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

Self-incompatibility (SI) is used by many angiosperms to reject self-pollen and avoid inbreeding. In field poppy ( ), SI recognition and rejection of self-pollen is facilitated by a female -determinant, , and a male -determinant, belongs to the cysteine-rich peptide family, whose members activate di...

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Published inPlant physiology (Bethesda) Vol. 183; no. 4; pp. 1765 - 1779
Main Authors Lin, Zongcheng, Xie, Fei, Triviño, Marina, Karimi, Mansour, Bosch, Maurice, Franklin-Tong, Vernonica E., Nowack, Moritz K.
Format Journal Article
LanguageEnglish
Published United States American Society of Plant Biologists 01.08.2020
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Abstract Self-incompatibility (SI) is used by many angiosperms to reject self-pollen and avoid inbreeding. In field poppy ( ), SI recognition and rejection of self-pollen is facilitated by a female -determinant, , and a male -determinant, belongs to the cysteine-rich peptide family, whose members activate diverse signaling networks involved in plant growth, defense, and reproduction. and 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 and to Arabidopsis ( ) pollen and pistil. Here, we show that and , 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 resulted in hallmark features of the SI response, including -specific growth inhibition and PCD of root cells. Moreover, inducible expression of in -expressing seedlings resulted in rapid death of the entire seedling. This demonstrates that, besides specifying SI, the bipartite 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.
AbstractList 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.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.
Papaver rhoeasS-determinants, which specify self-incompatibility and rejection of self-pollen, trigger growth arrest and programmed cell death in vegetative Arabidopsis tissues when expressed ectopically. 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.
Self-incompatibility (SI) is used by many angiosperms to reject self-pollen and avoid inbreeding. In field poppy ( ), SI recognition and rejection of self-pollen is facilitated by a female -determinant, , and a male -determinant, belongs to the cysteine-rich peptide family, whose members activate diverse signaling networks involved in plant growth, defense, and reproduction. and 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 and to Arabidopsis ( ) pollen and pistil. Here, we show that and , 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 resulted in hallmark features of the SI response, including -specific growth inhibition and PCD of root cells. Moreover, inducible expression of in -expressing seedlings resulted in rapid death of the entire seedling. This demonstrates that, besides specifying SI, the bipartite 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.
Author Triviño, Marina
Franklin-Tong, Vernonica E.
Xie, Fei
Lin, Zongcheng
Nowack, Moritz K.
Bosch, Maurice
Karimi, Mansour
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Senior authors.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Moritz K. Nowack (monow@psb.vib-ugent.be).
www.plantphysiol.org/cgi/doi/10.1104/pp.20.00292
Z.L. designed and performed the research and analyzed data; F.X. contributed to the live-cell imaging; M.T. and M.K. contributed to the vector construction and generation of transgenic lines; Z.L., V.E.F.-T., M.K.N., and M.B. wrote the article.
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Snippet Self-incompatibility (SI) is used by many angiosperms to reject self-pollen and avoid inbreeding. In field poppy ( ), SI recognition and rejection of...
Self-incompatibility (SI) is used by many angiosperms to reject self-pollen and avoid inbreeding. In field poppy (Papaver rhoeas), SI recognition and rejection...
Papaver rhoeasS-determinants, which specify self-incompatibility and rejection of self-pollen, trigger growth arrest and programmed cell death in vegetative...
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StartPage 1765
SubjectTerms Apoptosis - genetics
Apoptosis - physiology
Arabidopsis - genetics
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Cell Death - genetics
Cell Death - physiology
Flowers - genetics
Flowers - metabolism
Pollen - genetics
Pollen - metabolism
Signal Transduction - genetics
Signal Transduction - physiology
Title Ectopic Expression of a Self-Incompatibility Module Triggers Growth Arrest and Cell Death in Vegetative Cells
URI https://www.ncbi.nlm.nih.gov/pubmed/32561539
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