Acta agriculturae Slovenica, 119/3, 1–11, Ljubljana 2023 doi:10.14720/aas.2023.119.3.2971 Review article / pregledni znanstveni članek Mycoviruses: trends in plant-fungus-mycovirus interactions and ‘biocon- trol’ prospects in agriculture and the environment Elias Mjaika NDIFON 1, 2 , Gilbert Nchongboh CHOFONG 3 Received December 23, 2022; accepted August 06, 2023. Delo je prispelo 23. decembra 2022, sprejeto 6. avgusta 2023 1 Alex Ekwueme Federal University Ndufu-Alike, Faculty of Agriculture, Department of Crop Science, Abakaliki, Nigeria 2 Corresponding author, e-mail: emndi4nn@yahoo.com 3 Julius Kühn Institut, Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, Germany Mycoviruses: trends in plant-fungus-mycovirus interactions and ‘biocontrol’ prospects in agriculture and the environment Abstract: Mycoviruses are cosmopolitan in plants, ani- mals, fungi, bacteria, in soils, and water. There is a scarcity of information about them, which necessitated this review to pro- vide some leads on where research should focus. Mycoviruses are able to persist in disparate types of hosts by utilizing diverse measures. They may engage either parasitic, pathogenic, or mutualistic tendencies. Mycoviruses employ many existential strategies that can be utilized by man. Hypovirulence may be induced in fungal hosts by mycoviruses via RNA silencing, al- teration of genetic expression, and disruption of the transcrip- tome. Mycoviruses interact with killer phenotypes of yeasts and Ustilago spp. and proffer advantages to these fungi. Mycovirus interaction with some plants result in provision of thermal tol- erance to plants. Based on their mode of microbe destruction mycoviruses may be used for waste disposal and termination of some life processes. For instance, grazer viruses completely oxidize the organic content of their host into carbon dioxide and inorganic nutrients, while lytic viruses release the organic material from their hosts without modification. Viruses may be utilized to facilitate the exchange of genetic material from one host to another. However, pathogenic mycoviruses exist espe- cially in mushrooms. Key words: control, disease complex, fungi synergy, in- tegrated pest management, phage, relationship Mikovirusi: trendi v interakcijah rastlina-gliva-mikovirus in izgledi ‘biokontrole’ v kmetijstvu in okolju Izvleček: Mikovirusi so kozmopoliti v rastlinah, živalih, glivah, bakterijah, v tleh in vodi. O njih je le malo informacij, kar je bilo vodilo za ta pregled kot smernico za bodoče raziska- ve. Mikovirusi so sposobni bivati v različnih gostiteljih z različ- nimi načini preživetja. Uporabljajo lahko zajedalske, patološke ali mutualistične strategije, ki jih lahko koristimo tudi ljudje. Hipovirulenca je v glivnem gostitelju lahko vzpodbujena z mi- kovirusi preko RNA utišanja, spremembe izražanja genov in razgradnje transkriptoma. Mikovirusi sodelujejo z ubijalskimi fenotipi kvasovk in sneti (Ustilago spp.), kar daje prednosti tem glivam. Sodelovanje mikovirusov in nekaterih rastlin rezultira v njihovi toleranci na termperaturne spremembe. Na osnovi njihovega uničevanja mikrobov bi lahko mikoviruse uporabi- li za razgradnjo odpadkov in za zaključek nekaterih bioloških procesov. Na primer, virusi, ki se “pasejo” na mikrobih (grazer viruses) popolnoma oksidirajo organsko vsebino gostitelja do ogljikovega dioksida in anorganskih hranil med tem, ko litični virusi sproščajo organske snovi iz njihovih gostiteljev. Virusi se lahko uporabljajo za olajševanje izmenjave dednine iz enega gostitelja v drugega. Še posebej veliko patogenih mikovirusov živi v gobah. Ključne besede: nadzor, bolezenski kompleks, glivno so- delovanje, integrirano uravnavanje škodljivcev, fag, odnosi Acta agriculturae Slovenica, 119/3 – 2023 2 E. M. NDIFON and G. N. CHOFONG 1 INTRODUCTION The discovery of bacteriophages and ultimately of mycoviruses/mycophages has been a great leap forward for researchers. Mycoviruses (mycophages) are a group of viruses that are naturally associated with fungi (in- cluding fungi associated with plants, mushrooms, mi- crobes, soil, and water) (SDSU, 2021; Hu et al., 2022). Mycoviruses interact with four phyla of true fungi (eu- fungi): the Chytridiomycota (chytrids), Zygomycota (bread molds), Ascomycota (yeasts and sac fungi), and the Basidiomycota (club fungi). The relation of myovi- ruses with Pseudofungi like those in the Phyla Oomycota and Hyphochytridiomycota (in Kingdom Chromista i.e. some water moulds or Straminipila) and as well as slime moulds - other fungi-like organisms (Ghabrial and Suzu- ki, 2009; Pearson et al., 2009; Beakes et al., 2014; Xie and Jiang, 2014; Zhong et al., 2016; Calvalier-Smith, 2018; Myers et al., 2020; Zhou et al., 2021; Hough et al., 2023) was not covered in this review. Fungi are frequently in- fected with two or more unrelated viruses (Ghabriel and Suzuki, 2008; Howitt et al., 2006). Fungi may also act as vectors of viruses of higher life forms (Adams, 1991). The mycovirus-host fungus relationship take the form of mu- tualistism, commensalism, or parasitism. Viruses associated with fungi or mycoviruses as- sociated with higher life forms usually do not induce symptoms in their host fungi, except in the case of hyper- virulence (increase in virulence of the symptoms of the infection of the fungus on its host: extremely or unusu- ally virulent) and hypovirulence (decrease of the symp- toms of the infection of the fungus on its host: extremely or unusually reduced virulence) (Ghabrial and Suzuki (2009). On the other hand, the diseases on some fungi and mushrooms/macrofungi are caused by the mycovi- ruses themselves. Ghabrial and Suzuki (2009) reported that mycoviruses are associated with latent infections of all major groups of plant pathogenic fungi. Some myco- viruses cause debilitating diseases and/or reduce the vir- ulence of their phytopathogenic fungal hosts and these may lead to attenuation (hypovirulence) or enhancement of fungal virulence (hypervirulence). Kong et al. (1997), Nuss (2005), Ong et al. (2016), García-Pedrajas et al. (2019), and Siddique (2020) reiter- ated that some mycoviruses reduce the virulence of the host fungus (hypovirulence), which can make the fungus less harmful to plants, whereas other mycoviruses have been shown to enhance the virulence of the host fungus (hypervirulence). However mycoviruses may be patho- genic on their hosts. For instance, la France virus disease of cultivated mushrooms (Agaricus bisporus (J.E. Lange) Pilat was first reported in the late 1940s (Hollings, 1962; Ghabrial and Suzuki, 2009). Alvarez-Jubete et al. (2011) reported that Mushroom Virus X affects important traits associated with mushroom quality (including colour and appear- ance). Another instance is the effective virus-control of chestnut blight (caused by the fungus - Cryphonectria parasitica (Murrill) M.E. Barr) as a consequence of the infection of the fungus by the mycovirus - Cryphonec- tria parasitica hypovirus 1 (CHV1) in Europe (Hollings, 1962). The natural distribution of mycoviruses seems to follow a normal distribution spectrum with avirulent, mutualistic, and virulent members being commonplace. Many mycoviruses have been shown to be mutualists. Mycoviruses can alter host’s tolerance to environ- mental stresses, e.t.c. Most of these mycoviruses have not been described to date or are unrelated to any known vi- ruses. According to the PVEN (Plant Virus Ecology Net- work) (2011) viruses are widely distributed entities that can cause substantial mortality of plants and animals. Secondly, viruses can move genetic elements between hosts e.g. potentially between genetically engineered plants and non-target species. Studies of host–mycovirus–vector interactions in nature offer both opportunities and challenges that will ultimately produce multi-faceted understanding of the role of mycoviruses in shaping ecological and evolution- ary dynamics (Fargette et al., 2006; PVEN, 2011). Studies of pathogenic viruses have probably left out a vast ma- jority of viruses. Mycovirus diversity is another area of mycovirology that has barely been explored. Virtually all plant (and perhaps all animal) species harbor pathogenic or mutualistic fungi in their tissues. Kotta-Loizou (2019) pointed out that our current understanding of mycoviruses is not as detailed as in other fields of virology and currently not based on cut- ting-edge methodology. The general assumption is that much information is yet to be generated on mycoviruses especially considering that the majority of these myco- viruse are viruses of microorganisms (VOMs). With the advent of high-throughput sequencing and bioinformat- ics analysis pipelines in mycovirology, different types of mycoviruses are being discovered in all the four phyla of true fungi. Recent research has revealed an unexpected diversity of these mycoviruses, their interactions with plants, and modulation of some plant biotic and abiotic stresses. Mycoviruses can be useful in molecular biology and biotechnology. We are just beginning to tap this poten- tial. This appraisal was set up to document the literature on mycoviruses, diversity of currently known host-par- asite interactions and biocontrol prospects possible in agriculture and the environment. Acta agriculturae Slovenica, 119/3 – 2023 3 Mycoviruses: trends in plant-fungus-mycovirus interactions and ‘biocontrol’ prospects in agriculture and the environment 2 PLANT-FUNGI-MYCOVIRUS INTERAC- TIONS Recently, researchers reported that viruses are the most abundant and dynamic entities in the hydro- sphere (Weinbauer, 2004; Suttle, 2007) although Payet et al. (2014) contested that little is known about viruses in these water habitats. Viruses are major agents of mi- crobial mortality and account for about 50% of bacterial mortality in the hydrosphere (Kirchman, 2018). Daily, between 20–50% of heterotrophic bacteria, cyanobacte- ria and phytoplankton are infected by viruses (Brussaard, 2004; Suttle, 2007). Viral lysis releases organic cellular content and nu- trients necessary for autotrophic and heterotrophic mi- crobial life forms (Shelford et al., 2012). This essentially result in major changes in the biogeochemical nutrient (carbon, nitrogen and phosphorus) cycles and flow of en- ergy in the oceans (Suttle, 2007; O‘Malley, 2016). Kirch- man (2018) stated that apparently viruses infecting fungi do not lyse their host and are rather transmitted from one fungus to another intracellularly, without being re- leased into the external environment. True mycoviruses demonstrate an ability to be transmitted and infect other still healthy fungi cells. The interaction between the mycovirus (Cryphonectria para- sitica hypovirus 1 (CHV1)) with Cryphonectria parasitica (the causative agent of chestnut blight)), in Europe re- sulted in hypovirulence in the fungus. Thus the blight was controlled whenever a virulent strain of the virus at- tacked the plant. However, this ‘biocontrol’ is restricted to a small number of plant vegetation compatibility groups (pVCGs). For instance, in North America plant vegeta- tion incompatibility reactions prevent plant roots from fusing and exchanging their cytoplasmic content, thus hypovirulent strains of mycoviruses are hindered from spreading (See Anagnostakis et al., 1998). Hence in the USA, China and Japan this ‘biocontrol’ measure tends to fail due to a large number of different plant VCGs (Liu and Milgroom, 2007). The natural host range of a mycovirus is supposed to be confined to taxa performing cytoplasmic fusion (Buck, 1986) but some mycoviruses can replicate in un- related taxa not allowing anastomosis of the fungal hy- phae. This is the case with two fungal species (Sclerotinia homoeocarpa Benn. and Ophiostoma novo-ulmi Braiser) associated with chestnut tree (Deng and Boland, 2003; Nuss et al., 2005). Chen et al. (1994) extended the natural host range of CHV1 to several phylogenetically unrelated fungal species associating with chestnut and supported their hypothesis using in vitro virus transfection tech- niques. In line with this, CHV1 can also propagate in the genera Endothia Murrill species (Cryphonectriaceae) and Valsa Fr. species (Diaporthales, Valsaceae) (Ghabriel and Suzuki, 2008). Various studies revealed that the same mycovirus can be transmitted between different species of the same genus found in the same habitat. For instance the same mycovirus was transmitted between Cryphonectria spp. (i.e.; Cryphonectria parasitica and Cryphonectria sp.), Sclerotinia spp. (i.e.; Sclerotinia sclerotiorum (Lib.) de Bary and Sclerotinia minor Jagger), and Ophiostoma spp. (Ophiostoma ulmi (Buism.) Nannf. syn. Ceratocystis ulmi (Buism.) C. Moreau and Ophiostoma novo-ulmi) (Liu et al., 2003; Melzer et al., 2005). Moreover, interspecies transmission has been re- ported between Fusarium poae (Peck) Wollenw and Aspergillus species (van Diepeningen et al., 2006). The mode of transmission in these instances is unknown and is still subject to guess work. Mycovirus infections are common even in humans as is the case with the mycovi- ruses in Aspergillus fumigatus Fresenius (i.e. AfuPmV-1) and Talaromyces marneffei Segretain, Capponi & Sureau) Samson, Yilmaz, Frisvad & Seffert (i.e. TmPV1) (Kotta- Loizou and Coutts, 2017; Lau et al., 2018). Research on mycoviruses is hindered by many fac- tors amongst which is the lack of appropriate infectiv- ity assays (McCabe et al., 1999) and mixed infection or unknown numbers of infecting viruses. These situa- tions make it difficult to ascribe a particular phenotypic change in the host to a particular virus under investiga- tion. Moreover, neutral co-existence (likely due to co- evolutionary processes) may be in operation in a virus- fungus interaction (Araújo et al., 2003). These difficulties have hindered the studies on hypovirulent strains of my- coviruses. This is often due to lack of correlation between phenotypes and specific genomes or particular metabolic pathways (Xie et al., 2006). Equilibrium offsetting conditions could also be responsible for changes in host-parasite relationships. Possibly, this is due to changes from mutual to neutral then to deleterious, and so on. Other relationships exist in the same habitat. Vidhyasekaran (2004) reported that satellite viruses are dependent on other viruses to sup- ply the enzyme replicase and other enzymes necessary for replication. A satellite virus associated with Tobacco necrosis is not serologically related to Tobacco necrosis virus (TNV). TNV multiply indefinitely without causing the production of a satellite virus. However, the satellite virus is entirely dependent on TNV for its multiplication. The satellite virus has a viral coat and a small genome of its own. Both viruses are transmitted among roots by the fungus Olpidium brassicae (Woronin) P .A. Dang. Sometimes satellite viruses also have satellite RNAs e.g., the satellite of Tobacco necrosis virus (TNV) has a Acta agriculturae Slovenica, 119/3 – 2023 4 E. M. NDIFON and G. N. CHOFONG small satellite RNA that is dependent on Tobacco ne- crosis virus for replication and on the satellite virus for encapsulation (Vidhyasekaran, 2004). Moreover, various plant viruses (of the Tombusviridae) generate defective interfering RNA viruses during replication (Rubio et al., 1999). This new relationship may result in viral symptom amelioration (Roux et al., 1991; Kong et al., 1997) or in- tensification as observed in the case of the Turnip crin- kle virus (Li et al., 1989; Kong et al. 1997). Hough et al. (2023) stated that mycoviruses have the ability to reduce the virulence of their hosts. Rowley (2016), and Moonil et al. (2015) reported that asymptomatic associations with fungi and by myco- viruses are very common. Furthermore, fungi are often associated with unrelated viruses or ‘defective dsRNA’ and/or satellite dsRNA (Howitt et al., 2006; Ghabrial and Suzuki, 2009). Moreover, some viruses simply use fungi as vectors (which differentiate them from mycoviruses) since they do not replicate inside the fungus (Adams, 1991). Tran et al. (2019) reported that very little is known about mycoviruses infecting Monilinia species although virus-like particles (VLPs) resembling those of partiti- viruses, totiviruses, tobraviruses, and furoviruses have been reported from these hosts. McCabe et al. (1999) and Rowley (2016) argued that the virulence of a virus is ultimately limited by the need for the host to survive and thus permit the virus to replicate and continue to exist. This has not been proven. Based on the obligate parasitic nature of viruses, the majority of mycoviruses should have some negative effect(s) on fungal growth or survival. This depends on the mode of infection and the population of the viruses. More than 250 mycoviruses infect true fungi in the afore- mentioned phyla (Bozarth, 1972; Rochon et al., 2004; Hacker et al., 2005; Ghabrial and Suzuki, 2009; Rowley, 2016; Tran et al., 2019; Xia et al., 2020). Many viruses can simultaneously infect a single fungus (Hollings, 1962). Based on O‘Malley (2016) viruses may operate in hosts with or without being pathogenic. De Filippis and Villarreal (2000) stated that a competition between diffe- rent viral strains or individuals inside a host may result in selection of the fittest. Viruses have both general and specific requirements for replication and existence. The direction and extent of this change is determined by a combination of stochastic and environmental factors that are specific for a given time, space, and taxon. Though viruses of plants have long been recognized as important components of plant ecosystems, only a few notable mycovirus have been studied in detail. Marzano et al. (2015) reported that a comprehensive picture of mycoviral diversity is lacking. Tran et al. (2019) lamented that the influence of mycoviruses on the ecosystem has not been well studied. For instance, the lack of studies on how some mycoviruses reduce the ability of their fungal host to cause plant diseases. Besides, it has been assumed that the natural host range of mycoviruses is confined to closely related vegetation-compatibility groups (VCGs) which allow fusion of cytoplasm (Buck, 1986). These assumptions may or may not be true, and are based on assumptions. Zhang et al. (2020) attested that it is unclear how mycovirus that cause hypovirulence prevail in the field. Myers and James (2022) suggested the presence of mutu- alism between mycoviruses and their hosts. Pearson et al. (2009) agreed that our understanding of the interaction between mycoviruses and their hosts is largely limited to a few well‐studied, possibly atypical systems. Coupled with the problem of mixed infections by multiple viruses (for example the mixed infection of Botrytis cinerea virus F (BCVF) and Botrytis virus X (BVX) in Botrytis cinerea Pers.) it may not be easy to ascribe a definite role to a mycovirus (Howitt et al., 2006). De Filippis and Villarreal (2000) emphasized that viral infection of a host may not necessarily involve tissue destruction, mortality or even full/partial mobilization of host antiviral mechanisms. Indeed, virus association with hosts may result in mutu- alistic relationships. Most mycoviruses do not cause symptomatic in- fections in their hosts (Ghabrial et al., 2015; Khan et al., 2022). Symptom expression usually occur when there is hypersensitive reaction or incompatibility of the host and parasite. Rowley (2016) reported that fungal hosts defend themselves from mycoviruses using RNA interfe- rence (RNAi), which inhibit mycovirus replication. This may result in cell death thus blocking mycovirus tran- smission. De Filippis and Villarreal (2000) reported that disabling antiviral systems in fungi improves the chances of virus continuity. Bacteria hosts can employ abortive infection as a last resort to escape from the effects of bac- teriophages (Weinbauer 2004). However, many mycovi- ruses interfer with fungal RNAi to prevent the inhibition of their replication. Interactions between vegetatively incompatible plants and fungal isolates culminate in programmed cell death (PCD) thus hindering any ex- change of infected cellular contents (Nuss, 2011). Biella et al. (2002) affirmed that mycovirus infec- tion is influenced by the rate of PCD which could mean that mycoviruses may have developed mechanisms for delaying or hindering occurrence of PCD. RNA silenc- ing (as a defence mechanism in fungi) invoked by fungi against viruses may be made inefficient by some viruses including mycoviruses (Segers et al., 2007). Furthermore, Moonil et al. (2015), and Rowley (2016) pointed out that some mycoviruses are associated with killer satellite vi- rus particles which induce their fungus host to secrete Acta agriculturae Slovenica, 119/3 – 2023 5 Mycoviruses: trends in plant-fungus-mycovirus interactions and ‘biocontrol’ prospects in agriculture and the environment toxins that kill competing fungi. This host fungus ben- eficial mechanism is exhibited by the budding yeasts (Sacharomyces cerevisiae (Desm.) Meyen) in fermented foodstuffs. These dsRNA satellite viruses are dependent on the Totiviridae mycoviruses for their stability. Alone, totivi- ruses have a minimal impact upon S. cerevisiae, but the additional presence of satellite RNAs provide additional capabilities to the virus which is an important example of a beneficial virus system. In fact, these killer systems are so beneficial to their hosts that in some cases, they have resulted in the loss of host RNAi systems (Drinnen- berg et al., 2011; Moonil et al., 2015). Thus symptomless or latent mycoviruses may have unknown functions in their hosts. Somehow, some mycoviruses may act as ex- tra‐chromosomal genes that confer an advantage to the host as can be observed with the killer systems in yeast (Schmitt and Breinig, 2006). Another example of beneficial relationship with a mycovirus, is a three-way symbiosis (among a mycovi- rus, an endophytic fungus, and tropical panic grass). The endophytic fungus (Curvularia protuberata Boedijn), pa- nic grass (Dichanthelium lanuginosum (Elliott) Gould), and other plants can only survive high soil temperatures in the presence of the mycovirus (Márquez et al., 2007; Moonil et al., 2015). The mycovirus in turn obtains its basic necessities from its hosts. The mechanisms invol- ves two distinct viral dsRNAs. A mutualistic relationship is also found in an interaction among Trichoderma Pers. species and their mycoviruses, and the host plant (Beilei et al., 2020). The fungus is required for thermal tolerance of the plants. A parasite often tend to reduce its impact on its host, thus many parasites have co-evolved to an equilib- rium state resulting in minimal impact. Therefore there is great variability in reactions between a single host and different viruses or dsRNAs. Furthermore, Khan et al. (2022) reported that se- veral types of virus-virus interactions (i.e.; synergistic, antagonistic, and mutualistic interactions) have been reported in fungal hosts. Co-infections of single fungal strains by over ten mycoviruses has been reported for several phytopathogenic fungi, which implies that much work has to be carried out to determine the type of re- lathionships that are created in such co-infections. The effects of a mycovirus seems to be dependent on other factors like environment and presence of other invaders. For instance, Chu et al. (2002) reported a wide spectrum of reactions: reduced growth, increased pigmentation, reduced virulence, and a 60‐fold decrea- sed production of trichothecene mycotoxins associated with a dsRNA during a study of Fusarium graminearum Schwabe (syn Gibberella zeae (Schwein.) Petch) on whe- at. Fine (1975) assumed that mycoviruses may be una- ble to persist if they lower the fitness of their hosts, be- cause they are limited to vertical transmission only. In a detailed study of the effects of dsRNA on the fitness of asexual Aspergillus species, no beneficial effects were ob- served (V an Diepeningen et al., 2006) in vitro. In contrast Tran et al. (2007) observed higher growth rates of BVX‐ infected fungus compared to the same uninfected isolate. It has been postulated that the virus environment is both multidimensional and continually changing thus constantly driving the increase in population fitness. It could also be argued that based on quantity of variables in the environment, viruses exhibit greater mobility through the space of their selective or adaptive environ- ments than do more complex organisms (Moya, 1997). De Filippis and Villarreal (2000) reported that the many levels of viral characters (point mutations, coding region products, multigene assemblages, behavioral traits, and even populational characters) can be conside- red as adaptations and may all endow their possessors with replication advantages. The adaptive viral characters favored within the relatively closed system of one indi- vidual host arise and persist due to intra-host selection pressure, the nature and strength of which is determined by the environmental conditions and other virus strains contained therein. De Filippis and Villarreal (2000) reported that the host’s cellular, tissue, and organismal environments are vitally important selective realms that contribute pro- foundly to the adaptation and diversity of viruses inclu- ding mycoviruses. Also by disabling antiviral systems the virus reduces its own population decline. In the eco- system the fittest mycovirus optimizes its utilization of host resources and does not maximize the utilization of host resources. This permits them to continue to persist despite the intrahost selection pressure. Thus the fittest individuals are not the ones that maximizes the use of host resources, rather the fittest individuals are those that optimizes the utilization of host resources. To ensure continuity in most viral infections, less than 1 % of the susceptible host tissue is actually infec- ted/harvested (Griffin, 1997). Such a host-parasite inte- raction could persist and be observed as any of the for- ms of guilds depending on the colorations and flavours added to it. In micro-ecosytems, the essential portion of the environment that is of most concern is the inorga- nic nutrients and energy derivable from the hosts. The mycovirus should therefore be properly adapted to avo- id depleting these resources unnecessarily. In the case of bacteriophages, they impact the movement of nutrients and energy within the micro-ecosystems primarily by ly- sing bacteria and secondarily by encoding of exotoxins (a subset of which are capable of solubilizing the biolo- Acta agriculturae Slovenica, 119/3 – 2023 6 E. M. NDIFON and G. N. CHOFONG gical tissues of living hosts/animals) (Weinbauer, 2004). Much has been reported already about viruses of plants, humans and animals so this will only be discussed brie- fly as antagonistic components of the micro-ecostystem. Kazinczi et al. (2004) pointed out that weeds, as alterna- tive hosts of plant viruses can act as alternative nutrient sources for viruses and virus vectors. Weeds play im- portant role in virus ecology and epidemiology. Alemu et al. (2002) reported that chronic infection with viruses is a major constraint that often force farmers to ban hot pepper production. This can result in decrease in the po- pulation of virus and mycovirus entities in an area. The presence of infected weeds throughout the year means, that they are reservoirs and sources of viruses for secon- dary spread. Yudin et al. (1986) reported that western flower thrips (Frankliniella occidentalis Pergande, 1895 - a known vector of tomato spotted wilt virus, was found to be associated with 48 plant species growing within the Kula vegetable-growing region on the island of Maui, Hawaii. This type of vector can be very vital for continual existence of mycoviruses even when the host plant and fungus are facing difficult times in the dry season. Weeds are widely infected by viruses. For instance, McGovern et al. (2008) reported that Solanum viarum Dunal (the invasive tropical soda apple) in Florida was infected by nine viruses which can in turn infect solanaceous crops. 3 IMPLICATION OF MYCOVIRUS IN- TERACTIONS WITH PLANTS IN CROP PROTECTION: TRENDS IN RESEARCH, APPLICATIONS, AND ‘BIOLOGICAL ’ CONTROL POTENTIALS USING THESE AGENTS We have just seen how the killer phenotypes can provide some advantages to yeasts and Ustilago (Pers.) Roussel species due to their interactions with viruses (Schmitt and Breing, 2002; Marquina et al., 2007). Killer isolates secrete proteinous toxins (mostly cell wall de- grading enzymes) against sensitive cells of the same or closely related species, while the producing cells them- selves are immune. These types of killer isolates could be beneficial in medicine, agriculture and industry (Schmitt and Breing, 2002). We have also seen that three-part interaction pro- vide thermal tolerance by the plant (Marquez et al., 2007). Another example is the A78 virus of Aspergillus fumigatus Fresen causing mild hypervirulence on Gal- leria mellonella (L., 1758) (Greater wax moth) (Ozkan and Coutts, 2015). Likewise, TmPV1 associated with T. marneffei caused hypervirulence on T. marneffei in the mouse host (Lau et al., 2018). Liu et al. (2022) reported that mycovirus Stemphyli- um lycopersici alternavirus 1 (SlAV1) from a necrotroph- ic plant pathogen (Stemphylium lycopersici) that causes altered colony pigmentation and hypovirulence by spe- cifically interfering host biosynthesis of Altersolanol A, a polyketide phytotoxin. Li et al. (2019) reported that most Fusarium myco- viruses establish latent infections, but some mycoviruses such as Fusarium graminearum virus 1 (FgV1), Fusarium graminearum virus-ch9 (FgV-ch9), Fusarium gramine- arum hypovirus 2 (FgHV2), and Fusarium oxysporum f. sp. dianthi mycovirus 1 (FodV1) cause hypovirulence. Khan et al. (2023) emphasized that among members of the genus Sclerotinia, a huge number of mycoviruses have been identified; some of them have a hypovirulent effect on the fitness of their fungal hosts. Zhou et al. (2021) revealed that mycoviruses have been associated with plant adaptation to extreme envi- ronments, conferring heat tolerance to plants that con- tain fungal endophytes. They reported that endophytic fungi, can confer fitness to the host plants. It is unclear whether biological factors can modulate the parasitic and mutualistic traits of a fungus. Kotta-Loizou (2021) affirmed that in fungus-mycovirus-environmental in- teractions, the environment and both abiotic and biotic factors play crucial roles in whether and how mycovirus mediated phenotypes are manifest. Connor (2021) reported that soybean leaf-associ- ated gemycircularvirus-1 (SlaGemV-1) is capable of in- ducing hypovirulence in the highly pathogenic fungus Sclerotinia sclerotiorum as does the hypovirus 1 (CHV1) controlling C. parasitica in chestnut in Europe. It is an excellent model organism for studying hypovirulence in fungi (Anagnostakis et al., 1998; Liu and Milgroom, 2007). Kirchman (2018) pointed out that viruses infecting fungi do not appear to lyse their host. The use of myco- virus can open many avenues for handling waste and de- composition, or terminating some life processes. For in- stance grazers completely oxidize the organic content of their host into carbon dioxide and inorganic nutrients. A third mode of employing viruses may theoretically be to facilitate the exchange of genetic material from one host to another. Most of these processes have been relatively poorly studied (Pearson et al., 2009). Hypovirulence may be induced in hosts by myco- viruses via RNA silencing, alteration of genetic expres- sion, and disruption of the transcriptome that can re- sult in phenotypic changes like reduction in growth or changes in pigmentation (Nuss, 2005). Alterations of miRNAs expressions using viral suppressors of RNA si- lencing (VSRs) occurs by applying papain-like protease p29 (Segers et al., 2006) and potyvirus HC-Pro (Maia et Acta agriculturae Slovenica, 119/3 – 2023 7 Mycoviruses: trends in plant-fungus-mycovirus interactions and ‘biocontrol’ prospects in agriculture and the environment al., 1996). Also, C. parasitica when infected by the hy- povirulence-inducing mycovirus undergoes RNA silenc- ing thereby affecting the MAPK cascade and G-protein signaling. Moreover, direct disruption of the fungal tran- scriptome may occur (Nuss, 2005). Proof of the ability of a mycovirus being able to con- trol a pathogen in the field is either scarse or unavailable (Griffin 1986, MacDonald et al. 1991) but mycoviruses have been shown to be able to control fungi in modified environments (MacDonald et al., 1991; Milgroom et al., 2004). Two major forms of defense signaling include: sys- temic acquire resistance (SAR) and induced systemic re- sistance (ISR). (Vidhyasekaran, 2015). Another theoriti- cal approach usable to increase a plant resistance against pathogenic infection is resistance priming like that in- volved in SsHADV-1 allowing S. sclerotiorum to induce priming in plants. ‘Priming is the process of inoculating plants, often the seeds, with beneficial microorganisms to improve nutrient use efficiency and to potentially improve resistance to pathogens’ (Rakshit et al., 2015). Actually, Qu et al. (2020) demonstrated that SsHADV-1-infected, hypovirulent S. sclerotiorum is reprogrammed to act as a beneficial, bio-priming mycorrhiza in rapeseed due to Sclerotinia Fuckel stem rot reduction and improved yield. Mycoviruses have been shown to be involved in all forms of interactions (e.g. mutualism) with fungi hosts. In the future, mycoviruses may be required for manipulating micro-ecosystems within plants, humans, animals and so on. They are simple enough for direct insertion and removal of genes here and there if the right equipment is available. However, pathogenic mycoviruses have been reported and they can severely ravage host populations especially domesticated mushrooms e.g. la France dis- ease on Agaricus bisporus. Thus, mycoviruses have to be controlled in fungus-fungus, fungus-plant, fungus-ani- mal systems, etc. Ruiz-Padilla et al. (2021) propounded that products based on microorganisms (including mycoviruses senso lato) can be used in biocontrol strategies alternative to chemical control. Keçeli (2017) reported that the use of mycoviruses in the treatment of invasive fungal infec- tions in humans has not been suggested yet. Xie and Jiang (2014) suggested that fungal vegetative incompatibility is likely to be the limiting factor in the widescale utilization of mycoviruses to control crop diseases. 4 CONCLUSION Past, present and future trends in mycovirus re- search are of interest to humans. They can reveal the prospects of mycoviruses in agriculture and the environ- ment in terms of pathogen control and amelioration of the environment. Use of mycoviruse to induce hypoviru- lence in fungi host isolates has shown great potentials e.g. using the A78 virus of Aspergillus fumigatus, TmPV1 on T. marneffei, soybean leaf-associated gemycircular- virus-1 (SlaGemV-1) in Sclerotinia sclerotiorum, the hypovirus 1 (CHV1) in Cryphonectria parasitica. Hypo- virulence may be induced in fungi hosts by mycoviruses via RNA silencing, alteration of genetic expression, and disruption of the transcriptome which can result in phe- notypic changes like reduction in growth or changes in pigmentation. Moreover, direct disruption of the fungal transcriptome may occur. Another approach to increase a plant’s resistance against pathogenic infection is resist- ance priming that may be required for manipulating mi- cro-ecosystems within the plants. However, pathogenic mycoviruses have been reported and they can severely ravage host populations especially domesticated mush- rooms 5 REFERENCES Adams, M. J. (1991). 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