New Insights into Mycoviruses and Exploration for the Biological Control of Crop Fungal Diseases

Xiè, Jiǎtāo; Jiāng, Dàohóng

doi:10.1146/annurev-phyto-102313-050222

Cited by 368 publications

(309 citation statements)

References 138 publications

Supporting

Mentioning

275

Contrasting

Unclassified

Order By: Relevance

“…These genes could then be disrupted as described in this report to broaden the effectiveness of the SD strains. Both the comparative genomics approach for identifying vic genes and the multilocus vic gene disruption strategy to promote mycovirus transmission should find general applicability for enhancing the biological control potential for the growing list of pathogenic fungi/mycovirus hypovirulence systems (2,6,39).…”

Section: Discussionmentioning

confidence: 99%

Engineering super mycovirus donor strains of chestnut blight fungus by systematic disruption of multilocus vic genes

Zhang

Nuss

2016

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Transmission of mycoviruses that attenuate virulence (hypovirulence) of pathogenic fungi is restricted by allorecognition systems operating in their fungal hosts. We report the use of systematic molecular gene disruption and classical genetics for engineering fungal hosts with superior virus transmission capabilities. Four of five diallelic virus-restricting allorecognition [vegetative incompatibility (vic)] loci were disrupted in the chestnut blight fungus Cryphonectria parasitica using an adapted Cre-loxP recombination system that allowed excision and recycling of selectable marker genes (SMGs). SMG-free, quadruple vic mutant strains representing both allelic backgrounds of the remaining vic locus were then produced through mating. In combination, these super donor strains were able to transmit hypoviruses to strains that were heteroallelic at one or all of the virus-restricting vic loci. These results demonstrate the feasibility of modulating allorecognition to engineer pathogenic fungi for more efficient transmission of virulence-attenuating mycoviruses and enhanced biological control potential.M ycovirus infections have been reported to reduce virulence (hypovirulence) for a wide range of plant pathogenic fungi, providing potential for biological disease control (1-6). For hypovirulence to be effective, the virulence-attenuating viruses must be efficiently transmitted from infected hypovirulent strains to uninfected virulent strains (5, 7). Mycoviruses generally have evolved exclusive intracellular lifestyles (8). With very few exceptions (9), mycovirus infections cannot be initiated by exposure of uninfected hyphae to cell extracts or secretions from infected fungal isolates. Transmission is limited to intracellular mechanisms, vertical transmission through asexual spores, and horizontal transmission through anastomosis (fusion of hyphae).Horizontal mycovirus transmission to uninfected isolates of the same fungal species is complicated by nonself allorecognition genetic systems, termed "heterokaryon" or "vegetative incompatibility" (vic), which operate widely in filamentous fungi (10). Interactions between genetically distinct individuals of the same species result in an incompatible reaction that triggers localized programmed cell death (PCD), forming a line of demarcation, or barrage, along the zone of contact (10-12) and restricting cytoplasmic transmission of viruses and other cytoplasmic elements (1,(13)(14)(15).A negative correlation between vic diversity and virus transmission has been reported for several fungal hosts (1, 16), but has most extensively been demonstrated for the chestnut blight fungus Cryphonectria parasitica infected with virulence-attenuating hypoviruses (7,(17)(18)(19)(20). Genetic analyses have defined six diallelic vic genetic loci for C. parasitica (21). These loci and associated genes were recently identified at the molecular level through a comparative genomics approach (22, 23) ( Table 1). Independent gene disruption analysis of 12 genes associated with these loci (22, 23) ...

show abstract

Section: Discussionmentioning

confidence: 99%

Engineering super mycovirus donor strains of chestnut blight fungus by systematic disruption of multilocus vic genes

Zhang

Nuss

2016

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…Consequently, there is an urgent need to develop novel methods to reduce the dosage of chemicals used to control plant diseases. In nature, some mycoviruses are known to be responsible for debilitation/hypovirulence of plant pathogens, and hence, they represent potential agents that can be exploited in combating fungal disease (3)(4)(5). Moreover, a classical example of mycovirus-based biocontrol was implemented successfully in Europe to help manage chestnut blight caused by Cryphonectria parasitica (6).…”

mentioning

confidence: 99%

“…Because there is a lack of resistant cultivars, Sclerotinia diseases are controlled at low efficiency via fungicides and cultural approaches, e.g., crop rotation (29). Since hypovirulence and dsRNA elements (possibly mycoviruses) in S. sclerotiorum were first reported in the early 1990s (30), many novel mycoviruses, including members of the families Hypoviridae, Alphaflexiviridae, Partitiviridae, and Narnaviridae and an unassigned, single-stranded DNA (ssDNA) mycovirus, were isolated recently from S. sclerotiorum and are well characterized (5,8,9,31). Furthermore, most of these viruses were shown to be responsible for reducing the virulence and growth of S. sclerotiorum (5,9,31,32).…”

mentioning

confidence: 99%

A Novel Partitivirus That Confers Hypovirulence on Plant Pathogenic Fungi

Xiao

Chéng

Tang

et al. 2014

J Virol

Self Cite

128

103

View full text Add to dashboard Cite

Members of the family Partitiviridae have bisegmented double-stranded RNA (dsRNA) genomes and are not generally known to cause obvious symptoms in their natural hosts. An unusual partitivirus, Sclerotinia sclerotiorum partitivirus 1 (SsPV1/WF-1), conferred hypovirulence on its natural plant-pathogenic fungal host, Sclerotinia sclerotiorum strain WF-1. Cellular organelles, including mitochondria, were severely damaged. Hypovirulence and associated traits of strain WF-1 and SsPV1/WF-1 were readily cotransmitted horizontally via hyphal contact to different vegetative compatibility groups of S. sclerotiorum and interspecifically to Sclerotinia nivalis and Sclerotinia minor. S. sclerotiorum strain 1980 transfected with purified SsPV1/WF-1 virions also exhibited hypovirulence and associated traits similar to those of strain WF-1. Moreover, introduction of purified SsPV1/WF-1 virions into strain KY-1 of Botrytis cinerea also resulted in reductions in virulence and mycelial growth and, unexpectedly, enhanced conidial production. However, virus infection suppressed hyphal growth of most germinating conidia of B. cinerea and was eventually lethal to infected hyphae, since very few new colonies could develop following germ tube formation. Taken together, our results support the conclusion that SsPV1/WF-1 causes hypovirulence in Sclerotinia spp. and B. cinerea. Cryo-EM (cryo-electron microscopy) reconstruction of the SsPV1 particle shows that it has a distinct structure with similarity to the closely related partitiviruses Fusarium poae virus 1 and Penicillium stoloniferum virus F. These findings provide new insights into partitivirus biological activities and clues about molecular interactions between partitiviruses and their hosts. IMPORTANCEMembers of the Partitiviridae are believed to occur commonly in their phytopathogenic fungal and plant hosts. However, most partitiviruses examined so far appear to be associated with latent infections. Here we report a partitivirus, SsPV1/WF-1, that was isolated from a hypovirulent strain of Sclerotinia sclerotiorum and describe its biological and molecular features. We have demonstrated that SsPV1 confers hypovirulence. Furthermore, SsPV1 can infect and cause hypovirulence in Botrytis cinerea. Our study also suggests that SsPV1 has a vigorous ability to proliferate and spread via hyphal contact. SsPV1 can overcome vegetative incompatibility barriers and can be transmitted horizontally among different vegetative compatibility groups of S. sclerotiorum, even interspecifically. Cryo-EM reconstruction of SsPV1 shows that it has a distinct structure with similarity to closely related partitiviruses. Our studies exploit a novel system, SsPV1 and its hosts, which can provide the means to explore the mechanisms by which partitiviruses interact with their hosts.

show abstract

“…As a part of the virus world, mycoviruses may play an ecologically important role in nature (2). Furthermore, hypovirulence-associated mycoviruses that infect fungal plant pathogens may have potential to control plant diseases (1,(3)(4)(5). Moreover, mycoviruses could potentially be explored to control human fungal diseases (6).…”

mentioning

confidence: 99%

Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector

Liu

Xiè

Chéng

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

147

View full text Add to dashboard Cite

Mycoviruses are usually transmitted horizontally via hyphal anastomosis and vertically via sexual/asexual spores. Previously, we reported that a gemycircularvirus, Sclerotinia sclerotiorum hypovirulenceassociated DNA virus 1 (SsHADV-1), could infect its fungal host extracellularly. Here, we discovered that SsHADV-1 could infect a mycophagous insect, Lycoriella ingenua, and use it as a transmission vector. Virus acquired by larvae feeding on colonies of a virus-infected strain of S. sclerotiorum was replicated and retained in larvae, pupae, adults, and eggs. Virus could be transmitted to insect offspring when larvae were injected with virus particles and allowed to feed on a nonhost fungus. Virus replication in insect cells was further confirmed by inoculating Spodoptera frugiperda cells with virus particles and analyzing with RT-PCR, Northern blot, immunofluorescence, and flow cytometry assays. Larvae could transmit virus once they acquired virus by feeding on virus-infected fungal colony. Offspring larvae hatched from viruliferous eggs were virus carriers and could also successfully transmit virus. Virus transmission between insect and fungus also occurred on rapeseed plants. Virus-infected isolates produced less repellent volatile substances to attract adults of L. ingenua. Furthermore, L. ingenua was easily observed on Sclerotinia lesions in rapeseed fields, and viruliferous adults were captured from fields either sprayed with a virus-infected fungal strain or nonsprayed. Our findings may facilitate the exploration of mycoviruses for control of fungal diseases and enhance our understanding of the ecology of SsHADV-1 and other newly emerging SsHADV-1-like viruses, which were recently found to be widespread in various niches including human HIV-infected blood, human and animal feces, insects, plants, and even sewage. mycovirus | biological control | mycophagous insect | mutualism | gemycircularvirus

show abstract

New Insights into Mycoviruses and Exploration for the Biological Control of Crop Fungal Diseases

Cited by 368 publications

References 138 publications

Engineering super mycovirus donor strains of chestnut blight fungus by systematic disruption of multilocus vic genes

Engineering super mycovirus donor strains of chestnut blight fungus by systematic disruption of multilocus vic genes

A Novel Partitivirus That Confers Hypovirulence on Plant Pathogenic Fungi

Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector

Contact Info

Product

Resources

About