A resilient mutualistic interaction between cucumber mosaic virus and its natural host to adapt to an excess zinc environment and drought stress

doi:10.1007/s10265-024-01573-w

. 2024 Nov;137(6):1151-1164.

doi: 10.1007/s10265-024-01573-w. Epub 2024 Aug 27.

A resilient mutualistic interaction between cucumber mosaic virus and its natural host to adapt to an excess zinc environment and drought stress

Midori Tabara^{1

2

3}, Shimpei Uraguchi⁴, Masako Kiyono⁴, Izumi Watanabe⁵, Atsushi Takeda⁶, Hideki Takahashi⁷, Toshiyuki Fukuhara^{8

9}

Affiliations

¹ Ritsumeikan-Global Innovation Research Organization, Ritsumeikan University, 1-1-1, Noji-Higashi, Kusatsu, Shiga, 525-8577, Japan.
² Institute of Global Innovation Research, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509, Japan.
³ Department of Applied Biological Sciences, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509, Japan.
⁴ Department of Public Health, School of Pharmacy, Kitasato University, Tokyo, 108-8641, Japan.
⁵ Department of Environmental and Natural Resource Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509, Japan.
⁶ College of Life Sciences, Ritsumeikan University, 1-1-1, Noji-Higashi, Kusatsu, Shiga, 525-8577, Japan.
⁷ Graduate School of Agricultural Science, Tohoku University, Aramaki-Aza-Aoba, 468-1, Sendai, 980-0845, Japan.
⁸ Institute of Global Innovation Research, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509, Japan. fuku@cc.tuat.ac.jp.
⁹ Department of Applied Biological Sciences, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509, Japan. fuku@cc.tuat.ac.jp.

PMID: 39190237
DOI: 10.1007/s10265-024-01573-w

A resilient mutualistic interaction between cucumber mosaic virus and its natural host to adapt to an excess zinc environment and drought stress

Midori Tabara et al. J Plant Res. 2024 Nov.

. 2024 Nov;137(6):1151-1164.

doi: 10.1007/s10265-024-01573-w. Epub 2024 Aug 27.

Authors

Midori Tabara^{1

2

3}, Shimpei Uraguchi⁴, Masako Kiyono⁴, Izumi Watanabe⁵, Atsushi Takeda⁶, Hideki Takahashi⁷, Toshiyuki Fukuhara^{8

9}

Affiliations

¹ Ritsumeikan-Global Innovation Research Organization, Ritsumeikan University, 1-1-1, Noji-Higashi, Kusatsu, Shiga, 525-8577, Japan.
² Institute of Global Innovation Research, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509, Japan.
³ Department of Applied Biological Sciences, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509, Japan.
⁴ Department of Public Health, School of Pharmacy, Kitasato University, Tokyo, 108-8641, Japan.
⁵ Department of Environmental and Natural Resource Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509, Japan.
⁶ College of Life Sciences, Ritsumeikan University, 1-1-1, Noji-Higashi, Kusatsu, Shiga, 525-8577, Japan.
⁷ Graduate School of Agricultural Science, Tohoku University, Aramaki-Aza-Aoba, 468-1, Sendai, 980-0845, Japan.
⁸ Institute of Global Innovation Research, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509, Japan. fuku@cc.tuat.ac.jp.
⁹ Department of Applied Biological Sciences, Tokyo University of Agriculture and Technology, 3-5-8 Saiwaicho, Fuchu, Tokyo, 183-8509, Japan. fuku@cc.tuat.ac.jp.

PMID: 39190237
DOI: 10.1007/s10265-024-01573-w

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.

Keywords: Arabidopsis halleri; Cucumber mosaic virus; Drought tolerance; Excess zinc; Mutualistic interaction.

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Latent infection of Vigna unguiculata with seed-borne bean common mosaic virus modulates plant growth and may contribute to mutualistic symbiosis between the virus and host plant.
Takahashi H, Xu N, Kanayama Y, Tabara M, Takeda A, Fukuhara T, Miyashita S. Takahashi H, et al. Front Microbiol. 2025 Apr 9;16:1524787. doi: 10.3389/fmicb.2025.1524787. eCollection 2025. Front Microbiol. 2025. PMID: 40270808 Free PMC article.

References

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[1] Aguilar E, Cutrona C, Del Toro FJ, Vallarino JG, Osorio S, Pérez-Bueno ML, Barón M, Chung BN, Canto T, Tenllado F (2017) Virulence determines beneficial trade-offs in the response of virus-infected plants to drought via induction of salicylic acid. Plant Cell Environ 40:2909–2930. https://doi.org/10.1111/pce.13028 - DOI - PubMed

[2] Aguilar E, Cutrona C, Del Toro FJ, Vallarino JG, Osorio S, Pérez-Bueno ML, Barón M, Chung BN, Canto T, Tenllado F (2017) Virulence determines beneficial trade-offs in the response of virus-infected plants to drought via induction of salicylic acid. Plant Cell Environ 40:2909–2930. https://doi.org/10.1111/pce.13028 - DOI - PubMed

[3] Alexander HM, Bruns E, Schebor H, Malmstrom CM (2017) Crop-associated virus infection in a native perennial grass: reduction in plant fitness and dynamic patterns of virus detection. J Ecol 105:1021–1031. https://doi.org/10.1111/1365-2745.12723 - DOI

[4] Alexander HM, Bruns E, Schebor H, Malmstrom CM (2017) Crop-associated virus infection in a native perennial grass: reduction in plant fitness and dynamic patterns of virus detection. J Ecol 105:1021–1031. https://doi.org/10.1111/1365-2745.12723 - DOI

[5] Bhat AI, Rao GP (2020) Isolation and diagnosis of virus through indicator hosts. In: Bhat AI, Rao GP (eds) Characterization of Plant Viruses. Springer, New York, pp 23–27 - DOI

[6] Bhat AI, Rao GP (2020) Isolation and diagnosis of virus through indicator hosts. In: Bhat AI, Rao GP (eds) Characterization of Plant Viruses. Springer, New York, pp 23–27 - DOI

[7] Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176. https://doi.org/10.1007/s11104-007-9240-6 - DOI

[8] Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176. https://doi.org/10.1007/s11104-007-9240-6 - DOI

[9] Briskine RV, Paape T, Shimizu-Inatsugi R, Nishiyama T, Akama S, Sese J, Shimizu KK (2017) Genome assembly and annotation of Arabidopsis halleri, a model for heavy metal hyperaccumulation and evolutionary ecology. Mol Ecol Resour 17:1025–1036. https://doi.org/10.1111/1755-0998.12604 - DOI - PubMed

[10] Briskine RV, Paape T, Shimizu-Inatsugi R, Nishiyama T, Akama S, Sese J, Shimizu KK (2017) Genome assembly and annotation of Arabidopsis halleri, a model for heavy metal hyperaccumulation and evolutionary ecology. Mol Ecol Resour 17:1025–1036. https://doi.org/10.1111/1755-0998.12604 - DOI - PubMed

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A resilient mutualistic interaction between cucumber mosaic virus and its natural host to adapt to an excess zinc environment and drought stress

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A resilient mutualistic interaction between cucumber mosaic virus and its natural host to adapt to an excess zinc environment and drought stress

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