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Title: Whole-Genome Sequencing Identifies a Rice Grain Shape Mutant, gs9–1

Abstract

Breeding for genes controlling key agronomic traits is an important goal of rice genetic improvement. To gain insight into genes controlling grain morphology, we screened M3 plants derived from 1,000 whole-genome sequenced (WGS) M2 Kitaake mutants to identify lines with altered grain size. RESULTS:In this study, we isolated a mutant, named fast-neutron (FN) 60-4, which exhibits a significant reduction in grain size. We crossed FN60-4 with the parental line Kitaake and analyzed the resulting backcross population. Segregation analysis of 113 lines from the BC2F2 population revealed that the mutant phenotype is controlled by a single semi-dominant locus. Mutant FN60-4 is reduced 20% in plant height and 8.8% in 1000-grain weight compared with Kitaake. FN60-4 also exhibits an 8% reduction in cell number and a 9% reduction in cell length along the vertical axis of the glume. We carried out whole-genome sequencing of DNA pools extracted from segregants with long grains or short grains, and revealed that one gene, LOC_Os09g02650, cosegregated with the grain size phenotype in the BC1F2 and BC2F2 populations. This mutant allele was named grain shape 9-1 (gs9-1). gs9-1 carries a 3-bp deletion that affects two amino acids. This locus is a new allele of the BC12/GDD1/MTD1 genemore » that encodes a kinesin-like protein involved in cell-cycle progression, cellulose microfibril deposition and gibberellic acid (GA) biosynthesis. The GA biosynthesis-related gene KO2 is down-regulated in gs9-1. The dwarf phenotype of gs9-1 can be rescued by adding exogenous GA3. In contrast to the phenotypes for the other alleles, the gs9-1 is less severe, consistent with the nature of the mutation, which does not disrupt the open reading frame as observed for the other alleles. In this study, we isolated a mutant, which exhibits altered grain shape and identified the mutated gene, gs9-1. Our study reveals that gs9-1 is a semi-dominant gene that carries a two-amino acid mutation. gs9-1 is allelic to the BC12/GDD1/MTD1 gene involved in GA biosynthesis. These results demonstrate the efficiency and convenience of cloning genes from the whole-genome sequenced Kitaake mutant population to advance investigations into genes controlling key agronomic traits in rice.« less

Authors:
ORCiD logo [1];  [2];  [3];  [3];  [3];  [4];  [4];  [5];  [3];  [6];  [6];  [3]
+ Show Author Affiliations
  1. Xiamen Univ., Xiamen (People’s Republic of China); Univ. of California, Davis, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of California, Davis, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Huazhong Agricultural Univ., Hubei (China)
  3. Univ. of California, Davis, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Huazhong Agricultural Univ., Hubei (China)
  6. Xiamen Univ., Xiamen (People's Republic of China)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1545157
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Rice
Additional Journal Information:
Journal Volume: 12; Journal Issue: 1; Journal ID: ISSN 1939-8425
Publisher:
Springer Nature
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Oryza sativaL.; Whole-genome sequencing; Grain shape; Fast-neutron-induced mutant population; Kitaake mutant database

Citation Formats

Jiang, Liangrong, Li, Guotian, Chern, Mawsheng, Jain, Rashmi, Pham, Nhan T., Martin, Joel A., Schackwitz, Wendy S., Zhao, Juan, Ruan, Deling, Huang, Rongyu, Zheng, Jingsheng, and Ronald, Pamela C. Whole-Genome Sequencing Identifies a Rice Grain Shape Mutant, gs9–1. United States: N. p., 2019. Web. doi:10.1186/s12284-019-0308-8.
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Jiang, Liangrong, Li, Guotian, Chern, Mawsheng, Jain, Rashmi, Pham, Nhan T., Martin, Joel A., Schackwitz, Wendy S., Zhao, Juan, Ruan, Deling, Huang, Rongyu, Zheng, Jingsheng, & Ronald, Pamela C. Whole-Genome Sequencing Identifies a Rice Grain Shape Mutant, gs9–1. United States. doi:10.1186/s12284-019-0308-8.
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Jiang, Liangrong, Li, Guotian, Chern, Mawsheng, Jain, Rashmi, Pham, Nhan T., Martin, Joel A., Schackwitz, Wendy S., Zhao, Juan, Ruan, Deling, Huang, Rongyu, Zheng, Jingsheng, and Ronald, Pamela C. Thu . "Whole-Genome Sequencing Identifies a Rice Grain Shape Mutant, gs9–1". United States. doi:10.1186/s12284-019-0308-8. https://www.osti.gov/servlets/purl/1545157.
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@article{osti_1545157,
title = {Whole-Genome Sequencing Identifies a Rice Grain Shape Mutant, gs9–1},
author = {Jiang, Liangrong and Li, Guotian and Chern, Mawsheng and Jain, Rashmi and Pham, Nhan T. and Martin, Joel A. and Schackwitz, Wendy S. and Zhao, Juan and Ruan, Deling and Huang, Rongyu and Zheng, Jingsheng and Ronald, Pamela C.},
abstractNote = {Breeding for genes controlling key agronomic traits is an important goal of rice genetic improvement. To gain insight into genes controlling grain morphology, we screened M3 plants derived from 1,000 whole-genome sequenced (WGS) M2 Kitaake mutants to identify lines with altered grain size. RESULTS:In this study, we isolated a mutant, named fast-neutron (FN) 60-4, which exhibits a significant reduction in grain size. We crossed FN60-4 with the parental line Kitaake and analyzed the resulting backcross population. Segregation analysis of 113 lines from the BC2F2 population revealed that the mutant phenotype is controlled by a single semi-dominant locus. Mutant FN60-4 is reduced 20% in plant height and 8.8% in 1000-grain weight compared with Kitaake. FN60-4 also exhibits an 8% reduction in cell number and a 9% reduction in cell length along the vertical axis of the glume. We carried out whole-genome sequencing of DNA pools extracted from segregants with long grains or short grains, and revealed that one gene, LOC_Os09g02650, cosegregated with the grain size phenotype in the BC1F2 and BC2F2 populations. This mutant allele was named grain shape 9-1 (gs9-1). gs9-1 carries a 3-bp deletion that affects two amino acids. This locus is a new allele of the BC12/GDD1/MTD1 gene that encodes a kinesin-like protein involved in cell-cycle progression, cellulose microfibril deposition and gibberellic acid (GA) biosynthesis. The GA biosynthesis-related gene KO2 is down-regulated in gs9-1. The dwarf phenotype of gs9-1 can be rescued by adding exogenous GA3. In contrast to the phenotypes for the other alleles, the gs9-1 is less severe, consistent with the nature of the mutation, which does not disrupt the open reading frame as observed for the other alleles. In this study, we isolated a mutant, which exhibits altered grain shape and identified the mutated gene, gs9-1. Our study reveals that gs9-1 is a semi-dominant gene that carries a two-amino acid mutation. gs9-1 is allelic to the BC12/GDD1/MTD1 gene involved in GA biosynthesis. These results demonstrate the efficiency and convenience of cloning genes from the whole-genome sequenced Kitaake mutant population to advance investigations into genes controlling key agronomic traits in rice.},
doi = {10.1186/s12284-019-0308-8},
journal = {Rice},
number = 1,
volume = 12,
place = {United States},
year = {2019},
month = {7}
}
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DOI:  10.1186/s12284-019-0308-8
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Works referenced in this record:

Genetic bases of appearance quality of rice grains in Shanyou 63, an elite rice hybrid
journal, October 2000

  • Tan, Y. F.; Xing, Y. Z.; Li, J. X.
  • Theoretical and Applied Genetics, Vol. 101, Issue 5-6
  • DOI: 10.1007/s001220051549

A Novel and Pleiotropic Factor SLENDER GRAIN3 Is Involved in Regulating Grain Size in Rice
journal, May 2018

A Kinesin-Like Protein Is Essential for Oriented Deposition of Cellulose Microfibrils and Cell Wall Strength
journal, December 2002

  • Zhong, Ruiqin; Burk, David H.; Morrison, W. Herbert
  • The Plant Cell, Vol. 14, Issue 12
  • DOI: 10.1105/tpc.005801

Full genome re-sequencing reveals a novel circadian clock mutation in Arabidopsis
journal, January 2011

  • Ashelford, Kevin; Eriksson, Maria E.; Allen, Christopher M.
  • Genome Biology, Vol. 12, Issue 3
  • DOI: 10.1186/gb-2011-12-3-r28

Genome Resilience and Prevalence of Segmental Duplications Following Fast Neutron Irradiation of Soybean
journal, September 2014

Characterization of hemizygous deletions in Citrus using array-Comparative Genomic Hybridization and microsynteny comparisons with the poplar genome
journal, January 2008

  • Ríos, Gabino; Naranjo, Miguel A.; Iglesias, Domingo J.
  • BMC Genomics, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2164-9-381

The million mutation project: A new approach to genetics in Caenorhabditis elegans
journal, June 2013

  • Thompson, O.; Edgley, M.; Strasbourger, P.
  • Genome Research, Vol. 23, Issue 10
  • DOI: 10.1101/gr.157651.113

Map-based cloning of a gene controlling omega-3 fatty acid desaturation in Arabidopsis
journal, November 1992

A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21
journal, December 1995

Genome-Wide Sequencing of 41 Rice (Oryza sativa L.) Mutated Lines Reveals Diverse Mutations Induced by Fast-Neutron Irradiation
journal, July 2016

Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes
journal, December 2011

  • Xu, Xun; Liu, Xin; Ge, Song
  • Nature Biotechnology, Vol. 30, Issue 1
  • DOI: 10.1038/nbt.2050

The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality
journal, July 2015

  • Wang, Shaokui; Li, Shan; Liu, Qian
  • Nature Genetics, Vol. 47, Issue 8
  • DOI: 10.1038/ng.3352

Exploiting a fast neutron mutant genetic resource in Pisum sativum (pea) for functional genomics
journal, January 2013

  • Domoney, Claire; Knox, Maggie; Moreau, Carol
  • Functional Plant Biology, Vol. 40, Issue 12
  • DOI: 10.1071/FP13147

‘Green revolution’ genes encode mutant gibberellin response modulators
journal, July 1999

  • Peng, Jinrong; Richards, Donald E.; Hartley, Nigel M.
  • Nature, Vol. 400, Issue 6741
  • DOI: 10.1038/22307

MULTI-TILLERING DWARF1, a new allele of BRITTLE CULM 12, affects plant height and tiller in rice
journal, December 2016

High-Precision, Whole-Genome Sequencing of Laboratory Strains Facilitates Genetic Studies
journal, August 2008

OsSPL13 controls grain size in cultivated rice
journal, March 2016

  • Si, Lizhen; Chen, Jiaying; Huang, Xuehui
  • Nature Genetics, Vol. 48, Issue 4
  • DOI: 10.1038/ng.3518

The origin of the naked grains of maize
journal, August 2005

  • Wang, Huai; Nussbaum-Wagler, Tina; Li, Bailin
  • Nature, Vol. 436, Issue 7051
  • DOI: 10.1038/nature03863

Overexpression of the Endoplasmic Reticulum Chaperone BiP3 Regulates XA21-Mediated Innate Immunity in Rice
journal, February 2010

Mapping epigenetic mutations in fission yeast using whole-genome next-generation sequencing
journal, May 2009

EMS- and relation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh
journal, March 1982

  • Koornneeff, M.; Dellaert, L. W. M.; van der Veen, J. H.
  • Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 93, Issue 1
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Deletion in a gene associated with grain size increased yields during rice domestication
journal, July 2008

  • Shomura, Ayahiko; Izawa, Takeshi; Ebana, Kaworu
  • Nature Genetics, Vol. 40, Issue 8
  • DOI: 10.1038/ng.169

Caenorhabditis elegans mutant allele identification by whole-genome sequencing
journal, August 2008

  • Sarin, Sumeet; Prabhu, Snehit; O'Meara, M. Maggie
  • Nature Methods, Vol. 5, Issue 10
  • DOI: 10.1038/nmeth.1249

GS9 acts as a transcriptional activator to regulate rice grain shape and appearance quality
journal, March 2018

Analysis of the early-flowering mechanisms and generation of T-DNA tagging lines in Kitaake, a model rice cultivar
journal, August 2013

  • Kim, Song Lim; Choi, Minkyung; Jung, Ki-Hong
  • Journal of Experimental Botany, Vol. 64, Issue 14
  • DOI: 10.1093/jxb/ert226

Genetic bases of rice grain shape: so many genes, so little known
journal, April 2013

Overexpression of a rice BAHD acyltransferase gene in switchgrass (Panicum virgatum L.) enhances saccharification
journal, September 2018

Rpr1, a gene required for Rpg1-dependent resistance to stem rust in barley
journal, July 2006

The Sequences of 1504 Mutants in the Model Rice Variety Kitaake Facilitate Rapid Functional Genomic Studies
journal, June 2017

  • Li, Guotian; Jain, Rashmi; Chern, Mawsheng
  • The Plant Cell, Vol. 29, Issue 6
  • DOI: 10.1105/tpc.17.00154
    [ × clear filter / sort ]

    Works referencing / citing this record:

    Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes
    journal, December 2011

    • Xu, Xun; Liu, Xin; Ge, Song
    • Nature Biotechnology, Vol. 30, Issue 1
    • DOI: 10.1038/nbt.2050

    GS9 acts as a transcriptional activator to regulate rice grain shape and appearance quality
    journal, March 2018

    Genome-Wide Sequencing of 41 Rice (Oryza sativa L.) Mutated Lines Reveals Diverse Mutations Induced by Fast-Neutron Irradiation
    journal, July 2016

    MINI SEED 2 (MIS2) Encodes a Receptor-like Kinase that Controls Grain Size and Shape in Rice
    journal, January 2020

    Exploiting a fast neutron mutant genetic resource in Pisum sativum (pea) for functional genomics
    journal, January 2013

    • Domoney, Claire; Knox, Maggie; Moreau, Carol
    • Functional Plant Biology, Vol. 40, Issue 12
    • DOI: 10.1071/fp13147

    Rpr1, a gene required for Rpg1-dependent resistance to stem rust in barley
    journal, July 2006

    Deletion in a gene associated with grain size increased yields during rice domestication
    journal, July 2008

    • Shomura, Ayahiko; Izawa, Takeshi; Ebana, Kaworu
    • Nature Genetics, Vol. 40, Issue 8
    • DOI: 10.1038/ng.169

    Overexpression of the Endoplasmic Reticulum Chaperone BiP3 Regulates XA21-Mediated Innate Immunity in Rice
    journal, February 2010

    ‘Green revolution’ genes encode mutant gibberellin response modulators
    journal, July 1999

    • Peng, Jinrong; Richards, Donald E.; Hartley, Nigel M.
    • Nature, Vol. 400, Issue 6741
    • DOI: 10.1038/22307

    A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21
    journal, December 1995

    Overexpression of a rice BAHD acyltransferase gene in switchgrass (Panicum virgatum L.) enhances saccharification
    journal, September 2018

    EMS- and relation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh
    journal, March 1982

    • Koornneeff, M.; Dellaert, L. W. M.; van der Veen, J. H.
    • Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 93, Issue 1
    • DOI: 10.1016/0027-5107(82)90129-4

    Genetic bases of rice grain shape: so many genes, so little known
    journal, April 2013

    High-Precision, Whole-Genome Sequencing of Laboratory Strains Facilitates Genetic Studies
    journal, August 2008

    Map-based cloning of a gene controlling omega-3 fatty acid desaturation in Arabidopsis
    journal, November 1992

    The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality
    journal, July 2015

    • Wang, Shaokui; Li, Shan; Liu, Qian
    • Nature Genetics, Vol. 47, Issue 8
    • DOI: 10.1038/ng.3352

    Genetic bases of appearance quality of rice grains in Shanyou 63, an elite rice hybrid
    journal, October 2000

    • Tan, Y. F.; Xing, Y. Z.; Li, J. X.
    • Theoretical and Applied Genetics, Vol. 101, Issue 5-6
    • DOI: 10.1007/s001220051549

    Analysis of the early-flowering mechanisms and generation of T-DNA tagging lines in Kitaake, a model rice cultivar
    journal, August 2013

    • Kim, Song Lim; Choi, Minkyung; Jung, Ki-Hong
    • Journal of Experimental Botany, Vol. 64, Issue 14
    • DOI: 10.1093/jxb/ert226

    A Novel and Pleiotropic Factor SLENDER GRAIN3 Is Involved in Regulating Grain Size in Rice
    journal, May 2018

    OsSPL13 controls grain size in cultivated rice
    journal, March 2016

    • Si, Lizhen; Chen, Jiaying; Huang, Xuehui
    • Nature Genetics, Vol. 48, Issue 4
    • DOI: 10.1038/ng.3518

    A Kinesin-Like Protein Is Essential for Oriented Deposition of Cellulose Microfibrils and Cell Wall Strength
    journal, December 2002

    • Zhong, Ruiqin; Burk, David H.; Morrison, W. Herbert
    • The Plant Cell, Vol. 14, Issue 12
    • DOI: 10.1105/tpc.005801

    The million mutation project: A new approach to genetics in Caenorhabditis elegans
    journal, June 2013

    • Thompson, O.; Edgley, M.; Strasbourger, P.
    • Genome Research, Vol. 23, Issue 10
    • DOI: 10.1101/gr.157651.113

    MULTI-TILLERING DWARF1, a new allele of BRITTLE CULM 12, affects plant height and tiller in rice
    journal, December 2016

    The origin of the naked grains of maize
    journal, August 2005

    • Wang, Huai; Nussbaum-Wagler, Tina; Li, Bailin
    • Nature, Vol. 436, Issue 7051
    • DOI: 10.1038/nature03863

    Caenorhabditis elegans mutant allele identification by whole-genome sequencing
    journal, August 2008

    • Sarin, Sumeet; Prabhu, Snehit; O'Meara, M. Maggie
    • Nature Methods, Vol. 5, Issue 10
    • DOI: 10.1038/nmeth.1249

    Full genome re-sequencing reveals a novel circadian clock mutation in Arabidopsis
    journal, January 2011

    • Ashelford, Kevin; Eriksson, Maria E.; Allen, Christopher M.
    • Genome Biology, Vol. 12, Issue 3
    • DOI: 10.1186/gb-2011-12-3-r28

    Mapping epigenetic mutations in fission yeast using whole-genome next-generation sequencing
    journal, May 2009

    Characterization of hemizygous deletions in Citrus using array-Comparative Genomic Hybridization and microsynteny comparisons with the poplar genome
    journal, January 2008

    • Ríos, Gabino; Naranjo, Miguel A.; Iglesias, Domingo J.
    • BMC Genomics, Vol. 9, Issue 1
    • DOI: 10.1186/1471-2164-9-381

    Genome Resilience and Prevalence of Segmental Duplications Following Fast Neutron Irradiation of Soybean
    journal, September 2014

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