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      The intriguing phenomenon of cross-kingdom infections of plant and insect viruses to fungi: Can other animal viruses also cross-infect fungi?

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          Abstract

          Fungi are highly widespread and commonly colonize multicellular organisms that live in natural environments. Notably, studies on viruses infecting plant-associated fungi have revealed the interesting phenomenon of the cross-kingdom transmission of viruses and viroids from plants to fungi. This implies that fungi, in addition to absorbing water, nutrients, and other molecules from the host, can acquire intracellular parasites that reside in the host. These findings further suggest that fungi can serve as suitable alternative hosts for certain plant viruses and viroids. Given the frequent coinfection of fungi and viruses in humans/animals, the question of whether fungi can also acquire animal viruses and serve as their hosts is very intriguing. In fact, the transmission of viruses from insects to fungi has been observed. Furthermore, the common release of animal viruses into the extracellular space (viral shedding) could potentially facilitate their acquisition by fungi. Investigations of the cross-infection of animal viruses in fungi may provide new insights into the epidemiology of viral diseases in humans and animals.

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          Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes

          Some pathogens and pests deliver small RNAs (sRNAs) into host cells to suppress host immunity. Conversely, hosts also transfer sRNAs into pathogens and pests to inhibit their virulence. Although sRNA trafficking has been observed in a wide variety of interactions, how sRNAs are transferred, especially from hosts to pathogens/pests, is still unknown. Here we show that host Arabidopsis cells secrete exosome-like extracellular vesicles to deliver sRNAs into fungal pathogen Botrytis cinerea. These sRNA-containing vesicles accumulate at the infection sites and are taken up by the fungal cells. Transferred host sRNAs induce silencing of fungal genes critical for pathogenicity. Thus, Arabidopsis has adapted exosome-mediated cross-kingdom RNA interference as part of its immune responses during the evolutionary arms race with the pathogen.
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            Fungal Diversity Revisited: 2.2 to 3.8 Million Species.

            The question of how many species of Fungi there are has occasioned much speculation, with figures mostly posited from around half a million to 10 million, and in one extreme case even a sizable portion of the spectacular number of 1 trillion. Here we examine new evidence from various sources to derive an updated estimate of global fungal diversity. The rates and patterns in the description of new species from the 1750s show no sign of approaching an asymptote and even accelerated in the 2010s after the advent of molecular approaches to species delimitation. Species recognition studies of (semi-)cryptic species hidden in morpho-species complexes suggest a weighted average ratio of about an order of magnitude for the number of species recognized after and before such studies. New evidence also comes from extrapolations of plant:fungus ratios, with information now being generated from environmental sequence studies, including comparisons of molecular and fieldwork data from the same sites. We further draw attention to undescribed species awaiting discovery in biodiversity hot spots in the tropics, little-explored habitats (such as lichen-inhabiting fungi), and material in collections awaiting study. We conclude that the commonly cited estimate of 1.5 million species is conservative and that the actual range is properly estimated at 2.2 to 3.8 million. With 120,000 currently accepted species, it appears that at best just 8%, and in the worst case scenario just 3%, are named so far. Improved estimates hinge particularly on reliable statistical and phylogenetic approaches to analyze the rapidly increasing amount of environmental sequence data.
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              Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection

              Aggressive fungal pathogens such as Botrytis and Verticillium spp. cause severe crop losses worldwide. We recently discovered that Botrytis cinerea delivers small RNAs (Bc-sRNAs) into plant cells to silence host immunity genes. Such sRNA effectors are mostly produced by B. cinerea Dicer-like protein 1 (Bc-DCL1) and Bc-DCL2. Here we show that expressing sRNAs that target Bc-DCL1 and Bc-DCL2 in Arabidopsis and tomato silences Bc-DCL genes and attenuates fungal pathogenicity and growth, exemplifying bidirectional cross-kingdom RNAi and sRNA trafficking between plants and fungi. This strategy can be adapted to simultaneously control multiple fungal diseases. We also show that Botrytis can take up external sRNAs and double-stranded RNAs (dsRNAs). Applying sRNAs or dsRNAs that target Botrytis DCL1 and DCL2 genes on the surface of fruits, vegetables, and flowers significantly inhibits gray mold disease. Such pathogen gene-targeting RNAs represent a new generation of environmentally-friendly fungicides.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Funding acquisitionRole: Writing – original draftRole: Writing – review & editing
                Role: Funding acquisitionRole: ValidationRole: Writing – review & editing
                Role: Funding acquisitionRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Funding acquisitionRole: ValidationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Pathog
                PLoS Pathog
                plos
                PLOS Pathogens
                Public Library of Science (San Francisco, CA USA )
                1553-7366
                1553-7374
                26 October 2023
                October 2023
                : 19
                : 10
                : e1011726
                Affiliations
                [1 ] College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao, China
                [2 ] Shandong Agricultural University, Tai’an, China
                [3 ] Shouguang International Vegetable Sci-tech Fair Management Service Center, Shouguang, China
                [4 ] Institute of Plant Science and Resources, Okayama University, Kurashiki, Japan
                [5 ] State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Xianyang, China
                Boston Children’s Hospital, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-9220-5350
                Article
                PPATHOGENS-D-23-00932
                10.1371/journal.ppat.1011726
                10602238
                37883353
                476388f4-ca2e-4a97-8201-c3107a43f4db
                © 2023 Andika et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Page count
                Figures: 2, Tables: 0, Pages: 10
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31970159
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 32001867
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31970163
                Award Recipient :
                Funded by: Natural Science Foundation of Shandong Province of China
                Award ID: ZR2020QC129
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 23H02214
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 23K18029
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 21K18222
                Award Recipient :
                This research was supported in part by grants from National Natural Science Foundation of China (31970159) to I.B.A., (32001867) to X.C. and (31970163) to LS, respectively, Natural Science Foundation of Shandong Province of China (ZR2020QC129) to X.C. and Japan Society for the Promotion of Science/Ministry of Education, Culture, Sports, Science and Technology of Japan (KAKENHI: 23H02214, 23K18029 and 21K18222) to HK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Opinion
                Biology and Life Sciences
                Organisms
                Eukaryota
                Fungi
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Fungal Diseases
                Biology and Life Sciences
                Plant Science
                Plant Pathology
                Plant Pathogens
                Plant Viral Pathogens
                Biology and Life Sciences
                Plant Science
                Plant Pathology
                Plant Pathogens
                Plant Fungal Pathogens
                Biology and Life Sciences
                Genetics
                Fungal Genetics
                Fungal Genomics
                Biology and Life Sciences
                Mycology
                Fungal Genetics
                Fungal Genomics
                Biology and Life Sciences
                Genetics
                Genomics
                Fungal Genomics
                Biology and Life Sciences
                Plant Science
                Plant Pathology
                Plant Pathogens
                Viroids
                Biology and Life Sciences
                Organisms
                Viruses
                Viroids
                Biology and life sciences
                Organisms
                Viruses
                RNA viruses
                dsRNA viruses
                Biology and Life Sciences
                Microbiology
                Virology
                Viral Transmission and Infection

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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