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Hijacking of N-fixing legume albumin-1 genes enables the cyclization and stabilization of defense peptides

Author

Listed:
  • Edward K. Gilding

    (The University of Queensland
    The University of Queensland)

  • Mark A. Jackson

    (The University of Queensland
    The University of Queensland)

  • Linh T. T. Nguyen

    (The University of Queensland
    The University of Queensland)

  • Brett R. Hamilton

    (The University of Queensland)

  • Katherine A. Farquharson

    (The University of Queensland
    The University of Sydney)

  • Wing L. Ho

    (The University of Queensland
    The University of Queensland)

  • Kuok Yap

    (The University of Queensland
    The University of Queensland)

  • Carolyn J. Hogg

    (The University of Queensland
    The University of Sydney)

  • Katherine Belov

    (The University of Queensland
    The University of Sydney)

  • David J. Craik

    (The University of Queensland
    The University of Queensland)

Abstract

The legume albumin-1 gene family, arising after nodulation, encodes linear a- and b-chain peptides for nutrient storage and defense. Intriguingly, in one prominent legume, Clitoria ternatea, the b-chains are replaced by domains producing ultra-stable cyclic peptides called cyclotides. The mechanism of this gene hijacking is until now unknown. Cyclotides require recruitment of ligase-type asparaginyl endopeptidases (AEPs) for maturation (cyclization), necessitating co-evolution of two gene families. Here we compare a chromosome-level C. ternatea genome with grain legumes to reveal an 8 to 40-fold expansion of the albumin-1 gene family, enabling the additional loci to undergo diversification. Iterative rounds of albumin-1 duplication and diversification create four albumin-1 enriched genomic islands encoding cyclotides, where they are physically grouped by similar pI and net charge values. We identify an ancestral hydrolytic AEP that exhibits neofunctionalization and multiple duplication events to yield two ligase-type AEPs. We propose cyclotides arise by convergence in C. ternatea where their presence enhances defense from biotic attack, thus increasing fitness compared to lineages with linear b-chains and ultimately driving the replacement of b-chains with cyclotides.

Suggested Citation

  • Edward K. Gilding & Mark A. Jackson & Linh T. T. Nguyen & Brett R. Hamilton & Katherine A. Farquharson & Wing L. Ho & Kuok Yap & Carolyn J. Hogg & Katherine Belov & David J. Craik, 2024. "Hijacking of N-fixing legume albumin-1 genes enables the cyclization and stabilization of defense peptides," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50742-x
    DOI: 10.1038/s41467-024-50742-x
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    References listed on IDEAS

    as
    1. Karen S. Harris & Thomas Durek & Quentin Kaas & Aaron G. Poth & Edward K. Gilding & Brendon F. Conlan & Ivana Saska & Norelle L. Daly & Nicole L. van der Weerden & David J. Craik & Marilyn A. Anderson, 2015. "Efficient backbone cyclization of linear peptides by a recombinant asparaginyl endopeptidase," Nature Communications, Nature, vol. 6(1), pages 1-10, December.
    2. M. A. Jackson & E. K. Gilding & T. Shafee & K. S. Harris & Q. Kaas & S. Poon & K. Yap & H. Jia & R. Guarino & L. Y. Chan & T. Durek & M. A. Anderson & D. J. Craik, 2018. "Molecular basis for the production of cyclic peptides by plant asparaginyl endopeptidases," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Samira Mafi Moghaddam & Atena Oladzad & Chushin Koh & Larissa Ramsay & John P. Hart & Sujan Mamidi & Genevieve Hoopes & Avinash Sreedasyam & Andrew Wiersma & Dongyan Zhao & Jane Grimwood & John P. Ham, 2021. "The tepary bean genome provides insight into evolution and domestication under heat stress," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    4. Junqiao Du & Kuok Yap & Lai Yue Chan & Fabian B. H. Rehm & Fong Yang Looi & Aaron G. Poth & Edward K. Gilding & Quentin Kaas & Thomas Durek & David J. Craik, 2020. "A bifunctional asparaginyl endopeptidase efficiently catalyzes both cleavage and cyclization of cyclic trypsin inhibitors," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
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