Phytopathogenic fungus hosts a plant virus: A naturally occurring cross-kingdom viral infection

Edited by James L. Van Etten, University of Nebraska–Lincoln, Lincoln, NE, and approved October 6, 2017 (received for review August 23, 2017)
October 30, 2017
114 (46) 12267-12272

Significance

Virus cross-infection is an important topic in understanding the course of virus dissemination and evolution. Viruses may spread between the same host species or into taxonomically distinct organisms. The occurrences of cross-kingdom viral infection for certain virus groups are suggested by the current virus taxonomic data. In particular, several plants and fungal viruses show close phylogenetic relationships, but productive transmission of virus between plant and fungal hosts in nature has not been directly demonstrated. Here, we describe the natural infection of Rhizoctonia solani fungus by a plant virus, cucumber mosaic virus (CMV). We further demonstrate that R. solani can acquire and transmit CMV during plant infection. Our findings are evidence of cross-kingdom virus transmission from the plant to fungus.

Abstract

The transmission of viral infections between plant and fungal hosts has been suspected to occur, based on phylogenetic and other findings, but has not been directly observed in nature. Here, we report the discovery of a natural infection of the phytopathogenic fungus Rhizoctonia solani by a plant virus, cucumber mosaic virus (CMV). The CMV-infected R. solani strain was obtained from a potato plant growing in Inner Mongolia Province of China, and CMV infection was stable when this fungal strain was cultured in the laboratory. CMV was horizontally transmitted through hyphal anastomosis but not vertically through basidiospores. By inoculation via protoplast transfection with virions, a reference isolate of CMV replicated in R. solani and another phytopathogenic fungus, suggesting that some fungi can serve as alternative hosts to CMV. Importantly, in fungal inoculation experiments under laboratory conditions, R. solani could acquire CMV from an infected plant, as well as transmit the virus to an uninfected plant. This study presents evidence of the transfer of a virus between plant and fungus, and it further expands our understanding of plant–fungus interactions and the spread of plant viruses.

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Acknowledgments

We thank Drs. N. Suzuki, Z. Ma, B. Liu, and X. Wang for research materials; Dr. C. Han for helpful discussions; and Dr. A. J. Gibbs for valuable comments on the manuscript. This work was supported in part by National Key Research and Development Program of China Grant 2017YFD0201100; National Natural Science Foundation of China Grants 31260416 and 31550110222; 111 program for crop breeding for disease resistance and genetic improvement, Science Foundation of Shaanxi Grant 2016KW-069 (to L. Sun); and Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research Grants 15K07312, 16H06436, and 17H01463 (to H.K.).

Supporting Information

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References

1
C Harak, V Lohmann, Ultrastructure of the replication sites of positive-strand RNA viruses. Virology 479-480, 418–433 (2015).
2
PD Nagy, J Pogany, The dependence of viral RNA replication on co-opted host factors. Nat Rev Microbiol 10, 137–149 (2011).
3
M Hashimoto, Y Neriya, Y Yamaji, S Namba, Recessive resistance to plant viruses: Potential resistance genes beyond translation initiation factors. Front Microbiol 7, 1695 (2016).
4
J Pommerville Alcamo’s Fundamentals of Microbiology: Body Systems (Jones & Bartlett Publ, Burlington, MA, 2012).
5
AE Whitfield, BW Falk, D Rotenberg, Insect vector-mediated transmission of plant viruses. Virology 479-480, 278–289 (2015).
6
SA Hogenhout, D Ammar, AE Whitfield, MG Redinbaugh, Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46, 327–359 (2008).
7
S Liu, et al., Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector. Proc Natl Acad Sci USA 113, 12803–12808 (2016).
8
T Mascia, et al., Gene silencing and gene expression in phytopathogenic fungi using a plant virus vector. Proc Natl Acad Sci USA 111, 4291–4296 (2014).
9
PD Nagy, Yeast as a model host to explore plant virus-host interactions. Annu Rev Phytopathol 46, 217–242 (2008).
10
PD Nagy, J Pogany, J-Y Lin, How yeast can be used as a genetic platform to explore virus-host interactions: From ‘omics’ to functional studies. Trends Microbiol 22, 309–316 (2014).
11
L Nerva, GC Varese, BW Falk, M Turin, Mycoviruses of an endophytic fungus can replicate in plant cells: Evolutionary implications. Sci Rep 7, 1908 (2017).
12
M Janda, P Ahlquist, RNA-dependent replication, transcription, and persistence of brome mosaic virus RNA replicons in S. cerevisiae. Cell 72, 961–970 (1993).
13
BH Selling, RF Allison, P Kaesberg, Genomic RNA of an insect virus directs synthesis of infectious virions in plants. Proc Natl Acad Sci USA 87, 434–438 (1990).
14
EV Koonin, VV Dolja, M Krupovic, Origins and evolution of viruses of eukaryotes: The ultimate modularity. Virology 479-480, 2–25 (2015).
15
VV Dolja, EV Koonin, Common origins and host-dependent diversity of plant and animal viromes. Curr Opin Virol 1, 322–331 (2011).
16
MJ Roossinck, Plant virus ecology. PLoS Pathog 9, e1003304 (2013).
17
W Knogge, Fungal infection of plants. Plant Cell 8, 1711–1722 (1996).
18
RC Staples, Nutrients for a rust fungus: The role of haustoria. Trends Plant Sci 6, 496–498 (2001).
19
LJ Szabo, WR Bushnell, Hidden robbers: The role of fungal haustoria in parasitism of plants. Proc Natl Acad Sci USA 98, 7654–7655 (2001).
20
K Laluk, T Mengiste, Necrotroph attacks on plants: Wanton destruction or covert extortion? Arabidopsis Book, e0136. (2010).
21
J Stone, Necrotroph. Encycl Plant Pathol 2, 676–677 (2001).
22
L Lo Presti, et al., Fungal effectors and plant susceptibility. Annu Rev Plant Biol 66, 513–545 (2015).
23
M Koeck, AR Hardham, PN Dodds, The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cell Microbiol 13, 1849–1857 (2011).
24
W Ye, W Ma, Filamentous pathogen effectors interfering with small RNA silencing in plant hosts. Curr Opin Microbiol 32, 1–6 (2016).
25
DC Baulcombe, VIGS, HIGS and FIGS: Small RNA silencing in the interactions of viruses or filamentous organisms with their plant hosts. Curr Opin Plant Biol 26, 141–146 (2015).
26
A Weiberg, M Wang, M Bellinger, H Jin, Small RNAs: A new paradigm in plant-microbe interactions. Annu Rev Phytopathol 52, 495–516 (2014).
27
L Han, Y-S Luan, Horizontal transfer of small RNAs to and from plants. Front Plant Sci 6, 1113 (2015).
28
J Xie, D Jiang, New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52, 45–68 (2014).
29
MN Pearson, RE Beever, B Boine, K Arthur, Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol 10, 115–128 (2009).
30
ML Nibert, et al., 3D structures of fungal partitiviruses. Adv Virus Res 86, 59–85 (2013).
31
MJ Roossinck, Lifestyles of plant viruses. Philos Trans R Soc Lond B Biol Sci 365, 1899–1905 (2010).
32
MJ Roossinck Persistent Plant Viruses: Molecular Hitchhikers or Epigenetic Elements? Viruses: Essential Agents of Life (Springer, Dordrecht, The Netherlands), pp. 177–186 (2012).
33
NA Anderson, The genetics and pathology of Rhizoctonia solani. Annu Rev Phytopathol 20, 329–347 (1982).
34
GN Agrios Plant Pathology (Academic, London, 2005).
35
B Sneh, S Jabaji-Hare, S Neate, G Dijst Rhizoctonia Species: Taxonomy, Molecular Biology, Ecology, Pathology and Disease Control (Springer Sci & Business Media, Dordrecht, The Netherlands, 2013).
36
L Zheng, M Zhang, Q Chen, M Zhu, E Zhou, A novel mycovirus closely related to viruses in the genus Alphapartitivirus confers hypovirulence in the phytopathogenic fungus Rhizoctonia solani. Virology 456-457, 220–226 (2014).
37
L Zheng, H Liu, M Zhang, X Cao, E Zhou, The complete genomic sequence of a novel mycovirus from Rhizoctonia solani AG-1 IA strain B275. Arch Virol 158, 1609–1612 (2013).
38
J Zhong, C-Y Chen, B-D Gao, Genome sequence of a novel mycovirus of Rhizoctonia solani, a plant pathogenic fungus. Virus Genes 51, 167–170 (2015).
39
A Bartholomäus, et al., Identification of a novel mycovirus isolated from Rhizoctonia solani (AG 2-2 IV) provides further information about genome plasticity within the order Tymovirales. Arch Virol 162, 555–559 (2017).
40
A Bartholomäus, et al., Deep sequencing analysis reveals the mycoviral diversity of the virome of an avirulent isolate of Rhizoctonia solani AG-2-2 IV. PLoS One 11, e0165965 (2016).
41
S Das, RE Falloon, A Stewart, AR Pitman, Molecular characterisation of an endornavirus from Rhizoctonia solani AG-3PT infecting potato. Fungal Biol 118, 924–934 (2014).
42
AM King, E Lefkowitz, MJ Adams, EB Carstens Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses (Elsevier, London, 2011).
43
M Jacquemond, Cucumber mosaic virus. Adv Virus Res 84, 439–504 (2012).
44
P Palukaitis, MJ Roossinck, RG Dietzgen, RI Francki, Cucumber mosaic virus. Adv Virus Res 41, 281–348 (1992).
45
DE Carling, Grouping in Rhizoctonia solani by hyphal anastomosis reaction. Rhizoctonia Species: Taxonomy, Molecular Biology, Ecology, Pathology and Disease Control (Springer, Dordrecht, The Netherlands), pp. 37–47 (1996).
46
TM Rizzo, P Palukaitis, Nucleotide sequence and evolutionary relationships of cucumber mosaic virus (CMV) strains: CMV RNA 1. J Gen Virol 70, 1–11 (1989).
47
TM Rizzo, P Palukaitis, Nucleotide sequence and evolutionary relationships of cucumber mosaic virus (CMV) strains: CMV RNA 2. J Gen Virol 69, 1777–1787 (1988).
48
SA Ghabrial, N Suzuki, Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47, 353–384 (2009).
49
F Nienhaus, Tobacco mosaic virus strains extracted from conidia of powdery mildews. Virology 46, 504–505 (1971).
50
C Yarwood, E Hecht-Poinar, Viruses from rusts and mildews. Phytopathology 63, 1111–1115 (1973).
51
C Bragard, et al., Status and prospects of plant virus control through interference with vector transmission. Annu Rev Phytopathol 51, 177–201 (2013).
52
SA Ghabrial, JR Castón, D Jiang, ML Nibert, N Suzuki, 50-plus years of fungal viruses. Virology 479-480, 356–368 (2015).
53
R Hull Plant Virology (Academic, London, 2013).
54
X Yu, et al., Extracellular transmission of a DNA mycovirus and its use as a natural fungicide. Proc Natl Acad Sci USA 110, 1452–1457 (2013).
55
T Mascia, D Gallitelli, P Palukaitis, Something new to explore: Plant viruses infecting and inducing gene silencing in filamentous fungi. Mob Genet Elements 4, e29782 (2014).
56
D Nowara, et al., HIGS: Host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22, 3130–3141 (2010).
57
IB Andika, H Kondo, L Sun, Interplays between soil-borne plant viruses and RNA silencing-mediated antiviral defense in roots. Front Microbiol 7, 1458 (2016).
58
MJ Adams, JF Antoniw, JG Mullins, Plant virus transmission by plasmodiophorid fungi is associated with distinctive transmembrane regions of virus-encoded proteins. Arch Virol 146, 1139–1153 (2001).
59
MG Guerret, MJ Barbetti, MP You, RA Jones, Effects of temperature on disease severity in plants of subterranean clover infected singly or in mixed infection with Bean yellow mosaic virus and Kabatiella caulivora. J Phytopathol 164, 608–619 (2016).
60
L-H Ji, S-W Ding, The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol Plant Microbe Interact 14, 715–724 (2001).
61
MG Lewsey, et al., Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant Microbe Interact 23, 835–845 (2010).
62
GP Martelli, MJ Adams, JF Kreuze, VV Dolja, Family flexiviridae: A case study in virion and genome plasticity. Annu Rev Phytopathol 45, 73–100 (2007).
63
J Xie, et al., Characterization of debilitation-associated mycovirus infecting the plant-pathogenic fungus Sclerotinia sclerotiorum. J Gen Virol 87, 241–249 (2006).
64
RL Howitt, RE Beever, MN Pearson, RL Forster, Genome characterization of Botrytis virus F, a flexuous rod-shaped mycovirus resembling plant ‘potex-like’ viruses. J Gen Virol 82, 67–78 (2001).
65
RL Howitt, RE Beever, MN Pearson, RL Forster, Genome characterization of a flexuous rod-shaped mycovirus, Botrytis virus X, reveals high amino acid identity to genes from plant ‘potex-like’ viruses. Arch Virol 151, 563–579 (2006).
66
M Shi, et al., Redefining the invertebrate RNA virosphere. Nature 540, 539–543 (2016).
67
M Fiers, et al., Genetic diversity of Rhizoctonia solani associated with potato tubers in France. Mycologia 103, 1230–1244 (2011).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 114 | No. 46
November 14, 2017
PubMed: 29087346

Classifications

Submission history

Published online: October 30, 2017
Published in issue: November 14, 2017

Keywords

  1. plant virus
  2. fungus
  3. transmission
  4. cross-kingdom

Acknowledgments

We thank Drs. N. Suzuki, Z. Ma, B. Liu, and X. Wang for research materials; Dr. C. Han for helpful discussions; and Dr. A. J. Gibbs for valuable comments on the manuscript. This work was supported in part by National Key Research and Development Program of China Grant 2017YFD0201100; National Natural Science Foundation of China Grants 31260416 and 31550110222; 111 program for crop breeding for disease resistance and genetic improvement, Science Foundation of Shaanxi Grant 2016KW-069 (to L. Sun); and Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research Grants 15K07312, 16H06436, and 17H01463 (to H.K.).

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Ida Bagus Andika
State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, China;
Institute of Plant Science and Resources, Okayama University, Kurashiki, 710-0046, Japan;
Shuang Wei
State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, China;
Chunmei Cao
Potato Research Center, Inner Mongolia Academy of Agricultural & Animal Husbandry Sciences, Hohhot, China;
Lakha Salaipeth
State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, China;
School of Bioresources and Technology, King Mongkut’s University of Technology Thonburi, Bangkok, Thailand
Hideki Kondo
Institute of Plant Science and Resources, Okayama University, Kurashiki, 710-0046, Japan;
State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, China;

Notes

1
To whom correspondence should be addressed. Email: [email protected].
Author contributions: I.B.A. and L. Sun designed research; I.B.A., S.W., C.C., L. Salaipeth, and L. Sun performed research; I.B.A., H.K., and L. Sun analyzed data; and I.B.A., H.K., and L. Sun wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Phytopathogenic fungus hosts a plant virus: A naturally occurring cross-kingdom viral infection
    Proceedings of the National Academy of Sciences
    • Vol. 114
    • No. 46
    • pp. 12087-12349

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