent in
recent years. The proliferation and virulence of some plant pathogens,
such as F. solani, are influenced by elevated H2O2 and lowered pH (Kriaa
et al., 2015).
In Martinez-Medina et al., 2017, reported that using T. hamatum with
decomposed peat mixture provided considerable defense against Xan­
thomonas euvesicatoria that causes tomato bacterial spot. In Tricho­
derma-induced plants, they also looked at the SA-and JA-regulated
defence pathways to see how T. hamatum can minimise pathogen in­
vasion through multiple mechanisms. Tomato leaves were examined for
the expression pattern of 164 genes using high-density oligonucleotide
microarrays to investigate the methods through which T. hamatum 382
produced resistances. The findings demonstrated that the expression of
several genes was constantly changing in T. hamatum 382. Across the
treatments, there were 45 genes identified as being differentially
expressed. There are 41 genes that fit into at least one of the seven
functional categories. T. hamatum 382 also promoted the expression
pattern of four extension and genes replicated to extensin-like protein in
tomato plants (Alfano et al., 2007).
When Trichoderma spp. applied with Penicillium sp., it also showed
potential efficacy in disease management (Latha et al., 2011). Pythium
oligandrum is a mycoparasitic oomycete that has also shown biocontrol
effectiveness against phytopathogens related to the tomato (Rey et al.,
2017). P. oligandrum colonises tomato root tissues quickly and thor­
oughly, similar to pathogenic Pythium spp., although colonisation is not
linked with host wall breakage or host cell changes, and is followed by
induction of various broad host defence mechanisms. Researchers
discovered that P. oligandrum cell wall protein fraction comprising two
elicitin-like proteins, POD-1 and POD-2 (Takenaka et al., 2011), elicited
defence reactions in tomato plants. Some non-pathogenic isolates of
F. oxysporum have also been used as FBCAs to control Fusarium wilt in
tomatoes by triggering positive defence responses (Olivain et al., 2006).
Using Pythium and Fusarium as FBCAs, on the other hand, is difficult
because the same species or others have been discovered pathogenic to
tomato plants (Sain and Pandey, 2016).
Plant immunological responses can also be induced by several
ectomycorrhizal fungi and arbuscular mycorrhizal (AM) fungi that
belong to Glomeromycotina (Rey et al., 2017). A root endophytic fun­
gus, Piriformospora indica, possesses plant growth-promoting properties
(Lahrmann et al., 2013). In tomatoes, this fungus has been found to
diminish disease symptoms produced by F. oxysporum (Sarma et al.,
2011) and Verticillium dahliae (Fakhro et al., 2010). The pattern of
6
Plant Stress 6 (2022) 100110
colonisation of P. indica on tomato roots has yet to be determined.
Nevertheless, a general statement based on other findings appears to be
that there are two main symbiotic periods (Vos et al., 2014). The hostile
pathogen must escape or inhibit in some way the whole complex of plant
defensive measures, including physical barriers and various secondary
metabolites and antimicrobial compounds produced by plants, in order
to successfully invade a potential host (Bruce and Pickett, 2007).
Plant defence genes code for proteins that help plants defend
themselves. UDP-glucosyltransferase, transcription factors like ERFs and
WRKYs, hormones, calcium signal transducer, peroxidase, PR proteins,
and lignin synthase are all possible precursors and encoded proteins
(Wang et al., 2015). Hydroquinone that is dependent on UDP-glucose:
Arbutin synthase (O-glucosyltransferase) is a glycosyltransferase that
catalyses the production of arbutin in flowering plants, which possesses
antifungal and antibacterial properties. The first enzyme in the pro­
duction route of JA is LOX1, which encodes lipoxygenase (Reymond and
Farmer, 1998). Plant adaptation to pathogen attack and herbivore, as
well as various other challenges like abiotic factors such as ozone and
UV radiation, is regulated by JAs, which are lipid-derived stress hor­
mones. Genes encoding coronatine-insensitive 1 (COI1), leucine
aminopeptidase, and allene oxide cyclase (AOC) are required for proper
JA signaling pathway function in tomato (Fowler et al., 2009). In
particular, COI1, which codes for a protein which binds to the negative
regulator (also known as JAZ protein) of JA-responsive genes, is an
important component of the JA receptor (Katsir et al., 2008). AOC, on
the other hand, catalyses the synthesis of cis-(+)-12-oxophytodienoic
acid, a key step in the biosynthesis of jasmonates (Stenzel et al., 2008).
CTR1 also inhibits and switches off ET signaling pathways, preventing
interference. CTR1 which is produced by ETR gene, contains kinase
activity in its C-terminal domain, which is necessary to make CTR1
functional and its interaction with ET receptor (Huang et al., 2003).
ISR is influenced by a number of transcription factors. ERF family
members are transcription factors that are involved in the SA or ET/JA
signalling pathways and generate resistance or tolerance responses in
plants to biotic and abiotic stressors, respectively (Abbasi et al., 2020).
The transcriptional alterations of a few selected genes in two plant tis­
sues revealed that the plants reacted differentially to H2O2 build-up and
the ERF gene expression ratio. The ERF gene’s expression pattern may
differ in plant tissues, as well as in response to different pathogens and
combinations of bioagents (Abbasi et al., 2020). Genes that belong to the
PR12 family, a group of proteins known as defensins, are also identified
from tomato plants. The PDF1.2 gene in tomatoes has been demon­
strated to play a role in flower development as well as resistance to
B. cinerea (Stotz et al., 2009).
Peroxidase is an oxide-reductive enzyme that helps in the manufac­
ture of cell wall polysaccharides. Peroxidase affects the phenols oxida­
tion, lignification, and suberization of host plant cells and tissues during
the pathogen defence response (Chittoor et al., 1997). In Moran-Diez
et al., 2015, used hybridization on microarrays of 11645 designed oli­
gonucleotides to evaluate gene expression in T. virens (cultured along
with tomato). They discovered that differentially expressed genes were
mostly related to enzyme synthesis, transporters, and small secreted
proteins, with glycoside hydrolases being the most abundant, implying
that they play a significant role in the host cell walls metabolism during
fungi colonisation of the outer layers of roots. The plants altered the
fungal transcriptome for their own benefit, as evidenced by expression
pattern of host-specific gene (Shikata and Ezura, 2016).
To further understand the molecular pathways involved in interac­
tion between tomato and T. longibrachiatum under lab conditions, De
Palma et al. (2016) used the suppression subtractive hybridization
approach. The subtractive library revealed the presence of forty distinct
transcripts based on observations and sequence analysis. The findings
suggested that this fungus may boost plant disease resistance by stim­
ulating cell defences and fundamental plant metabolic processes. To
promote and support tomato research, a Micro-Tom mutant database
called "TOMATOMA" has been established in Shikata and Ezura, 2016.
A.K. Pandey et al.
Plant mutants with a deficiency in a defensive gene can be used to un­
cover gene function in pathogens. cv. NahG-Moneymaker, a
JA-insensitive mutant of the tomato NahG-Moneymaker, which cannot
accumulate SA. Micro-Tom (jai1-Micro-Tom), Nr-Rutgers (an
ET-insensitive mutant), and Micro-Tom (jai1-Micro-Tom) are three
popular mutants according to Arie et al. (2007). The associated genes
and transcription factors (for example, ERF) can be altered, and mutants
with variable responses should be tested against diverse diseases in
future research.
4. Beneficial fungi for control of major insect pests of tomato
crop
About 700 species in the kingdom fungi are putative entomopath­
ogens. Fungi used for IPM belong to four major orders namely, Neo­
zygitales, Entomophthorales of Entomophthoromycota, Onygenales and
Hypocreales of Ascomycota (Mora et al., 2017). Researchers have been
studying EPFs for several decades, including their ability to control in­
sect and mite pests, promote plant growth, and provide a number of
other benefits to crops in addition to controlling pests. An
agro-ecosystem where RH is over 80% is best suited for EPFs (Sain and
Pandey, 2016). Rhizosphere of major tomato growing countries feature
a diversity of EPFs, and some as endophytes (Canassa et al., 2020). In
general, EPF thrive at higher humidity, and tomato plants are an ideal
microclimate for their multiplication and growth. However, very few of
them have been used as bioformulations for controlling insect and mite
pests. Overall, Akanthomyces lecanii (Zimm) Spatafora (formerly known
as Verticillium lecanii Zare & Gams), Akanthomyces spp. (syn. Cepha­
losporium spp.), Beauveria spp., Cordyceps spp. (formerly known as Pae­
cilomyces sp.), Metarhizium spp., and Purpureocillium sp. have been
deployed as bio-insecticides for reduction of insect pests’ populations
(Mugala et al., 2022). Some of them are discussed in this review.
4.1. Beauveria bassiana s.l
There has been a great deal of interest in Beauveria bassiana s.l. as a
mycopathogen of insects and mites, which is employed as a fungal
insecticide against the pests affecting tomato crop. In both laboratories
and in the field, B. bassiana s.l. has been tested for its pathogenicity
against several tomato pests (Wei et al., 2020). Beauveria bassiana s.l. is a
widely used fungal entomopathogen against many of the insect pests like
thrips, aphids, lepidopteran insects etc. It comes in contact with insects
and causes infection in suitable environmental conditions. In the labo­
ratory when B. bassiana s.l. was tested against Bemisia tabaci, it causes
62.7-97.3% mortality in adults after the 7th day of treatment (Abdel-­
Raheem and Ahmed, 2017). Further, field application of B. bassiana s.l.
resulted in 90-92% reduction in whitefly/leaf in tomato in greenhouse
conditions (Abdel-Raheem and Ahmed, 2017).
In addition, field experiments with this EPF have also shown prom­
ising results to manage H. armigera in tomato. When three sprays of
B. bassiana s.l. and M. robertsii (syn. M. anisopliae s.l.) were applied at 2
× 109 spore/ml, both fungi caused 68% larval mortality in field followed
by A. lecanii with 2 × 109 spore/ml causing 64.20% mortality which
emphasises the potency of these fungi in field conditions (Kumar et al.,
2016). It is reported that some of the strains are endophytic in nature
and metabolites produced by them inside plants might be harmful for
the insect pests on the plants (Jaber Lara and Ownley, 2017). Endo­
phytic establishment of B. bassiana s.l. Bb 115 isolate at 1 × 109 con­
idia/ml concentration could reduce the mean survival times (MST) and
leaf consumption by 3rd-instar H. armigera larvae on tomato (Toffa et al.,
2021). Similarly, WG-40 isolate (isolated from a wild tomato plant) of
B. bassiana s.l. was found to be very effective compared to other two
isolates (WG-14 and WG-1 isolated from soil) to cause highest mortality
in 2nd instar of H. armigera when carried out by root dip method
(Qayyum et al., 2015). The variations in pathogenic activity of isolates
might be due to their origin from different geographical regions or
7
Plant Stress 6 (2022) 100110
differential behaviour towards insects.
Beauveria bassiana (isolates lot TGAI 97-10-1, GHA) and Cordyceps
fumosoroseus (Wize) Brown & Smith (isolates lot 940917, 612) at
respective concentration of 1.4 × 1011 and 1.8 × 1011 conidia/ml were
found to be more effective against the 3rdinstar nymphs of whitefly,
Trialeurodes vaporariorum reared on cucumber than reared on tomato
plants (Poprawski et al., 2000). It could be due to the presence of alpha
tomatine (steroidal form of tomatine) which is known for antifungal
properties. One of the field studies conducted in Nepal found the various
formulations of EPFs such as Bio Magic (M. robertsii), Mealikil (A. lecanii)
and Bio Power (B. bassiana s.l.) were found effective against whitefly in
tomato killing, 91.64%, 93.55% and 88.91% population of nymphs,
respectively (Sharma et al., 2015).
There are reports on EPFs targeting different stages of T. absoluta. Its
pupae are found in the soil, within mines or on the leaves of plants.
Targeting pupae could help to reduce population size of this pest.
Beauveria bassiana s.l. emulsifiable suspensions have been reported to
cause 98.8% pupal mortality of 2-3 days old pupae and approximately
70% of six-day-old pupae of T. absoluta (Erasmus et al., 2021).
Furthermore, the emerged moths from treated pupae showed very less
fecundity and helped in reducing the subsequent generation of this pest
(Erasmus et al., 2021). Similarly, in greenhouse study, B. bassiana s.l.
together with M. robertsii at concentration of 2.5 × 109 conidia/ml
caused 84.04% and 76.31% larval mortality on 10th day after treatment
application (Tadele and Emana, 2017). Abdel-Raheem et al. (2015)
found effectiveness of these both entomopathogens against egg and
neonate of T. absoluta when used at higher concentration (107con­
idia/ml). Moreover, B. bassiana s.l. has also found to be decreased egg
hatching of tomato pinworm (Abdel-Raheem et al., 2015).
The genus Beauveria is compatible with synthetic insecticides/acar­
icides but not with synthetic fungicides, according to several research.
For example, Shi et al. (2005) found that during testing against eggs of a
spider mite, T. cinnabarinus Boisduval (Trombidiformes: Tetranychidae),
pyridaben, hexythiazox, and propargite were found to be extremely
compatible with B. bassiana s.l. In contrast, Liu et al. (2012) investigated
the effects of six insecticides and fungicides against B. bassiana s.l. and
reported that all synthetic pesticides, including carbendazim, mancozeb
(fungicides), imidacloprid, bifenthrin (insecticides), and qingyuanbao,
veratrine (veratrine), had an inhibitory effect on EPFs. At lower doses
than those commonly employed, bifenthrin, on the other hand, had no
influence on the mycelial proliferation of B. bassiana s.l. More study is
needed in this area to find more acceptable pesticides that may be
employed as part of integrated pest management strategies when
Beauveria alone fails to control insect and mite pests, in order to improve
the bio-efficacy of FBCAs.
4.2. Metarhizium robertsii
In varied crops, the genus Metarhizium has shown potential patho­
genic activity against a variety of foliar and soil-dwelling insect pests,
including tomato. Green muscardin fungus, M. robertsii is a potent
biocontrol agent against eggs, larvae and pupae of tomato pinworm. The
sub-lethal concentration of M. robertsii (isolate DEMI 001) affected
biological parameters like developmental period (from egg to puape)
fecundity, longevity and various life table parameters of T. absoluta
(Alikhani et al., 2019). Pupal stage of the T. absoluta was found to be
controlled by using M. robertsii at concentration of 4.46 × 109 viable
conidia/ml when applied together with irrigation water (Contreras
et al., 2014). In Ethiopia, three strains of M. robertsii (AAUM78,
AAUM39 and AAUM 76) proved to be pathogenic to cause 88-95% and
90-95.7% mortality against 2nd and 3rd larval instars of T. absoluta,
respectively (Ayele et al., 2020). Similarly, commercial formulation of
EPFs (strain J25 Beauvitech® WP: B. bassiana and Strain FCM Ar 23B3,
Metatech®WP: M. robertsii) were found effective in reducing leaf and
leaflet damage due to T. absoluta (Ndereyimana et al., 2020). Meta­
rhizium robertsii was also found effective in reducing larval population of
A.K. Pandey et al.
H. armigera in tomato and reduction in fruit damage to the tune of 87
percent (Phukon et al., 2014). Some other M. robertsii isolates those have
been used with B. bassiana s.l. against major tomato pests are described
under Beauveria section.
4.3. Other EPFs infecting insect pests
Several Cordyceps (=Paecilomyces spp.) species, like C. fumosorosea
and C. tenuipes (Peck) Kepler, have been used against insect and mite
pests of many crops, although only a few species have been tested
against tomato insect pests. Cordyceps fumosorosea previously known as
Paecilomyces fumosoroseus is a fungus reported to infect B. tabaci (Pan­
yasiri et al., 2007). The isolate FWA3 of this EPF was found to be
effective against both whitefly and thrips in tomato under net house
conditions (Panyasiri et al., 2007). For thrips (Ceratothripoides claratris),
conidial suspensions of isolate FWA3 at concentration of 5 × 109 con­
idia/ml caused 80.7% mortality in thrips and at 6.85 × 109 conidia/ml
caused 92.6% mortality of B. tabaci (Panyasiri et al., 2007). Cordyceps
fumosorosea has also been found to cause 70% percent nymphal mor­
tality of B. argentifolii Bellows and Perring in tomato within a week of
treatment (Vidal et al., 1998). After three spraying, both A. lecanii and
M. robertsii at the concentration of 1 × 109 spores/ml caused 100% and
76.2% mortality of whitefly in tomato under greenhouse conditions,
respectively (Abdel-Raheem and Ahmed, 2017). Abdel-Raheem et al.
(2015) observed pathogenicity of A. lecanii on the neonate and third
larval stage of T. absoluta. A recent report also found that A. lacanii was
pathogenic on B. tabaci infesting tomato plants (Keerio et al., 2020). The
variability in the pathogenic activity of Cordyceps sp. and Acanthomyces
sp. might be due to presence of various active metabolites present in
them, and their mode of action on insect body.
5. Beneficial fungi for plant growth promotion
FBCAs are known to produce many growth hormones including
auxins, cytokinins, and gibberellins, which are utilised to control pests
and diseases of tomato crop (Paramanandham et al., 2017). These hor­
mones play an important function in both growth inhibition of patho­
gens and encouragement of host plant growth. In the present
environment, various beneficial fungi have been used as soil or plant
inoculants in different crops including tomato. These bio-inoculants also
function as growth regulators along with biotic stress management
(Singh et al., 2017; Raymaekers et al., 2020). Several studies on use of
fungal antagonists (Trichoderma spp., and Xylaria spp.) and entomo­
pathogens (Beauveria sp., Metarhizium sp. etc.) have been conducted for
their deployment as growth promoters along with pest controlling
properties. One study found that Xylaria feejeensis along with control of
early blight and Fusarium wilt in tomatoes, significantly increased
growth of plants (Brooks et al., 2022). Likewise, You et al. (2016) also
observed that application of T. koningiopsis increased seedling height,
number of leaves, diameter of stem, and fresh weight of plants.
Köhl et al. (2020) used 100 fungal and bacterial isolates to assess
their growth promoting properties and found that only Alternaria sp.
isolate was capable of promoting tomato plant growth and yield. How­
ever, it remains controversial to use Alternaria species as growth pro­
moters, as they cause early blight disease (Pandey et al., 2021). In a
study conducted in 2018, among 58 isolates of Trichoderma, Li et al.,
2018. found plant growth promoting activity in terms of plant height
only with T. asperellum along with its Fusarium wilt controlling prop­
erties. However, researchers found the poor efficacy of T. asperellum
over bacterial antagonist, Bacillus subtilis (Kipngeno et al., 2015) and
B. amyloliquefaciens (Chien and Huang, 2020) in terms of increasing P, K,
and Mg contents in tomato plants and other plant growth promoting
attributes. In another study, Bader et al. (2020) reported that
T. harzianum was a potential agent than T. brevicompactum and T. gamsii
in terms of increasing chlorophyll content, shoot length, fresh and dry
weight of shoot and roots. T. harzianum also increased tomato yield in
8
Plant Stress 6 (2022) 100110
comparison to control plants when applied in combination with my­
corrhiza (AMF) + Pseudomonas fluorescens. Conversely, Jamil (2021)
reported that in comparison to T. harzianum, T. viride enhanced higher
plant growth and yield parameters. The variation in efficiency might be
due to variations in volatile compounds found in Trichoderma species.
Prabhukarthikeyan et al. (2014) used a combination of endophytic
Bacillus and B. bassiana s.l. to assess their Fusarium wilt controlling and
growth-promoting properties and found that a reduction in the inci­
dence of wilt (90.9%) and also higher growth attributes compared with
control. In a study published in Elena et al., 2011 found that M. robertsii
strain Ma8 was effective in terms of increasing plant height (P <
0.0001), root length (P = 0.0002), shoot (P < 0.0001) and root (P <
0.0001) dry weight. In another study, Ownley et al. (2008) reported that
B. bassiana s.l. protects tomato plants against R. solani and Pythium
myriotylum with increased yield over control. Similar studies by Deb and
Dutta, (2021) reported that among 22 native isolates of B. bassiana s.l.,
isolate BP1.1 was a potential agent with 33.45% disease incidence due
to Pythium myriotylum, higher germination percentage of seedling
(87.34%), and also produces enhanced level of amylase, caseinase,
chitinase, cellulase, lipase, and protease. Culebro-Ricaldi et al. (2017)
reported that in comparison to three strains of B. bassiana s.l., strain
1215 was found efficient against Fusarium wilt with 72% disease control
and also promotes plant growth parameters. In a similar line, Shriv­
astava et al., (2015) reported that the combination of arbuscular
mycorrhizal fungus and B. bassiana s.l. induces levels of terpenoids.
Besides, Clark (2006) reported that B. bassiana s.l. was found effective
against Pythium damping-off by induce systemic resistance and also
increase in stem diameter. Thus, these studies suggest that FBCAs like
Trichoderma and Beauveria have multi-fold actions, i.e., along with dis­
ease control Trichoderma also induces growth of tomato plants in various
aspects. Likewise, Beauveria along with insect controlling properties,
also possess disease controlling and growth promotion activity. There­
fore, these fungal agents can be used as biopesticides and growth
enhancer for tomato crop.
6. Advantages in using beneficial fungi over synthetic pesticides
Worldwide, yield production of tomatoes is limited by several pests
and diseases. Furthermore, the majority of synthetic pesticides used in
tomato production have minimal effects on natural enemies, entomo­
pathogens, microbial antagonists, and phytotoxicity (Phukon et al.,
2014). Nevertheless, regular usage of synthetic pesticides may interrupt
the natural balance between tomato pests and parasitoids and predators.
In the tomato field, parasitoids and predators assist as macrobial agents
against various insect and mite pests for safeguarding ecological bal­
ance, henceforth termed biological indicators (Qayyum et al., 2015).
Unfortunately, there are few reports available that evidenced synthetic
pesticides have harmful impacts on FBCAs (Schutter et al., 2002) and
natural enemies found in tomato fields (Consoli et al., 1998). For
example, Miranda et al. (2005) reported that excessive use of synthetic
pesticides severely reduced the population of predators like Anthicus sp.
(Coleoptera: Anthicidae), Orius sp. and Xylocoris sp. (Hemiptera:
Anthocoridae), Staphylinidae spp. (Coleoptera), Cycloneda sanguinea (L.)
(Coleoptera: Coccinellidae), and parasitoids (Bracon sp. and Chelonus
sp.), and Trichogrammatidae, Trichogramma pretiosum Riley.
In addition, crop pests and pathogens have started evolving resis­
tance to fungicides and insecticides due to climate change. For example,
in an experiment Ghosal et al. (2020) found that F. oxysporum isolates
displayed tolerance to carbendazim (1.2 mg/l) and thiophanate methyl
(100 mg/l) with less effectiveness was observed for thiophanate methyl
in terms of conidial inhibition. Likewise, in Brazil, T. absoluta developed
resistance to Pyrethroids and Organophosphates (Haddi et al., 2012;
2017), Indoxacarb (Roditakis et al., 2017a), and Diamides (Roditakis
et al., 2017b). In addition, H. armigera has also shown insecticides
resistance towards abamectin, deltamethrin, and profenofos in Senegal
(Sene et al., 2020), and Spodoptera frugiperda towards diamides in
A.K. Pandey et al.
Germany (Boaventura et al., 2020). However, excessive use of synthetic
fungicides and pesticides has resulted in higher crop production costs
and several negative effects on both the environment and humans, and
the demand for pesticide-free, high-quality tomato fruits has prompted a
shift towards non-chemical pest management and long-term tomato
production (Moura et al., 2020). Alternative management strategies
with negligible harmful effects on useful macrobials and microbials,
eco-friendly and cost-effective mitigation approaches for both posts and
diseases in tomato, and beneficial fungi are desirable in this regard, have
been implemented to return the production and sustainability of soil as
well as plants.
As like several other crops, tomato crop is also considered highly
suitable for biological management programs using fungal entomo­
pathogens and antagonists. The EPFs deployed as commercial bio-
insecticides are non-pathogenic to insect specific predators and para­
sitoids. For example, Cordyceps spp., Hirsutella spp., B. bassiana s.l., and
M. robertsii. were non-pathogenic to Dicyphus tamaninii Wagner (Heter­
optera: Miridae), Coccinella septempunctata L. (Coleoptera: Coccinelli­
dae), Chrysoperla carnea Stephens (Neuroptera: Chrysopidae),
S. gilviforns and Oxyopes sp. (Araneae: Oxyopidae) (Mamun et al., 2014)
and against a beneficial soil insect, Heteromurus nitidus Templeton
(Entognatha: Entomobryidae) (Portilla et al., 2017), since after field
application, these natural enemies had no effect on population levels.
More recently, Corallo et al. (2021) found non-significant effect of
B. bassiana s.l. and M. robertsii on the coccinellid and lacewing predators
of Diaphorina citri Kuwayama (Hemiptera: Liviidae), suggesting that EPF
and predators had compatible effects. Ullah et al. (2019) made similar
observations and proposed that C. fumosorosea, in conjunction with the
predator, might be utilised to improve the biological control of S. litura
in commercial crops. B. bassiana s.l., a broad-spectrum EPF, has proven
nontoxic to apiculture, according to Peng et al. (2020). This indicates
that the EPF may be extremely specialised, infecting only a specific sort
of host.
Conversely, few studies evidenced that M. robertsii was pathogenic to
D. tamaninii and C. carnea with 10% and 4% mortalities, respectively as
reported by Thungrabeab and Tongma (2007). As a result, before EPFs
are recommended as bioinsecticides, they must be tested against natural
enemies. Furthermore, since the European Union (EU) has established
severe limitations on the use of synthetic pesticides in tomato crop, the
presence of maximum residue limits of synthetic pesticides in tomato
and related products is currently a global concern. The EU has set
maximum residue limits (MRLs) for routinely used pesticides (ranging
from >0.01 to 0.15 mg/kg) that will not be met in practice. As a result,
in tomato exporting countries like China, India, USA, Turkey, and Egypt
and others, complying with an MRL set for pesticides as a food safety
norm is a huge difficulty. FBCAs are compatible with natural enemies
and particular pesticides, according to the research papers reviewed,
and may have a role in plant growth promotion. As a result, using FBCAs
in between fungicide/insecticide applications could be a viable option
for lowering pesticide residue levels in tomato crop. Insecticide residual
levels in tomatoes have frequently exceeded EU standards (Wu et al.,
2020). As a result, very limited use of chemical pesticides is recom­
mended, with a focus on IPM, so that native beneficial fungi and natural
enemies found in the rhizosphere of tomato crop can be conserved for
long-term crop protection.
7. Conclusions and future perspectives
The hunt for beneficial fungi, their diverse formulation processes,
mass production, and applications in tomato crop have all progressed
significantly in recent years, as numerous researchers have reviewed
(Culebro-Ricaldi et al., 2017). As a result, these commercially available
antagonists and EPFs could be employed as environmentally friendly
and safer bio-pesticides against pests and diseases, as well as one of the
key wings of an IPM strategy to reduce synthetic insecticides and fun­
gicides burden in the tomato crop. Yet, some gaps will need to be filled
9
Plant Stress 6 (2022) 100110
in the future. Traditional and molecular methods were used to discover
the FBCAs described in this work, includes sequencing of the ITS regions
and conserved genes like translation elongation factor 1 alpha and beta
tubulin, as well as numerous markers (Hassan et al., 2019). The
increasing use of omics technologies such as genomics, metabolomics,
and proteomics, on the other hand, will modernise our understanding
with respect to interactions of insects/pathogens with beneficial fungi,
influencing decisions, particularly during selection of antagonist/EPF,
and future biological control strategies. If FBCAs are accepted by a
diverse set of tomato producers, this knowledge will be beneficial in
generating regulatory genetic changes to improve their tolerance and
potency. The mode of action of fungal antagonists and EPFs and related
active metabolites has been investigated against pests and pathogens in
numerous food crops (Vinale and Sivasithamparam, 2020), but study on
the tomato crop has been restricted, and more research is needed. More
efficient isolates of beneficial fungi/FBCAs with multi-fold action can be
found in the tomato rhizosphere soil, which can then be mass multiplied
in the lab before being used in the tomato field. EPFs like M. rileyi
(Farlow), Kepler, Rehner, and Humber (formerly in the genus Spicaria,
Botrytis, or Nomuraea), as well as the genus Hirsutella species, have been
deployed against lepidopteran insect pests damaging a variety of food
crops (Fronza et al., 2017). Nonetheless, none of these EPFs have been
tested against tomato pests, and this is something that has to be
addressed in future study.
In addition to commercial insecticides/fungicides, biological man­
agement of biotic stressors in tomato crop has been established. Many
EPFs and fungal antagonists have been investigated with positive results
in many major tomato-growing nations, either in conjunction with
synthetics or on their own (Panyasiri et al., 2007; Bader et al., 2020).
Many reports show that FBCAs used for traditional biocontrol reduced
the populations of target insect pests and phytopathogens into control­
lable levels, but additional quantitative post-introduction analyses are
desirable. Furthermore, research on the long-term durability of benefi­
cial fungi used in traditional pest and disease management is needed to
answer concerns that they can easily transfer to new hosts on ecological
timescales after being introduced in the tomato rhizosphere. Making and
distributing FBCA-based bio-pesticides in underprivileged countries
under the leadership of non-profit organisations should be explored
further. Similarly, exploitation of M. robertsii, B. bassiana s.l., and
A. lacanii for pest control and Trichoderma for major disease manage­
ment is a promising study topic in tropical and subtropical
tomato-growing countries.
In addition, study should be focused on discovering bioactive
chemicals from efficient beneficial fungi and then using them to treat
tomato pests. Furthermore, before commercialization and advice to to­
mato producers, toxicity tests for newly found FBCAs such as Xylaria
spp. and other ascomycetes should be done. Finally, the reviewed study
indicates that EPFs like Beauveria, Metarhizium, Acanthomyces, and
Cordyceps, as well as antagonists like Trichoderma spp., have a lot of
promise for bio-pesticide synthesis and subsequent usage in tomato for
management of major pests and diseases, and for growth promotion.
When compared to other management options, FBCAs are safe, natural,
and cost-effective. The early registration and patenting of these FBCAs
having fungicidal/insecticidal properties will allow for their de­
ployments in future that will also make rich microbial diversity of the
tomato rhizosphere.
Declaration of Competing Interest
Authors declare no conflict of interest.
Acknowledgements
Authors are thankful to Department of Biotechnology, Government
of India for providing grant through Biotech-KISAN Program (BT/KIS/
123/SP45224/2022) for this crop.
A.K. Pandey et al. Plant Stress 6 (2022) 100110

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