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Elucidation of Spartina dimethylsulfoniopropionate synthesis genes enables engineering of stress tolerant plants

Author

Listed:
  • Rocky D. Payet

    (University of East Anglia, Norwich Research Park)

  • Lorelei J. Bilham

    (University of East Anglia, Norwich Research Park)

  • Shah Md Tamim Kabir

    (University of East Anglia, Norwich Research Park)

  • Serena Monaco

    (University of East Anglia, Norwich Research Park)

  • Ash R. Norcott

    (University of East Anglia, Norwich Research Park)

  • Mellieha G. E. Allen

    (University of East Anglia, Norwich Research Park)

  • Xiao-Yu Zhu

    (University of East Anglia, Norwich Research Park)

  • Anthony J. Davy

    (University of East Anglia, Norwich Research Park)

  • Charles A. Brearley

    (University of East Anglia, Norwich Research Park)

  • Jonathan D. Todd

    (University of East Anglia, Norwich Research Park
    Ocean University of China)

  • J. Benjamin Miller

    (University of East Anglia, Norwich Research Park)

Abstract

The organosulfur compound dimethylsulfoniopropionate (DMSP) has key roles in stress protection, global carbon and sulfur cycling, chemotaxis, and is a major source of climate-active gases. Saltmarshes are global hotspots for DMSP cycling due to Spartina cordgrasses that produce exceptionally high concentrations of DMSP. Here, in Spartina anglica, we identify the plant genes that underpin high-level DMSP synthesis: methionine S-methyltransferase (MMT), S-methylmethionine decarboxylase (SDC) and DMSP-amine oxidase (DOX). Homologs of these enzymes are common in plants, but differences in expression and catalytic efficiency explain why S. anglica accumulates such high DMSP concentrations and other plants only accumulate low concentrations. Furthermore, DMSP accumulation in S. anglica is consistent with DMSP having a role in oxidative and osmotic stress protection. Importantly, administration of DMSP by root uptake or over-expression of Spartina DMSP synthesis genes confers plant tolerance to salinity and drought offering a route for future bioengineering for sustainable crop production.

Suggested Citation

  • Rocky D. Payet & Lorelei J. Bilham & Shah Md Tamim Kabir & Serena Monaco & Ash R. Norcott & Mellieha G. E. Allen & Xiao-Yu Zhu & Anthony J. Davy & Charles A. Brearley & Jonathan D. Todd & J. Benjamin , 2024. "Elucidation of Spartina dimethylsulfoniopropionate synthesis genes enables engineering of stress tolerant plants," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51758-z
    DOI: 10.1038/s41467-024-51758-z
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    References listed on IDEAS

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    1. W. Sunda & D. J. Kieber & R. P. Kiene & S. Huntsman, 2002. "An antioxidant function for DMSP and DMS in marine algae," Nature, Nature, vol. 418(6895), pages 317-320, July.
    2. Kathleen Thume & Björn Gebser & Liang Chen & Nils Meyer & David J. Kieber & Georg Pohnert, 2018. "The metabolite dimethylsulfoxonium propionate extends the marine organosulfur cycle," Nature, Nature, vol. 563(7731), pages 412-415, November.
    3. Alessio Milanese & Daniel R Mende & Lucas Paoli & Guillem Salazar & Hans-Joachim Ruscheweyh & Miguelangel Cuenca & Pascal Hingamp & Renato Alves & Paul I Costea & Luis Pedro Coelho & Thomas S. B. Schm, 2019. "Microbial abundance, activity and population genomic profiling with mOTUs2," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    4. Yanfen Zheng & Jinyan Wang & Shun Zhou & Yunhui Zhang & Ji Liu & Chun-Xu Xue & Beth T. Williams & Xiuxiu Zhao & Li Zhao & Xiao-Yu Zhu & Chuang Sun & Hong-Hai Zhang & Tian Xiao & Gui-Peng Yang & Jonath, 2020. "Bacteria are important dimethylsulfoniopropionate producers in marine aphotic and high-pressure environments," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
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