Insights into the transcriptional and post-transcriptional regulation of the rice SUMOylation machinery and into the role of two rice SUMO proteases

Abstract Background SUMOylation is an essential eukaryotic post-translation modification that, in plants, regulates numerous cellular processes, ranging from seed development to stress response. Using rice as a model crop plant, we searched for potential regulatory points that may influence the acti...

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Main Authors: Margarida T. G. Rosa, Diego M. Almeida, Inês S. Pires, Daniel da Rosa Farias, Alice G. Martins, Luciano Carlos da Maia, António Costa de Oliveira, Nelson J. M. Saibo, M. Margarida Oliveira, Isabel A. Abreu
Format: Article
Language:English
Published: BMC 2018-12-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-018-1547-3
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spelling doaj-bbd683aee5cf4bb9a7861374b955176a2020-11-25T02:33:31ZengBMCBMC Plant Biology1471-22292018-12-0118111810.1186/s12870-018-1547-3Insights into the transcriptional and post-transcriptional regulation of the rice SUMOylation machinery and into the role of two rice SUMO proteasesMargarida T. G. Rosa0Diego M. Almeida1Inês S. Pires2Daniel da Rosa Farias3Alice G. Martins4Luciano Carlos da Maia5António Costa de Oliveira6Nelson J. M. Saibo7M. Margarida Oliveira8Isabel A. Abreu9Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB-UNL)Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB-UNL)Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB-UNL)Plant Genomics and Breeding Center, Faculdade de Agronomia Eliseu Maciel, Universidade Federal de PelotasInstituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB-UNL)Plant Genomics and Breeding Center, Faculdade de Agronomia Eliseu Maciel, Universidade Federal de PelotasPlant Genomics and Breeding Center, Faculdade de Agronomia Eliseu Maciel, Universidade Federal de PelotasInstituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB-UNL)Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB-UNL)Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB-UNL)Abstract Background SUMOylation is an essential eukaryotic post-translation modification that, in plants, regulates numerous cellular processes, ranging from seed development to stress response. Using rice as a model crop plant, we searched for potential regulatory points that may influence the activity of the rice SUMOylation machinery genes. Results We analyzed the presence of putative cis-acting regulatory elements (CREs) within the promoter regions of the rice SUMOylation machinery genes and found CREs related to different cellular processes, including hormone signaling. We confirmed that the transcript levels of genes involved in target-SUMOylation, containing ABA- and GA-related CREs, are responsive to treatments with these hormones. Transcriptional analysis in Nipponbare (spp. japonica) and LC-93-4 (spp. indica), showed that the transcript levels of all studied genes are maintained in the two subspecies, under normal growth. OsSUMO3 is an exceptional case since it is expressed at low levels or is not detectable at all in LC-93-4 roots and shoots, respectively. We revealed post-transcriptional regulation by alternative splicing (AS) for all genes studied, except for SUMO coding genes, OsSIZ2, OsOTS3, and OsELS2. Some AS forms have the potential to alter protein domains and catalytic centers. We also performed the molecular and phenotypic characterization of T-DNA insertion lines of some of the genes under study. Knockouts of OsFUG1 and OsELS1 showed increased SUMOylation levels and non-overlapping phenotypes. The fug1 line showed a dwarf phenotype, and significant defects in fertility, seed weight, and panicle architecture, while the els1 line showed early flowering and decreased plant height. We suggest that OsELS1 is an ortholog of AtEsd4, which was also supported by our phylogenetic analysis. Conclusions Overall, we provide a comprehensive analysis of the rice SUMOylation machinery and discuss possible effects of the regulation of these genes at the transcriptional and post-transcriptional level. We also contribute to the characterization of two rice SUMO proteases, OsELS1 and OsFUG1.http://link.springer.com/article/10.1186/s12870-018-1547-3SUMOylationcis-elementsRice (Oryza sativa)Alternative splicingT-DNASUMO proteases
collection DOAJ
language English
format Article
sources DOAJ
author Margarida T. G. Rosa
Diego M. Almeida
Inês S. Pires
Daniel da Rosa Farias
Alice G. Martins
Luciano Carlos da Maia
António Costa de Oliveira
Nelson J. M. Saibo
M. Margarida Oliveira
Isabel A. Abreu
spellingShingle Margarida T. G. Rosa
Diego M. Almeida
Inês S. Pires
Daniel da Rosa Farias
Alice G. Martins
Luciano Carlos da Maia
António Costa de Oliveira
Nelson J. M. Saibo
M. Margarida Oliveira
Isabel A. Abreu
Insights into the transcriptional and post-transcriptional regulation of the rice SUMOylation machinery and into the role of two rice SUMO proteases
BMC Plant Biology
SUMOylation
cis-elements
Rice (Oryza sativa)
Alternative splicing
T-DNA
SUMO proteases
author_facet Margarida T. G. Rosa
Diego M. Almeida
Inês S. Pires
Daniel da Rosa Farias
Alice G. Martins
Luciano Carlos da Maia
António Costa de Oliveira
Nelson J. M. Saibo
M. Margarida Oliveira
Isabel A. Abreu
author_sort Margarida T. G. Rosa
title Insights into the transcriptional and post-transcriptional regulation of the rice SUMOylation machinery and into the role of two rice SUMO proteases
title_short Insights into the transcriptional and post-transcriptional regulation of the rice SUMOylation machinery and into the role of two rice SUMO proteases
title_full Insights into the transcriptional and post-transcriptional regulation of the rice SUMOylation machinery and into the role of two rice SUMO proteases
title_fullStr Insights into the transcriptional and post-transcriptional regulation of the rice SUMOylation machinery and into the role of two rice SUMO proteases
title_full_unstemmed Insights into the transcriptional and post-transcriptional regulation of the rice SUMOylation machinery and into the role of two rice SUMO proteases
title_sort insights into the transcriptional and post-transcriptional regulation of the rice sumoylation machinery and into the role of two rice sumo proteases
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2018-12-01
description Abstract Background SUMOylation is an essential eukaryotic post-translation modification that, in plants, regulates numerous cellular processes, ranging from seed development to stress response. Using rice as a model crop plant, we searched for potential regulatory points that may influence the activity of the rice SUMOylation machinery genes. Results We analyzed the presence of putative cis-acting regulatory elements (CREs) within the promoter regions of the rice SUMOylation machinery genes and found CREs related to different cellular processes, including hormone signaling. We confirmed that the transcript levels of genes involved in target-SUMOylation, containing ABA- and GA-related CREs, are responsive to treatments with these hormones. Transcriptional analysis in Nipponbare (spp. japonica) and LC-93-4 (spp. indica), showed that the transcript levels of all studied genes are maintained in the two subspecies, under normal growth. OsSUMO3 is an exceptional case since it is expressed at low levels or is not detectable at all in LC-93-4 roots and shoots, respectively. We revealed post-transcriptional regulation by alternative splicing (AS) for all genes studied, except for SUMO coding genes, OsSIZ2, OsOTS3, and OsELS2. Some AS forms have the potential to alter protein domains and catalytic centers. We also performed the molecular and phenotypic characterization of T-DNA insertion lines of some of the genes under study. Knockouts of OsFUG1 and OsELS1 showed increased SUMOylation levels and non-overlapping phenotypes. The fug1 line showed a dwarf phenotype, and significant defects in fertility, seed weight, and panicle architecture, while the els1 line showed early flowering and decreased plant height. We suggest that OsELS1 is an ortholog of AtEsd4, which was also supported by our phylogenetic analysis. Conclusions Overall, we provide a comprehensive analysis of the rice SUMOylation machinery and discuss possible effects of the regulation of these genes at the transcriptional and post-transcriptional level. We also contribute to the characterization of two rice SUMO proteases, OsELS1 and OsFUG1.
topic SUMOylation
cis-elements
Rice (Oryza sativa)
Alternative splicing
T-DNA
SUMO proteases
url http://link.springer.com/article/10.1186/s12870-018-1547-3
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