Identification of the rice Rc gene as a main regulator of seed survival under dry storage conditions.

Seed deterioration during storage results in poor germination, reduced vigor, and non-uniform seedling emergence. The aging rate depends on storage conditions and genetic factors. This study aims to identify these genetic factors determining the longevity of rice (Oryza sativa L.) seeds stored under experimental aging conditions mimicking long-term dry storage. Genetic variation for tolerance to aging was studied in 300 Indica rice accessions by storing dry seeds under an elevated partial pressure of oxygen (EPPO) condition. A genome-wide association analysis identified eleven unique genomic regions for all measured germination parameters after aging, differing from those previously identified in rice under humid experimental aging conditions. The significant single nucleotide polymorphism in the most prominent region was located within the Rc gene, encoding a bHLH transcription factor. Storage experiments using near-isogenic rice lines (SD7-1D (Rc) and SD7-1d (rc)) with the same allelic variation confirmed the role of the wildtype Rc gene, providing stronger tolerance to dry EPPO aging. In the seed pericarp, a functional Rc gene results in accumulation of proanthocyanidins, an important sub-class of flavonoids having strong antioxidant activity, which may explain the variation in tolerance to dry EPPO aging. This article is protected by copyright. All rights reserved.

[1]  R. D. de Vos,et al.  Experimental rice seed aging under elevated oxygen pressure: Methodology and mechanism , 2022, Frontiers in Plant Science.

[2]  Sibin Yu,et al.  Insights into the Regulation of Rice Seed Storability by Seed Tissue-Specific Transcriptomic and Metabolic Profiling , 2022, Plants.

[3]  C. Na,et al.  Does oxygen affect ageing mechanisms of Pinus densiflora seeds? A matter of cytoplasmic physical state. , 2022, Journal of experimental botany.

[4]  L. Bentsink,et al.  Evaluating the EPPO method for seed longevity analyses in Arabidopsis. , 2020, Plant science : an international journal of experimental plant biology.

[5]  Shuhong Zhao,et al.  rMVP: A Memory-efficient, Visualization-enhanced, and Parallel-accelerated Tool for Genome-wide Association Study , 2020, bioRxiv.

[6]  Hongkai Wu,et al.  The rice ( Oryza sativa ) Rc gene improves resistance to preharvest sprouting and retains seed and milled rice quality , 2020 .

[7]  R. Serrano,et al.  Identification of novel seed longevity genes related to oxidative stress and seed coat by genome-wide association studies and reverse genetics. , 2020, Plant, cell & environment.

[8]  F. Gawthrop,et al.  The effects of high oxygen partial pressure on vegetable Allium seeds with a short shelf-life , 2020, Planta.

[9]  A. Kohli,et al.  Brown Rice, a Diet Rich in Health Promoting Properties. , 2019, Journal of nutritional science and vitaminology.

[10]  L. Tian,et al.  Genetic Dissection of Seed Storability and Validation of Candidate Gene Associated with Antioxidant Capability in Rice (Oryza sativa L.) , 2019, International journal of molecular sciences.

[11]  Heng Ye,et al.  Assembling seed dormancy genes into a system identified their effects on seedbank longevity in weedy rice , 2019, Heredity.

[12]  Hafiz Ansar Rasul Suleria,et al.  Proanthocyanidins: A comprehensive review. , 2019, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[13]  Ahmed S. M. Saleh,et al.  Brown Rice Versus White Rice: Nutritional Quality, Potential Health Benefits, Development of Food Products, and Preservation Technologies. , 2019, Comprehensive reviews in food science and food safety.

[14]  Kenneth L. McNally,et al.  Variation in seed longevity among diverse Indica rice varieties , 2019, Annals of botany.

[15]  W. Waterworth,et al.  Seeds and the Art of Genome Maintenance , 2019, Front. Plant Sci..

[16]  Lana S. Martin,et al.  Population structure in genetic studies: Confounding factors and mixed models , 2018, PLoS genetics.

[17]  F. Hay,et al.  Seed longevity phenotyping: recommendations on research methodology. , 2018, Journal of experimental botany.

[18]  Chi Zhang,et al.  PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files , 2018, Bioinform..

[19]  Eric L. Patterson,et al.  Exploring the fate of mRNA in aging seeds: protection, destruction, or slow decay? , 2018, Journal of experimental botany.

[20]  Hongxia Zhang,et al.  Phytochemical Profile of Brown Rice and Its Nutrigenomic Implications , 2018, Antioxidants.

[21]  L. Bentsink,et al.  Seed dormancy release accelerated by elevated partial pressure of oxygen is associated with DOG loci , 2018, Journal of experimental botany.

[22]  Kenneth L. McNally,et al.  Genomic variation in 3,010 diverse accessions of Asian cultivated rice , 2018, Nature.

[23]  Chen Yang,et al.  Genome-wide investigation of pentatricopeptide repeat gene family in poplar and their expression analysis in response to biotic and abiotic stresses , 2018, Scientific Reports.

[24]  S. Balzergue,et al.  An Integrated “Multi-Omics” Comparison of Embryo and Endosperm Tissue-Specific Features and Their Impact on Rice Seed Quality , 2017, Front. Plant Sci..

[25]  M. Yoon,et al.  Contrasting tocol ratios associated with seed longevity in rice variety groups , 2017, Seed Science Research.

[26]  Zhen-yu Liu,et al.  Identification of QTLs for seed storability in rice under natural aging conditions using two RILs with the same parent Shennong 265 , 2017 .

[27]  A. R. Vennapusa,et al.  Aldo-ketoreductase 1 (AKR1) improves seed longevity in tobacco and rice by detoxifying reactive cytotoxic compounds generated during ageing , 2017, Rice.

[28]  R. Francis,et al.  pophelper: an R package and web app to analyse and visualize population structure , 2017, Molecular ecology resources.

[29]  Inna Dubchak,et al.  Rice SNP-seek database update: new SNPs, indels, and queries , 2016, Nucleic Acids Res..

[30]  J. Buitink,et al.  Late seed maturation: drying without dying. , 2016, Journal of experimental botany.

[31]  Zhiwu Zhang,et al.  GAPIT Version 2: An Enhanced Integrated Tool for Genomic Association and Prediction , 2016, The plant genome.

[32]  P. Verma,et al.  Rice PROTEIN l-ISOASPARTYL METHYLTRANSFERASE isoforms differentially accumulate during seed maturation to restrict deleterious isoAsp and reactive oxygen species accumulation and are implicated in seed vigor and longevity. , 2016, The New phytologist.

[33]  H. Hilhorst,et al.  Galactinol as marker for seed longevity. , 2016, Plant science : an international journal of experimental plant biology.

[34]  U. Lohwasser,et al.  The inheritance of wheat grain longevity: a comparison between induced and natural ageing , 2016, Journal of Applied Genetics.

[35]  A. Marion-Poll,et al.  Staying Alive: Molecular Aspects of Seed Longevity. , 2016, Plant & cell physiology.

[36]  A. Börner,et al.  Barley Seed Aging: Genetics behind the Dry Elevated Pressure of Oxygen Aging and Moist Controlled Deterioration , 2016, Front. Plant Sci..

[37]  E. Glaab,et al.  Inference of Longevity-Related Genes from a Robust Coexpression Network of Seed Maturation Identifies Regulators Linking Seed Storability to Biotic Defense-Related Pathways , 2015, Plant Cell.

[38]  L. Bentsink,et al.  A role for seed storage proteins in Arabidopsis seed longevity , 2015, Journal of experimental botany.

[39]  R. Ellis,et al.  Increases in the longevity of desiccation-phase developing rice seeds: response to high-temperature drying depends on harvest moisture content , 2015, Annals of botany.

[40]  H. Rolletschek,et al.  Genome-wide association mapping and biochemical markers reveal that seed ageing and longevity are intricately affected by genetic background and developmental and environmental conditions in barley. , 2015, Plant, cell & environment.

[41]  Ling Jiang,et al.  Mapping QTLs related to rice seed storability under natural and artificial aging storage conditions , 2015, Euphytica.

[42]  A. Mahender,et al.  Early seedling vigour, an imperative trait for direct-seeded rice: an overview on physio-morphological parameters and molecular markers , 2015, Planta.

[43]  M. Yano,et al.  Fine mapping of a major quantitative trait locus, qLG-9, that controls seed longevity in rice (Oryza sativa L.) , 2015, Theoretical and Applied Genetics.

[44]  Carson C Chow,et al.  Second-generation PLINK: rising to the challenge of larger and richer datasets , 2014, GigaScience.

[45]  rice genomes The 3,000 rice genomes project , 2014, GigaScience.

[46]  Ling Jiang,et al.  OsLOX2, a rice type I lipoxygenase, confers opposite effects on seed germination and longevity , 2014, Transgenic Research.

[47]  J. Kodde,et al.  Prolonging the longevity of ex situ conserved seeds by storage under anoxia , 2014, Plant Genetic Resources.

[48]  Y. Gan,et al.  AtEXP2 Is Involved in Seed Germination and Abiotic Stress Response in Arabidopsis , 2014, PloS one.

[49]  V. Brunaud,et al.  ARABIDOPSIS THALIANA HOMEOBOX25 Uncovers a Role for Gibberellins in Seed Longevity1[C][W] , 2013, Plant Physiology.

[50]  W. Buckley,et al.  Seed Ethanol Emission and Radicle Protrusion are Better Measures of Canola-Seed Vigor Than Standard Germination , 2013 .

[51]  Ling Jiang,et al.  Molecular genetic characterization of rice seed lipoxygenase 3 and assessment of its effects on seed longevity , 2013, Journal of Plant Biology.

[52]  A. Korte,et al.  The advantages and limitations of trait analysis with GWAS: a review , 2013, Plant Methods.

[53]  R. De Vos,et al.  Seed storage at elevated partial pressure of oxygen, a fast method for analysing seed ageing under dry conditions , 2012, Annals of botany.

[54]  Heng Ye,et al.  Association Between Seed Dormancy and Pericarp Color Is Controlled by a Pleiotropic Gene That Regulates Abscisic Acid and Flavonoid Synthesis in Weedy Red Rice , 2011, Genetics.

[55]  M. van Zanten,et al.  Seed maturation in Arabidopsis thaliana is characterized by nuclear size reduction and increased chromatin condensation , 2011, Proceedings of the National Academy of Sciences.

[56]  K. Bradford,et al.  Oxygen interacts with priming, moisture content and temperature to affect the longevity of lettuce and onion seeds , 2011, Seed Science Research.

[57]  W. Friedt,et al.  Seed longevity in oilseed rape (Brassica napus L.) – genetic variation and QTL mapping , 2011, Plant Genetic Resources.

[58]  H. Pan,et al.  Identification of QTLs for seed germination capability after various storage periods using two RIL populations in rice , 2011, Molecules and cells.

[59]  K. Bradford,et al.  Quantitative trait loci associated with longevity of lettuce seeds under conventional and controlled deterioration storage conditions , 2010, Journal of experimental botany.

[60]  M. Moutschen-Dahmen,et al.  CHROMOSOME DISTURBANCES AND MUTATION PRODUCED IN PLANT SEEDS BY OXYGEN AT HIGH PRESSURES , 2010 .

[61]  Zhiwu Zhang,et al.  Mixed linear model approach adapted for genome-wide association studies , 2010, Nature Genetics.

[62]  David H. Alexander,et al.  Fast model-based estimation of ancestry in unrelated individuals. , 2009, Genome research.

[63]  A. Xiong,et al.  Identification of quantitative trait loci for seed storability in rice (Oryza sativa L.) , 2008, Euphytica.

[64]  Sébastien Lê,et al.  FactoMineR: An R Package for Multivariate Analysis , 2008 .

[65]  Tomohiko Yoshida,et al.  Role of maternal tissues in qLG-9 control of seed longevity in rice (Oryza sativa L.) , 2008 .

[66]  M. Purugganan,et al.  The Extent of Linkage Disequilibrium in Rice (Oryza sativa L.) , 2007, Genetics.

[67]  Edward S. Buckler,et al.  TASSEL: software for association mapping of complex traits in diverse samples , 2007, Bioinform..

[68]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[69]  T. D. Hong,et al.  Seed longevity - moisture content relationships in hermetic and open storage , 2007 .

[70]  A. Baudry,et al.  Genetics and biochemistry of seed flavonoids. , 2006, Annual review of plant biology.

[71]  Q. Qian,et al.  QTL analysis of seed storability in rice , 2006 .

[72]  M. Thomson,et al.  Caught Red-Handed: Rc Encodes a Basic Helix-Loop-Helix Protein Conditioning Red Pericarp in Rice[W][OA] , 2006, The Plant Cell Online.

[73]  Y. Fukuta,et al.  Mapping of quantitative trait loci controlling seed longevity of rice (Oryza sativa L.) after various periods of seed storage , 2005 .

[74]  M. Daly,et al.  Haploview: analysis and visualization of LD and haplotype maps , 2005, Bioinform..

[75]  M. Pollard,et al.  Vitamin E Is Essential for Seed Longevity and for Preventing Lipid Peroxidation during Germination , 2004, The Plant Cell Online.

[76]  C. Bailly Active oxygen species and antioxidants in seed biology , 2004, Seed Science Research.

[77]  H. Tsukaya,et al.  Regulation of the biosynthesis of plant hormones by cytochrome P450s , 2002, Journal of Plant Research.

[78]  S. Lin,et al.  Mapping quantitative trait loci controlling seed longevity in rice (Oryza sativa L.) , 2002, Theoretical and Applied Genetics.

[79]  M. Koornneef,et al.  Genetic analysis of seed-soluble oligosaccharides in relation to seed storability of Arabidopsis. , 2000, Plant physiology.

[80]  F. Chen,et al.  Expression of an expansin is associated with endosperm weakening during tomato seed germination. , 2000, Plant physiology.

[81]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[82]  E. Vierling,et al.  The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. , 2000, Plant physiology.

[83]  M. Koornneef,et al.  Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. , 2000, Plant physiology.

[84]  M. Mcdonald Seed deterioration: Physiology, repair and assessment , 1999 .

[85]  C. Walters Understanding the mechanisms and kinetics of seed aging , 1998, Seed Science Research.

[86]  D. A. Priestley Seed aging : implications for seed storage and persistence in the soil , 1987 .

[87]  K. Thompson,et al.  Seeds: Physiology of Development and Germination , 1986 .

[88]  B. Halliwell,et al.  Free radicals in biology and medicine , 1985 .

[89]  J. Ohlrogge,et al.  Oxygen-dependent aging of seeds. , 1982, Plant physiology.

[90]  Oren L. Justice,et al.  Principles and practices of seed storage , 1978 .

[91]  E. Roberts The Viability of Rice Seed in relation to Temperature, Moisture Content, and Gaseous Environment , 1961 .

[92]  Marco F. Schmidt Genomic Variation , 2022, Chemical Biology.

[93]  Yi-Ju Hsu,et al.  Arabidopsis HIT4, a regulator involved in heat-triggered reorganization of chromatin and release of transcriptional gene silencing, relocates from chromocenters to the nucleolus in response to heat stress. , 2015, The New phytologist.

[94]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[95]  E. Kalemba,et al.  Possible roles of LEA proteins and sHSPs in seed protection: a short review , 2007 .

[96]  R. Dixon,et al.  Proanthocyanidins--a final frontier in flavonoid research? , 2005, The New phytologist.

[97]  E. H. Roberts,et al.  Improved Equations for the Prediction of Seed Longevity , 1980 .

[98]  E. H. Roberts,et al.  Effects of Temperature, Moisture, and Oxygen on the Induction of Chromosome Damage in Seeds of Barley, Broad Beans, and Peas during Storage , 1968 .