Elevated mitochondrial alternative oxidase activity in dsRNA-free, hypovirulent isolates of Cryphonectria parasitica

Mahanti, N.; Bertrand, Helmut; Monteiro-Vitorello, Cláudia Barros; Fulbright, D. W.

doi:10.1006/pmpp.1993.1034

Cited by 33 publications

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“…C. parasitica strains with virulence-attenuating mtDNA mutations have been found in field populations and have been induced under laboratory conditions (8,33,37). In contrast to hypoviruses, mitochondrial hypovirulence also is transmissible sexually (37).…”

Section: Discussionmentioning

confidence: 99%

Differential Transfer and Dissemination of Hypovirus and Nuclear and Mitochondrial Genomes of a Hypovirus-Infected Cryphonectria parasitica Strain after Introduction into a Natural Population

Hoegger

Heiniger

Holdenrieder

et al. 2003

Appl Environ Microbiol

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Biological control of plant diseases generally requires release of living organisms into the environment. Cryphonectria hypoviruses function as biological control agents for the chestnut blight fungus, Cryphonectria parasitica, and hypovirus-infected C. parasitica strains can be used to treat infected trees. We used naturally occurring molecular marker polymorphisms to examine the persistence and dissemination of the three genomes of a hypovirus-infected C. parasitica strain, namely, the double-stranded RNA genome of Cryphonectria hypovirus 1 (CHV1) and the nuclear and mitochondrial genomes of its fungal host. The hypovirus-infected strain was experimentally introduced into a blight-infested chestnut coppice forest by treating 73 of 246 chestnut blight cankers. Two years after introduction, the hypovirus had disseminated to 36% of the untreated cankers and to 35% of the newly established cankers. Spread of the hypovirus was more frequent within treated sprout clusters than between sprout clusters. Mitochondrial DNA of the introduced fungus also was transferred into the resident C. parasitica population. Concomitant transfer of both the introduced hypovirus and mitochondrial DNA was detected in almost one-half of the treated cankers analyzed. The introduced mitochondrial DNA haplotype also was found in three resident isolates from newly established cankers. The nuclear genome of the introduced strain persisted in the treated cankers but did not spread beyond them.Hypovirulence in the chestnut blight fungus, Cryphonectria parasitica (Murr.) Barr, has been responsible for the natural recovery of many European chestnut (Castanea sativa Mill.) stands (reviewed in reference 25). Unlike the situation in Europe, hypovirulence has not become well established in North America except in isolated chestnut stands, and the American chestnut [Castanea dentata (Marsh.) Borkh.] has been reduced to an understory shrub in its natural range due to the disease (reviewed in references 2, 4, 19, 32, and 43).Hypovirulence of C. parasitica is caused by unencapsidated double-stranded RNA (dsRNA) viruses of the family Hypoviridae (13,17,18,26). These viruses are located in the cytoplasm of the fungus and can be transmitted from infected to uninfected C. parasitica strains via hyphal anastomosis (44). Horizontal transmission is restricted by a vegetative incompatibility system (vic) of the fungus involving at least six vic loci (14,15,30). The low diversity of vegetative compatibility (vc) types favors dissemination of the hypovirus and probably is a critical factor in the success of hypovirulence in Europe (7,11,16,34). Dissemination of the hypovirus within a fungal population can occur through infected asexual conidia or mycelial fragments but not through sexual ascospores (reviewed in reference 25).Hypovirulence is being exploited for the biological control of chestnut blight (5, 25, 41). Since the Cryphonectria hypovirus has no extracellular phase, it can be released into a population only by hypovirus-infected C. parasitica strains. T...

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Section: Discussionmentioning

confidence: 99%

Differential Transfer and Dissemination of Hypovirus and Nuclear and Mitochondrial Genomes of a Hypovirus-Infected Cryphonectria parasitica Strain after Introduction into a Natural Population

Hoegger

Heiniger

Holdenrieder

et al. 2003

Appl Environ Microbiol

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“…parasitica with the presence of RNA viruses, particularly those of the hypovirus type, is the paradigm for the causation of hypovirulence by cytoplasmically transmissible genetic factors in phytopathogenic fungi (3,31,32). Therefore, the appearance of cytoplasmically transmissible forms of hypovirulence in C. parasitica strains devoid of viruses was a paradox, particularly since they were isolated from healing cankers on chestnut trees (4,5). The frequent appearance of elevated alternative oxidase activity in the virus-free, attenuated isolates implicated mitochondria in the generation of hypovirulence phenotypes (5).…”

Section: Resultsmentioning

confidence: 99%

“…Therefore, the appearance of cytoplasmically transmissible forms of hypovirulence in C. parasitica strains devoid of viruses was a paradox, particularly since they were isolated from healing cankers on chestnut trees (4,5). The frequent appearance of elevated alternative oxidase activity in the virus-free, attenuated isolates implicated mitochondria in the generation of hypovirulence phenotypes (5). In isolates derived from trees, a direct connection between the attenuated virulence phenotypes and mtDNA mutations cannot be established easily because C. parasitica has a rather large and highly variable mtDNA (27).…”

Section: Resultsmentioning

confidence: 99%

“…Spontaneous natural control of this disease occurs in areas where the fungus is infected by hypovirulence-causing double-stranded RNA (dsRNA) viruses (1)(2)(3). However, some attenuated isolates from recovering chestnut trees exhibit cytoplasmically transmissible hypovirulence but do not contain dsRNAs (4,5). Unlike virulent and dsRNA-containing hypovirulent strains, a high proportion of the virus-free hypovirulent isolates constitutively express high levels of cyanide (CN)-resistant, salicylhydroxamate-sensitive respiration (alternative oxidase activity) (5).…”

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confidence: 99%

“…However, some attenuated isolates from recovering chestnut trees exhibit cytoplasmically transmissible hypovirulence but do not contain dsRNAs (4,5). Unlike virulent and dsRNA-containing hypovirulent strains, a high proportion of the virus-free hypovirulent isolates constitutively express high levels of cyanide (CN)-resistant, salicylhydroxamate-sensitive respiration (alternative oxidase activity) (5). Such strains resemble dsRNA-containing hypovirulent strains in that, relative to virulent strains, they grow more slowly, produce fewer conidia, and form morphologically abnormal colonies.…”

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A cytoplasmically transmissible hypovirulence phenotype associated with mitochondrial DNA mutations in the chestnut blight fungus Cryphonectria parasitica.

Monteiro-Vitorello

Bell

Fulbright

et al. 1995

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

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Mutations causing mitochondrial defects were induced in a virulent strain of the chestnut blight fungus Cryphonectria parasitica (Murr.) Barr The ascomycetous fungus Cryphonectriaparasitica is the causal agent of the blight responsible for the virtual disappearance of chestnut trees (Castanea dentata) from North American forests. Spontaneous natural control of this disease occurs in areas where the fungus is infected by hypovirulence-causing double-stranded RNA (dsRNA) viruses (1-3). However, some attenuated isolates from recovering chestnut trees exhibit cytoplasmically transmissible hypovirulence but do not contain dsRNAs (4, 5). Unlike virulent and dsRNA-containing hypovirulent strains, a high proportion of the virus-free hypovirulent isolates constitutively express high levels of cyanide (CN)-resistant, salicylhydroxamate-sensitive respiration (alternative oxidase activity) (5). Such strains resemble dsRNA-containing hypovirulent strains in that, relative to virulent strains, they grow more slowly, produce fewer conidia, and form morphologically abnormal colonies. These traits suggest that this type of hypovirulence may be affiliated with mitochondrial dysfunctions similar to those found in cytoplasmic mutants of well-characterized filamentous fungi (6, 7), particularly Neurospora, Podospora, and Aspergillus (8,9). Mitochondria also might be involved in the attenuation of Cryphonectria and other fungi by prolonged asexual propagation in the laboratory (10). However, direct evidence for the association of mtDNA mutations with the spontaneous appearance of hypovirulence in dsRNA-free strains of C. parasitica is still lacking.To explore the possible involvement of mitochondrial genes in the attenuation of virulence in C. parasitica, mutations that cause respiratory defects were induced and selected in a highlyThe publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

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Management of Disease Resistance

Saharan

Mehta

Meena

2021

Genomics of Crucifer’s Host-Resistance

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Elevated mitochondrial alternative oxidase activity in dsRNA-free, hypovirulent isolates of Cryphonectria parasitica

Cited by 33 publications

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Differential Transfer and Dissemination of Hypovirus and Nuclear and Mitochondrial Genomes of a Hypovirus-Infected Cryphonectria parasitica Strain after Introduction into a Natural Population

Differential Transfer and Dissemination of Hypovirus and Nuclear and Mitochondrial Genomes of a Hypovirus-Infected Cryphonectria parasitica Strain after Introduction into a Natural Population

A cytoplasmically transmissible hypovirulence phenotype associated with mitochondrial DNA mutations in the chestnut blight fungus Cryphonectria parasitica.

Management of Disease Resistance

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