Pathogen-driven coevolution across the CBP60 plant immune regulator subfamilies confers resilience on the regulator module

Qi Zheng, Kristina Majsec, Fumiaki Katagiri

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

Components of the plant immune signaling network need mechanisms that confer resilience against fast-evolving pathogen effectors that target them. Among eight Arabidopsis CaM-Binding Protein (CBP) 60 family members, AtCBP60g and AtSARD1 are partially functionally redundant, major positive immune regulators, and AtCBP60a is a negative immune regulator. We investigated possible resilience-conferring evolutionary mechanisms among the CBP60a, CBP60g and SARD1 immune regulatory subfamilies. Phylogenetic analysis was used to investigate the times of CBP60 subfamily neofunctionalization. Then, using the pairwise distance rank based on the newly developed analytical platform Protein Evolution Analysis in a Euclidean Space (PEAES), hypotheses of specific coevolutionary mechanisms that could confer resilience on the regulator module were tested. The immune regulator subfamilies diversified around the time of angiosperm divergence and have been evolving very quickly. We detected significant coevolutionary interactions across the immune regulator subfamilies in all of 12 diverse core eudicot species lineages tested. The coevolutionary interactions were consistent with the hypothesized coevolution mechanisms. Despite their unusually fast evolution, members across the CBP60 immune regulator subfamilies have influenced the evolution of each other long after their diversification in a way that could confer resilience on the immune regulator module against fast-evolving pathogen effectors.

Original languageEnglish (US)
Pages (from-to)479-495
Number of pages17
JournalNew Phytologist
Volume233
Issue number1
Early online dateOct 5 2021
DOIs
StatePublished - Jan 2022

Bibliographical note

Funding Information:
We thank Gane Ka‐Shu Wong and Eric Carpenter for allowing us access to the 1000 Plants transcriptomic sequence database and Fay‐Wei Li for allowing us access to the Waterfern and Floating fern genome sequences, before their publications. We also thank Yaniv Brandvain, Ya Yang, and Emma Goldberg for technical advice and discussion and Jane Glazebrook for editing of the manuscript. QZ was supported by a scholarship from China Scholarship Council and funds from the Zhiming Zhang Laboratory. This work was supported by National Science Foundation (grant nos. MCB‐1518058 and IOS‐1645460 to FK).

Publisher Copyright:
© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation

Keywords

  • Arabidopsis
  • CBP60
  • immune signaling
  • land plants
  • neofunctionalization
  • network resilience
  • plant immunity
  • protein subfamily coevolution

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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