Advertisement

Euphytica

, Volume 211, Issue 1, pp 41–56 | Cite as

Seed dormancy QTL identification across a Sorghum bicolor segregating population

  • Renata Cantoro
  • Luis G. Fernández
  • Gerardo D. L. Cervigni
  • María V. Rodríguez
  • Jorge O. Gieco
  • Norma Paniego
  • Ruth A. Heinz
  • Roberto L. Benech-Arnold
Article

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.

Keywords

Pre-harvest sprouting QTL Seed dormancy Sorghum bicolor SSRs 

Notes

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).

Supplementary material

10681_2016_1717_MOESM1_ESM.docx (1.3 mb)
Supplementary material 1 (DOCX 1282 kb)

References

  1. 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 164:711–729PubMedPubMedCentralGoogle Scholar
  2. Anderson JA, Sorrells ME, Tanksley SD (1993) Detection of QTLsaffecting pre-harvest sprouting resistance in wheat by RFLPs. Crop Sci 33:453–459CrossRefGoogle Scholar
  3. 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):93PubMedPubMedCentralCrossRefGoogle Scholar
  4. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  5. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  6. 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 274–278Google Scholar
  7. 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):988–1002Google Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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. 379–392Google Scholar
  10. 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 PubMedCrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  13. 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 PubMedCrossRefGoogle Scholar
  14. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138(3):963–971PubMedPubMedCentralGoogle Scholar
  15. Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16(22):10881–10890. doi: 10.1093/nar/16.22.10881 PubMedPubMedCentralCrossRefGoogle Scholar
  16. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 PubMedCrossRefGoogle Scholar
  21. 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):133–142PubMedGoogle Scholar
  22. 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 PubMedCrossRefGoogle Scholar
  23. Hu Z, Bao J, Reecy JM (2008) CateGOrizer: a Web-based program to batch analyze gene ontology classification categories. Online J Bioinform 9(2):108–112Google Scholar
  24. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  25. Jiang C, Zeng ZB (1995) Multiple trait analysis of genetic mapping for quantitative trait loci. Genetics 140(3):1111–1127PubMedPubMedCentralGoogle Scholar
  26. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 PubMedCrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. Lijavetzky D, Martínez MC, Carrari F, Esteban Hopp H (2000) QTL analysis and mapping of pre-harvest sprouting resistance in Sorghum. Euphytica 112(2):125–135CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 9:13PubMedPubMedCentralCrossRefGoogle Scholar
  34. 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 PubMedCrossRefGoogle Scholar
  35. 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):1236–1244CrossRefGoogle Scholar
  36. 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 PubMedGoogle Scholar
  37. 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 PubMedCrossRefGoogle Scholar
  38. 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 Google Scholar
  39. 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):551–556PubMedCrossRefGoogle Scholar
  40. Powell W, Machray GC, Provan J (1996) Polymorphism revealed by simple sequence repeats. Trends Plant Sci 1(7):215–222CrossRefGoogle Scholar
  41. 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 PubMedCrossRefGoogle Scholar
  42. 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 PubMedCrossRefGoogle Scholar
  43. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  44. 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 PubMedCrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 PubMedCrossRefGoogle Scholar
  47. 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 PubMedGoogle Scholar
  48. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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 PubMedPubMedCentralGoogle Scholar
  51. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. 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 PubMedCrossRefGoogle Scholar
  54. Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0 Software for the calculation of genetic linkage maps. Plant Research International, WageningenGoogle Scholar
  55. Wan JM, Cao YJ, Wang CM, Ikehashi H (2005) Quantitative trait loci associated with seed dormancy in rice. Crop Sci 45(2):712–716CrossRefGoogle Scholar
  56. Wang S, Basten CJ, Zeng ZB (2006) Windows QTL cartographer 2.5. Raleigh, NCGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. Watson JC, Thompson WF (1986) Purification and restriction endonuclease analysis of plant nuclear DNA. Methods Enzymol 118:57–75CrossRefGoogle Scholar
  59. 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 PubMedCrossRefGoogle Scholar
  60. 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 16:187–193PubMedPubMedCentralCrossRefGoogle Scholar
  61. Zeng ZB (1993) Theoretical basis of separation of multiple linked gene effects on mapping quantitative trait loci. Proc Natl Acad Sci 90:10972–10976PubMedPubMedCentralCrossRefGoogle Scholar
  62. Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136(4):1457–1468PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Renata Cantoro
    • 1
  • Luis G. Fernández
    • 2
  • Gerardo D. L. Cervigni
    • 3
    • 6
  • María V. Rodríguez
    • 1
    • 6
  • Jorge O. Gieco
    • 4
    • 8
  • Norma Paniego
    • 2
    • 5
    • 6
  • Ruth A. Heinz
    • 2
    • 5
    • 6
  • Roberto L. Benech-Arnold
    • 1
    • 6
    • 7
  1. 1.IFEVA, Universidad de Buenos Aires, CONICET, Facultad de AgronomíaBuenos AiresArgentina
  2. 2.Instituto de Biotecnología, CICVyAInstituto Nacional de Tecnología Agropecuaria (INTA)-CastelarHurlingham, Buenos AiresArgentina
  3. 3.Centro de Estudios Fotosintéticos y Bioquímicos (CEFOBI), Facultad de Ciencias Bioquímicas y FarmacéuticasUniversidad Nacional de RosarioRosarioArgentina
  4. 4.Estación Experimental Agropecuaria ManfrediInstituto Nacional de Tecnología Agropecuaria (INTA)CórdobaArgentina
  5. 5.Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresCiudad Autónoma de Buenos AiresArgentina
  6. 6.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Ciudad Autónoma De Buenos AiresArgentina
  7. 7.Cátedra de Cultivos Industriales, Facultad de AgronomíaUniversidad de Buenos AiresCiudad Autónoma de Buenos AiresArgentina
  8. 8.Facultad de Ciencias AgrariasUniversidad Nacional del LitoralEsperanzaArgentina

Personalised recommendations