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Review

Transcription Factors in Biocontrol Fungi

by
Han-Jian Song
,
Xiao-Feng Li
,
Xin-Ran Pei
,
Zhan-Bin Sun
* and
Han-Xu Pan
*
School of Light Industry Science and Engineering, Beijing Technology and Business University, Beijing 100048, China
*
Authors to whom correspondence should be addressed.
J. Fungi 2025, 11(3), 223; https://doi.org/10.3390/jof11030223
Submission received: 16 February 2025 / Revised: 7 March 2025 / Accepted: 13 March 2025 / Published: 15 March 2025
(This article belongs to the Section Fungi in Agriculture and Biotechnology)
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Versions Notes

Abstract

:
Transcription factors are extensively found in fungi and are involved in the regulation of multiple biological processes, including growth, development, conidiation, morphology, stresses tolerance, and virulence, as well as the production of secondary metabolites. Biocontrol is a complex biological process through which several biocontrol behaviors, such as the secretion of cell wall-degrading enzymes and the production of secondary metabolites, are regulated by transcription factors. To date, biocontrol-related transcription factors have been reported in several biocontrol fungi, such as Beauveria bassiana, Clonostachys rosea, Coniothyrium minitans, and different species in the genera Metarhizium, Trichoderma, and Arthrobotrys. However, comprehensive reviews summarizing and analyzing transcription factors with biocontrol potential in these fungi are scarce. This review begins by giving a basic overview of transcription factors and their functions. Then, the role of biocontrol-related transcription factors in biocontrol fungi is discussed. Lastly, possible approaches for further work on transcription factors in biocontrol fungi are suggested. This review provides a basis for further elaborating the molecular mechanisms of transcription factors in the context of biocontrol.

1. Introduction

Biological control (biocontrol) generally refers to the usage of beneficial organisms—such as fungi and bacteria—to control pathogens, thereby lowering the incidence of plant diseases [1]. Biocontrol has the advantages of being safe, sustainable, and environmentally friendly, which has attracted significant attention. As important examples of biocontrol organisms, biocontrol fungi play crucial roles in controlling plant diseases.
There are a number of diverse mechanisms underlying the control of plant diseases by biocontrol fungi. Biocontrol agents can secrete cell wall-degrading enzymes, including chitinases, glucanases, and some proteases, to degrade the cell walls of plant pathogens [2]. Biocontrol agents can also produce antibiotics or toxins to inhibit the growth of plant pathogens or even kill them [3]. Some fungal mycoparasites can also coil around plant pathogens through a mycoparasitism mechanism to control plant diseases [4]. These behaviors in biocontrol fungi are regulated by the expression activities of transcription factors through upstream signal-transduction pathways, such as the MAPK and cAMP pathways. Deletion of MAPK encoding genes could influence the biocontrol activity of Trichoderma brevicrassum in disease control and also affect the expression of biocontrol-related genes, such as genes encoding fungal cell wall-degrading enzymes and genes involved in secondary metabolism [5]. Similarly, disruption of an adenylate cyclase (an important component of the cAMP pathway) encoding gene crac could reduce the ability of Clonostachys rosea to control plant disease, and the expression of genes encoding cell wall-degrading enzymes were also influenced after crac deletion in Clonostachys rosea [6]. During the process of biocontrol fungi against plant pathogens, biocontrol-related signals are transmitted through signal-transduction pathways, affecting the expression of transcription factors and, finally, regulating the expression of biocontrol-related genes in biocontrol fungi, thereby controlling plant pathogens. Therefore, transcription factors in biocontrol fungi play important roles in controlling plant diseases.
In this review, the roles and applications of transcription factors in the processes of biocontrol fungi-controlling plant diseases are detailed and discussed. This review demonstrates the importance of understanding the regulatory mechanisms underlying transcription factors in biocontrol fungi.

2. Transcription Factors

Transcription factors, commonly known as trans-acting factors, are a type of protein that can specifically interact with related cis-acting elements. Through binding to cis-acting elements, transcription factors can regulate (i.e., activate or inhibit) the expression of downstream genes with specific intensity under specific conditions or circumstances. Common transcription factors contain four functional domains: DNA-binding domain, transcription regulation domain, oligomerization site, and nuclear localization signal [7].
To date, 61 transcription factor families containing 123,899 transcription factors, identified from 61 fungal and three oomycete species, have been reported through fungal transcription factor databases (http://ftfd.snu.ac.kr/index.php?a=view). The bZIP, C2H2 zinc finger, Myb, Forkhead, GATA-type zinc finger, Heteromeric CCAAT factors, Homeodomain-like, Winged helix repressor DNA-binding, Zinc finger, CCHC-type, HMG, and Homeobox families have reportedly had the highest number of transcription factors (262) identified in fungi. The Zn2Cys6 and Zinc finger, CCHC-type transcription factor families have the highest numbers of transcription factors, 29,247 in fungal species and 966 in oomycete species, out of all transcription factor families.
The Zn2Cys6 transcription factor contains a DNA-binding domain consisting of six cysteine combined with two zinc. The Zn2Cys6 transcription factor family is found widely in fungi and is involved in the regulation of multiple biological processes, including growth, development, virulence, secondary metabolite production, nutrient utilization, stress response, and drug resistance. In the Valsa pyri mutant, the deletion of the Zn2Cys6 transcription factor gene VpxlnR reduced growth and virulence and caused a loss of fruiting body formation function, and led to higher susceptibility to hydrogen peroxide and salicylic acid, compared with the wild-type strain [8]. In Fusarium pseudograminearum, the knockout of the Zn2Cys6 transcription factor gene Fp487 significantly reduced conidiogenesis, pathogenicity, and 3-acetyl-deoxynivalenol production, and increased sensitivity to oxidative and cytomembrane stress in the mutant [9]. A mutant of Sclerotinia sclerotiorum with SsZNC1 gene deletion in the Zn2Cys6 transcription factor exhibited reduced sclerotial development ability, growth ability, and virulence compared with the wild-type strain [10]. The Zn2Cys6 transcription factor family is also important in nutrient utilization and drug resistance. The deletion of the Zn2Cys6 transcription factor gene clr-5 could significantly influence the growth of Neurospora crassa through use of leucine or histidine as the sole nitrogen source [11]. The knockout of the Zn2Cys6 transcription factor gene in Magnaporthe oryzae could influence resistance to isoprothiolane [12].

3. Functions of Transcription Factors in Biocontrol Fungi

Transcription factors are found widely in fungi and have been reported to be involved in the regulation of multiple important biological processes, including fungal growth, development, secondary metabolite production, virulence, and tolerance to environmental stress [13,14,15]. During the process of biocontrol, transcription factors can influence the biocontrol efficiency of biocontrol fungi through regulating the formation of infection structures and stress tolerance, producing cell well-degrading enzymes and secondary metabolites, and participating in other biocontrol behaviors (Figure 1). Hence, transcription factors play crucial roles in biocontrol fungi. To date, transcription factors have been reported as being involved in biocontrol processes in a number of fungal species, such as Beauveria bassiana, Metarhizium sp., Coniothyrium minitans, Clonostachys rosea, Trichoderma sp., Hirsutella minnesotensis, Arthrobotrys sp., Drechslerella dactyloides, Paecilomyces lilacinus, Purpureocillium lilacinum, and Papiliotrema terrestris. Among these biocontrol fungi, Beauveria bassiana and Metarhizium sp. (M. acridum, M. robertsii, and M. rileyi) have the most biocontrol-related transcription factors (Table 1).

3.1. Beauveria bassiana

Beauveria bassiana is wildly used in microbial insecticides to control insect pests in agriculture. Many commercial products have been developed to control a range of insect pests worldwide [16,17]. Multiple transcription factors belonging to different families, including bZIP, Zn2Cys6, MADS-box, NDT80, p53-like, GATA-type, HSF-type, Homeobox, and C2H2-type, have been reported to be involved in the biocontrol of insect pests in B. bassiana.
Transcription factors might regulate the virulence to insect pests associated with conidial quality, cell wall integrity, oxidative stress response, hyphal body production, appressorium formation, cuticle-degrading proteases, extracellular chitinase, and lipolytic activity.
Transcription factors from the Zn(II)2Cys6 family are most reported as being involved in virulence in Beauveria bassiana. A Zn(II)2Cys6 transcription factor-encoding gene BbTpc1 in B. bassiana ARSEF 2860 was deleted, and the mutant exhibited reduced virulence to Galleria mellonella. The decrease in virulence in the BbTpc1-deletion mutant is mainly due to defects in cell wall integrity, as well as growth and resistance, which are important in B. bassiana infection [18]. In B. bassiana Bb0062, two Zn(II)2Cys6 transcription factors encoding genes Bbotf1 and Thm1 were positively related to virulence. After disruption to Bbotf1 in B. bassiana, conidia recovered from cadavers killed by the disruption mutant showed obviously impaired virulence to G. mellonella compared with wild-type and complemented strains. Moreover, Bbotf1 could also influence resistance to oxidants in B. bassiana [19]. The BbThm1 mutant of B. bassiana reduced virulence to G. mellonella compared with the wild-type strain. Deep study found that BbThm1 deletion can influence hyphal body formation and host immune prophenol oxidase response activity in B. bassiana, which may result in decreased virulence in the BbThm1-deletion mutant [20].
Except for positivity related to virulence, two Zn2Cys6 transcription factors encoding genes BbCDR1 and NirA1 negatively regulate the virulence of Beauveria bassiana to insect pests. Disruption to BbCDR1 in B. bassiana CGMCC7.34 can improve virulence to G. mellonella and increase yield in conidia. Interestingly, BbCDR1 can impact conidial development, cell wall integrity, and trehalose synthesis in conidia [21]. Similarly, the NirA1-deletion mutant of B. bassiana Bb0062 increases virulence to G. mellonella [22].
Several transcription factors from the C2H2-type family, including BbKlf1, crz1, and zafa, have also been reported to be involved in Beauveria bassiana virulence. The deletion of BbKlf1 in B. bassiana ARSEF 2860 reduced virulence to G. mellonella. The reason for attenuated virulence in the BbKlf1-deletion mutant might be due to the secretion of cuticle-degrading Pr1 proteases in the mutant being reduced. In addition, the hyphal bodies were delayed in the BbKlf1-deletion mutant compared with the wild type [23]. The crz1-deletion mutant of B. bassiana ARSEF 2860 remarkably reduced virulence to Spodoptera litura compared with the wild-type strain. Conidiation and tolerance to stresses of B. bassiana were also influenced by the deletion of crz1 [24]. Disruption to zafa in B. bassiana Q2505 could influence growth, spore germination, and sensitivity to stresses, as well as remarkably reduce virulence to G. mellonella [25].
Except for positivity related to virulence, a C2H2-type transcription factor-encoding gene Bbsmr1 in Beauveria bassiana ARSEF 2860 negatively regulated virulence to insect pests. Disruption to Bbsmr1 could significantly improve virulence to G. mellonella compared with the wild-type strain. The increased virulence of the Bbsmr1 disruption mutant may be due to Bbsmr1 being related to the production of red-pigmented dibenzoquinone oosporein, which is involved in host immune evasion [26].
Two MADS-box transcription factors encoding genes Bbmcm1 and Mb1 in Beauveria bassiana Bb0062 have been reported to be involved in virulence. Disruption to Bbmcm1 in B. bassiana significantly decreased virulence to G. mellonella compared with the wild-type strain. Further studies have found that the deletion of Bbmcm1 can reduce the production of cuticle-degrading enzyme, which might lead to decreased virulence in the Bbmcm1-deletion mutant. Meanwhile, growth, conidiogenesis, and cell integrity in B. bassiana could also be influenced by Bbmcm1 deletion, which also impacts the virulence of B. bassiana [27]. In the Mb1-deletion mutant of B. bassiana, growth and virulence to G. mellonella were reduced and cell wall integrity was influenced [28].
Two bZIP transcription factors encoding genes BbYap1 and BbHapX are involved in Beauveria bassiana ARSEF 2860 virulence. The deletion of BbYap1 could impact lipid homeostasis in B. bassiana, as well as sensitivity to stress, especially decreasing the virulence to G. mellonella compared with the wild-type strain. Deep studies have found that BbYap1 regulates virulence to insects, mainly through eluding the host humoral defense [29]. The BbHapX-deletion mutant influences conidia germination in B. bassiana and delays the formation of conidia development into hyphal bodies. In addition, the virulence of B. bassiana to G. mellonella is reduced in the BbHapX disruption mutant compared with the wild-type strain [30].
Transcription factors of the Homeobox, GATA-type, NDT80-like, and p53-like encoding genes Bbhox2, BbAreA, Ron1, and BbTFO1, respectively, are involved in Beauveria bassiana virulence. The knockout of Bbhox2 in B. bassiana CGMCC7.34 could reduce virulence to G. mellonella remarkably compared with the wild-type strain. An in-depth study found that Bbhox2 was important in appressorium formation and hyphal body development, which is crucial in B. bassiana infection. The appressoria and hyphal body were reduced in the Bbhox2 knockout mutant compared with the wild-type strain [31]. The BbAreA mutant of B. bassiana decreased the virulence to G. mellonella compared with the wild-type strain. Further study found that the production of hyphal bodies was reduced in BbAreA knockdown mutants [32]. Disruption to Ron1 in B. bassiana ARSEF 2860 can dramatically reduce virulence to G. mellonella. Extracellular chitinase activity is reduced in the Ron1-deletion mutant compared with the wild-type strain, which is very important in B. bassiana infection. Hyphal bodies are barely visible in the Ron1-deletion mutant during infection compared to the wild-type strain, which may be another reason for the decrease in fungal virulence. Moreover, cell wall defects caused by the deletion of Ron1 could lead B. bassiana to adapt environmental stress and may also reduce the virulence of B. bassiana [33]. The BbTFO1-deletion mutant of B. bassiana ARSEF 2860 impacted antioxidant activity, conidial germination, heat stress resistance, and conidial quality. The virulence of the BbTFO1-deletion mutant to G. mellonella was reduced compared with the wild-type strain. Moreover, the hyphal bodies in the BbTFO1-deletion mutant were fewer than that in the wild-type strain, which is important in B. bassiana infection [34].
The transcription factor-encoding gene Bbmsn2 in different Beauveria bassiana strains exhibits similar roles in virulence. The deletion of Bbmsn2 in B. bassiana Bb0062 reduced virulence to Rhipicephalus microplus, which might be due to the lower protease activity of the Bbmsn2-deletion mutant compared with the wild-type and complemented strains during treatment with tick cuticles. The virulence of B. bassiana Bb0062 to G. mellonella was also impaired after Bbmsn2 deletion [35]. For the B. bassiana strain ARSEF 2860, Bbmsn2 disruption in B. bassiana resulted in significantly reduced virulence to Spodoptera litura compared with the wild-type strain. Moreover, the conidia yield and tolerance to stresses of B. bassiana ARSEF2860 were also impacted after Bbmsn2 deletion [36].
Moreover, three HSF transcription factor-encoding genes hsf1, sfl1, and skn7, and two Far/CTF1-type transcription factor-encoding genes Bbctf1α and Bbctf1β, are involved in Beauveria bassiana virulence. The hsf1, sfl1, and skn7-deletion mutants of B. bassiana exhibited a remarkably decreased virulence to G. mellonella. The deletion of three HSF transcription factors encoding genes also impacted the conidiation, cell wall integrity, and stress tolerance of B. bassiana [37]. Bbctf1α and Bbctf1β were disrupted in B. bassiana CICC 41021. Disruption to two genes influenced phenotypic characters, including growth and conidium formation, as well as tolerance to oxidation stress and virulence to G. mellonella. The significantly reduced virulence of disruption mutants might be due to the impediment of extracellular lipolytic activities caused by Bbctf1α and Bbctf1β deletion, which are important in the cuticular penetration of B. bassiana by insect pests [38].
The transcription factor-encoding genes BbpacC and Fkh2 positively regulated the virulence of Beauveria bassiana. The deletion of BbpacC in B. bassiana ATCC 90517 resulted in defects in the production of the insecticidal compound dipicolinic acid, and the deletion of BbpacC only slightly influenced the virulence of B. bassiana to G. mellonella and T. molitor [39]. Fkh2 deletion in B. bassiana Bb2860 reduced virulence to G. mellonella, as well as tolerance to environment stresses, compared with the wild-type strain [40]. The transcription factor-encoding gene BbStf1 negatively regulated the virulence of B. bassiana. The deletion of BbStf1 in B. bassiana Bb0062 increased virulence to G. mellonella compared with the wild-type strain. The cell wall integrity and oxidative stress responses were also negatively regulated by BbStf1, which is vital in B. bassiana infection [41].

3.2. Members of the Genus Metarhizium

Metarhizium is another commonly used microbial insecticide in agriculture, and several products have been developed for its commercial application [42,43]. Similarly to B. bassiana, multiple transcription factors, belonging to different families, including C2H2-type, APSES-type, GATA-type, Zn2Cys6, Homeobox, bZIP, GATA-type, and HSF-type, have been reported as being involved in the control of insect pests in Metarhizium acridum, Metarhizium robertsii, and Metarhizium rileyi.
For Metarhizium acridum, C2H2-type is the transcription factor family most reported to be involved in the virulence to insect pests. Five C2H2-type transcription factors encoding genes MaMsn2, MaPacC, MaSte12, MaCrz1, and MaNCP1, were reported as being involved in the virulence of M. acridum CQMa102. The deletion of MaMsn2 reduced the virulence of M. acridum to L. migratoria remarkably [44]. Disruption to MaPacC also significantly reduced the virulence of M. acridum to L. migratoria manilensis. Meanwhile, the deletion of MaPacC delayed appressorium formation and impacted the expression of some insect cuticle hydrolases, which may be a reason for the decreased virulence [45]. Similarly, MaSte12 deletion in M. acridum significantly reduced the virulence to L. migratoria. Further studies showed that MaSte12 deletion could influence appressorium formation, as well as penetration, in M. acridum [46]. MaCrz1 disruption in M. acridum caused decreased virulence to L. migratoria manilensis, as well as impaired the penetration ability in the host cuticle in the mutant. Meanwhile, tolerance to stress and cell walls were also affected in the MaCrz1-deletion mutant, which may be another factor influencing virulence. Additionally, cuticle-degrading genes were associated with virulence in M. acridum [47]. MaNCP1 deletion in M. acridum influenced cuticular penetration ability and decrease virulence to L. migratoria manilensis. Further studies found that the expression levels of cuticle-degrading genes were downregulated after MaNCP1 deletion [48].
The GATA-type and Zn(II)2Cys6 transcription factors encoding genes MaAreB and MaAzaR were associated with virulence in Metarhizium acridum CQMa102. The deletion of MaAreB decreased the virulence of M. acridum to locusts, which may be due to defects in appressorium formation and appressorial turgor pressure after MaAreB deletion. In addition, the cell wall integrity was also affected in the MaAreB-deletion mutant [49]. MaAzaR deletion also decreased the virulence of M. acridum to L. migratoria. The decreased virulence in the MaAzaR-deletion mutant is mainly due to defects in appressoria, including appressorium formation, appressorial turgor pressure, and hydrolytic enzymes compared with the wild-type strain [50].
Two other transcription factors encoding genes MaFTF1 and MaSom1 were related to virulence in Metarhizium acridum CQMa102. The overexpression of MaSom1 enhanced the virulence of M. acridum to L. migratoria manilensis. Besides the virulence to insect pests, stress tolerance and conidiation were also altered in M. acridum after MaSom1 overexpression [51], while MaFTF1 negatively regulated the virulence of M. acridum. The knockout of MaFTF1 caused increased virulence in M. acridum to Locusta migratoria manilensis. An in-depth study found that the deletion of MaFTF1 accelerated the development of appressoria, together with higher appressorial turgor pressure, compared with the wild-type strain [52].
In Metarhizium rileyi, the C2H2-type family is the transcription factor family most reported as being involved in the virulence to insect pests. Three C2H2-type transcription factors encoding genes MripacC, MrSte12, and MrMsn2 have been reported as being involved in the virulence of M. rileyi CQNr01. The virulence of M. rileyi to S. litura was reduced after the deletion of MripacC. Deep study found that the conidium surface structure was smoother in the MripacC-deletion mutant compared with the wild-type strain, which is important in the conidia-adhesion ability of M. rileyi. Moreover, the ability to secrete protein-degrading enzymes was decreased after MripacC deletion, which might be the reason for the decreased virulence of the MripacC-deletion mutant [53]. MrSte12 deletion significantly reduced the virulence of M. rileyi to S. litura. The decreased virulence in the MrSte12-deletion mutant may be due to impaired appressorium formation after MrSte12 deletion. Moreover, the deletion of MrSte12 also influenced growth, conidiation, and tolerance to stress [54]. The deletion of MrMsn2 also decreased virulence of M. rileyi to S. litura, as well as microsclerotia formation, remarkably [55].
Besides C2H2-type transcription factors, genes encoding bZIP (Mrap1), GATA-type (MrNsdD), and APSES-type (MrStuA and MrXbp) transcription factors are involved in the virulence of Metarhizium rileyi CQNr01. The deletion of Mrap1 in M. rileyi decreased the virulence to S. litura, as well as conidial and microsclerotial yield, compared with the wild-type strain [56]. MrNsdD disruption in M. rileyi affected virulence to S. litura, as well as microsclerotium formation and conidiation in the MrNsdD-deletion mutant compared with the wild-type strain [57]. M. rileyi mutants with the deletion of MrStuA and MrXbp, respectively, exhibited impaired virulence to S. litura, as well as microsclerotium formation, conidiation, and stress tolerance compared with the wild-type strain [58]. Similarly, the deletion of the transcription factor-encoding gene MrSwi6 in M. rileyi resulted in reduced virulence toward S. litura, as well as conidiation and microsclerotia formation compared with the wild-type and complemented strains [59].
In Metarhizium robertsii, three different transcription factor families, including genes encoding bZIP (MBZ1), C2H2-type (MrpacC), and Zn2Cys6 (Aftf1), have been found to be related to virulence in M. robertsii ARSEF 2575. The deletion of MrpacC impacted the virulence of M. robertsii to Bombyx mori, as well as reduced chitinase activity, compared with the wild-type strain. The impaired virulence in the MrpacC-deletion mutant may be due to MrpacC deletion influencing the cuticle-penetration ability [60]. The MBZ1-deletion mutant exhibited impaired virulence to B.mori and G. mellonella. Moreover, growth, conidiogenesis, and cell wall integrity were influenced by MBZ1 deletion in M. robertsii [61]. The Aftf1-disruption mutant also showed remarkably reduced virulence to G. mellonella, as well as delayed appressorial formation, compared with the wild-type strain [62].
Genes encoding three types of transcription factors, homeobox (MrHOX7), HSF (MrSkn7), and APSES (MrStuA), are involved in virulence in Metarhizium robertsii ARSEF 23. The MrHOX7-disruption mutant shows inhibited virulence to G. mellonella. An in-depth study found that appressorium formation and conidial adhesion were reduced and the expression of adhesion- and appressorium-related encoding genes were downregulated in the MrHOX7-disruption mutant compared with the wild-type strain, which may be the reason behind the inhibited virulence after MrHOX7 disruption [63]. The deletion of MrStuA and MrSkn7 reduced virulence to G. mellonella. In addition, appressorium-formation ability was lost after MrSkn7 deletion compared with the wild-type strain, which may be a reason for the reduced virulence in the MrSkn7-deletion mutant [64,65].
Two other transcription factors encoding genes MrSt12 and Mrmsn2 have been associated with virulence in Metarhizium robertsii ARSEF 2575. Disruption to MrSt12 causes M. robertsii to lose virulence to G. mellonella, which may be due to the appressoria not being produced in the MrSt12-deletion mutant compared with the wild-type and complemented strains [66]. The Mrmsn2-deletion mutant showed remarkably reduced virulence to T. molitor compared with the wild-type strain. In addition, conidiation and tolerance to environmental stresses were influenced by Mrmsn2 deletion [36].

3.3. Arthrobotrys Oligospora, Arthrobotrys Flagrans, and Drechslerella Dactyloides

Arthrobotrys oligospora and Arthrobotrys flagrans are nematode-trapping fungi that capture plant-pathogenic nematodes by producing specialized trap structures [67,68]. Several different types of transcription factors have been reported as being involved in the pathogenesis of Arthrobotrys sp. Two C2H2-type transcription factors encoding genes AoMsn2 and AoSte12 are deleted in A. oligospora ATCC 24927. Both deletion mutants influence pathogenicity to Caenorhabditis elegans. Deep study found that the deletion of AoMsn2 significantly decreased the number of traps compared with the wild-type strain [69]. In the AoSte12 mutant, both the hyphal ring traps and electron-dense bodies were increased compared with the wild-type strain [70].
Disruption to the genes encoding two other types of transcription factors, MADS-box (AoRlmA) and APSES (AoStuA), in Arthrobotrys oligospora ATCC 24927, also impacted pathogenicity to C. elegans. In the AoRlmA-disruption mutant, growth, sporulation, trap formation, and stress tolerance were also influenced compared with the wild-type strain [71]. The AoStuA-deletion mutant could not form traps and thereby lost the ability to capture C. elegans. Meanwhile, proteolytic activity was decreased after AoStuA deletion [72].
Besides Arthrobotrys oligospora, transcription factors in Arthrobotrys flagrans have also been reported to be involved in pathogenicity to nematodes. The knockout of the APSES transcription factor-encoding gene AfSwi6 impacted the pathogenicity of A. flagrans YMF1.07536 to C. elegans. The number of traps was reduced after AfSwi6 deletion. In addition, the extracellular protease activity was remarkably reduced in the mutant compared with the wild-type strain [73].
Drechslerella dactyloides is another type of nematode-trapping fungi used to control nematodes [74]. The deletion of the C2H2-type transcription factor gene DdaCrz1 in D. dactyloides 29 resulted in fewer traps being formed and lower constricting ring inflation compared with the wild-type strain after the introduction of C. elegans. In addition, growth, conidiation, stress tolerance, and cell wall integrity were influenced by DdaCrz1 deletion [75]. Similarly, with the deletion of another C2H2-type transcription factor gene, DdaSTE12, in D. dactyloides 29, trap formation and ring cell inflation were also decreased compared with the wild-type strain after the introduction of C. elegans [76].

3.4. Members of the Genus Trichoderma

Trichoderma is an important mycoparasite agent that is used widely to control fungal plant pathogens such as Rhizoctonia solani, Sclerotinia sclerotiorum, Botrytis cinerea, and Fusarium oxysporum [77,78,79]. Several transcription factors, belonging to different families, such as C2H2-type, GATA-type, and MYB, have been reported as being involved in the biocontrol of T. atroviride, T. asperellum, and T. harzianum.
In Trichoderma harzianum, transcription factor genes belonging to C2H2-type (Tha09974), C6 zinc finger (Thc6), and Cys6Zn(II)2 (Thctf1) have been associated with the biocontrol potential of T. harzianum toward pathogens. The deletion of Tha09974 in T. harzianum Th33 could reduce its antagonistic ability toward B. cinerea and F. oxysporum compared with the wild-type strain. Tha09974 deletion could also influence the biomass and spore production of T. harzianum [80]. Knockout and overexpression were performed to analyze the role of Thc6 in T. harzianum Th22 against Curvularia lunata. Compared with the wild-type strain, the overexpression mutant reduced the disease index caused by C. lunata to maize, while the knockout mutant increased the disease index [81]. The Thctf1 disruption mutant of T. harzianum CECT 2413 showed a significantly reduced antifungal ability toward B. cinerea. The production of 2-pentyl furan and benzaldehyde, which are antifungal volatiles, was influenced by Thctf1 deletion [82].
Two other transcription factors, pac1 and ThpacC, have also been related to the antagonistic ability of Trichoderma harzianum. The mutation of pac1 in T. harzianum CECT 2413 was performed through RNA interference. The antagonistic ability of the mutant toward R. solani, R. meloni, and Phytophthora citrophthora was reduced compared with the wild-type strain. As well as the expression of genes involved in antagonism, such as chit42, chitinase was reduced compared with the wild-type strain [83]. The knockout of ThpacC in T. harzianum 3.9236 could reduce the antagonistic ability toward S. sclerotiorum compared with the wild-type strain and overexpression mutant. An in-depth study found that the production of two antifungal compounds, homodimericin A and 8-epi-homodimericin A, were abolished after knockout, which may be the reason behind the reduced antagonistic ability of the ThpacC-deletion mutant [84].
A C2H2-type transcription factor-encoding gene Ste12, and a GATA-type transcription factor-encoding gene Are1, are involved in the mycoparasitic ability of Trichoderma atroviride P1. Disruption to Ste12 and Are1 could reduce the mycoparasitic ability of T. atroviride P1 to R. solani and B. cinerea, respectively, compared with the wild type [85]. Moreover, diffusible metabolites from the Are1 deletion mutant exhibit reduced antifungal capacity compared with the wild-type strain [86].
Trichoderma asperellum and Trichoderma virens are also transcription factors that have been reported as being involved in the biocontrol of pathogens. The role of the MYB transcription factor-encoding gene MYB36 in T. asperellum Tas653 against Alternaria alternata was analyzed through gene knockout and overexpression. Compared with the wild-type strain, the MYB36-knockout mutant reduced the inhibition ability against A. alternata, while the MYB36-overexpression mutant improved the hyperparasitic ability. In addition, the activities of superoxide dismutase, peroxidase, and catalase were also reduced after MYB36 deletion [87]. The deletion of the transcription factor-encoding gene pacC in T. virens IMI 304061 reduced the biocontrol potential toward R. solani and S. rolfsii, which might be due to pacC deletion impairing the adaptability of T. virens to an alkaline pH or its capacity to perceive ambient pH [88].

3.5. Clonostachys Rosea and Coniothyrium Minitans

Similarly to Trichoderma, Clonostachys rosea is a very important biocontrol mycoparasite that can control numerous fungal plant pathogens [89,90]. The bHLH transcription factor-encoding gene sre1 plays different regulation roles in C. rosea IK726 antagonism. The deletion of sre1 improved the antagonistic ability toward B. cinerea but led to a decreased antagonistic ability to R. solani. A further study found that the expression of antagonism-related genes such as polyketide synthases and chitinases were downregulated in the sre1-deletion mutant compared with the wild-type strain [91]. The deletion of the transcription factor-encoding gene pacC in C. rosea 611 could significantly decrease its virulence to Panagrellus redivivus. The expression level of extracellular serine protease in the pacC-deletion mutant was downregulated [92]. crtf is a gene encoding the Tubby transcription factor; the crtf-deletion mutant of C. chloroleuca 67-1 reduced its parasitic ability of sclerotia in S. sclerotiorum and significantly lowered the biocontrol capacity toward soybean Sclerotinia white mold caused by S. sclerotiorum [93].
Similarly to Trichoderma and Clonostachys, Coniothyrium minitans is commonly used as a biocontrol agent to control plant disease [94,95]. Disruption to the transcription factor-encoding gene CmpacC in C. minitans Chy-1 remarkably reduces mycoparasitic ability to sclerotia in S. sclerotiorum. The production of the mycoparasitism-related enzymes chitinase and β-1,3-glucanse is notably suppressed in the CmpacC-deletion mutant compared with the wild-type and complemented strains [96]. The NDT80-like transcription factor-encoding gene CmNdt80a in C. minitans ZS-1 has been found to play a similar role in mycoparasitic ability. The deletion of CmNdt80a in C. minitans ZS-1 significantly reduced the parasitic ability to sclerotia of S. sclerotiorum. The cell wall integrity and conidiation were also affected by CmNdt80a deletion [97].

3.6. Other Biocontrol Fungi

Transcription factors from other biocontrol fungi, including Hirsutella minnesotensis, Candida oleophila, Papiliotrema terrestris, Paecilomyces lilacinus (synonyms of Purpureocillium lilacinum) and Purpureocillium lilacinum, have been reported as being involved in biocontrol. The deletion of the Zn(II)2Cys6 transcription factor-encoding gene rolP in P. lilacinus Pl36-1 could significantly impact its pathogenicity to Meloidogyne incognita. Moreover, the nematotoxin leucinostatin A was absent from the rolP-deletion mutant compared with the wild-type strain [98]. Disruption of the HSF transcription factor-encoding gene HIM-SKN7 in Hirsutella minnesotensis 3608 could reduce its endoparasitic ability to Heterodera glycines compared with the wild-type and overexpression strains. Moreover, conidiation and stress tolerance were affected after HIM-SKN7 deletion [99].
Two bZIP transcription factor-encoding genes Yap1 and lcsL, have been disrupted in Papiliotrema terrestris and Purpureocillium lilacinum, respectively. Yap1 deletion in P. terrestris LS28 decreased its biocontrol activity against Penicillium expansum and Monilinia fructigena [100]. lcsL was disrupted in Purpureocillium lilacinum PLBJ-1. The lcsL-disruption mutant lost its antagonistic ability to Phytophthora infestans; moreover, no leucinostatins were detected, in contrast to the wild-type and overexpression strains [101]. Besides the two bZIP transcription factors, the MADS-box transcription factor-encoding gene Rlm1 has also been found to be involved in biocontrol. The deletion of the MADS-box transcription factor-encoding gene Rlm1 in C. oleophila I-182 resulted in decreased biocontrol efficacy to gray mold on kiwifruit caused by B. cinerea compared with the wild-type strain. In addition, the deletion of Rlm1 also influenced tolerance to stresses [102].

4. Conclusions and Future Prospects

Transcription factors are involved in the regulation of multiple biological processes, including fungal growth, development, morphological characteristics, cell wall integrity, tolerance to stresses, virulence, conidiation, and the production of secondary metabolites. Biocontrol is a complex biological process that, mainly through the production of cell wall-degrading enzymes, toxins, and/or antibiotics, exerts activity using biocontrol fungi. Many of these biocontrol behaviors are regulated by transcription factors. Therefore, we investigated the roles of transcription factors in biocontrol and the corresponding regulation mechanisms. The presented studies may be useful for further analyses of the molecular mechanisms underlying biocontrol and in improving the control efficiency of biocontrol fungi. At present, the transcription factors reported as being involved in biocontrol belong to the families C2H2, bZIP, GATA, Zn2Cys6, MADS-box, HSF, APSES, and Homeobox. To date, biocontrol-related transcription factors have been reported in biocontrol fungi including Beauveria bassiana, Metarhizium acridum, M. robertsii, M. rileyi, Arthrobotrys oligospora, A. flagrans, Drechslerella dactyloides, Clonostachys rosea, Coniothyrium minitans, Trichoderma harzianum, T. asperellum, T. virens, and T. atroviride, which have been used to control insect pests, plant pathogenic nematodes, and fungal plant pathogens. Although numerous studies on biocontrol transcription factors have been reported, systematic and comprehensive reviews summarizing and analyzing transcription factors in biocontrol fungi are rare. Therefore, this review mainly introduced and discussed the roles of transcription factors in biocontrol fungi, as well as the potential underlying biocontrol mechanisms. This review provides a basis for the further elaboration of the molecular mechanisms behind biocontrol and further improvements to control efficiency in biocontrol fungi.
In biocontrol fungi, transcription factors were involved in regulation of the physiological characteristics of fungus, including growth, conidial development, spore germination, microsclerotium formation, cell wall integrity, stress tolerance, formation of appressorium, traps, and hyphal body. As well as biochemical traits containing activities of cell wall-degrading enzymes of cuticle-degrading proteases, chitinase and β-1,3-glucanse; the activities of superoxide dismutase, peroxidase, and catalase; and production of secondary metabolites of homodimericin A, 8-epi-homodimericin A, 2-pentyl furan and benzaldehyde and nematotoxin leucinostatin A were also regulated by transcription factors of biocontrol fungus. Moreover, the expression of genes involved in biocontrol, including genes encoding serine protease, chitinases, adhesion- and appressorium-related, polyketide synthases, were affected after transcription factor disruption.
Future studies should focus on the development of more transcription factors for use in biocontrol, the construction of gene-engineered stains through the overexpression of biocontrol-related transcription factors encoding genes to improve control efficacy, and the elucidation of regulation networks of transcription factors that are active during the processes of biocontrol.
(1)
Developing more biocontrol-related transcription factors: Compared with the currently reported biocontrol fungal species, there are fewer corresponding types of transcription factors involved in biocontrol. There are many types of biocontrol fungi in which no biocontrol transcription factors have been reported. Moreover, at present, among the total transcription factor families, the reported transcription factor families related to biocontrol only cover a small proportion. Developing more types of transcription factors from more families will be useful in comprehensively elaborating the mechanisms underlying the regulation of biocontrol using transcription factors.
(2)
The construction of transcription factor engineering strains: The overexpression of biocontrol-related transcription factors encoding genes in the same biocontrol fungi or the expression of the above genes in different biocontrol fungi can be useful to improve control efficacy.
(3)
The screening of transcription factors upstream of regulated genes and downstream of target genes and the analysis of the roles of these genes in biocontrol: This will allow for the construction of a regulation network of biocontrol-related transcription factors and a comprehensive exploration of the molecular mechanisms behind the regulation of biocontrol using transcription factors.

Author Contributions

Conceptualization, Z.-B.S. and H.-X.P.; investigation, Z.-B.S. and H.-J.S.; data curation, X.-F.L. and X.-R.P.; writing—original draft preparation, H.-J.S.; writing—review and editing, Z.-B.S. and H.-X.P.; Supervision, Z.-B.S. and H.-X.P.; funding acquisition, H.-X.P. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by National Natural Science Foundation of China (NSFC), grant number 32302245.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Mechanisms of transcription factors regulate plant diseases control in biocontrol fungi.
Figure 1. Mechanisms of transcription factors regulate plant diseases control in biocontrol fungi.
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Table 1. Transcription factors in biocontrol fungi.
Table 1. Transcription factors in biocontrol fungi.
Biocontrol FungusTranscription FactorsFamilyPathogensReference
Beauveria bassianaBbYap1bZIPGalleria mellonella29
BbCDR1Zn2Cys6Galleria mellonella21
BbSmr1C2H2-type Galleria mellonella26
Bbotf1Zn(II)2Cys6Galleria mellonella19
Bbhox2HomeoboxGalleria mellonella31
Bbklf1C2H2-typeGalleria mellonella23
Ron1NDT80Galleria mellonella33
Mb1MADS-boxGalleria mellonella28
Bbctf1αFar/CTF1-type Galleria mellonella38
Bbctf1βFar/CTF1-type Galleria mellonella38
BbHapXbZIPGalleria mellonella30
BbTpc1Zn(II)2Cys6Galleria mellonella18
BbStf1Leucine zipper dimerizationGalleria mellonella41
BbTFO1p53-likeGalleria mellonella34
Bbmsn2—Galleria mellonella; Spodoptera litura;
Rhipicephalus microplus		35, 36
BbThm1Zn(II)2Cys6Galleria mellonella20
Bbmcm1MADS-boxGalleria mellonella27
Crz1C2H2-type Spodoptera litura24
BbPacC—Galleria mellonella; Tenebrio molitor39
zafaC2H2-typeGalleria mellonella25
NirA1Zn2Cys6Galleria mellonella22
Fkh2—Galleria mellonella40
BbAreAGATA-type Galleria mellonella32
hsf1HSF-typeGalleria mellonella37
skn7HSF-typeGalleria mellonella37
sfl1HSF-typeGalleria mellonella37
Metarhizium acridumMaFTF1—Locusta migratoria manilensis52
MaAzaRZn(II)2Cys6Locusta migratoria manilensis50
MaSom1—Locusta migratoria manilensis51
MaAreBGATA-typeLocust49
MaPacCC2H2-typeLocusta migratoria manilensis45
MaSte12C2H2-typeLocusta migratoria46
MaCrz1C2H2-typeLocusta migratoria manilensis47
MaMsn2C2H2-typeLocusta migratoria44
MaNCP1C2H2-typeLocusta migratoria manilensis48
Metarhizium robertsiiMrHOX7HomeoboxGalleria mellonella63
MrSt12—Galleria mellonella66
MrStuAAPSES-typeGalleria mellonella58
MrSkn7HSF-typeGalleria mellonella65
MBZ1bZIPGalleria mellonella;
Bombyx mori		61
MrpacCC2H2-typeBombyx mori60
Mrmsn2—Tenebrio molitor36
Aftf1Zn2Cys6Galleria mellonella62
Metarhizium rileyiMrSte12C2H2-typeSpodoptera litura54
MrNsdDGATA-typeSpodoptera litura57
MrStuAAPSES-typeSpodoptera litura64
MrXbpAPSES-typeSpodoptera litura58
MrSwi6—Spodoptera litura59
MrMsn2C2H2-typeSpodoptera litura36
Mrap1bZIPSpodoptera litura56
MripacCC2H2-typeSpodoptera litura53
Coniothyrium minitansCmNdt80aNDT80Sclerotinia sclerotiorum97
CmpacC—Sclerotinia sclerotiorum96
Clonostachys roseapacC—Panagrellus redivivus92
sre1bHLHBotrytis cinerea; Rhizoctonia solani91
Clonostachys chloroleucacrtfTubbySclerotinia sclerotiorum93
Trichoderma harzianumThpacC—Sclerotinia sclerotiorum84
Thctf1Cys6Zn(II)2Botrytis cinerea82
pac1—Rhizoctonia solani; Rhizoctonia meloni; Phytophthora citrophthora83
Thc6C6 zinc finger Curvularia lunata81
Tha09974C2H2-typeBotrytis cinerea; Fusarium oxysporum80
Trichoderma asperellumMYB36MYBAlternaria alternata87
Trichoderma virenspacC—Rhizoctonia solani; Sclerotium rolfsii88
Trichoderma atrovirideSte12C2H2-typeRhizoctonia solani; Botrytis cinerea85
are1GATA-typeRhizoctonia solani; Botrytis cinerea86
Hirsutella minnesotensisHIM-SKN7HSF-typeHeterodera glycines99
Candida oleophilaRlm1MADS-boxBotrytis cinerea102
Arthrobotrys flagransAfSwi6APSES-typeCaenorhabditis elegans73
Arthrobotrys oligosporaAomsn2C2H2-typeCaenorhabditis elegans69
AoRlmAMADS-boxCaenorhabditis elegans71
AoStuAAPSES-typeCaenorhabditis elegans72
AoSte12C2H2-typeCaenorhabditis elegans70
Drechslerella dactyloidesDdaCrz1C2H2-typeCaenorhabditis elegans75
DdaSTE12C2H2-typeCaenorhabditis elegans76
Paecilomyces lilacinusrolPZn(II)2Cys6Meloidogyne incognita98
Purpureocillium lilacinumlcsLbZIPPhytophthora infestans101
Papiliotrema terrestrisyap1bZIPPenicillium expansum; Monilinia fructigena100
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Song, H.-J.; Li, X.-F.; Pei, X.-R.; Sun, Z.-B.; Pan, H.-X. Transcription Factors in Biocontrol Fungi. J. Fungi 2025, 11, 223. https://doi.org/10.3390/jof11030223

AMA Style

Song H-J, Li X-F, Pei X-R, Sun Z-B, Pan H-X. Transcription Factors in Biocontrol Fungi. Journal of Fungi. 2025; 11(3):223. https://doi.org/10.3390/jof11030223

Chicago/Turabian Style

Song, Han-Jian, Xiao-Feng Li, Xin-Ran Pei, Zhan-Bin Sun, and Han-Xu Pan. 2025. "Transcription Factors in Biocontrol Fungi" Journal of Fungi 11, no. 3: 223. https://doi.org/10.3390/jof11030223

APA Style

Song, H.-J., Li, X.-F., Pei, X.-R., Sun, Z.-B., & Pan, H.-X. (2025). Transcription Factors in Biocontrol Fungi. Journal of Fungi, 11(3), 223. https://doi.org/10.3390/jof11030223

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