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An analysis of sugary endosperm in sorghum: Characterization of mutant phenotypes depending on alleles of the corresponding starch debranching enzyme

Sorghum is the fifth most important cereal crop. Here we performed molecular genetic analyses of the ‘SUGARY FETERITA’ (SUF) variety, which shows typical sugary endosperm traits (e.g., wrinkled seeds, accumulation of soluble sugars, and distorted starch). Positional mapping indicated that the corres...

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Autores principales: Hashimoto, Shumpei, Okada, Satoshi, Araki-Nakamura, Satoko, Ohmae-Shinohara, Kozue, Miura, Kotaro, Kawaguchi, Hideo, Ogino, Chiaki, Kasuga, Shigemitsu, Sazuka, Takashi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9969085/
https://www.ncbi.nlm.nih.gov/pubmed/36860899
http://dx.doi.org/10.3389/fpls.2023.1114935
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author Hashimoto, Shumpei
Okada, Satoshi
Araki-Nakamura, Satoko
Ohmae-Shinohara, Kozue
Miura, Kotaro
Kawaguchi, Hideo
Ogino, Chiaki
Kasuga, Shigemitsu
Sazuka, Takashi
author_facet Hashimoto, Shumpei
Okada, Satoshi
Araki-Nakamura, Satoko
Ohmae-Shinohara, Kozue
Miura, Kotaro
Kawaguchi, Hideo
Ogino, Chiaki
Kasuga, Shigemitsu
Sazuka, Takashi
author_sort Hashimoto, Shumpei
collection PubMed
description Sorghum is the fifth most important cereal crop. Here we performed molecular genetic analyses of the ‘SUGARY FETERITA’ (SUF) variety, which shows typical sugary endosperm traits (e.g., wrinkled seeds, accumulation of soluble sugars, and distorted starch). Positional mapping indicated that the corresponding gene was located on the long arm of chromosome 7. Within the candidate region of 3.4 Mb, a sorghum ortholog for maize Su1 (SbSu) encoding a starch debranching enzyme ISA1 was found. Sequencing analysis of SbSu in SUF uncovered nonsynonymous single nucleotide polymorphisms (SNPs) in the coding region, containing substitutions of highly conserved amino acids. Complementation of the rice sugary-1 (osisa1) mutant line with the SbSu gene recovered the sugary endosperm phenotype. Additionally, analyzing mutants obtained from an EMS-induced mutant panel revealed novel alleles with phenotypes showing less severe wrinkles and higher Brix scores. These results suggested that SbSu was the corresponding gene for the sugary endosperm. Expression profiles of starch synthesis genes during the grain-filling stage demonstrated that a loss-of-function of SbSu affects the expression of most starch synthesis genes and revealed the fine-tuned gene regulation in the starch synthetic pathway in sorghum. Haplotype analysis using 187 diverse accessions from a sorghum panel revealed the haplotype of SUF showing severe phenotype had not been used among the landraces and modern varieties. Thus, weak alleles (showing sweet and less severe wrinkles), such as in the abovementioned EMS-induced mutants, are more valuable for grain sorghum breeding. Our study suggests that more moderate alleles (e.g. produced by genome editing) should be beneficial for improving grain sorghum.
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spelling pubmed-99690852023-02-28 An analysis of sugary endosperm in sorghum: Characterization of mutant phenotypes depending on alleles of the corresponding starch debranching enzyme Hashimoto, Shumpei Okada, Satoshi Araki-Nakamura, Satoko Ohmae-Shinohara, Kozue Miura, Kotaro Kawaguchi, Hideo Ogino, Chiaki Kasuga, Shigemitsu Sazuka, Takashi Front Plant Sci Plant Science Sorghum is the fifth most important cereal crop. Here we performed molecular genetic analyses of the ‘SUGARY FETERITA’ (SUF) variety, which shows typical sugary endosperm traits (e.g., wrinkled seeds, accumulation of soluble sugars, and distorted starch). Positional mapping indicated that the corresponding gene was located on the long arm of chromosome 7. Within the candidate region of 3.4 Mb, a sorghum ortholog for maize Su1 (SbSu) encoding a starch debranching enzyme ISA1 was found. Sequencing analysis of SbSu in SUF uncovered nonsynonymous single nucleotide polymorphisms (SNPs) in the coding region, containing substitutions of highly conserved amino acids. Complementation of the rice sugary-1 (osisa1) mutant line with the SbSu gene recovered the sugary endosperm phenotype. Additionally, analyzing mutants obtained from an EMS-induced mutant panel revealed novel alleles with phenotypes showing less severe wrinkles and higher Brix scores. These results suggested that SbSu was the corresponding gene for the sugary endosperm. Expression profiles of starch synthesis genes during the grain-filling stage demonstrated that a loss-of-function of SbSu affects the expression of most starch synthesis genes and revealed the fine-tuned gene regulation in the starch synthetic pathway in sorghum. Haplotype analysis using 187 diverse accessions from a sorghum panel revealed the haplotype of SUF showing severe phenotype had not been used among the landraces and modern varieties. Thus, weak alleles (showing sweet and less severe wrinkles), such as in the abovementioned EMS-induced mutants, are more valuable for grain sorghum breeding. Our study suggests that more moderate alleles (e.g. produced by genome editing) should be beneficial for improving grain sorghum. Frontiers Media S.A. 2023-02-13 /pmc/articles/PMC9969085/ /pubmed/36860899 http://dx.doi.org/10.3389/fpls.2023.1114935 Text en Copyright © 2023 Hashimoto, Okada, Araki-Nakamura, Ohmae-Shinohara, Miura, Kawaguchi, Ogino, Kasuga and Sazuka https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Hashimoto, Shumpei
Okada, Satoshi
Araki-Nakamura, Satoko
Ohmae-Shinohara, Kozue
Miura, Kotaro
Kawaguchi, Hideo
Ogino, Chiaki
Kasuga, Shigemitsu
Sazuka, Takashi
An analysis of sugary endosperm in sorghum: Characterization of mutant phenotypes depending on alleles of the corresponding starch debranching enzyme
title An analysis of sugary endosperm in sorghum: Characterization of mutant phenotypes depending on alleles of the corresponding starch debranching enzyme
title_full An analysis of sugary endosperm in sorghum: Characterization of mutant phenotypes depending on alleles of the corresponding starch debranching enzyme
title_fullStr An analysis of sugary endosperm in sorghum: Characterization of mutant phenotypes depending on alleles of the corresponding starch debranching enzyme
title_full_unstemmed An analysis of sugary endosperm in sorghum: Characterization of mutant phenotypes depending on alleles of the corresponding starch debranching enzyme
title_short An analysis of sugary endosperm in sorghum: Characterization of mutant phenotypes depending on alleles of the corresponding starch debranching enzyme
title_sort analysis of sugary endosperm in sorghum: characterization of mutant phenotypes depending on alleles of the corresponding starch debranching enzyme
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9969085/
https://www.ncbi.nlm.nih.gov/pubmed/36860899
http://dx.doi.org/10.3389/fpls.2023.1114935
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