Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming

Starch properties can be modified by mutating genes responsible for the synthesis of amylose and amylopectin in the endosperm. However, little is known about the effects of such targeted modifications on the overall starch biosynthesis pathway and broader metabolism. Here we investigated the effects...

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Authors: Baysal, Can, He, Wenshu, Drapal, Margit, Villorbina Noguera, Gemma, Medina Piles, Vicente, Capell Capell, Teresa, Khush, Gurdev S., Zhu, Changfu, Fraser, Paul, Christou, Paul
Format: article
Status:Versión aceptada para publicación
Publication Date:2020
Country:España
Institution:Universitat de Lleida (UdL)
Repository:Repositori Obert UdL
OAI Identifier:oai:repositori.udl.cat:10459.1/69729
Online Access:https://doi.org/10.1073/pnas.2014860117
http://hdl.handle.net/10459.1/69729
Access Level:Open access
Keyword:Endosperm
High-amylose rice
metabolomics
Starch biosynthesis
transcriptomics
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spelling Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogrammingBaysal, CanHe, WenshuDrapal, MargitVillorbina Noguera, GemmaMedina Piles, VicenteCapell Capell, TeresaKhush, Gurdev S.Zhu, ChangfuFraser, PaulChristou, PaulEndospermHigh-amylose ricemetabolomicsStarch biosynthesistranscriptomicsStarch properties can be modified by mutating genes responsible for the synthesis of amylose and amylopectin in the endosperm. However, little is known about the effects of such targeted modifications on the overall starch biosynthesis pathway and broader metabolism. Here we investigated the effects of mutating the OsSBEIIb gene encoding starch branching enzyme IIb, which is required for amylopectin synthesis in the endosperm. As anticipated, homozygous mutant plants, in which OsSBEIIb was completely inactivated by abolishing the catalytic center and C-terminal regulatory domain, produced opaque seeds with depleted starch reserves. Amylose content in the mutant increased from 19.6 to 27.4% and resistant starch (RS) content increased from 0.2 to 17.2%. Many genes encoding isoforms of AGPase, soluble starch synthase, and other starch branching enzymes were up-regulated, either in their native tissues or in an ectopic manner, whereas genes encoding granule-bound starch synthase, debranching enzymes, pullulanase, and starch phosphorylases were largely down-regulated. There was a general increase in the accumulation of sugars, fatty acids, amino acids, and phytosterols in the mutant endosperm, suggesting that intermediates in the starch biosynthesis pathway increased flux through spillover pathways causing a profound impact on the accumulation of multiple primary and secondary metabolites. Our results provide insights into the broader implications of perturbing starch metabolism in rice endosperm and its impact on the whole plant, which will make it easier to predict the effect of metabolic engineering in cereals for nutritional improvement or the production of valuable metabolites.We would like to acknowledge funding from Ministry of Economy and Competitiveness, Spain (RTI2018-097613-BI00 to C.Z., PGC2018-097655-B-I00 to P.C., and AGL2017-85377-R to T.C.); Generalitat de Catalunya Grant 2017 SGR 828 to the Agricultural Biotechnology and Bioeconomy Unit; and the European Union Framework Program DISCO (from discovery to final products: a next-generation pipeline for the sustainable generation of high-value plant products; Project 613513) to P.D.F.National Academy of Sciences2020info:eu-repo/semantics/articleinfo:eu-repo/semantics/acceptedVersionapplication/pdfhttps://doi.org/10.1073/pnas.2014860117http://hdl.handle.net/10459.1/69729reponame:Repositori Obert UdL instname:Universitat de Lleida (UdL)Inglésinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-097613-B-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-097655-B-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/AGL2017-85377-RVersió postprint del document publicat a: https://doi.org/10.1073/pnas.2014860117Proceedings of the National Academy of Sciences of the United States of America, 2020, vol. 117, num. 42, p. 26503-26512info:eu-repo/grantAgreement/EC/FP7/613513(c) Baysal, Can et al., 2020info:eu-repo/semantics/openAccessoai:repositori.udl.cat:10459.1/697292026-06-24T12:42:17Z
dc.title.none.fl_str_mv Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming
title Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming
spellingShingle Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming
Baysal, Can
Endosperm
High-amylose rice
metabolomics
Starch biosynthesis
transcriptomics
title_short Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming
title_full Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming
title_fullStr Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming
title_full_unstemmed Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming
title_sort Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming
dc.creator.none.fl_str_mv Baysal, Can
He, Wenshu
Drapal, Margit
Villorbina Noguera, Gemma
Medina Piles, Vicente
Capell Capell, Teresa
Khush, Gurdev S.
Zhu, Changfu
Fraser, Paul
Christou, Paul
author Baysal, Can
author_facet Baysal, Can
He, Wenshu
Drapal, Margit
Villorbina Noguera, Gemma
Medina Piles, Vicente
Capell Capell, Teresa
Khush, Gurdev S.
Zhu, Changfu
Fraser, Paul
Christou, Paul
author_role author
author2 He, Wenshu
Drapal, Margit
Villorbina Noguera, Gemma
Medina Piles, Vicente
Capell Capell, Teresa
Khush, Gurdev S.
Zhu, Changfu
Fraser, Paul
Christou, Paul
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Endosperm
High-amylose rice
metabolomics
Starch biosynthesis
transcriptomics
topic Endosperm
High-amylose rice
metabolomics
Starch biosynthesis
transcriptomics
description Starch properties can be modified by mutating genes responsible for the synthesis of amylose and amylopectin in the endosperm. However, little is known about the effects of such targeted modifications on the overall starch biosynthesis pathway and broader metabolism. Here we investigated the effects of mutating the OsSBEIIb gene encoding starch branching enzyme IIb, which is required for amylopectin synthesis in the endosperm. As anticipated, homozygous mutant plants, in which OsSBEIIb was completely inactivated by abolishing the catalytic center and C-terminal regulatory domain, produced opaque seeds with depleted starch reserves. Amylose content in the mutant increased from 19.6 to 27.4% and resistant starch (RS) content increased from 0.2 to 17.2%. Many genes encoding isoforms of AGPase, soluble starch synthase, and other starch branching enzymes were up-regulated, either in their native tissues or in an ectopic manner, whereas genes encoding granule-bound starch synthase, debranching enzymes, pullulanase, and starch phosphorylases were largely down-regulated. There was a general increase in the accumulation of sugars, fatty acids, amino acids, and phytosterols in the mutant endosperm, suggesting that intermediates in the starch biosynthesis pathway increased flux through spillover pathways causing a profound impact on the accumulation of multiple primary and secondary metabolites. Our results provide insights into the broader implications of perturbing starch metabolism in rice endosperm and its impact on the whole plant, which will make it easier to predict the effect of metabolic engineering in cereals for nutritional improvement or the production of valuable metabolites.
publishDate 2020
dc.date.none.fl_str_mv 2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv https://doi.org/10.1073/pnas.2014860117
http://hdl.handle.net/10459.1/69729
url https://doi.org/10.1073/pnas.2014860117
http://hdl.handle.net/10459.1/69729
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-097613-B-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-097655-B-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/AGL2017-85377-R
Versió postprint del document publicat a: https://doi.org/10.1073/pnas.2014860117
Proceedings of the National Academy of Sciences of the United States of America, 2020, vol. 117, num. 42, p. 26503-26512
info:eu-repo/grantAgreement/EC/FP7/613513
dc.rights.none.fl_str_mv (c) Baysal, Can et al., 2020
info:eu-repo/semantics/openAccess
rights_invalid_str_mv (c) Baysal, Can et al., 2020
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv National Academy of Sciences
publisher.none.fl_str_mv National Academy of Sciences
dc.source.none.fl_str_mv reponame:Repositori Obert UdL
instname:Universitat de Lleida (UdL)
instname_str Universitat de Lleida (UdL)
reponame_str Repositori Obert UdL
collection Repositori Obert UdL
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,81155

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