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

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 viroi...

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Main Authors: Mengyuan Tian, Shuang Wei, Ruiling Bian, Jingxian Luo, Haris Ahmed Khan, Huanhuan Tai, Hideki Kondo, Ahmed Hadidi, Ida Bagus Andika, Liying Sun
Format: Article
Language:English
Published: MDPI AG 2022-11-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/11/22/3686
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author Mengyuan Tian
Shuang Wei
Ruiling Bian
Jingxian Luo
Haris Ahmed Khan
Huanhuan Tai
Hideki Kondo
Ahmed Hadidi
Ida Bagus Andika
Liying Sun
author_facet Mengyuan Tian
Shuang Wei
Ruiling Bian
Jingxian Luo
Haris Ahmed Khan
Huanhuan Tai
Hideki Kondo
Ahmed Hadidi
Ida Bagus Andika
Liying Sun
author_sort Mengyuan Tian
collection DOAJ
description 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 <i>Alternaria alternata</i> 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 <i>A. alternata</i> 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 <i>Epicoccum nigrum</i>. 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 <i>Alternaria</i> 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.
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spelling doaj.art-997807a44da44ec18aa67e2920cdf7972023-11-24T07:59:25ZengMDPI AGCells2073-44092022-11-011122368610.3390/cells11223686Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to FungiMengyuan Tian0Shuang Wei1Ruiling Bian2Jingxian Luo3Haris Ahmed Khan4Huanhuan Tai5Hideki Kondo6Ahmed Hadidi7Ida Bagus Andika8Liying Sun9State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling 712100, ChinaCollege of Agronomy, Northwest A&F University, Yangling 712100, ChinaInstitute of Plant Science and Resources, Okayama University, Kurashiki 710-0046, JapanU.S. Department of Agriculture, Agricultural Research Service, Beltsville, MD 20705, USACollege of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling 712100, ChinaViroids 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 <i>Alternaria alternata</i> 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 <i>A. alternata</i> 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 <i>Epicoccum nigrum</i>. 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 <i>Alternaria</i> 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.https://www.mdpi.com/2073-4409/11/22/3686Viroidfilamentous fungicross-infectionhypovirulenceMycobiome
spellingShingle Mengyuan Tian
Shuang Wei
Ruiling Bian
Jingxian Luo
Haris Ahmed Khan
Huanhuan Tai
Hideki Kondo
Ahmed Hadidi
Ida Bagus Andika
Liying Sun
Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi
Cells
Viroid
filamentous fungi
cross-infection
hypovirulence
Mycobiome
title Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi
title_full Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi
title_fullStr Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi
title_full_unstemmed Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi
title_short Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi
title_sort natural cross kingdom spread of apple scar skin viroid from apple trees to fungi
topic Viroid
filamentous fungi
cross-infection
hypovirulence
Mycobiome
url https://www.mdpi.com/2073-4409/11/22/3686
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