Abstract
Pre-harvest sprouting (PHS) in Sorghum bicolor is one of the main constrains for its production in the central region of Argentina, as grain maturation often coincides with rainy or high environmental humidity conditions. The obtention of more dormant genotypes with higher PHS resistance has always been a desirable trait for breeders but the typical quantitative nature of seed dormancy makes its manipulation difficult through classical breeding. Dissecting this quantitative variability into quantitative trait loci (QTL) is a main concern especially in cereal species. In this work, a sorghum segregating population including 190 families was genotyped with microsatellite markers and the SbABI5 candidate gene. A genetic map encompassing 96 markers and a total length of 1331 cM was built. Seed dormancy was phenotyped in F3 and F4 panicles in two contrasting Argentinean environments (Castelar and Manfredi). Six seed dormancy QTL for mature grains were identified (qGI-1, qGI-3, qGI-4, qGI-6, qGI-7 and qGI-9) with the aid of QTL Cartographer and QTLNetwork, three of them (qGI-3, qGI-7 and qGI-9) being co-localised by both approaches. No epistasis was detected for the identified QTL but QTL-by-environment interaction was significant for qGI-7 and qGI-9. Interestingly, seed dormancy candidate genes SbABI3/VP1 and SbGA20ox3 were located within qGI-3, which makes them noteworthy candidate genes for this QTL.
Similar content being viewed by others
References
Alonso-Blanco C, Bentsink L, Hanhart C, Blankestijn-de Vries H, Koornneef M (2003) Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. Genetics 164:711–729
Anderson JA, Sorrells ME, Tanksley SD (1993) Detection of QTLsaffecting pre-harvest sprouting resistance in wheat by RFLPs. Crop Sci 33:453–459
Barrero J, Cavanagh C, Verbyla K, Tibbits J, Verbyla A, Huang B, Rosewarne G, Stephen S, Wang P, Whan A, Rigault P, Hayden M, Gubler F (2015) Transcriptomic analysis of wheat near-isogenic lines identifies PM19-A1 and A2 as candidates for a major dormancy QTL. Genome Biol 16(1):93
Bentsink L, Jowett J, Hanhart CJ, Koornneef M (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc Natl Acad Sci 103(45):17042–17047. doi:10.1073/pnas.0607877103
Bentsink L, Hanson J, Hanhart CJ, Blankestijn-de Vries H, Coltrane C, Keizer P, El-Lithy M, Alonso-Blanco C, de Andrés MT, Reymond M, van Eeuwijk F, Smeekens S, Koornneef M (2010) Natural variation for seed dormancy in Arabidopsis is regulated by additive genetic and molecular pathways. Proc Natl Acad Sci 107(9):4264–4269. doi:10.1073/pnas.1000410107
Bhatt G, Ellison F, Mares D (1983) Inheritance studies on dormancy in three wheat crosses. In: Kruger JE, Laberge DE (eds) Proceedings of the 3rd international symposium on pre-harvest sprouting in cereals. Boulder, Colorado, USA, pp 274–278
Bhattramakki D, Dong J, Chhabra AK, Hart GE (2000) An integrated SSR and RFLP linkage map of Sorghum bicolor (L.) Moench. Genome/National Research Council Canada 43(6):988–1002
Biddulph TB, Mares DJ, Plummer JA, Setter TL (2005) Drought and high temperature increases preharvest sprouting tolerance in a genotype without grain dormancy. Euphytica 143(3):277–283. doi:10.1007/s10681-005-7882-0
Black M, Butler J, Hughes M (1987) Control and development of dormancy in cereals. In: Mares DE (ed) Proceedings of the 4th symposium on pre-harvest sprouting in cereals. Westview Press, Boulder, Colorado, USA, pp. 379–392
Brown SM, Hopkins MS, Mitchell SE, Senior ML, Wang TY, Duncan RR, Gonzalez-Candelas F, Kresovich S (1996) Multiple methods for the identification of polymorphic simple sequence repeats (SSRs) in sorghum [Sorghum bicolor (L.) Moench]. Theor Appl Genet 93(1–2):190–198. doi:10.1007/bf00225745
Buraas T, Skinnes H (1984) Genetic investigations on seed dormancy in barley. Hereditas 101(2):235–244. doi:10.1111/j.1601-5223.1984.tb00921.x
Cabral AL, Jordan MC, McCartney CA, You FM, Humphreys DG, MacLachlan R, Pozniak CJ (2014) Identification of candidate genes, regions and markers for pre-harvest sprouting resistance in wheat (Triticum aestivum L.). BMC Plant Biol 14:340. doi:10.1186/s12870-014-0340-1
Cai H, Morishima H (2002) QTL clusters reflect character associations in wild and cultivated rice. Theor Appl Genet 104(8):1217–1228. doi:10.1007/s00122-001-0819-7
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138(3):963–971
Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16(22):10881–10890. doi:10.1093/nar/16.22.10881
Glover NM, Daron J, Pingault L, Vandepoele K, Paux E, Feuillet C, Choulet F (2015) Small-scale gene duplications played a major role in the recent evolution of wheat chromosome 3B. Genome Biol 16:188. doi:10.1186/s13059-015-0754-6
Gu X-Y, Zhang L, Glover KD, Chu C, Xu SS, Faris JD, Friesen TL, Ibrahim A (2010) Genetic variation of seed dormancy in synthetic hexaploid wheat-derived populations. Crop Sci 50(4):1318–1324. doi:10.2135/cropsci2009.11.0645
Gualano N, Benech-Arnold R (2009) The effect of water and nitrogen availability during grain filling on the timing of dormancy release in malting barley crops. Euphytica 168(3):291–301. doi:10.1007/s10681-009-9948-x
Gualano N, Carrari F, Verónica Rodríguez M, Pérez-Flores L, Sánchez R, Iusem N, Benech-Arnold R (2007) Reduced embryo sensitivity to abscisic acid in a sprouting-susceptible sorghum (Sorghum bicolor) variety is associated with altered ABA signalling. Seed Sci Res 17(02):81–90. doi:10.1017/S0960258507708115
Han F, Ullrich SE, Clancy JA, Jitkov V, Kilian A, Romagosa I (1996) Verification of barley seed dormancy loci via linked molecular markers. Theor Appl Genet 92(1):87–91. doi:10.1007/bf00222956
Haussmann B, Mahalakshmi V, Reddy B, Seetharama N, Hash C, Geiger H (2002) QTL mapping of stay-green in two sorghum recombinant inbred populations. Theor Appl Genet 106(1):133–142
Hori K, Sato K, Takeda K (2007) Detection of seed dormancy QTL in multiple mapping populations derived from crosses involving novel barley germplasm. Theor Appl Genet 115(6):869–876. doi:10.1007/s00122-007-0620-3
Hu Z, Bao J, Reecy JM (2008) CateGOrizer: a Web-based program to batch analyze gene ontology classification categories. Online J Bioinform 9(2):108–112
Imtiaz M, Ogbonnaya FC, Oman J, van Ginkel M (2008) Characterization of quantitative trait loci controlling genetic variation for preharvest sprouting in synthetic backcross-derived wheat lines. Genetics 178(3):1725–1736. doi:10.1534/genetics.107.084939
Jiang C, Zeng ZB (1995) Multiple trait analysis of genetic mapping for quantitative trait loci. Genetics 140(3):1111–1127
Kim J-S, Islam-Faridi MN, Klein PE, Stelly DM, Price HJ, Klein RR, Mullet JE (2005) Comprehensive molecular cytogenetic analysis of sorghum genome architecture: distribution of euchromatin, heterochromatin, genes and recombination in comparison to rice. Genetics 171(4):1963–1976. doi:10.1534/genetics.105.048215
Kong L, Dong J, Hart GE (2000) Characteristics, linkage-map positions, and allelic differentiation of Sorghum bicolor (L.) Moench DNA simple-sequence repeats (SSRs). Theor Appl Genet 101(3):438–448. doi:10.1007/s001220051501
Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugen 12(1):172–175. doi:10.1111/j.1469-1809.1943.tb02321.x
Kronholm I, Picó FX, Alonso-Blanco C, Goudet J, Meaux Jd (2012) Genetic basis of adaptation in Arabidopsis thaliana: local adaptation at the seed dormancy QTL DOG1. Evolution 66(7):2287–2302. doi:10.1111/j.1558-5646.2012.01590.x
Li M, Yuyama N, Luo L, Hirata M, Cai H (2009) In silico mapping of 1758 new SSR markers developed from public genomic sequences for sorghum. Mol Breed 24(1):41–47. doi:10.1007/s11032-009-9270-2
Lijavetzky D, Martínez MC, Carrari F, Esteban Hopp H (2000) QTL analysis and mapping of pre-harvest sprouting resistance in Sorghum. Euphytica 112(2):125–135
Lin SY, Sasaki T, Yano M (1998) Mapping quantitative trait loci controlling seed dormancy and heading date in rice, Oryza sativa L., using backcross inbred lines. Theor Appl Genet 96(8):997–1003. doi:10.1007/s001220050831
Mace ES, Rami JF, Bouchet S, Klein PE, Klein RR, Kilian A, Wenzl P, Xia L, Halloran K, Jordan DR (2009) A consensus genetic map of sorghum that integrates multiple component maps and high-throughput diversity array technology (DArT) markers. BMC Plant Biol 9:13
Mares D, Mrva K (2014) Wheat grain preharvest sprouting and late maturity alpha-amylase. Planta 240(6):1167–1178. doi:10.1007/s00425-014-2172-5
Menz MA, Klein RR, Unruh NC, Rooney WL, Klein PE, Mullet JE (2004) Genetic diversity of public inbreds of sorghum determined by mapped AFLP and SSR markers. Crop Sci 44(4):1236–1244
Miura K, Lin S, Yano M, Nagamine T (2002) Mapping quantitative trait loci controlling seed longevity in rice (Oryza sativa L.). Theor Appl Genet 104(6–7):981–986. doi:10.1007/s00122-002-0872-x
Mori M, Uchino N, Chono M, Kato K, Miura H (2005) Mapping QTLs for grain dormancy on wheat chromosome 3A and the group 4 chromosomes, and their combined effect. Theor Appl Genet 110(7):1315–1323. doi:10.1007/s00122-005-1972-1
Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T, Utsugi S, Ogawa T, Handa H, Ishida H, Mori M, Kawaura K, Ogihara Y, Miura H (2011) A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell Online. doi:10.1105/tpc.111.088492
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob ur R, Ware D, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556
Powell W, Machray GC, Provan J (1996) Polymorphism revealed by simple sequence repeats. Trends Plant Sci 1(7):215–222
Prada D, Ullrich SE, Molina-Cano JL, Cistué L, Clancy JA, Romagosa I (2004) Genetic control of dormancy in a Triumph/Morex cross in barley. Theor Appl Genet 109(1):62–70. doi:10.1007/s00122-004-1608-x
Ramu P, Kassahun B, Senthilvel S, Ashok Kumar C, Jayashree B, Folkertsma RT, Reddy LA, Kuruvinashetti MS, Haussmann BIG, Hash CT (2009) Exploiting ricesorghum synteny for targeted development of EST-SSRs to enrich the sorghum genetic linkage map. Theor Appl Genet 119(7):1193–1204. doi:10.1007/s00122-009-1120-4
Rodríguez MV, Mendiondo GM, Maskin L, Gudesblat GE, Iusem ND, Benech-Arnold RL (2009) Expression of ABA signalling genes and ABI5 protein levels in imbibed Sorghum bicolor caryopses with contrasting dormancy and at different developmental stages. Ann Bot 104(5):975–985. doi:10.1093/aob/mcp184
Rodríguez MV, Mendiondo GM, Cantoro R, Auge GA, Luna V, Masciarelli O, Benech-Arnold RL (2012) Expression of seed dormancy in grain Sorghum lines with contrasting pre-harvest sprouting behavior involves differential regulation of gibberellin metabolism genes. Plant Cell Physiol 53(1):64–80. doi:10.1093/pcp/pcr154
Rodríguez MV, Barrero JM, Corbineau F, Gubler F, Benech-Arnold RL (2015) Dormancy in cereals (not too much, not so little): about the mechanisms behind this trait. Seed Sci Res 25(Special Issue 02):99–119. doi:10.1017/S0960258515000021
Satish K, Srinivas G, Madhusudhana R, Padmaja PG, Reddy RN, Mohan SM, Seetharama N (2009) Identification of quantitative trait loci for resistance to shoot fly in sorghum [Sorghum bicolor (L.) Moench]. Theor Appl Genet 119(8):1425–1439. doi:10.1007/s00122-009-1145-8
Schloss S, Mitchell S, White G, Kukatla R, Bowers J, Paterson A, Kresovich S (2002) Characterization of RFLP probe sequences for gene discovery and SSR development in Sorghum bicolor (L.) Moench. Theor Appl Genet 105(6–7):912–920. doi:10.1007/s00122-002-0991-4
Silady RA, Effgen S, Koornneef M, Reymond M (2011) Variation in seed dormancy quantitative trait loci in Arabidopsis thaliana originating from one site. PLoS One 6(6):e20886. doi:10.1371/journal.pone.0020886
Steinbach HS, Benech-Arnold RL, Kristof G, Sanchez RA, Marcucci-Poltri S (1995) Physiological basis of pre-harvest sprouting resistance in Sorghum bicolor (L.) Moench. ABA levels and sensitivity in developing embryos of sprouting-resistant and -susceptible varieties. J Exp Bot 46(6):701–709. doi:10.1093/jxb/46.6.701
Steinbach HS, Benech-Arnold RL, Sanchez RA (1997) Hormonal regulation of dormancy in developing Sorghum seeds. Plant Physiol 113(1):149–154. doi:10.1104/pp.113.1.149
Sugimoto K, Takeuchi Y, Ebana K, Miyao A, Hirochika H, Hara N, Ishiyama K, Kobayashi M, Ban Y, Hattori T, Yano M (2010) Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. Proc Natl Acad Sci 107(13):5792–5797. doi:10.1073/pnas.0911965107
Upadhyaya H, Wang Y-H, Sharma S, Singh S, Hasenstein K (2012) SSR markers linked to kernel weight and tiller number in sorghum identified by association mapping. Euphytica 187(3):401–410. doi:10.1007/s10681-012-0726-9
Van Ooijen JW (1992) Accuracy of mapping quantitative trait loci in autogamous species. Theor Appl Genet 84(7–8):803–811. doi:10.1007/bf00227388
Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0 Software for the calculation of genetic linkage maps. Plant Research International, Wageningen
Wan JM, Cao YJ, Wang CM, Ikehashi H (2005) Quantitative trait loci associated with seed dormancy in rice. Crop Sci 45(2):712–716
Wang S, Basten CJ, Zeng ZB (2006) Windows QTL cartographer 2.5. Raleigh, NC
Wang Y-H, Bible P, Loganantharaj R, Upadhyaya H (2012) Identification of SSR markers associated with height using pool-based genome-wide association mapping in sorghum. Mol Breed 30(1):281–292. doi:10.1007/s11032-011-9617-3
Watson JC, Thompson WF (1986) Purification and restriction endonuclease analysis of plant nuclear DNA. Methods Enzymol 118:57–75
Yang J, Hu C, Hu H, Yu R, Xia Z, Ye X, Zhu J (2008) QTLNetwork: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24(5):721–723. doi:10.1093/bioinformatics/btm494
Yonemaru J, Ando T, Mizubayashi T, Kasuga S, Matsumoto T, Yano M (2009) Development of genome-wide simple sequence repeat markers using whole-genome shotgun sequences of sorghum (Sorghum bicolor (L.) Moench). DNA Res 16:187–193
Zeng ZB (1993) Theoretical basis of separation of multiple linked gene effects on mapping quantitative trait loci. Proc Natl Acad Sci 90:10972–10976
Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136(4):1457–1468
Acknowledgments
The authors would like to thank Verónica Lia and Andrea Puebla for their skilful assistance with SSR genotyping and Mirta Tinaro for her qualified technical help with dormancy phenotyping. This work was supported by a grant from the National Agency for Science and Technological Promotion (ANPCyT) PICT 2010 no. 2521 and INTA Project PNBIO 1131042. Renata Cantoro held a PhD grant from the Argentinean National Council of Scientific and Technical Research (CONICET).
Author information
Authors and Affiliations
Corresponding author
Additional information
Ruth A. Heinz and Roberto L. Benech-Arnold have contributed equally to this study.
An erratum to this article can be found at http://dx.doi.org/10.1007/s10681-016-1735-x.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Cantoro, R., Fernández, L.G., Cervigni, G.D.L. et al. Seed dormancy QTL identification across a Sorghum bicolor segregating population. Euphytica 211, 41–56 (2016). https://doi.org/10.1007/s10681-016-1717-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10681-016-1717-z