Fungal entomopathogens: a systematic review

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Sharma and Sharma Egyptian Journal of Biological Pest Control
https://doi.org/10.1186/s41938-021-00404-7
                                                                                (2021) 31:57
                                                                                                                                   Egyptian Journal of
                                                                                                                                Biological Pest Control

 REVIEW ARTICLE                                                                                                                                     Open Access

Fungal entomopathogens: a systematic
review
Rajat Sharma1*         and Priyanka Sharma2

  Abstract
  Background: Apprehensions about the safety and the environment regarding the insecticidal application against
  insect infestations have directed our attention toward advancement of biological mediators so that they are
  assimilated into the concept of integrated pest management stratagems to develop a more practical approach for
  the management of insect pests. Management of insect pests by making use of biological approaches (such as
  fungal entomopathogens (EPF) or others which are antagonistic to insect population) provides a substitute
  approach which reduces the continuous use of chemical amalgams against insect pests.
  Main body: The present review provides a framework of the present status of information on EPF as it identifies
  with their current use as biological control of pest infestations. To utilize a variety of biological control
  methodologies against insect hosts, it is essential to improve our comprehension of the ecology of EPF and also
  their role in nature. This article may assist us with understanding the virulence and the virulence factors related
  with EPF and present the latest developments and accomplishments in the significant field. We focus on recent
  instances of studies that show the overall patterns in interactions among insect pests and EPF prompting the
  advancement of epizootics. Also, we sum up the topical discoveries on current status of mycoinsecticides and
  propose future research needs.
  Conclusions: As the current mechanism of fungal pathogenesis on insects is moderately slow and needs
  improvement, there is likewise the requirement for additional comprehension of the interactions among
  entomopathogens and insect pests so as to grow soundly planned procedures by identifying potential targets and
  via the improvement of fungal strains for improving the adequacy of these organisms in field applications.
  Keywords: Entomopathogenic fungi, Biological control agents, Infection process, Enzymes, Pathogenesis, Host
  defense, Epizootiology, Mycoinsecticides

Background                                                                             suppressing the insect pest infestations due to their ab-
Insect pests are regarded as major deterrents which have                               stemiously minimal application effort, high usefulness
accounted for an estimated 10.80% crop losses on global                                and expediency (Sharma 2019), but concentrated appli-
scale in the era of post green revolution (Dhaliwal et al.                             cation of chemicals has brought about the advancement
2015). Also, an estimated loss of global annual crop pro-                              of resistance to either one or even more classes of insec-
duction corresponding to 18-26% valued at $470 billion                                 ticides in as much as 500 species of pests (Kumar and
has been observed recently (Mantzoukas and Eliopoulos                                  Kalita 2017).
2020). To reduce these losses, insecticides are employed                                  As a result, the microbial agents (entomopathogens)
and, as a result, have become an essential method for                                  are viewed as regulatory operators of pest infestations
                                                                                       and represent the different species of fungi, viruses,
* Correspondence: sharmarajat.ysp@gmail.com
                                                                                       protozoa, and bacteria. Initial studies in reference to
1
 Department of Plant Pathology, Dr. YS Parmar University of Horticulture and           entomopathogens were carried out by Agostino Bassi
Forestry, Nauni, Solan, Himachal Pradesh 173230, India                                 who established that the infectious agent, instigating the
Full list of author information is available at the end of the article

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Sharma and Sharma Egyptian Journal of Biological Pest Control   (2021) 31:57                                          Page 2 of 13

occurrence of muscardine disease in case of silkworms                 thus, the life cycle of entomopathogenic fungi is contin-
was Beauveria bassiana Bals. (Hypocreales: Cordycipita-               ued on new hosts.
ceae). Entomopathogens which befall naturally are sig-                  EPF also play an important role as either colonizer in
nificant controlling factors against insect populace (Roy             rhizosphere (Pava-Ripoll et al. 2011) or plant growth
and Cottrell 2008). Tanzini et al. (2001) used the term               promoters (Jaber and Enkerli 2017). EPF account for the
entomopathogenic for the micro-organisms which regu-                  principal number of taxa as in the diverse group of
late the population of insect pests to the levels wherein             fungi, there are more than 100 genera of EPF comprising
no economic damage to crop plants is observed. Delgado                of 750-1000 (St Leger and Wang 2010). The multi-
and Murcia (2011) defined the term in relation to the                 layered jobs played by EPF could likewise be utilized in a
microbial populace which is proficient in attacking in-               roundabout way as biofertilizers (Jaber and Enkerli
sect pests by incorporating them into their own life cycle            2017), and microbial control specialists in contradiction
and by utilizing them as hosts and also classified these              of both pests and plant infections (Mantzoukas and
micro-organisms as either facultative or obligate para-               Grammatikopoulos 2019).
sites attacking insect pests, having high potential for
survival.                                                             Main text
   Use of microbial population as control agents is not               Biological control of insects
only effective against insect pests but this approach is              Biological control of insect pests with EPF is one of the
also environmentally safe and sound for humans (re-                   most desirable and effectual practice involving uses of
duced pesticide residues) as well as the non-target or-               natural microorganisms, which hinder their activity and
ganisms. The provocation for the impression of using                  can be used as an alternative to the chemical insecti-
microbial insect pathogens against insect pests re-                   cides. There have been some genera of EPF, which are
sulted from close examination of the disease of silk-                 antagonistic toward field, greenhouse, forest, storage,
worm (Audoin 1837). Afterward, the recommendation                     and household pests. These can be incorporated as EPF,
to assign microbial insect pathogens against insects                  for instance Beauveria, Metarhizium, Isaria, Lecanicil-
came from LeConte (1874) and Pasteur (1874). The                      lium, and Hirsutella. The different species belonging to
first efficacious mass-produced microbial control ap-                 these genera are target specific and cause infection in
plication on large scale was carried out by Kras-                     many insects. EPF have several biological attributes, such
silstschik (1888) against Bothynoderes punctiventris                  as target-specificity, high reproductively, short gener-
(Germar) (Coleoptera: Curculionidae) (sugar beet wee-                 ation time, and long survival, which play significant roles
vil) by making use of the antagonistic nature of the                  in biocontrol of insect pest.
conidiospores of Metarhizium anisopliae (Metchni-                        EPF species are mostly isolated from the soil, which
koff) (Hypocreales: Clavipitaceae) in Russia. The                     protects them from the damaging solar radiation (Mey-
credit for examining infectious nature of M. aniso-                   ling and Eilenberg 2007). It has been noted that certain
pliae must be attributed to Elie Metchnikoff, who ini-                species of Beauveria and Metarhizium can infect and kill
tially identified the microbial agent as Entomopthora                 insects in soil and also EPF interact with roots of plant
anisopliae against wheat cockchafer, Anisoplia aus-                   for their growth and survival which predominately relies
triaca (Herbst) (Coleoptera: Scarabaeidae).                           on insects for carbon and not on soil (Inglis et al. 2001).
   Out of all the other microbial control agent, EPF are                 Endophytic EPF evolve inside the above ground plant
the most imperative due to accumulation of various fac-               tissues and do not produce any perceptible symptoms of
tors, such as easy distribution, easy manufacturing tech-             infection. Their usage provides numerous advantages
niques, availability of large number of already identified            consisting of high yield, cost-effectiveness, preservation
strains, and over-expression of exogenous toxins and en-              of beneficial organisms, safe to humans, no harmful ef-
dogenous proteins (St Leger and Wang 2010). EPF legit-                fect on environment, and varied biodiversity (Mantzou-
imately influence plants more than the most compound                  kas and Eliopoulos 2020). The most commonly applied
pesticides. For instance, endophytic EPF have been ar-                and naturally occurring EPF endophyte species are
chived in many plants, for example, soybeans, wheat, to-              Beauveria bassiana, Isaria fumosorosea Wize (Hypo-
matoes, and bananas (Jaber 2015). As per the action                   creales: Clavicipitaceae), and Metarhizium anisopliae
mechanism of EPF is concerned, they release spores                    (Akutse et al. 2013). The endophytic EPF gives protec-
thereby infecting the body of the insect host. The fungal             tion against numerous pests to host plant and aids to
spores initially propagate on the exterior of host body               ameliorate plant response through production of com-
and later penetrate the host. As a result, death of the in-           pounds and inducing systemic resistance in the host
sect is inevitable within 4-7 days (conditional on the                plant. The endophytic EPF and host plant upon
quantity of spores). Cadaver of the insect serves as the              colonization secrete several types of chemicals such as
origin of new spores, which further disseminate, and                  secondary metabolites and enzymes. The secondary
Sharma and Sharma Egyptian Journal of Biological Pest Control   (2021) 31:57                                          Page 3 of 13

plant metabolites (alkaloids, flavonoids, phenolics, etc.)                  and Pell 2003). The gypsy moth, Lymantria dispar
are produced by the host plant as defense against fungal                    Linnaeus (Lepidoptera: Erebidae), accidentally intro-
pathogens, and endophytic EPF produce secondary plant                       duced in the USA during the 1860s, and E. mai-
metabolites (benzopyranones, phenolic acids, quinones,                      maiga introduced from Japan in the 1900s by
and steroids) and enzymes (β-1,3-glucanases, chitinases,                    placing infected cadavers onto tree trunks and able
amylases, laccases, and cellulases) which helps in the                      to control larvae of Gypsy moth which feed on the
interaction between endophyte and plant host (Zaynab                        leaves of many trees (Hajek et al. 2004). The fungal
et al. 2018).                                                               movement of E. maimaiga can take place through
   Historical evidences show the application and efficacy                   air-borne conidia (Shah and Pell 2003). Z. radicans
of EPF have been many as the EPF M. anisopliae var                          were imported from Israel to release in Australia
acridum has been applied as spray suspension in Africa                      during 1970 to control spotted alfalfa aphid, Ther-
to control the locusts (Langewald and Kooyman 2007).                        ioaphis trifolii f. maculata (Buckton) (Hemiptera:
Spray preparation of hydrophobic conidia was articu-                        Aphididae), a serious pest of legume plants.
lated in oil or as wettable agent, and hydrophilic blasto-              ii. Augmentation. The biological control agents of
pores were formulated as wettable powders. The solar                        insect-pests are present in their indigenous pest
radiation affects the persistence of fungal propagules and                  populations in various circumstances. The natural
their effectiveness can be improved by solar blockers                       enemies are either few or active late to restrict the
(Inglis et al. 2001). Conidia of M. anisopliae were used                    crop damage. There are two strategies of augmenta-
on seeds of corn before planting to reduce the damage                       tion: Inoculation biological control and inundation
of wireworms and this increased fresh weight and dens-                      biological control (Shah and Pell 2003).
ity of corn (Kabaluk and Ericsson 2007).

Pest control by EPF (approaches)
Biological control is regarded as a pleasing technique for              a. Inoculation biological control. The intentional
regulating insects, due to its insignificant environmental                 release of a minute amount of fungal biological
impact and inhibiting the development of resistance in                     control agents so that it will multiply and control
vectors. EPF can be employed under three broad bio-                        the pest for an extended period and sustain the pest
logical control approaches, i.e., classical biological con-                population below the economic threshold level. The
trol, augmentation, and conservation, by making use of                     natural enemies are inoculated in small to moderate
living organisms to suppress the insect population and                     amounts in the early season of the crop, increase
making it less abundant or less damaging (Hajek 2004).                     the number of biological control agents, and spread
                                                                           over a period of time before the insect-pest popula-
  i.   Classical biological control. Classical biological                  tion reaches the maximum potential. The natural
       control has been a notable approach that includes                   enemies are not able to control the pest population
       the use of a biological control agent to manage the                 permanently at a high population density. After a
       insect pest population. The introduction of an                      regular interval of time, the new inoculations must
       exotic biological control agent for the permanent                   be made for reestablishment because the control is
       establishment and long-term sustainable and eco-                    not achieved from released natural enemies (Abdel-
       nomical pest control in the new location. The intro-                ghany 2018). Soil can be inoculated with mycor-
       duction of the Vidalia beetle, Rodolia cardinalis                   rhiza to intensify growth and to advance up a
       (Mulsant) (Coleoptera: Coccinellidae), from                         natural process. Beauveria brongniartii inoculated
       Australia to California in the late 1880s to control                on Barley seeds to produce mycelium and aerial co-
       the scale insect, Icerya purchase Maskell (Hemip-                   nidia for the control of European cockchafer, Melo-
       tera: Margarodidae), is the successful example of                   lontha melolontha Linnaeus (Coleoptera:
       classical biological control and this approach cannot               Scarabaeidae) in Central Europe (Keller et al. 1999).
       be better understood without this historical dimen-                 The consolidated use of Zoophthora radicans Batko
       sion (Abdelghany 2018). The classical biological                    (Entomophthorales: Entomophthoraceae) and semio-
       control needs strong, regional co-ordination of the                 chemicals for the control of Diamondback moth,
       efforts for the successful management of insect-                    Plutella xylostella Linnaeus (Lepidoptera: Plutelli-
       pests. There are few examples of classical biological               dae) which is a significant pest of Brassica (Furlong
       control with EPF such as Entomophthora maimaiga                     and Pell 2001).
       Humber, Shimazu and Soper (Entomophthorales:                     b. Inundation biological control. Inundation
       Entomophthoraceae), and Zoophthora radicans (Bre-                   biological control includes fungal biological control
       feld) (Entomophthorales: Entomophthoraceae) (Shah                   agent to control the population density of a nasty
Sharma and Sharma Egyptian Journal of Biological Pest Control   (2021) 31:57                                           Page 4 of 13

      pest. Inundative augmentation involves the release              examination of their digestive systems (e.g., production
      of a massive amount of natural enemy for                        of toxins and enzymes and utilization of nutrients) and
      accelerated short-term control of the insect-pest               utilizing genomic analysis (e.g., mtDNA restriction
      population (Liu and Li 2004). The control of the                length polymorphism, karyotyping, and rRNA sequences
      pest population is accomplished by the released nat-            (Khachatourians 1991).
      ural enemies themselves. The pest population is                   Fungi (true) are presently positioned in four legitimate
      controlled immediately, and the population of both              phyla (Basidiomycota, Ascomycota, Zygomycota, and
      pest and natural enemies diminishes with time. The              Chytridiomycota). An artificial phylum, Deuteromycota
      fungus is employed as a chemical pesticide and dif-             is also documented comprising of filamentous fungi
      ferent terms are used, i.e., mycopesticide, mycoin-             which exist in anamorphic forms (asexual). It is alleged
      secticide, and biopesticide have been associated                that the affiliates of this phylum are in fact either basid-
      with inundation biological control (Abdelghany                  iomycetes or ascomycetes which have lost their ability to
      2018). Verticillium lecanii (Zimmerman) (Hypo-                  multiply sexually or their sexual structures are not yet
      creales: Cordycipitaceae) is adopted to control                 described (Alexopoulos et al. 1996). In addition, teleo-
      aphids, whiteflies, and thrips inside the glasshouses           morphs for various genera of deuteromycete (entomo-
      in Europe. The mycoinsecticide “Vertalec” is applied            pathogenic) have along these lines been recognized, and
      against aphids and “Mycotal” against whiteflies and             a portion of these teleomorphs can likewise be in fact
      thrips. Beauveria bassiana “Mycotrol” as a commer-              entomopathogenic (e.g., Cordyceps and Torrubiella spp.
      cial mycoinsecticide by Mycotech used against a                 are identified teleomorphs of Paecilomyces spp. (Samson
      wide range of insect pests in North America.                    et al. 1988)).
      Metarhizium anisopliae var. acridum commercial                    The oomycetes, once positioned in Mastigomycotina,
      product “Green Muscle” effective against locust and             have now been set in the kingdom of Stramenopila,
      grasshopper pests in Africa (Shah and Pell 2003).               phylum Oomycota (Barr, 1992). Individuals from this
                                                                      kingdom offer different highlights of monophyletic ori-
                                                                      gin, including a comparative flagellum hair structure and
                                                                      incorporate labyrinthulids, diatoms, and algae (Patterson
  iii. Conservation biological control. Conservation                  1989). The phylogenetic connection among the four
       biological control concerns with the modification of           phyla of fungi has been proposed, in view of on ultra-
       the environment or farming practices to defend and             structural and morphological highlights, and to a great
       intensify specific entomopathogens to lessen the               extent affirmed by resulting analyses of DNA sequence
       effect of pests. This approach accommodates to                 (Alexopoulos et al. 1996) as stated earlier.
       distinguish effective indigenous biological control              Chytridiomycetes might be well-thought-out as the
       agents and the selection of practices to conserve              most “crude” organisms since the predecessor of this
       and raise their population. The practices which                group diverged primarily and retained flagella and cen-
       prefer fungal biological control agent may include             trioles (Barr, 1992). The zygomycetes diverged before
       irrigation and reduction in pesticide usage. The EPF           the occurrence of a dikaryotic stage and consistently
       increase in population size and their effective                septate mycelium, which are normal for the basidiomy-
       results in a low pest population. Natural enemies              cetes and ascomycetes and the flagella was lost eventu-
       include all types of biological regulation: macro-and          ally. After the progenitors of basidiomycetes and
       microorganisms controlling invertebrates, weeds,               ascomycetes veered, the basidiomycetes’ predecessor de-
       and plant diseases, including the antagonistic micro-          veloped basidiospores (meiospores ordinarily delivered
       organisms responsible for suppressive soils. The               four for each basidium), in addition to clamp connec-
       conservation biological control approach is corre-             tions and dolipore septa (barrel shaped) and the ascomy-
       lated to the chief principle of organic farming,               cetes’ progenitors developed ascospores (i.e., meiospores
       which has the protection of the present natural en-            for the most part delivered eight for every ascus). The
       emies (Shah and Pell 2003 and Abdelghany 2018).                scientific classification of the Ascomycota is all the more
                                                                      plainly characterized and contains two significant orders:
Classification of entomopathogenic fungi                              Laboulbeniales (Class: Laboulbeniomycetes) and Hypo-
The classification of fungal organisms has generally re-              creales (Class: Sordariomycetes; subclass: Hypocreomy-
lied on their respective ultrastructure (e.g., structure of           cetidae) (Hibbett et al. 2007).
septum and that of the cell wall) and their morphology                  Hibbett et al. (2007) suggested an arrangement of
(e.g., mechanism of conidiogenesis) as essential stan-                characterization for all fungal groups dependent on mo-
dards. The more exact arrangement of EPF into charac-                 lecular phylogenetic investigations. As stated in the
terized scientific taxa has been accomplished by the                  background section, there are 750-1000 EPF, these can
Sharma and Sharma Egyptian Journal of Biological Pest Control   (2021) 31:57                                           Page 5 of 13

be found primarily placed in two fundamental groups:                  and dispersal under preponderating environmental cir-
phylum Zygomycota, subphylum Entomophthoromyco-                       cumstances (Roy et al. 2006).
tina, order Entomophthorales, and phylum Ascomycota                     Metarhizium spp. and Beauveria spp. belonging to the
(subkingdom Dikarya). Nonetheless, the Zygomycota is                  order Hypocreales are opportunistic hemibiotrophic in
not an acknowledged phylum inside the re-examined                     nature while fungi belonging to the order Ento-
classification. Hence, the Entomophthorales have not                  mophthorales are biotrophic. Metarhizium spp. and
been allotted a phylum in the current arrangement.                    Beauveria spp. are entomophagous that infect living in-
Most of EPF recognized to date have been positioned in                sects and saprophagous that invade dead insect corpse.
the following classes: Zygomycetes (phylum Zygomy-                    Entomophthorales exterminate their host by the
cota), Hyphomycetes (phylum Deuteromycota), and Pyr-                  colonization of tissues (Freimoser et al. 2003). Time be-
enomycetes and Laboulbeniales (phylum Ascomycota)                     tween application of entomopathogens and revelation to
(Samson et al. 1988).                                                 the activity of various parasitoids is vital for the contin-
                                                                      ued existence of the respective parasitoids (Oreste et al.
Infection process                                                     2015). The application of EPF in context of the time of
EPF face numerous host challenges in each generation                  application has been found to affect the rate of
to produce adequate fresh infectious spores to sustain vi-            parasitization by a parasitoid. For instance, the treat-
able populations. The prosperous transmission usually                 ments of entomopathogens M. anisopliae and B. bassi-
needs the discharge of massive spore numbers and glu-                 ana and time of fungal treatment influenced the rate of
tinous spore surfaces that enhance adhesion (Vega et al.              parasitization by Encarsia formosa Gahan (Hymenoptera:
2012). The spores germinate and directly invade through               Aphelinidae) against Trialeurodes vaporariorum (West-
the hard exoskeleton of the host insect (Vega et al.                  wood) (Hemiptera: Aleyrodidae) (Oreste et al. 2015).
2012). The fungi do not necessitate to be ingested. The
EPF commonly invade through the mouthparts or spira-                  Fungal invasion
cles because of non-sclerotized integument, and smooth                The process of pathogenesis is initiated by the adhesion
penetration (Clarkson and Charnley 1996). The penetra-                of conidia to the insect cuticle. The attachment of fungal
tion of the epicuticle is directly by germ tubes or infec-            propagules to the host exoskeleton is the first and fore-
tion pegs originated from the underneath of appressoria               most step of the infection process (Sevim et al. 2015).
(Zacharuk 1981). The fungal cells propagate inside the                Fungi are heterotrophic organisms that consume the
hemocoel, tissues, and muscles of the host’s body so that             non-chemical compounds provided by different organ-
it dies (Vega et al. 2012). The EPF can infect non-                   isms as their chief source of energy. The non-specific ad-
feeding stages such as eggs and pupae. The fungal                     hesion mechanisms involved in binding are controlled
germlings are steadily crossing distinct environments                 by the hydrophobic attributes of the conidial cell wall
and counter to the variations invoking biochemical pro-               (Boucias et al. 1988). This process includes interaction
cesses and cellular differentiation to form particular                among the conidial proteins and the hydrophobic exo-
morphological structures. The fungal germlings conform                skeleton surface of the susceptive insects (Fang et al.
to colonize insect tissue and neutralize potential host re-           2005). This process happens in three consecutive stages:
sponses. Infection structures reasonably emerge as a                    1.Adsorption of the spores to the insect exoskeleton
mechanism to surmount host barriers (St Leger and                       2.Adhesion of pre-germinated spores to the host
Wang, 2010). The process of infection can be restrained               cuticle
by low humidity conditions because fungus requires high                 3.Germination and development till appressoria for-
humid conditions for germination and maturity of fungal               mation (Tellez-Jurado et al. 2009)
structures.                                                             The cuticle is a significant impediment to fungal inva-
  The perception of a susceptive host can involve chem-               sion. The insect epicuticle is differentiated into multi-
ical and topographical signals. The cuticle of tobacco                layers; the outer epicuticle is mechanically fragile while
hornworm, Manduca sexta Linnaeus (Lepidoptera:                        the inner epicuticle designates toughness, although the
Sphingidae), has been used to study the impact of sur-                enzymes produced by EPF conquer this obstruction
face topography on appressorium formation. The ap-                    (Charnley and St Leger, 1991). The outer epicuticle may
pressoria developed after extensive germination across                be penetrated by an inadequate force and prevent the
the micro folds of the exoskeleton of 1-day fifth-instar              passage of cuticle-degrading fungal enzymes. Once the
larvae. The fungus does not get induction signals from                epicuticle is passed, penetrant structures may expand
the exoskeleton due to micro folds. Contrastingly, the                laterally propagating penetrant plates. The lateral expan-
appressoria germinate close to conidium on 5-day fifth-               sions promote penetration by inducing fractures in the
instar larvae (St Leger and Wang, 2010). The entomo-                  insect cuticle (Brey et al. 1986) and expedite dispersal of
pathogen uses the host cadaver for spore production                   the pathogen cuticle-degrading enzymes (Goettel et al.
Sharma and Sharma Egyptian Journal of Biological Pest Control   (2021) 31:57                                          Page 6 of 13

1989). In addition, insect epicuticular lipids play import-           proteases, lipases, and chitinases synthesis help to de-
ant role in binding fungus to the host cuticle (Ferron                grade the cuticle and release nutrients for fungus ger-
1978). The procuticle is impermeable to pathogen secre-               mination (Franco et al. 2011).
tions; the degree of resistance depends on cuticle thick-               M. anisopliae and B. bassiana spores are hydrophobic
ness and hardening. Insects having heavily sclerotized                in nature so they bind to insect cuticle (Holder and Key-
body segments and cuticular melanisation induced by                   hani 2005). The conidia of M. anisopliae have cuticle-
physical damage or β-1,3 glucans on the fungal cell wall              degrading catalysts and the potential to modify the sur-
(Charnley 1989), is common (Butt et al. 1988). Melanisa-              face of the integument for the attachment. During pre-
tion support to prevent fast-growing pathogens (St Leger              germination development as the conidium dilates, excre-
1991), but evaluating these responses in disease resist-              tion of adhesive mucus takes place which improves the
ance is challenging because of inadequate understanding               initial hydrophobic interactions among the conidium
of the amounts of melanin expected to influence infec-                and cuticular surface (Boucias and Pendland 1991). M.
tion and how melanin reactions might prevent fungal                   anisopliae strains are more precise toward the scarabid
germination. The inhibitory compounds on the exoskel-                 beetles. The cuticle of scarabids has antifungal com-
eton such as phenols, quinones, and lipids lead to the                pounds such as short-chain fatty acids. The EPF must
failure of fungal invasion (Kerwin 1984).                             have the capability to endure antifungal compounds for
   The Beauveria, Metarhizium, and Isaria belonging to                the successful invasion (Boucias and Pendland 1991).
order Hypocreales have hydrophobic conidia due to                     The germ tubes of M. anisopliae develop appressoria at
hydrophobins (cysteine-rich proteins) in the cell wall                the surface of the cuticle, infection peg in epicuticle,
while Verticillium lecanii has hydrophilic conidia (Inglis            penetrant hyphae in procuticle, and yeast-like hyphal
et al. 2001). The conidia of the order Entomophthorales               bodies in the hemocoel. The infection structures
are large and originate from sporangia. The conidia at-               emerged as a mechanism to overwhelm host barriers.
tach themselves to the cuticle and support the adhesion                 M. anisopliae var acridum is specific for the locusts.
process (Papierok and Hajek 1997). In addition, Neozy-                The conidia may be produced in internal air spaces
gites and Zoophthora spp. exhibit elongated capillioconi-             as the corpse shrivels out under unpropitious cir-
dia and adhere to the exoskeleton through an adhesive                 cumstances (Wang and St Leger, 2005). Once the
droplet (Glare et al. 1985).                                          EPF invades the cuticle comprised of a polysacchar-
   The process of adhesion among the spore and the in-                ide network and enters into the hemocoel, this in-
sect cuticle is mediated by the presence of molecules                 duced biophysical or biochemical interruption in the
synthesized by the fungus, called adhesins. In M. aniso-              insect which leads to death of the host insect
pliae, MAD1 adhesin-like protein is present on the co-                (Charnley 2003). The fungus will burst out through
nidial surface to attach to the host surface, but for                 the exoskeleton of the host insect, producing aerial
adhesion to plant surfaces MAD2 is present (Pava-Ripoll               spores following high relative humidity conditions.
et al. 2011). MAD1 adhesin affects germination and blas-              The unrestricted germination of the fungus may
tospore formation, significantly reducing fungus viru-                happen on the corpse of the host insect. The life
lence (Wang and St Leger, 2007). The conidium                         cycle of the EPF gets completed if sporulated on the
develops and produces penetration structures under                    cadaver of the host (Samson et al. 1988 and Charn-
promising conditions of temperature, relative humidity,               ley 2003). Under adverse environmental conditions,
nutritional, and physical requirements in the cuticle.                resting spores produced within the dead insect may
The penetration structures such as appressoria or germ                facilitate the fungus to persist for long periods (Sam-
tubes penetrate the host insect through infection peg                 son et al. 1988).
(Shah and Pell 2003).
   Conidiobolus obscurus (Hall & Dunn), Pandora neoa-                 Host response
phidis (Remaud & Hennebert), Entomophthora plan-                      After a successful invasion, the EPF proliferate inside the
choniana Cornu, and Batkoa apiculata (Thaxt.)                         host insect and septicemia occurs. The fungus combats
(Entomophthorales: Entomophthoraceae) belong to                       the host-induced restrictions and poisonous compounds
order Entomophthorales. These can penetrate the cu-                   additionally; the infection depends on the genetic poten-
ticle directly from the germ tube without the forma-                  tial of the pathogen. Structural features such as
tion of appressoria (Hajek and Delalibera 2010). B.                   sclerotization hinder penetration while enzyme inhibi-
bassiana requires carbon and fatty acids for the ger-                 tors and tyrosinases generate antimicrobial melanins
mination of conidia. In addition, insect epicuticular                 comprise the frontline defense toward weak pathogens
lipids may help in the germination of conidia by pro-                 (Gillespie et al. 2000). The protease inhibitors are also
viding energy sources and have antifungal properties                  present in the hemolymph of infected insects to limit le-
(Ferron 1978). The hydrolytic enzymes such as                         thal infections. Moreover, the distinct behaviors of the
Sharma and Sharma Egyptian Journal of Biological Pest Control   (2021) 31:57                                           Page 7 of 13

host insect can defend. Mycosis provokes physiological                (Valadares-Inglis and Peberdy 1997). Bbchit1 encoding
symptoms of abnormalities in the insect-like lack of co-              gene was present in the B. bassiana genome and its
ordination, altered behavior, and paralysis. Death results            amino acid sequence is similar to endochitinase of Strep-
from a succession of effects that involve the physical de-            tomyces avermitilis Kim and Goodfellow, S. coelicolor,
terioration of tissues, toxicity, and dehydration of cells            and T. harzianum (Fang et al. 2005). The epicuticular
by loss of fluids, and consumption of nutrients (Bustillo             layer of the insect is made up of non-polar lipids which
2001). The grasshopper Camnula pellucida (Scudder)                    would be barriers to entomopathogenic fungi without
(Orthoptera: Acrididae) retrieved from the infection of               the action of lipases and lipoxygenases (Khachatourians
Entomophaga grylii (Fresenius) (Entomophthorales:                     and Qazi, 2008). The growth of EPF is also inhibited by
Entomophthoraceae)        by     raising  internal    body            the presence of saturated fatty acid chains. The cuticular
temperature (Carruthers et al. 1992). The prominent                   lipids affect the conidial germination of B. bassiana and
virulence constituent in M. anisopliae is PR1 protease,               P. fumosoroseus. Also, the nymphs of silver leaf whitefly,
which reduces the time of death by 25% in Manduca                     B. argentifolii, produce a thick coating of long-chain wax
sexta (St Leger et al. 1996). Spores can germinate swiftly            esters affecting spore germination (Lord et al. 2002).
in the digestive tract of the insect where the relative hu-              The destructive effects of these virulence enzymes on
midity is high but digestive fluids degrade germinating               cuticle can be attributed to the structure and enzyme ac-
hyphae (Charnley 2003).                                               cessibility of protein polymers in the cuticle. The ma-
                                                                      nipulation of pathogen enzymes helps to understand the
Virulence enzymes associated with EPF                                 best cuticle structure and its natural degradation. The
The process of pathogenesis is mediated by mechanical                 characterization of enzyme regulation will enable ma-
force and the enzymatic process. The EPF require viru-                nipulation of enzyme levels with the help of chemical
lence enzymes like proteases, peptidases, chitinases, and             and biotechnological procedure for insect control (Kra-
lipases for entry and successful growth (Khachatourians               mer et al. 1988).
and Qazi 2008). The proteases and peptidases help in
the degradation of the insect cuticle because insect cu-              Epizootiology of fungal diseases in insects
ticle is composed of chitin and protein. These also aid in            An epizootic of insect fungal diseases is a large number
the degradation of saprophytic fungi and activate pro-                of cases of a disease in a host population. The diseased
phenoloxidase in the hemolymph. The fungi B. bassiana,                hosts are usually very abundant during epizootics. Epizo-
B. brongniartii, Lagenidium giganteum (Schenk) (Oomy-                 otiology of fungal diseases involves the natural history of
cota: Lagenidiales), Nomuraea rileyi (Farl.) Samson                   the disease, phenology of both pathogen and host, im-
(Hypocreales: Clavicipitaceae), M. anisopliae, and V.                 pact of the pathogen on host populations, and associ-
lecanii have been identified with protein degrading en-               ation of epizootics with weather conditions. The disease
zymes (Sheng et al. 2006). B. bassiana has subtilisin-like            development and spread are affected by the host and
serine endoprotease (Pr1 and Pr1B) and M. anisopliae                  pathogen populations, the environment, and the impact
has chymotrypsin (CHY1) (Screen et al. 2001). St Leger                of human activities. The pathogen having different char-
et al. (1996) constructed an engineered mycoinsecticides              acteristics includes virulence, dispersal, survival, and in-
based on M. anisopliae by over-expressing the Pr1 toxic               oculum density. The disease incidence depends on the
protease from M. anisopliae genome. This was engi-                    insect age and position in the tree canopy. Abiotic fac-
neered to enhance the killing speed of M. anisopliae.                 tors such as moisture, temperature, and sunlight may
The Pr1 over-expression activates the phenoloxidase sys-              determine whether infection can occur. The moisture
tem in the hemolymph of Manduca sexta which causes                    helps in the germination and sporulation, and
a 25% reduction in the time of death. The EPF M. aniso-               temperature is a limiting factor for disease development.
pliae, B. bassiana, and V. Iecanii have grown in culture              The primary interactions within host-pathogen systems
containing cuticle of locust produce various hydrolytic               increase, appreciation of community-level influences
enzymes which are active against insect cuticle.                      may aid in understanding, and predicting the develop-
   The chitinases (endo and exo-chitinases) play import-              ment of epizootics. The low-density host populations
ant roles in the cleavage of N-acetylglucosamine. The                 have less infection, resulting in a host increase (preepi-
enzyme helps to break the insect cuticle polymer into                 zootic phase). Host populations reach high densities, and
monomers. The chitinolytic enzymes were present in M.                 disease epizootics cause population decline (epizootic
anisopliae, M. flavoviride, and B. bassiana culture sup-              phase). The reduced host populations have a high infec-
plemented with insect cuticles (St Leger et al. 1996). The            tion, owing to abundant fungi in the environment (post-
enzymatically produced protoplast and cell of M. aniso-               epizootic phase) (Goettel et al. 2005).
pliae have chitinolytic enzymes. These enzyme activities                The epizootiology of insect pathogenic fungi on insects in-
were cell-bound and located in the membrane fraction                  cludes Entomophthora muscae (Cohn) (Entomophthorales:
Sharma and Sharma Egyptian Journal of Biological Pest Control   (2021) 31:57                                         Page 8 of 13

Entomophthoraceae) infection on the onion fly, Delia an-              increased, resulting in greater infection of A. pisum
tique Meigen (Diptera: Anthomyiidae), and N. rileyi on                (Pickering and Gutierrez 1991). The pathogens and nat-
Anticarsia gematalis Hubner (Lepidoptera: Noctuidae) in               ural enemies’ interactions could potentially impact host
soybean (Carruthers and Haynes 1986). The EPF Erynia                  and pathogen populations. Diatraea saccharalis (Fabri-
radicans and Entomophaga aulicae Batko (Entomophthor-                 cius) (Lepidoptera: Crambidae) parasitized for 1-6 days
ales: Entomophthoraceae) produce the highest mortality in             were inoculated with M. anisopliae; the fungus was not
spruce budworm, Choristoneura fumiferana (Clemens)                    harmful to three species of parasitoids (Folegatti and
(Lepidoptera: Tortricidae), which is a major defoliator in bal-       Alves 1987). The fungal infection of hosts in more ad-
sam and spruce trees (Perry and Whitfield, 1984). E. grylli           vanced stages of parasitization impaired fungal develop-
causes high mortality in C. pellucida and Melanoplus bivit-           ment. As the primary interactions increases, the
tatus Say (Orthoptera: Acrididae) (Pickford and Riegert               appreciation of community-level influences may help in
1963). Soil is a complex habitat that harbors flora and fauna.        predicting and understanding the development of
M. anisopliae is the most frequent mycopathogens of soil in-          epizootics.
sects, particularly of beetles (Keller and Zimmermann 1989).
M. anisopliae and B. bassiana are isolated from temperate             Role of EPF in nature
soils and have a broad host range. B. brongniartii is primarily       EPF play important role as plant disease antagonists,
a pathogen of cockchafers, Melolontha spp., and other Scar-           rhizosphere colonizers, biocontrol agent of insect-pests,
abidae (Zimmermann 1992). Epizootics have been found on               plant growth promoting fungi, and fungal endophytes.
wireworms, Agrotis spp., and larvae of Amphimallon solsti-            The use of natural or modified fungi or bacteria that are
tialis Linnaeus (Coleoptera: Scarabaeidae). On the other              antagonists of plant pathogens is considered as biological
hand, under in vitro conditions, various native parasitoids           control. The survival or disease-causing activity of a
such as Leptopilina heterotoma Thomson (Hymenoptera:                  pathogen is reduced by the production of various metab-
Figitidae), Pachycrepoideus vindemiae Rondani (Hymenop-               olites, such as antibiotics, bioactive volatile compounds
tera: Pteromalidae), and Trichopria drosophilae Perkins (Hy-          (e.g., ammonia, hydrogen cyanide, alkyl pyrones, alco-
menoptera: Diapriidae), have been reported to distinguish             hols, acids, esters, ketones and lipids) and enzymes.
and parasitize invasive pest, Drosophila suzukii (Matsumura)          Some other mechanisms are also involved like competi-
(Diptera: Drosophilidae) at varying degrees of adequacy               tion, antibiosis, hypovirulence, parasitism, and induced
(Ibouh et al. 2019).                                                  systemic resistance (Ownley and Windham 2007). The
   Soil is a complex habitat that harbors flora and fauna.            EPF like B. bassiana, Lecanicillium spp., are antagonistic
M. anisopliae is the most frequent mycopathogens of                   toward insects but also antagonistic to plant pathogens
soil insects, particularly of beetles (Keller and Zimmer-             (Kim et al. 2008). B. bassiana utilizes different antagon-
mann 1989). M. anisopliae and B. bassiana are isolated                ism mechanism like antibiosis, competition, and induced
from temperate soils and have a broad host range. Beau-               systemic resistance (Benhamou and Brodeur 2001).
veria brongniartii is primarily a pathogen of cockchafers,              EPF in the Hypocreales are ubiquitous members of the
Melolontha spp., and other Scarabidae (Zimmermann                     soil microbiota. The EPF Beauveria, Isaria, and Metarhi-
1992). Epizootics have been found on wireworms, Agro-                 zium are isolated from soil. The soil not only protects
tis spp., and larvae of Amphimallon solstitialis Linnaeus             EPF from damaging solar radiation but also from the ex-
(Coleoptera: Scarabaeidae). Soil is a reservoir for fungi             tremes of temperature (Inglis et al. 2001). The plant
that infect insects present on aerial parts of plants. EPF            rhizosphere has free carbon in abundant amount and
persist in the soil as mycelium or pseudosclerotia. The               exploited by saprotrophic microorganisms (Whipps
spores of N. rileyi pathogenic to lepidopteran insects ad-            2001). EPF interact with plant roots for growth or sur-
here to the leaves of the plant (Ignoffo et al. 1977).                vival (St Leger and Wang, 2010). The ability of EPF has
   Cordyceps mycoflora is rich in humid and tropical for-             impaired through the antimicrobial metabolites secreted
ests and this EPF play a significant role in regulating in-           by microbes present in the soil. The B. bassiana applied
sect population because of the stable microclimates                   to control Colorado potato beetle, Leptinotarsa decemli-
(Evans 1982). The interactions between virulent and                   neata (Say) (Coleoptera: Chrysomelidae), but there is
avirulent isolates were complex and are the outcome of                low mortality due to increased soil fungistasis levels
dual infection in the leaf-cutting ant, Acromymex echin-              (Groden and Lockwood 1991). M. anisopliae applied as
tior Forel (Hymenoptera: Formicidae) (Hughes and                      conidia to corn seeds before planting to reduce damage
Boomsma, 2004). The virulent Aspergillus flavus Link                  from wireworms, and increased stand density and fresh
(Eurotiales: Trichocomaceae) dominated when inocu-                    weight of field corn (Kabaluk and Ericsson 2007). The
lated with M. anisopliae. P. neoaphidis infects the sym-              fungus which infect internal tissues of above ground
patric aphids, kills few Acyrthosiphon kondoi Shinji                  plant parts without causing symptoms are known as fun-
(Hemiptera: Aphididae), and pathogen density is                       gal endophytes (Arnold and Lutzoni 2007). The sum of
Sharma and Sharma Egyptian Journal of Biological Pest Control   (2021) 31:57                                           Page 9 of 13

fungal endophytes protects host plants against insect                 Thus, the market is presently directed by small to
pests (Rudgers et al. 2007). Acremonium, Beauveria, Cla-              medium-sized organizations.
dosporium, Clonostachys, and Isaria are some of the EPF                  Another explanation behind the small share of the
(Vega et al. 2008).                                                   overall industry of the fungi as mycoinsecticides is its
   EPF are also employed in integrated pest management                moderately slow killing rate and an expansion in share
programs as one of the natural enemies against arthro-                of the market value legitimately corresponds to the kill-
pods including insect pests. Nowadays, the usage of fun-              ing speed (St Leger and Wang 2010). In spite of the fact
gal pathogens is drawing special attention as a biological            that these products have the upside of a confined host
control agent of many insect pests and this approach is               range, this particularity is likewise one of the restricting
reliable, cost-effective, and environmentally safe                    elements for their commercial use (Ownley et al. 2004).
(Wraight et al. 2001). EPF possesses several attributes               In this manner, a mycopesticide with a more extensive
that make them a potential candidate to be utilized in                host extend however with next to zero impact on other
the IPM program. Some of the fungi including Beau-                    natural enemies of useful organisms may have an im-
veria, Metarhizium, Isaria, Lecanicillium, Hirsutella, and            portant commercial advantage in the event that it all the
Entomophthorales are used as entomopathogens. The B.                  while controls different insect pests and additionally
bassiana is effective against lepidopteran, coleopteran,              plant infections (Wraight and Carruthers 1999).
and hemipteran pests. B. bassiana has also been found                    However, since the advent of worries over the effect of
to be pathogenic in opposition to the larvae of Capnodis              synthetic compounds, cost of enlisting synthetic concoc-
tenebrionis (Linnaeus) (Coleoptera: Buprestidae) in la-               tions for high value crop plants, development of insecti-
boratory assays as reported by El Khoury et al. (2020)                cide resistance, and the developing enthusiasm for
wherein the mortality/transience of C. tenebrionis ran                “organic/natural” food has now guaranteed a business
between 26 and 76%.                                                   opportunity for biological agents of pest control, thereby
   Metarhizium anisopliae is effective against scarab bee-            incorporating formulations dependent on EPF. EPF have
tle grubs, weevils, termites, and cutworms. L. lecanii used           generally been utilized more broadly on forest pests than
against insects belong to order Hemiptera and Thysanop-               on pests of crops (Feng 2003).
tera. Paecilomyces lilacinus is used against nematodes                   Mycopesticide formulations depend on a confined
(Root-knot, cyst, lesion burrowing) (Skinner et al. 2014).            number of fungal species, fundamentally Beauveria
These fungal-based products are harmful to specific insect            bassiana, B. brongniartii, Lecanicillium muscarium, L.
pests (host-specific) and relatively safe to beneficial in-           longisporum, M. anisopliae, Paecilomyces fumosoroseus,
sects, non-target organisms, and ecosystems. There is no              and Verticillium lecanii. About 33.9% of the mycoinsec-
problem of toxic residues on crops as agrochemicals                   ticidal formulations are based on B. bassiana, trailed by
(Laird et al. 1990). The EPF has been developed or is being           M. anisopliae (33.9%), I. fumosorosea (5.8%), and B.
evaluated as an integral and essential component of IPM               brongniartii (4.1%) (Faria and Wraight 2007). However,
or IDM. Parasitoids have likewise been accounted for to               to build the share of the overall industry of EPF, the kill-
go about as vectors of EPF to the hosts during instances of           ing speed which is the significant deterrent restricting
foraging, as reported by Oreste et al. (2016), wherein                their utilization as mycoinsecticides ought to be en-
Encarsia formosa acted as a passive vector to transfer the            hanced (St Leger and Wang 2010).
fungal propagules from tainted to uninfected populaces                   As the natural strains of these EPF are deficient in terms
due to the virtue of its oviposition and host handling.               of adequate levels of virulence (Rangel et al. 2005), there-
                                                                      fore, manipulation at genetic level is important to improve
Mycoinsecticides: present scenario                                    their viability and ecological wellness (Fang et al. 2005)
The market of chemical pesticides represents as much as               Also, dual infection by different entomopathogens does
98% of the worldwide market of crop protection and                    not affect the mortality of insects. For instance, according
consequently, the portion of biopesticides is just 2%.                to Tarasco et al. (2011) when contrasted with the values
(Anon 2005). A more profound investigation of the                     which were noted when the two entomopathogens (ento-
share of the overall industry of biopesticides has uncov-             mopathogenic nematode Steinernema ichnusae (Nema-
ered that mycoinsecticides have contributed for an ex-                toda: Steinernematidae) and EPF B. bassiana) were
ceptionally little division of the market of biopesticide,            inoculated individually against Galleria mellonella Fabri-
on the grounds that a large share has been accounted by               cius (Lepidoptera: Pyralidae), concurrent infection showed
formulations which are based on the bacterium Bacillus                neither synergistic nor additive effects.
thuringiensis. The development of biopesticides for pest
control was at first upheld and contributed by multi-                 Future prospects
national agrochemical organizations yet a large portion               Future investigations on EPF should zero in on attempt-
of them have opted out since 1980s (Charnley 2003).                   ing to comprehend the ecosystem of the fungal growths
Sharma and Sharma Egyptian Journal of Biological Pest Control   (2021) 31:57                                         Page 10 of 13

in a setting that centers on their role as antagonists of             et al. 1988) and the staggering interest has been investi-
plant diseases. Most intriguing future prospect in terms              gating the potential for B. bassiana and M. anisopliae. A
of EPF is the possibility to devise stratagems for strain             few instances of late examinations are the investigations
improvement. Attributes which could be tended to in-                  on the rice water weevil, a pest of rice in North and
clude expanded killing power (reduced LD50), capacity                 South America (Chen et al. 2005), the Sunn pest, Eury-
to start disease at low humidity conditions, upgraded                 gaster integriceps Puton (Hemiptera: Scutelleridae), a
timeframe of realistic usability, and environmental                   major insect pest of wheat and barley in West and Cen-
steadiness (for example, temperature tolerance, and re-               tral Asia (Parker et al. 2003), and thrips (Ekesi and Man-
sistance against UV), augmented kill (reduced LT50), im-              iania 2003).
proved sporulation during large-scale manufacturing and                  Investigations into the strain improvement and poten-
extension of the host. Lane et al. (1991) suggested that              tial targets for mycoinsecticides will give insights into
culture conditions impact the attributes of contagious                enhanced disposition of mycoinsecticides for the best
fungal spores and can be controlled to increment                      pest control and improved development of formulations,
mycoinsecticide effectiveness. For instance, Blastospores             detailing to upgrade their adequacy so utilization of the
of B. bassiana from carbon-restricted cultures had lower              EPF can turn into an essential share of agricultural
groupings of starch and lipid and were fundamentally                  frameworks as well as the integrated pest management
less harmful toward the rice green leafhopper than were               stratagems.
the blastospores from nitrogen-restricted cultures.
   Direct manipulation at genetic level would give                    Conclusion
upgraded targeting for single genes or clusters of genes,             In the present review, an attempt is made to sum up the
for example, epizootic capability of Beauveria spp. and               utilization of fungal organisms as biopesticides, the au-
Metarhizium spp. was enhanced by genetic manipula-                    thors endeavor and gather the information about the
tion, thereby enhancing their saprophytic potential by                EPF as biocontrol operators. We gather knowledge on
Wang and St Leger (2005). ESTs and cDNA microarrays                   the past and present researches about EPF to investigate
were utilized to investigate gene expression during de-               approaches to improve their capacities. The action
velopment on a plant root exudate. Genetic manipula-                  mechanism of infection by the EPF is not only complex
tion needs the foundation of cloning and transformation               but specialized as well. Therefore, there is a need to ac-
frameworks, which have been accomplished for P. fumo-                 quire the knowledge of insect-fungus interaction as the
soroseus, B. bassiana, and M. anisopliae (Lima et al.                 host-pathogen interactions are basic determinants of
2006).                                                                pathogenicity and epizootic turn of events. Molecular
   Keeping the agro-ecosystems aside, EPF are also find-              and biochemical examinations of host-pathogen interac-
ing the exploit of their activity against the human and               tions are characterizing those properties yielding ex-
animal pests, for example, work on mosquitoes (Blanford               panded pathogenicity and are focused on the
et al. 2005) and tsetse flies (Maniania et al. 2003). Inves-          management of explicit fungal processes. Examinations
tigations on Brassica root flies (Delia floralis (Fallen)             at the level of an organism include investigations of the
(Diptera: Anthomyiidae) and Delia radicum Linnaeus                    turn of events and activity of different phases of host
(Diptera: Anthomyiidae)) (Eilenberg and Meadow 2003),                 and pathogen, which are regularly in association with
fire ants (Brinkman and Gardner 2004), and mound                      variations in natural conditions of the ecosystem. The
building termites (Milner 2003) show the assortment of                utilization of EPF in agro-ecosystems has expanded as of
expected targets for mycoinsecticides. Other potential                late because of the extraordinary potential they have in
targets researched for utilization of mycoinsecticides in-            the field of pest management, speaking to a productive
corporate bee parasite Varroa destructor Anderson &                   option in contrast to the utilization of synthetic chemical
Trueman (Arachnida: Varroidae) (Shaw et al. 2002),                    compounds, which are viewed as exceptionally hurtful to
blowflies (Wright et al. 2004), parasitic mites (Smith                the soundness of man and environment alike. Under-
et al. 2000), reduviid bugs such as Triatoma (Lazzarini               standing the components engaged with the process of
et al. 2006) and ticks (Samish et al. 2004).                          infection, will permit the development of new organic/
   On the other hand, EPF have potential for control of a             biological formulations that are compelling for field use
certain number of insect pests, and it is imperative to               and securing the beneficial species of insects. Be that as
distinguish potential targets for mycoinsecticide develop-            it may, there are various limitations on the utilization of
ment and advancement. For instance, beetles and larval                EPF as an insecticide, for instance, the potential out-
pests are every now and again host to fungal diseases                 comes of contamination with mycotoxins such as, citri-
however seem to have similarly not many viral and bac-                nin,     zearalenone,    aflatoxins,    fumonisins,    and
terial pathogens. Subsequently, fungi are frequently the              trichothecenes delivered by various saprophytic fungi as
microbes of choice for beetle and bug pests (Samson                   environmental toxins cannot be precluded. Other
Sharma and Sharma Egyptian Journal of Biological Pest Control                  (2021) 31:57                                                            Page 11 of 13

limitations include the facts that not only the application                          Audoin V (1837) Nouvelles expe´riences sur la nature de la maladie contagieuse
of EPF must coincide with high relative humidity condi-                                   qui attaque les Vers a` soie, et qu’on de´signe sous le nom de Muscardine.
                                                                                          Ann sci Nat 8:257–270
tions but also there is a need for a period where no                                 Barr DJS (1992) Evolution and kingdoms of organisms from the perspective of a
chemical fungicide application has taken place. More-                                     mycologist. Mycologia 84:1–11
over, the inoculum has short timeframe of realistic us-                              Benhamou N, Brodeur J (2001) Pre-inoculation of Ri T-DNA transformed
                                                                                          cucumber roots with the mycoparasite, Verticillium lecanii, induces host
ability and the formulation requires 2–3 weeks to kill                                    defense reactions against Pythium ultimum infection. Physiol Mol Plant
the insects. Along these lines, novel thoughts and specu-                                 Pathol 58:133–146
lation need to rise which will further assist in building                            Blanford S, Chan BHK, Jenkins N, Sim D, Turner RJ, Read AF, Thomas MB (2005)
                                                                                          Fungal pathogen reduces potential for malaria transmission. Science 308:
up the fungi’s abilities as biocontrol specialists.                                       1638–1641
                                                                                     Boucias DG, Pendland JC (1991) Attachment of mycopathogens to cuticle: the
Abbreviations
                                                                                          initial event of mycosis in arthropod hosts. In: Cole GT, Hoch HC (eds) The
mtDNA: Mitochondrial deoxyribonucleic acid; rRNA: Ribosomal ribonucleic
                                                                                          Fungal Spore and Disease Initiation in Plants and Animals. Plenum Press,
acid; PR1: Pathogenesis related protein-1; IPM: Integrated pest management;
                                                                                          New York, pp 101–128
IDM: Integrated disease management; LD: Lethal dose; LT: Lethal time;
                                                                                     Boucias DG, Pendland JC, Latge JP (1988) Nonspecific factors involved in
EST: Expressed sequence tag; cDNA: Complementary deoxyribonucleic acid
                                                                                          attachment of entomopathogenic Deuteromycetes to host insect cuticle.
                                                                                          Appl Environ Microbiol 54:1795–1805
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Not applicable
                                                                                          Acyrthosiphon pisum, by Conidiobolus obscurus. J Invertebr Pathol 48:34–41
                                                                                     Brinkman MA, Gardner WA (2004) Red imported fire ant (Hymenoptera:
Authors’ contributions
                                                                                          Formicidae) control in nursery pots treated with Beauveria bassiana and
Both RS and PS researched and reviewed the existing literature on the topic
                                                                                          bifenthrin. J Entomol Sci 39:75–187
at hand. RS worked on the “Background,” “Classification of
                                                                                     Bustillo A (2001) Hongos en insectos y poszibilidades de uso en el control
Entomopathogenic Fungi,” “Mycoinsecticides: Present Scenario,” “Future
                                                                                          biológico de plagas en Colombia. In: Seminario Uso de entomopatógenos
prospects,” and “Conclusion” sections of the manuscript. PS worked on
                                                                                          en Colombia. Sociedad Colombiana de Entomología, Bogotá, pp 30–53
sections titled “Biological Control of Insects,” “Pest Control by EPF
                                                                                     Butt TM, Wraight SP, Galaini-Wraight S, Humber RA, Roberts DW, Soper RS (1988)
(Approaches),” “Infection process,” “Virulence enzymes associated with EPF,”
“Epizootiology of fungal diseases in insects,” and “Role of EPF in Nature.” RS            Humoral encapsulation of the fungus Erynia radicalls (Entomophthorales) by
contributed to the critical review and editing of the manuscript. Both                    the potato leafhopper Empoasca fabae (Homoptera: Cicadellidae). J Vertebr
authors read and approved the final manuscript.                                           Pathol 52:49–56
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Not applicable                                                                            germination and survival in the onion agroecosystem. Environ Entomol 15:
                                                                                          1154–1160
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Not applicable                                                                            on the mycosis of a range land grasshopper. Ecology 73:190–204
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Declarations                                                                              Lumsden RD (eds) The biotechnology of fungi for improving plant growth.
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Ethics approval and consent to participate                                           Charnley AK (2003) Fungal pathogens of insects: cuticle degrading enzymes and
Not applicable                                                                            toxins. Adv Bot Res 40:241–321
                                                                                     Charnley AK, St Leger RJ (1991) The role of cuticle degrading enzymes in fungal
Consent for publication                                                                   pathogenesis in insects. In: Cole GT, Hoch HC (eds) The fungal spore and
Not applicable                                                                            disease initiation in plant and animals. Plenum Press, New York, pp 267–286
                                                                                     Chen H, Chen ZM, Zhou YS (2005) Rice water weevil (Coleoptera: Curculionidae)
Competing interests                                                                       in mainland China: invasion, spread and control. Crop Protect 24:695–702
The authors declare that they have no competing interests.                           Clarkson JM, Charnley AK (1996) New insights into the mechanisms of fungal
                                                                                          pathogenesis in insects. Trends Microbiol 4:197–203
Author details                                                                       Delgado PAM, Murcia OP (2011) Hongos entomopatógenos: Uma alternativa
1
 Department of Plant Pathology, Dr. YS Parmar University of Horticulture and              para la obtención de Biopesticidas. Ambi-Agua 6:77–90
Forestry, Nauni, Solan, Himachal Pradesh 173230, India. 2Department of               Dhaliwal GS, Jindal V, Mohindru B (2015) Crop losses due to insect pests: global
Entomology, Dr. YS Parmar University of Horticulture and Forestry, Nauni,                 and Indian scenario. Indian J Entomol 77:165–168
Solan, Himachal Pradesh 173230, India.                                               Eilenberg J, Meadow R (2003) Fungi for biological control of Brassica root flies,
                                                                                          Delia radicum, and Delia floralis. In: Upadhyay RK (ed) Advances in microbial
Received: 8 January 2021 Accepted: 15 March 2021                                          control of insect pests. Kluwer, New York, pp 181–192
                                                                                     Ekesi S, Maniania NK (2003) Metarhizium anisopliae: an effective biological control
                                                                                          agent for the management of thrips in horti-and floriculture in Africa. In:
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