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10.3390/cells11223686
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Article

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

by
Mengyuan Tian
1,†,
Shuang Wei
1,†,
Ruiling Bian
1,
Jingxian Luo
1,
Haris Ahmed Khan
1,
Huanhuan Tai
2,
Hideki Kondo
3,
Ahmed Hadidi
4,‡,
Ida Bagus Andika
5 and
Liying Sun
1,3,*
1
State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling 712100, China
2
College of Agronomy, Northwest A&F University, Yangling 712100, China
3
Institute of Plant Science and Resources, Okayama University, Kurashiki 710-0046, Japan
4
U.S. Department of Agriculture, Agricultural Research Service, Beltsville, MD 20705, USA
5
College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
‡
Ahmed Hadidi is Emeritus Lead Scientist of Agricultural Research Service.
Cells 2022, 11(22), 3686; https://doi.org/10.3390/cells11223686
Submission received: 21 October 2022 / Revised: 18 November 2022 / Accepted: 18 November 2022 / Published: 20 November 2022
(This article belongs to the Special Issue Celebrating 50 Years of Viroid Discovery)
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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.
Keywords: Viroid; filamentous fungi; cross-infection; hypovirulence; Mycobiome Viroid; filamentous fungi; cross-infection; hypovirulence; Mycobiome

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MDPI and ACS Style

Tian, M.; Wei, S.; Bian, R.; Luo, J.; Khan, H.A.; Tai, H.; Kondo, H.; Hadidi, A.; Andika, I.B.; Sun, L. Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi. Cells 2022, 11, 3686. https://doi.org/10.3390/cells11223686

AMA Style

Tian M, Wei S, Bian R, Luo J, Khan HA, Tai H, Kondo H, Hadidi A, Andika IB, Sun L. Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi. Cells. 2022; 11(22):3686. https://doi.org/10.3390/cells11223686

Chicago/Turabian Style

Tian, Mengyuan, Shuang Wei, Ruiling Bian, Jingxian Luo, Haris Ahmed Khan, Huanhuan Tai, Hideki Kondo, Ahmed Hadidi, Ida Bagus Andika, and Liying Sun. 2022. "Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi" Cells 11, no. 22: 3686. https://doi.org/10.3390/cells11223686

APA Style

Tian, M., Wei, S., Bian, R., Luo, J., Khan, H. A., Tai, H., Kondo, H., Hadidi, A., Andika, I. B., & Sun, L. (2022). Natural Cross-Kingdom Spread of Apple Scar Skin Viroid from Apple Trees to Fungi. Cells, 11(22), 3686. https://doi.org/10.3390/cells11223686

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