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Ovule identity mediated by pre-mRNA processing in Arabidopsis

Ovules are fundamental for plant reproduction and crop yield as they are the precursors of seeds. Therefore, ovule specification is a critical developmental program. In Arabidopsis thaliana, ovule identity is redundantly conferred by the homeotic D-class genes SHATTERPROOF1 (SHP1), SHP2 and SEEDSTIC...

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Autores principales: Rodríguez-Cazorla, Encarnación, Ortuño-Miquel, Samanta, Candela, Héctor, Bailey-Steinitz, Lindsay J., Yanofsky, Martin F., Martínez-Laborda, Antonio, Ripoll, Juan-José, Vera, Antonio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5785034/
https://www.ncbi.nlm.nih.gov/pubmed/29329291
http://dx.doi.org/10.1371/journal.pgen.1007182
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author Rodríguez-Cazorla, Encarnación
Ortuño-Miquel, Samanta
Candela, Héctor
Bailey-Steinitz, Lindsay J.
Yanofsky, Martin F.
Martínez-Laborda, Antonio
Ripoll, Juan-José
Vera, Antonio
author_facet Rodríguez-Cazorla, Encarnación
Ortuño-Miquel, Samanta
Candela, Héctor
Bailey-Steinitz, Lindsay J.
Yanofsky, Martin F.
Martínez-Laborda, Antonio
Ripoll, Juan-José
Vera, Antonio
author_sort Rodríguez-Cazorla, Encarnación
collection PubMed
description Ovules are fundamental for plant reproduction and crop yield as they are the precursors of seeds. Therefore, ovule specification is a critical developmental program. In Arabidopsis thaliana, ovule identity is redundantly conferred by the homeotic D-class genes SHATTERPROOF1 (SHP1), SHP2 and SEEDSTICK (STK), phylogenetically related to the MADS-domain regulatory gene AGAMOUS (AG), essential in floral organ specification. Previous studies have shown that the HUA-PEP activity, comprised of a suite of RNA-binding protein (RBP) encoding genes, regulates AG pre-mRNA processing and thus flower patterning and organ identity. Here, we report that the HUA-PEP activity additionally governs ovule morphogenesis. Accordingly, in severe hua-pep backgrounds ovules transform into flower organ-like structures. These homeotic transformations are most likely due to the dramatic reduction in SHP1, SHP2 and STK activity. Our molecular and genome-wide profiling strategies revealed the accumulation of prematurely terminated transcripts of D-class genes in hua-pep mutants and reduced amounts of their respective functional messengers, which points to pre-mRNA processing misregulation as the origin of the ovule developmental defects in such backgrounds. RNA processing and transcription are coordinated by the RNA polymerase II (RNAPII) carboxyl-terminal domain (CTD). Our results show that HUA-PEP activity members can interact with the CTD regulator C-TERMINAL DOMAIN PHOSPHATASE-LIKE1 (CPL1), supporting a co-transcriptional mode of action for the HUA-PEP activity. Our findings expand the portfolio of reproductive developmental programs in which HUA-PEP activity participates, and further substantiates the importance of RNA regulatory mechanisms (pre-mRNA co-transcriptional regulation) for correct gene expression during plant morphogenesis.
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spelling pubmed-57850342018-02-08 Ovule identity mediated by pre-mRNA processing in Arabidopsis Rodríguez-Cazorla, Encarnación Ortuño-Miquel, Samanta Candela, Héctor Bailey-Steinitz, Lindsay J. Yanofsky, Martin F. Martínez-Laborda, Antonio Ripoll, Juan-José Vera, Antonio PLoS Genet Research Article Ovules are fundamental for plant reproduction and crop yield as they are the precursors of seeds. Therefore, ovule specification is a critical developmental program. In Arabidopsis thaliana, ovule identity is redundantly conferred by the homeotic D-class genes SHATTERPROOF1 (SHP1), SHP2 and SEEDSTICK (STK), phylogenetically related to the MADS-domain regulatory gene AGAMOUS (AG), essential in floral organ specification. Previous studies have shown that the HUA-PEP activity, comprised of a suite of RNA-binding protein (RBP) encoding genes, regulates AG pre-mRNA processing and thus flower patterning and organ identity. Here, we report that the HUA-PEP activity additionally governs ovule morphogenesis. Accordingly, in severe hua-pep backgrounds ovules transform into flower organ-like structures. These homeotic transformations are most likely due to the dramatic reduction in SHP1, SHP2 and STK activity. Our molecular and genome-wide profiling strategies revealed the accumulation of prematurely terminated transcripts of D-class genes in hua-pep mutants and reduced amounts of their respective functional messengers, which points to pre-mRNA processing misregulation as the origin of the ovule developmental defects in such backgrounds. RNA processing and transcription are coordinated by the RNA polymerase II (RNAPII) carboxyl-terminal domain (CTD). Our results show that HUA-PEP activity members can interact with the CTD regulator C-TERMINAL DOMAIN PHOSPHATASE-LIKE1 (CPL1), supporting a co-transcriptional mode of action for the HUA-PEP activity. Our findings expand the portfolio of reproductive developmental programs in which HUA-PEP activity participates, and further substantiates the importance of RNA regulatory mechanisms (pre-mRNA co-transcriptional regulation) for correct gene expression during plant morphogenesis. Public Library of Science 2018-01-12 /pmc/articles/PMC5785034/ /pubmed/29329291 http://dx.doi.org/10.1371/journal.pgen.1007182 Text en © 2018 Rodríguez-Cazorla et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Rodríguez-Cazorla, Encarnación
Ortuño-Miquel, Samanta
Candela, Héctor
Bailey-Steinitz, Lindsay J.
Yanofsky, Martin F.
Martínez-Laborda, Antonio
Ripoll, Juan-José
Vera, Antonio
Ovule identity mediated by pre-mRNA processing in Arabidopsis
title Ovule identity mediated by pre-mRNA processing in Arabidopsis
title_full Ovule identity mediated by pre-mRNA processing in Arabidopsis
title_fullStr Ovule identity mediated by pre-mRNA processing in Arabidopsis
title_full_unstemmed Ovule identity mediated by pre-mRNA processing in Arabidopsis
title_short Ovule identity mediated by pre-mRNA processing in Arabidopsis
title_sort ovule identity mediated by pre-mrna processing in arabidopsis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5785034/
https://www.ncbi.nlm.nih.gov/pubmed/29329291
http://dx.doi.org/10.1371/journal.pgen.1007182
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