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

Zongcheng Lin,Marina Triviño,Mansour Karimi,Vernonica E Franklin-Tong,Maurice Bosch,Fei Xie,Moritz K Nowack

doi:10.1104/pp.20.00292

Zongcheng Lin, Marina Triviño + Show 5 more

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https://doi.org/10.1104/pp.20.00292

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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, PrpS PrsS 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 P rhoeas 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.

Highlights

Self-incompatibility (SI) is used by many angiosperms to reject self-pollen and avoid inbreeding
We previously demonstrated that a cognate PrpS-PrsS interaction in Arabidopsis (Arabidopsis thaliana) pollen growing in vitro triggered hallmark features of the P. rhoeas SI response and showed that PrpS and PrsS, when expressed in pollen and pistil, respectively, in Arabidopsis, function to prevent self-seed set, effectively rendering Arabidopsis self-incompatible (Lin et al, 2015)
To examine if the PrpS-PrsS module might work outside the specific context of pollen-pistil interactions, we examined if growth

Summary

Introduction

Self-incompatibility (SI) is used by many angiosperms to reject self-pollen and avoid inbreeding. We previously demonstrated that a cognate PrpS-PrsS interaction in Arabidopsis (Arabidopsis thaliana) pollen growing in vitro triggered hallmark features of the P. rhoeas SI response (de Graaf et al, 2012; Wang et al, 2020) and showed that PrpS and PrsS, when expressed in pollen and pistil, respectively, in Arabidopsis, function to prevent self-seed set, effectively rendering Arabidopsis self-incompatible (Lin et al, 2015). These findings demonstrated that the P. rhoeas S-determinants can be functionally transferred between highly diverged plant species (Bell et al, 2010). As the SI response is triggered within the unique, highly specialized context of the pollen, it was unclear whether the PrpS-PrsS module triggers a pollen-specific pathway or whether this pair of proteins can trigger growth arrest and cell death pathways in other parts of the plant

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