A Resilient Mutualistic Interaction Between Cucumber Mosaic Virus and Its Natural Host to Adapt to an Excess Zinc Environment and Drought Stress

Overview

Journal J Plant Res

Specialty Biology

Date 2024 Aug 27

PMID 39190237

Authors

Midori Tabara

Shimpei Uraguchi

Masako Kiyono

Izumi Watanabe

Atsushi Takeda

Hideki Takahashi

Toshiyuki Fukuhara

Affiliations

Soon will be listed here.

Abstract

A perennial pseudometallophyte Arabidopsis halleri is frequently infected with cucumber mosaic virus (CMV) in its natural habitat. The purpose of this study was to characterize the effect of CMV infection on the environmental adaptation of its natural host A. halleri. The CMV(Ho) strain isolated from A. halleri was inoculated into clonal virus-free A. halleri plants, and a unique plant-virus system consisting of CMV(Ho) and its natural wild plant host was established. In a control environment with ambient zinc supplementation, CMV(Ho) infection retarded growth in the above-ground part of host plants but conferred strong drought tolerance. On the other hand, in an excess zinc environment, simulating a natural edaphic environment of A halleri, host plants hyperaccumulated zinc and CMV(Ho) infection did not cause any symptoms to host plants while conferring mild drought tolerance. We also demonstrated in Nicotiana benthamiana as another host that similar effects were induced by the combination of excess zinc and CMV(Ho) infection. Transcriptomic analysis indicated that the host plant recognized CMV(Ho) as a mutualistic symbiont rather than a parasitic pathogen. These results suggest a resilient mutualistic interaction between CMV(Ho) and its natural host A. halleri in its natural habitat.

References

Aguilar E, Cutrona C, Del Toro F, Vallarino J, Osorio S, Perez-Bueno M . Virulence determines beneficial trade-offs in the response of virus-infected plants to drought via induction of salicylic acid. Plant Cell Environ. 2017; 40(12):2909-2930. DOI: 10.1111/pce.13028. View

Briskine R, Paape T, Shimizu-Inatsugi R, Nishiyama T, Akama S, Sese J . Genome assembly and annotation of Arabidopsis halleri, a model for heavy metal hyperaccumulation and evolutionary ecology. Mol Ecol Resour. 2016; 17(5):1025-1036. DOI: 10.1111/1755-0998.12604. View

Cabot C, Martos S, Llugany M, Gallego B, Tolra R, Poschenrieder C . A Role for Zinc in Plant Defense Against Pathogens and Herbivores. Front Plant Sci. 2019; 10:1171. PMC: 6794951. DOI: 10.3389/fpls.2019.01171. View

Cooper I, Jones R . Wild plants and viruses: under-investigated ecosystems. Adv Virus Res. 2006; 67:1-47. DOI: 10.1016/S0065-3527(06)67001-2. View

Drager D, Desbrosses-Fonrouge A, Krach C, Chardonnens A, Meyer R, Saumitou-Laprade P . Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J. 2004; 39(3):425-39. DOI: 10.1111/j.1365-313X.2004.02143.x. View

Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S . Requirement of salicylic Acid for the induction of systemic acquired resistance. Science. 1993; 261(5122):754-6. DOI: 10.1126/science.261.5122.754. View

Garcia-Ruiz H, Takeda A, Chapman E, Sullivan C, Fahlgren N, Brempelis K . Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip Mosaic Virus infection. Plant Cell. 2010; 22(2):481-96. PMC: 2845422. DOI: 10.1105/tpc.109.073056. View

Gonzalez R, Butkovic A, Elena S . From foes to friends: Viral infections expand the limits of host phenotypic plasticity. Adv Virus Res. 2020; 106:85-121. DOI: 10.1016/bs.aivir.2020.01.003. View

Gonzalez R, Butkovic A, Escaray F, Martinez-Latorre J, Melero I, Perez-Parets E . Plant virus evolution under strong drought conditions results in a transition from parasitism to mutualism. Proc Natl Acad Sci U S A. 2021; 118(6). PMC: 8017717. DOI: 10.1073/pnas.2020990118. View

10.

Goodin M, Zaitlin D, Naidu R, Lommel S . Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol Plant Microbe Interact. 2008; 21(8):1015-26. DOI: 10.1094/MPMI-21-8-1015. View

11.

Hily J, Poulicard N, Mora M, Pagan I, Garcia-Arenal F . Environment and host genotype determine the outcome of a plant-virus interaction: from antagonism to mutualism. New Phytol. 2015; 209(2):812-22. DOI: 10.1111/nph.13631. View

12.

Tsujimoto M, Araki K, Honjo M, Yasugi M, Nagano A, Akama S . Genet assignment and population structure analysis in a clonal forest-floor herb, , using RAD-seq. AoB Plants. 2020; 12(1):plz080. PMC: 6983914. DOI: 10.1093/aobpla/plz080. View

13.

Honjo M, Emura N, Kawagoe T, Sugisaka J, Kamitani M, Nagano A . Seasonality of interactions between a plant virus and its host during persistent infection in a natural environment. ISME J. 2019; 14(2):506-518. PMC: 6976672. DOI: 10.1038/s41396-019-0519-4. View

14.

Kamitani M, Nagano A, Honjo M, Kudoh H . RNA-Seq reveals virus-virus and virus-plant interactions in nature. FEMS Microbiol Ecol. 2016; 92(11). PMC: 5854034. DOI: 10.1093/femsec/fiw176. View

15.

Kamitani M, Nagano A, Honjo M, Kudoh H . A Survey on Plant Viruses in Natural Brassicaceae Communities Using RNA-Seq. Microb Ecol. 2018; 78(1):113-121. DOI: 10.1007/s00248-018-1271-4. View

16.

Kazemi-Dinan A, Thomaschky S, Stein R, Kramer U, Muller C . Zinc and cadmium hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore. New Phytol. 2014; 202(2):628-639. DOI: 10.1111/nph.12663. View

17.

Kim D, Langmead B, Salzberg S . HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015; 12(4):357-60. PMC: 4655817. DOI: 10.1038/nmeth.3317. View

18.

Klopfenstein D, Zhang L, Pedersen B, Ramirez F, Warwick Vesztrocy A, Naldi A . GOATOOLS: A Python library for Gene Ontology analyses. Sci Rep. 2018; 8(1):10872. PMC: 6052049. DOI: 10.1038/s41598-018-28948-z. View

19.

Kramer U . Metal hyperaccumulation in plants. Annu Rev Plant Biol. 2010; 61:517-34. DOI: 10.1146/annurev-arplant-042809-112156. View

20.

Liu D, Zhao Q, Cheng Y, Li D, Jiang C, Cheng L . Transcriptome analysis of two cultivars of tobacco in response to Cucumber mosaic virus infection. Sci Rep. 2019; 9(1):3124. PMC: 6395745. DOI: 10.1038/s41598-019-39734-w. View