Skip to main content

Advertisement

Log in

Genome-wide association study (GWAS) of germination and post-germination related seedling traits in rice

  • Published:
Euphytica Aims and scope Submit manuscript

A Correction to this article was published on 25 November 2022

This article has been updated

Abstract

Genome-wide association study (GWAS) has become an accepted and powerful method for understanding the associations between phenotypes and genotypes. In agricultural production, uniform and rapid germination is an important prerequisite in crop production. Here, the genetic diversity of rice (Oryza sativa L.) genotypes was put under scrutiny for germination and post-germination related seedling traits, and a rice GWAS analysis with 33,934 SNPs for eight traits including germination percentage (GP), shoot (SL) and root length (RL), root (RFW) and shoot fresh weight (SFW), root (RDW) and shoot (SDW) dry weight, and number of days to germinate (NDG) was performed to define genomic regions influencing seed germination and post-germination related seedling traits. By GWAS, 52 QTLs tagged to 93 significant trait-associated markers were detected across all rice chromosomes. The detected QTLs explained 5 to 58% of variation of different traits. More important candidate associated genes in the vicinity of the detected QTL regions were: LOC_Os01g26210 (OsWAK6) co-located with a seed vigor QTL, a gene with α-glucosidases/starch lyase activity (GH31, LOC_Os07g23944) associated with shoot length, UDP-glucuronic acid 4-epimerase 1 (LOC_Os03g14540) associated with root length, chloroplast outer envelope protein 86 (LOC_Os12g09570) associated with root fresh mass, vacuolar sorting receptor 7 (LOC_Os04g52190) and a gene cluster on chromosome 7 including LOC_Os07g07320 (glutathione S-transferase), LOC_Os07g07340 (glucan endo-1,3-beta-glucosidase) and LOC_Os08g42720 (solute carrier 35) affecting root dry mass, and LOC_Os06g47640 (calmodulin-related calcium sensor protein 29) involveing in the inhibition of ABA during seed germination, associated with germination rate. The associated genes for the studied traits can be generally classified as hydrolytic enzymes, kinases and transferases or transcription factors that can directly or indirectly influence germination and post-germination related seedling traits. Our GWAS results identified several putative candidate genes for germination and seedling traits that will greatly contribute to our understanding of the genetic complexity underlying the corresponding traits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Change history

Abbreviations

GWAS:

Genome-wide association study

LD:

Linkage disequilibrium

MLM:

Mixed linear model

PV:

Phenotypic variation

SNP:

Single nucleotide polymorphism

QTL:

Quantitative trait loci

GP:

Germination percentage

SL:

Shoot length

RL:

Root length

SFW:

Shoot fresh weight

RFW:

Root fresh weight

RDW:

Root dry weight

SDW:

Shoot dry weight

NDG:

Number of days to germinate

References

  • Facon T (2000) Water management in rice in Asia: some issues for the future. Bridging the Rice Yield gap in the Asia-Pacific Region 178

  • Fukao T, Kennedy RA, Yamasue Y, Rumpho ME (2003) Genetic and biochemical analysis of anaerobically-induced enzymes during seed germination of Echinochloa crus-galli varieties tolerant and intolerant of anoxia. J Exp Bot 54:1421–1429

    Article  CAS  PubMed  Google Scholar 

  • Guo J, Wang J, Xi L, Huang WD, Liang J, Chen JG (2009) RACK1 is a negative regulator of ABA responses in Arabidopsis. J Exp Bot 60:3819–3833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang H, Hwang I (2014) Vacuolar sorting receptor-mediated trafficking of soluble vacuolar proteins in plant cells. Plants 3:392–408

    Article  PubMed  PubMed Central  Google Scholar 

  • Miro B, Ismail AM (2013) Tolerance of anaerobic conditions caused by flooding during germination and early growth in rice (Oryza sativa L.). Front Plant Sci 4:269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nayyeripasand L, Garoosi GA, Ahmadikhah A (2021) Genome-wide association study (GWAS) to identify salt-tolerance QTLs carrying novel candidate genes in rice during early vegetative stage. Rice 14:1–21

    Article  Google Scholar 

  • Yang J, Sun K, Li D, Luo L, Liu Y, Huang M, Yang G, Liu H, Wang H, Chen Z, Guo T (2019a) Identification of stable QTLs and candidate genes involved in anaerobic germination tolerance in rice via high-density genetic mapping and RNA-Seq. BMC Genomics 20:1–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou YP, Wu JH, Xiao WH, Chen W, Chen QH, Fan T, Xie CP, Tian CE (2018b) Arabidopsis IQM4, a novel calmodulin-binding protein, is involved with seed dormancy and germination in Arabidopsis. Front Plant Sci 9:721

    Article  PubMed  PubMed Central  Google Scholar 

  • Almansouri M, Kinet JM, Lutts S (2001) Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum L.). Plant Soil 231:243–254

    Article  CAS  Google Scholar 

  • Alqudah AM, Sallam A, Baenziger PS, Börner A (2020) GWAS: Fast-forwarding gene identification and characterization in temperate Cereals: lessons from Barley–a review. J Adv Res 22:119–135

    Article  PubMed  Google Scholar 

  • Andriotis VM, Rejzek M, Barclay E, Rugen MD, Field RA, Smith AM (2016) Cell wall degradation is required for normal starch mobilisation in barley endosperm. Sci Rep 6:1–15

    Article  Google Scholar 

  • Araujo WL, Adriano N-N, Nikoloski Z, Sweetlove LJ, Fernie AR (2012) Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant Cell Env 35:1–21

    Article  CAS  Google Scholar 

  • Arunraj R, Skori L, Kumar A, Hickerson NM, Shoma N, Samuel MA (2020) Spatial regulation of alpha-galactosidase activity and its influence on raffinose family oligosaccharides during seed maturation and germination in Cicer arietinum. Plant Signal Behav 15:1709707

    Article  PubMed  PubMed Central  Google Scholar 

  • Bai X, Moraes TF, Reithmeier RA (2017) Structural biology of solute carrier (SLC) membrane transport proteins. Mol Membr Biol 34:1–32

    Article  PubMed  Google Scholar 

  • Bailly C, Leymarie J, Lehner A, Rousseau S, Côme D, Corbineau F (2004) Catalase activity and expression in developing sunflower seeds as related to drying. J Exp Bot 55:475–483

    Article  CAS  PubMed  Google Scholar 

  • Bastien M, Poirier P, Lemieux I, Després JP (2014a) Overview of epidemiology and contribution of obesity to cardiovascular disease. Prog Cardiovasc Dis 56:369–381

    Article  PubMed  Google Scholar 

  • Bastien M, Sonah H, Belzile F (2014b) Genome wide association mapping of Sclerotinia sclerotiorum resistance in soybean with a genotyping-by-sequencing approach. Plant Genome 7:195

    Article  Google Scholar 

  • Basu U, Upadhyaya HD, Srivastava R, Daware A, Malik N, Sharma A, Tripathi S (2019) ABC transporter-mediated transport of glutathione conjugates enhances seed yield and quality in chickpea. Plant Physiol 180:253–275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baute J, Polyn S, De Block J, Blomme J, Van Lijsebettens M, Inzé D (2017) F-box protein FBX92 affects leaf size in Arabidopsis thaliana. Plant Cell Physiol 58:962–975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beldman G, Osuga D, Whitaker JR (1996) Some characteristics of β-d-xylopyranosidases, α-l-arabinofuranosidases and an arabinoxylan α-l-arabinofuranohydrolase from wheat bran and germinated wheat. J Cereal Sci 23:169–180

    Article  CAS  Google Scholar 

  • Bellani LM, Guarnieri M, Scialabba A (2002) Differences in the activity and distribution of peroxidases from three different portions of germinating Brassica oleracea seeds. Physiol Plant 114:102–108

    Article  CAS  PubMed  Google Scholar 

  • Botto JF, Ibarra S, Jones AM (2009) The heterotrimeric G-protein complex modulates light sensitivity in Arabidopsis thaliana seed germination. Photochem Photobiol 85:949–954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Caspers MP, Lok F, Sinjorgo KM, Van Zeijl MJ, Nielsen KA, Cameron-Mills V (2001) Synthesis, processing and export of cytoplasmic endo-β-1, 4-xylanase from barley aleurone during germination. Plant J 26:191–204

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Xu Y, Luo W, Li W, Chen N, Zhang D, Chong K (2013) The F-box protein OsFBK12 targets OsSAMS1 for degradation and affects pleiotropic phenotypes, including leaf senescence, in rice. Plant Physiol 163:1673–1685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Huang H, Ng HKT (2016) Testing for association in case-control genome-wide association studies with shared controls. Stat Methods Med Res 25:954–967

    Article  PubMed  Google Scholar 

  • Cheng X, Wu Y, Guo J, Du B, Chen R, Zhu L, He G (2013) A rice lectin receptor-like kinase that is involved in innate immune responses also contributes to seed germination. Plant J 76:687–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Y, Zhang X, Sun T, Tian Q, Zhang WH (2018) Glutamate receptor homolog3. 4 is involved in regulation of seed germination under salt stress in Arabidopsis. Plant Cell Physiol 59:978–988

    Article  CAS  PubMed  Google Scholar 

  • Chuang HW, Feng JH, Feng YL, Wei MJ (2015) An Arabidopsis WDR protein coordinates cellular networks involved in light, stress response and hormone signals. Plant Sci 241:23–31

    Article  CAS  PubMed  Google Scholar 

  • Corbineau F, Xia Q, Bailly C, El-Maarouf-Bouteau H (2014) Ethylene, a key factor in the regulation of seed dormancy. Front Plant Sci 5:539

    Article  PubMed  PubMed Central  Google Scholar 

  • de Oliveira LFV, Christoff AP, de Lima JC, de Ross BCF, Sachetto-Martins G, Margis-Pinheiro M, Margis R (2014) The Wall-associated Kinase gene family in rice genomes. Plant Sci 229:181–192

    Article  PubMed  Google Scholar 

  • Debeaujon I, Leon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination and longevity in Arabidopsis. Plant Physiol 122:403–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dekkers BJ, Schuurmans JA, Smeekens S (2004) Glucose delays seed germination in Arabidopsis thaliana. Planta 218:579–588

    Article  CAS  PubMed  Google Scholar 

  • Deng K, Wang Q, Zeng J, Guo X, Zhao X, Tang D, Liu X (2009) A lectin receptor kinase positively regulates ABA response during seed germination and is involved in salt and osmotic stress response. J Plant Biol 52:493

    Article  CAS  Google Scholar 

  • Fedi F, O’Neill CM, Menard G, Trick M, Dechirico S, Corbineau F, Penfield S (2017) Awake1, an ABC-type transporter, reveals an essential role for suberin in the control of seed dormancy. Plant Physiol 174:276–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira CDS, Piedade MTF, Tiné MAS, Rossatto DR, Parolin P, Buckeridge MS (2009) The role of carbohydrates in seed germination and seedling establishment of Himatanthus sucuuba, an Amazonian tree with populations adapted to flooded and non-flooded conditions. Ann Bot 104:1111–1119

    Article  CAS  PubMed  Google Scholar 

  • Fulda M, Schnurr J, Abbadi A, Heinz E (2004) Peroxisomal Acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. Plant Cell 16:394–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Y, Gu H, Leburu M, Li X, Wang Y, Sheng J, Fang H, Gu M, Liang G (2019) The heterotrimeric G protein β subunit RGB1 is required for seedling formation in rice. Rice 12:1–14

    Article  Google Scholar 

  • Gao Y, Liu J, Chen Y, Tang H, Wang Y, He Y, Yao Y (2018) Tomato SlAN11 regulates flavonoid biosynthesis and seed dormancy by interaction with bHLH proteins but not with MYB proteins. Hortic Res 5:1–18

    Article  CAS  Google Scholar 

  • Gomez LD, Steele-King CG, Jones L, Foster JM, Vuttipongchaikij S, McQueen-Mason SJ (2009) Arabinan metabolism during seed development and germination in Arabidopsis. Mol Plant 2:966–976

    Article  CAS  PubMed  Google Scholar 

  • González-Calle V, Barrero-Sicilia C, Carbonero P, Iglesias-Fernández R (2015) Mannans and endo-β-mannanases (MAN) in Brachypodium Distachyon: expression profiling and possible role of the BdMAN genes during coleorhiza-limited seed germination. J Exp Bot 66:3753–3764

    Article  PubMed  PubMed Central  Google Scholar 

  • Grant MM, Briggs DE, Fitchett CS, Stimson E, Deery MJ (2003) Purification of an Arabinofuranosidase and Two β-Xylopyranosidases from Germinated Wheat. J Inst Brew 109:8–15

    Article  CAS  Google Scholar 

  • Gu L, Dou L, Guo Y, Wang H, Li L, Wang C, Yu S (2019) The WRKY transcription factor GhWRKY27 coordinates the senescence regulatory pathway in upland cotton (Gossypium hirsutum L.). BMC Plant Biol 19:1–14

    Article  Google Scholar 

  • Guo X, Hou X, Fang J, Wei P, Xu B, Chen M, Feng Y, Chu C (2013) The rice GERMINATION DEFECTIVE 1, encoding a B3 domain transcriptional repressor, regulates seed germination and seedling development by integrating GA and carbohydrate metabolism. Plant J 75:403–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guzmán-Ortiz FA, Castro-Rosas J, Gómez-Aldapa CA, Mora-Escobedo R, Rojas-León A, Rodríguez-Marín ML, Román-Gutiérrez AD (2019) Enzyme activity during germination of different cereals: a review. Food Rev Int 35:177–200

    Article  Google Scholar 

  • Hammer GL, Dong Z, McLean G, Doherty A, Messina C, Schussler J, Cooper M (2009) Can changes in canopy and/or root system architecture explain historical maize yield trends in the US corn belt? Crop Sci 49:299–312

    Article  Google Scholar 

  • Hayashi H, De Bellis L, Hayashi Y, Nitom K, Kato A, Hayashi M, Nishimura M (2002) Molecular characterization of an Arabidopsis acyl-coenzyme a synthetase localized on glyoxysomal membranes. Plant Physiol 130:2019–2026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu G, Li Z, Lu Y, Li C, Gong S, Yan S, Li G, Wang M, Ren H, Guan H, Zhang Z, Qin D, Chai M, Yu J, Yang D, Wang T, Zhang Z (2017) Genome-wide association study identified multiple genetic loci on chilling resistance during germination in maize. Sci Rep 7:1–11

    Google Scholar 

  • Huang LM, Lai CP, Chen LFO, Chan MT, Shaw JF (2015) Arabidopsis SFAR4 is a novel GDSL-type esterase involved in fatty acid degradation and glucose tolerance. Bot Stud 56:1–12

    Article  Google Scholar 

  • Hussain S, Kim SH, Bahk S, Ali A, Nguyen XC, Yun DJ, Chung WS (2020) The Auxin Signaling repressor IAA8 promotes seed germination through down-regulation of ABI3 transcription in Arabidopsis. Front Plant Sci 11:111

    Article  PubMed  PubMed Central  Google Scholar 

  • Ingelsson B, Shapiguzov A, Kieselbach T, Vener AV (2009) Peptidyl-prolyl isomerase activity in chloroplast thylakoid lumen is a dispensable function of immunophilins in Arabidopsis thaliana. Plant Cell Physiol 50:1801–1814

    Article  CAS  PubMed  Google Scholar 

  • Ismail AM, Ella ES, Vergara GV, Mackill DJ (2009) Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa L.). Ann Bot 103:197–209

    Article  CAS  PubMed  Google Scholar 

  • Ismail AM, Singh US, Singh S, Dar MH, Mackill DJ (2013) The contribution of submergence-tolerant (Sub1) rice varieties to food security in flood-prone rainfed lowland areas in Asia. Field Crops Res 152:83–93

    Article  Google Scholar 

  • Jia Y, Li W (2018) Phospholipase D antagonist 1-butanol inhibited the mobilization of triacylglycerol during seed germination in Arabidopsis. Plant Divers 40:292–298

    Article  PubMed  PubMed Central  Google Scholar 

  • Jung H, Jo SH, Park HJ, Lee A, Kim HS, Lee HJ, Cho HS (2020) Golgi-localized cyclophilin 21 proteins negatively regulate ABA signalling via the peptidyl prolyl isomerase activity during early seedling development. Plant Mol Biol 102:19–38

    Article  CAS  PubMed  Google Scholar 

  • Kanai M, Nishimura M, Hayashi M (2010) A peroxisomal ABC transporter promotes seed germination by inducing pectin degradation under the control of ABI5. Plant J 62:936–947

    CAS  PubMed  Google Scholar 

  • Kawiński A, Miklaszewskam M, Stelter S, Głąb B, Banaś A (2021) Lipases of germinating jojoba seeds efficiently hydrolyze triacylglycerols and wax esters and display wax ester-synthesizing activity. BMC Plant Biol 21:1–13

    Article  Google Scholar 

  • Kim J, Na YJ, Park SJ, Baek SH, Kim DH (2019) Biogenesis of chloroplast outer envelope membrane proteins. Plant Cell Rep 38:783–792

    Article  CAS  PubMed  Google Scholar 

  • Kim JK, Bamba T, Harada K, Fukusaki E, Kobayashi A (2007) Time-course metabolic pro fi ling in Arabidopsis thaliana cell cultures after salt stress treatment. J Exp Bot 58:415–424

    Article  CAS  PubMed  Google Scholar 

  • Ko D, Kang J, Kiba T, Park J, Kojima M, Do J, Martinoia E (2014) Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Nat Acad Sci 111:7150–7155

    Article  CAS  Google Scholar 

  • Kumar S, Trivedi PK (2018) Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. Front Plant Sci 9:751

    Article  PubMed  PubMed Central  Google Scholar 

  • Lakra N, Kaur C, Singla-Pareekm SL, Pareek A (2019) Mapping the ‘early salinity response’triggered proteome adaptation in contrasting rice genotypes using iTRAQ approach. Rice 12:1–22

    Article  Google Scholar 

  • Li DM, Wang Y, Han KL (2012a) Recent density functional theory model calculations of drug metabolism by cytochrome P450. Coord Chem Rev 256:1137–1150

    Article  CAS  Google Scholar 

  • Li G, Lin F, Xue HW (2007) Genome-wide analysis of the phospholipase D family in Oryza sativa and functional characterization of PLDβ1 in seed germination. Cell Res 17:881–894

    Article  CAS  PubMed  Google Scholar 

  • Li K, Yang F, Miao Y, Song CP (2017) Abscisic acid signaling is involved in regulating the mitogen-activated protein kinase cascade module, AIK1-MKK5-MPK6. Plant Signaling Behav 12:e1321188

    Article  Google Scholar 

  • Li Y, Li LL, Fan RC, Peng CC, Sun HL, Zhu SY, Wang X, Zhang L, Zhang DP (2012b) Arabidopsis sucrose transporter SUT4 interacts with cytochrome b5–2 to regulate seed germination in response to sucrose and glucose. Mol Plant 5:1029–1041

    Article  CAS  PubMed  Google Scholar 

  • Lilley JM, Kirkegaard JA (2007) Seasonal variation in the value of subsoil water to wheat: simulation studies in southern New South Wales. Aus J Agric Res 58:1115–1128

    Article  Google Scholar 

  • Lipka AE, Tian F, Wang QS, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang ZW (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28:2397–2399

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Bykova NV, Igamberdiev AU (2017) Cell signaling mechanisms and metabolic regulation of germination and dormancy in barley seeds. Crop J 5:459–477

    Article  Google Scholar 

  • Majee M, Kumar S, Kathare PK, Wu S, Gingerich D, Nayak NR, Dirk LM (2018) KELCH F-BOX protein positively influences Arabidopsis seed germination by targeting Phytochrome-Interacting factor1. PNAS 115:E4120–E4129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez M, Gómez-Cabellos S, Giménez MJ, Barro F, Diaz I, Diaz-Mendoza M (2019) Plant proteases: from key enzymes in germination to allies for fighting human gluten-related disorders. Front Plant Sci 10:721

    Article  PubMed  PubMed Central  Google Scholar 

  • Mather KA, Caicedo AL, Polato NR, Olsen KM, McCouch S, Purugganan MD (2007) The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 177:2223–2232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minic Z, Jouanin L (2006) Plant glycoside hydrolases involved in cell wall polysaccharide degradation. Plant Physiol Biochem 44:435–449

    Article  CAS  PubMed  Google Scholar 

  • Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41:697–709

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Okamoto M, Tatematsu K, Yano R, Seo M, Kamiya Y (2010) Abscisic acid and the control of seed dormancy and germination. Seed Sci Res 20:55

    Article  CAS  Google Scholar 

  • Naveed SA, Zhang F, Zhang J, Zheng TQ, Meng LJ, Pang YL, Xu J, Li ZK (2018) Identification of QTN and candidate genes for salinity tolerance at the germination and seedling stages in rice by genome-wide association analyses. Sci Rep 8:1–11

    Article  CAS  Google Scholar 

  • Pagnussat LA, Oyarburo N, Cimmino C, Pinedo ML, De La Canal L (2015) On the role of a lipid-transfer protein. Arabidopsis ltp3 mutant is compromised in germination and seedling growth. Plant Signaling Behav. 10:e1105417

    Article  Google Scholar 

  • Pandey S, Chen JG, Jones AM, Assmann SM (2006) G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development. Plant Physiol 141:243–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parthibane V, Iyappan R, Vijayakumar A, Venkateshwari V, Rajasekharan R (2012) Serine/threonine/tyrosine protein kinase phosphorylates oleosin, a regulator of lipid metabolic functions. Plant Physiol 159:95–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pudelski B, Schock A, Hoth S, Radchuk R, Weber H, Hofmann J, Sonnewald U, Soll J, Philippar K (2012) The plastid outer envelope protein OEP16 affects metabolic fluxes during ABA-controlled seed development and germination. J Exp Bot 63:1919–1936

    Article  CAS  PubMed  Google Scholar 

  • Ritchie S, Swanson SJ, Gilroy S (2000) Physiology of the aleurone layer and starchy endosperm during grain development and early seedling growth: new insights from cell and molecular biology. Seed Sci Res 10:193–212

    Article  CAS  Google Scholar 

  • Roy S (2016) Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome. Plant Signaling Behav 11:1117723

    Article  Google Scholar 

  • Rozeboom HJ, Yu S, Madrid S, Kalk KH, Zhang R, Dijkstra BW (2013) Crystal structure of α-1, 4-glucan lyase, a unique glycoside hydrolase family member with a novel catalytic mechanism. Biol Chem 288:26764–26774

    Article  CAS  Google Scholar 

  • Siao W, Chen JY, Hsiao HH, Chung P, Wang SJ (2011) Characterization of OsSUT2 expression and regulation in germinating embryos of rice seeds. Rice 4:39–49

    Article  Google Scholar 

  • Singpho NL, Sharma JG (2021) Importance of Cytochrome P450 gene family from metabolite biosynthesis to stress tolerance: A review. In IOP Conference Series: earth and environmental science (Vol. 775, No. 1, p. 012012). IOP Publishing.

  • Sun XL, Yu QY, Tang LL, Ji W, Bai X, Cai H, Zhu YM (2013) GsSRK, a G-type lectin S-receptor-like serine/threonine protein kinase, is a positive regulator of plant tolerance to salt stress. Plant Physiol 170:505–515

    Article  CAS  Google Scholar 

  • Sung HG, Shin HT, Ha JK, Lai HL, Cheng KJ, Lee JH (2005) Effect of germination temperature on characteristics of phytase production from barley. Bioresour Technol 96:1297–1303

    Article  CAS  PubMed  Google Scholar 

  • Szymanski DB, Cosgrove DJ (2009) Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr Biol 19:R800-811

    Article  CAS  PubMed  Google Scholar 

  • Takesawa T, Ito M, Kanzaki H, Kameya N, Nakamura I (2002) Over-expression of glutathione S-transferase in transgenic rice enhances germination and growth at low temperature. Mol Breed 9:93–101

    Article  CAS  Google Scholar 

  • Tian S, Wu J, Li F, Zou J, Liu Y, Zhou B, Bai Y, Sun MX (2016) NtKRP, a kinesin-12 protein, regulates embryo/seed size and seed germination via involving in cell cycle progression at the G2/M transition. Sci Rep 6:1–16

    Article  Google Scholar 

  • Tsao HE, Lui SN, Lo AHF, Chen S, Wong HY, Wong CK, Jiang L, Wong KB (2022) Structural insights into how vacuolar sorting receptors recognize the sorting determinants of seed storage proteins. PNAS 1191:e2111281119

    Article  Google Scholar 

  • Turbant A, Fournet F, Lequart M, Zabijak L, Pageau K, Bouton S, Van Wuytswinkel O (2016) PME58 plays a role in pectin distribution during seed coat mucilage extrusion through homogalacturonan modification. J Exp Bot 67:2177–2190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turner SD (2014) qqman: a R package for visualizing GWAS results using QQ and manhattan plots. Biorxiv, 005165.

  • Ul Haq TU, Gorham J, Akhtar J, Akhtar N, Steele KA (2010) Dynamic quantitative trait loci for salt stress components on chromosome 1 of rice. Funct Plant Biol 37:634–645

    Article  Google Scholar 

  • Ullah H, Chen JG, Wang S, Jones AM (2002) Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination. Plant Physiol 129:897–907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Usadel B, Schlüter U, Mølhøj M, Gipmans M, Verma R, Kossmann J, Reiter W, Pauly M (2004) Identification and characterization of a UDP-D-glucuronate 4-epimerase in Arabidopsis. FEBS Lett 569:327–331

    Article  CAS  PubMed  Google Scholar 

  • Vadovič P, Šamajová O, Takáč T, Novák D, Zapletalová V, Colcombet J, Šamaj J (2019) Biochemical and genetic interactions of phospholipase D alpha 1 and mitogen-activated protein kinase 3 affect Arabidopsis stress response. Front Plant Sci 10:275

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Ooijen G, Mayr G, Kasiem MM, Albrecht M, Cornelissen BJ, Takken FL (2008) Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. J Exp Bot 59(6):1383–1397

    Article  PubMed  Google Scholar 

  • Vijayakumar KR, Gowda LR (2012) Temporal expression profiling of lipase during germination and rice caryopsis development. Plant Physiol Biochem 57:245–253

    Article  CAS  PubMed  Google Scholar 

  • Voegele A, Linkies A, Muller K, Leubner-Metzger G (2011) Members of the gibberellin receptor gene family GID1 (GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Exp Bot 62:5131–5147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang GM, Yin H, Qiao X, Tan X, Gu C, Wang BH, Zhang SL (2016) F-box genes: genome-wide expansion, evolution and their contribution to pollen growth in pear (Pyrus bretschneideri). Plant Sci 253:164–175

    Article  CAS  PubMed  Google Scholar 

  • Wilson RL, Kim H, Bakshi A, Binder BM (2014) The ethylene receptors Ethylene Response1 and Ethylene Response2 have contrasting roles in seed germination of Arabidopsis during salt stress. Plant Physiol 165:1353–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wynd FL (1933) Sources of carbohydrate for germination and growth of orchid seedlings. Ann Mo Bot Gard 20:569–581

    Article  CAS  Google Scholar 

  • Xin Z, Wang A, Yang G, Gao P, Zheng ZL (2009) The Arabidopsis A4 subfamily of lectin receptor kinases negatively regulates abscisic acid response in seed germination. Plant Physiol 149:434–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Wan W, Jiang G, Xi Y, Huang H, Cai J, Chang Y, Duan C, Mangrauthia SK, Peng X, Zhu J, Zhu G (2019) Nucleocytoplasmic trafficking of the Arabidopsis WD40 repeat protein XIW1 regulates ABI5 stability and abscisic acid responses. Mol Plant 12:1598–1611

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi S, Kamiya Y (2001) Gibberellins and light-stimulated seed germination. J Plant Growth Regul 20:369–376

    Article  CAS  PubMed  Google Scholar 

  • Yang B, Song Z, Li C, Jiang J, Zhou Y, Wang R, Fan LM (2018) RSM1, an Arabidopsis MYB protein, interacts with HY5/HYH to modulate seed germination and seedling development in response to abscisic acid and salinity. PLOS Genet 14:1007839

    Article  Google Scholar 

  • Yang L, Wang X, Chang N, Nan W, Wang S, Ruan M, Bi Y (2019b) Cytosolic glucose-6-phosphate dehydrogenase is involved in seed germination and root growth under salinity in Arabidopsis. Front Plant Sci 10:182

    Article  PubMed  PubMed Central  Google Scholar 

  • Yonekura-Sakakibara K, Higashi Y, Nakabayashi R (2019) The origin and evolution of plant flavonoid metabolism. Front Plant Sci 10:943

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang GZ, Jin SH, Jiang XY, Dong RR, Li P, Li YJ, Hou BK (2016) Ectopic expression of UGT75D1, a glycosyltransferase preferring indole-3-butyric acid, modulates cotyledon development and stress tolerance in seed germination of Arabidopsis thaliana. Plant Mol Biol 90:77–93

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zhang J, Xu Q, Wang D, Di H, Huang J, Yang X, Wang Z, Zhang L, Dong L, Wang Z, Zhou Y (2020) Identification of candidate tolerance genes to low-temperature during maize germination by GWAS and RNA-seqapproaches. BMC Plant Biol 20:1–17

    Article  Google Scholar 

  • Zhang T, Wei W, Zhao B, Wang R, Li M, Yang L, Wang J, Sun Q (2018a) a) A reliable methodology for determining seed viability by using hyperspectral data from two sides of wheat seeds. Sensors 18:813

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Zhao Y, Wang Y, Liu Z, Gao C (2018b) Comprehensive analysis of MYB gene family and their expressions under abiotic stresses and hormone treatments in Tamarix hispida. Front Plant Sci 9:1303

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu H, Arnett DK, Ordovas MJ, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao K, Tung W, Eizenga C, Wright H, Ali L, Price H, Norton J, Islam R, Reynolds A, Mexey J, McClung A, Bustamante D, Mccouch S (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa L. Nat Commun 2:1–10

    Article  Google Scholar 

  • Zhao P, Hou S, Guo X, Jia J, Yang W, Liu Z, Cheng L (2019) A MYB-related transcription factor from sheepgrass, LcMYB2, promotes seed germination and root growth under drought stress. BMC Plant Biol 19:1–15

    Article  Google Scholar 

  • Zhao X, Liu N, Shang N, Zeng W, Ebert B, Rautengarten C, Zeng Q, Li H, Chen X, Beahan C, Bacic A, Heazlewood JH, Wu AM (2018) Three UDP-xylose transporters participate in xylan biosynthesis by conveying cytosolic UDP-xylose into the Golgi lumen in Arabidopsis. J Exp Bot 69:1125–1134

    Article  CAS  PubMed  Google Scholar 

  • Zhou YP, Wu JH, Xiao WH, Chen W, Chen QH, Fan T, Tian CE (2018a) Arabidopsis IQM4, a novel calmodulin-binding protein, is involved with seed dormancy and germination in Arabidopsis. Front Plant Sci 9:721

    Article  PubMed  PubMed Central  Google Scholar 

  • Linkies A, Graeber K, Knight C, Leubner‐Metzger G (2010) The evolution of seeds. New Phytologist, 186(4): 817–831.

    Article  CAS  PubMed  Google Scholar 

  • Mrva K, Wallwork M, Mares D J (2006) α- Amylase and programmed cell death in aleurone of ripening wheat grains. Journal of Experimental Botany, 57(4): 877–885.

    Article  CAS  PubMed  Google Scholar 

  • Wickham H (2016) Programming with ggplot2. In ggplot2 (pp. 241–253). Springer, Cham.

Download references

Acknowledgements

This research was conducted in Biotechnology laboratory, Department of Plant Sciences and Biotechnology, Shahid Beheshti University, Iran. We thank Sari Agricultural Sciences and Natural Resources University, Sari, Iran for providing paddy land for planting rice genotypes. In addition, we express grateful thanks to International Rice Research Institute (IRRI) in Philippines for providing the seeds of rice cultivars.

Funding

Shahid Beheshti University partially supported the research.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Asadollah Ahmadikhah or Naser Farrokhi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest. All authors affirm that the article is the authors' original work. This manuscript has not been submitted for publication nor has it been published in whole or in part elsewhere. We attest to the fact that all authors listed here have contributed notably to the effort, have read the manuscript, attest to the validity and legitimacy of the data and its interpretation, and agree to its submission to the journal of Euphytica. On behalf of all co-authors, the corresponding author stands complete responsibility for the submission.

Ethical statement

This article does not contain any studies involving human participants performed by any of the authors. Also, it does not contain any studies involving animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original version of this article was revised: the first author's name contained a typo and should read: Rahele Panahabadi

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 106 KB)

Supplementary file2 (DOCX 511 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Panahabadi, R., Ahmadikhah, A., Farrokhi, N. et al. Genome-wide association study (GWAS) of germination and post-germination related seedling traits in rice. Euphytica 218, 112 (2022). https://doi.org/10.1007/s10681-022-03069-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-022-03069-x

Keywords

Navigation