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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Main Authors: Encarnación Rodríguez-Cazorla, Samanta Ortuño-Miquel, Héctor Candela, Lindsay J Bailey-Steinitz, Martin F Yanofsky, Antonio Martínez-Laborda, Juan-José Ripoll, Antonio Vera
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-01-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC5785034?pdf=render
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spelling doaj-e7f3647645a248ac9ae41b61ce77a2922020-11-25T01:19:27ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042018-01-01141e100718210.1371/journal.pgen.1007182Ovule identity mediated by pre-mRNA processing in Arabidopsis.Encarnación Rodríguez-CazorlaSamanta Ortuño-MiquelHéctor CandelaLindsay J Bailey-SteinitzMartin F YanofskyAntonio Martínez-LabordaJuan-José RipollAntonio VeraOvules 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.http://europepmc.org/articles/PMC5785034?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Encarnación Rodríguez-Cazorla
Samanta Ortuño-Miquel
Héctor Candela
Lindsay J Bailey-Steinitz
Martin F Yanofsky
Antonio Martínez-Laborda
Juan-José Ripoll
Antonio Vera
spellingShingle Encarnación Rodríguez-Cazorla
Samanta Ortuño-Miquel
Héctor Candela
Lindsay J Bailey-Steinitz
Martin F Yanofsky
Antonio Martínez-Laborda
Juan-José Ripoll
Antonio Vera
Ovule identity mediated by pre-mRNA processing in Arabidopsis.
PLoS Genetics
author_facet Encarnación Rodríguez-Cazorla
Samanta Ortuño-Miquel
Héctor Candela
Lindsay J Bailey-Steinitz
Martin F Yanofsky
Antonio Martínez-Laborda
Juan-José Ripoll
Antonio Vera
author_sort Encarnación Rodríguez-Cazorla
title Ovule identity mediated by pre-mRNA processing in Arabidopsis.
title_short 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_sort ovule identity mediated by pre-mrna processing in arabidopsis.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2018-01-01
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.
url http://europepmc.org/articles/PMC5785034?pdf=render
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