Ectopic Expression of a Self-Incompatibility Module Triggers Growth Arrest and Cell Death in Vegetative Cells

Research output: Contribution to journalArticlepeer-review

Authors

  • Zongcheng Lin
  • Fei Xie
  • Marina Triviño
  • Mansour Karimi
  • Maurice Bosch
  • Moritz K Nowack

Colleges, School and Institutes

External organisations

  • Biology Department, Ghent University, 9000 Ghent, Belgium; Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, 9052 Ghent, Belgium.
  • Aberystwyth University

Abstract

Self-incompatibility (SI) is used by many angiosperms to reject self-pollen and avoid inbreeding. In field poppy (Papaver rhoeas), SI recognition and rejection of self-pollen is facilitated by a female S-determinant, PrsS, and a male S-determinant, PrpSPrsS belongs to the cysteine-rich peptide family, whose members activate diverse signaling networks involved in plant growth, defense, and reproduction. PrsS and PrpS are tightly regulated and expressed solely in pistil and pollen cells, respectively. Interaction of cognate PrsS and PrpS triggers pollen tube growth inhibition and programmed cell death (PCD) of self-pollen. We previously demonstrated functional intergeneric transfer of PrpS and PrsS to Arabidopsis (Arabidopsis thaliana) pollen and pistil. Here, we show that PrpS and PrsS, when expressed ectopically, act as a bipartite module to trigger a self-recognition:self-destruct response in Arabidopsis independently of its reproductive context in vegetative cells. The addition of recombinant PrsS to seedling roots expressing the cognate PrpS resulted in hallmark features of the Prhoeas SI response, including S-specific growth inhibition and PCD of root cells. Moreover, inducible expression of PrsS in PrpS-expressing seedlings resulted in rapid death of the entire seedling. This demonstrates that, besides specifying SI, the bipartite PrpS-PrsS module can trigger growth arrest and cell death in vegetative cells. Heterologous, ectopic expression of a plant bipartite signaling module in plants has not been shown previously and, by extrapolation, our findings suggest that cysteine-rich peptides diversified for a variety of specialized functions, including the regulation of growth and PCD.

Bibliographic note

© 2020 American Society of Plant Biologists. All Rights Reserved.

Details

Original languageEnglish
Pages (from-to)1765-1779
Number of pages15
JournalPLANT PHYSIOLOGY
Volume183
Issue number4
Publication statusPublished - 3 Aug 2020