Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi

Abstract

Viroids are the smallest known infectious agents that are thought to only infect plants. Here, we reveal that several species of plant pathogenic fungi that were isolated from apple trees infected with apple scar skin viroid (ASSVd) carried ASSVd naturally. This finding indicates the spread of viroids to fungi under natural conditions and further suggests the possible existence of mycoviroids in nature. A total of 117 fungal isolates were isolated from ASSVd-infected apple trees, with the majority (85.5%) being an ascomycete Alternaria alternata and the remaining isolates being other plant-pathogenic or -endophytic fungi. Out of the examined samples, viroids were detected in 81 isolates (69.2%) including A. alternata as well as other fungal species. The phenotypic comparison of ASSVd-free specimens developed by single-spore isolation and ASSVd-infected fungal isogenic lines showed that ASSVd affected the growth and pathogenicity of certain fungal species. ASSVd confers hypovirulence on ascomycete Epicoccum nigrum. The mycobiome analysis of apple tree-associated fungi showed that ASSVd infection did not generally affect the diversity and structure of fungal communities but specifically increased the abundance of Alternaria species. Taken together, these data reveal the occurrence of the natural spread of viroids to plants; additionally, as an integral component of the ecosystem, viroids may affect the abundance of certain fungal species in plants. Moreover, this study provides further evidence that viroid infection could induce symptoms in certain filamentous fungi.

Viroids, Satellite RNAs and Prions: Folding of Nucleic Acids and Misfolding of Proteins

“…Retrotransposons with hammerhead ribozymes, called retrozymes, have been found encoded in diverse plant genomes [ 17 ] and have stimulated new ideas about the possible origin of viroid and viroid-like RNAs [ 128 , 129 , 130 , 131 ]. Viroid-like RNAs, termed mycoviroids, have been detected in fungi [ 132 , 133 , 134 ]. Knowledge of circular RNAs in mammals has expanded in recent years; for example, they are produced by a process called back-splicing from mRNAs and are involved in (mis)regulation of many processes [ 135 , 136 , 137 ].…”

“…Retrotransposons with hammerhead ribozymes, called retrozymes, have been found encoded in diverse plant genomes [ 17 ] and have stimulated new ideas about the possible origin of viroid and viroid-like RNAs [ 128 , 129 , 130 , 131 ]. Viroid-like RNAs, termed mycoviroids, have been detected in fungi [ 132 , 133 , 134 ].…”

Viroids of the Mediterranean Basin

“…Two independent metagenomic analyses of environmental samples indicate that fungi provide an evolutionary hub for RNA viruses and viroid-like elements [ 242 , 243 ]. Furthermore, evidence has been presented for the transmission of the apple scar skin viroid from plant to plant-associated fungi under natural conditions [ 244 ]. The term “mycoviroids or fungal viroids” has been introduced to denote these viroids [ 245 , 246 ].…”

“…In addition to viroids spreading by plant pathogenic fungi [ 244 ], viroids may also spread via vegetative propagules, mechanical damage, seed, pollen, or biological vectors [ 245 ]. Vegetative propagation is the most prevalent mode of spread at the global, national, and local level, while further dissemination can readily occur by mechanical transmission through crop handling with viroid-contaminated hands or pruning and harvesting tools [ 245 ].…”

New Insights into Hop Latent Viroid Detection, Infectivity, Host Range, and Transmission

“…Viroids are pathogenic circular RNAs that infect members of the kingdom Plantae and are among the economically significant phytopathogens for numerous species of herbaceous and woody plants [ 1 , 2 ]. Viroids are generally highly contagious and can be transmitted mechanically by farm tools, insects, pollen, seeds, parasitic plants, shoot/root grafting, and recently fungal phytopathogens [ 1 , 3 , 4 , 5 , 6 ]. Notably, viroids such as citrus exocortis viroid (CEVd) have a wide host range, infecting plants from different botanical groups like trees and herbaceous plants [ 1 , 7 ].…”