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...
| Authors: | ; ; ; ; ; ; ; ; ; |
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| Format: | Article |
| Status: | Accepted version |
| 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 |
| _version_ | 1878736663772921856 |
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| author | Baysal, Can |
| 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 |
| author_browse | Baysal, Can Capell Capell, Teresa Christou, Paul Drapal, Margit Fraser, Paul He, Wenshu Khush, Gurdev S. Medina Piles, Vicente Villorbina Noguera, Gemma Zhu, Changfu |
| 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 |
| collection | Repositori Obert UdL |
| 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. |
| eu_rights_str_mv | openAccess |
| format | article |
| id | ES_9312d45a261970b59052d5653cbdaf8b |
| institution | Universitat de Lleida (UdL) |
| instname_str | Universitat de Lleida (UdL) |
| network_acronym_str | ES |
| network_name_str | España |
| oai_identifier_str | oai:repositori.udl.cat:10459.1/69729 |
| publishDate | 2020 |
| publishDateSort | 2020 |
| publisher | National Academy of Sciences |
| publisherStr | National Academy of Sciences |
| reponame_str | Repositori Obert UdL |
| spelling | Inactivation of rice starch branching enzyme IIb triggers broad and unexpected changes in metabolism by transcriptional reprogramming Baysal, Can He, Wenshu Drapal, Margit Villorbina Noguera, Gemma Medina Piles, Vicente Capell Capell, Teresa Khush, Gurdev S. Zhu, Changfu Fraser, Paul Christou, Paul Endosperm High-amylose rice metabolomics Starch biosynthesis transcriptomics 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. 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 Sciences https://doi.org/10.1073/pnas.2014860117 http://hdl.handle.net/10459.1/69729 |
| 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 |
| status_str | acceptedVersion |
| title | 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_short | 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 |
| topic | Endosperm High-amylose rice metabolomics Starch biosynthesis transcriptomics |
| topic_facet | Endosperm High-amylose rice metabolomics Starch biosynthesis transcriptomics |
| url | https://doi.org/10.1073/pnas.2014860117 http://hdl.handle.net/10459.1/69729 |