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Theoretical and Applied Genetics

, Volume 111, Issue 4, pp 619–629 | Cite as

The self-incompatibility locus (S) and quantitative trait loci for self-pollination and seed dormancy in sunflower

  • Sonali D. Gandhi
  • Adam F. Heesacker
  • Carrie A. Freeman
  • Jason Argyris
  • Kent Bradford
  • Steven J. KnappEmail author
Original Paper

Abstract

Wild populations of common sunflower (Helianthus annuus L.) are self-incompatible and have deep seed dormancy, whereas modern cultivars, inbreds, and hybrids are self-compatible and partially-to-strongly self-pollinated, and have shallow seed dormancy. Self-pollination (SP) and seed dormancy are genetically complex traits, the number of self-compatibility (S) loci has been disputed, and none of the putative S loci have been genetically mapped in sunflower. We genetically mapped quantitative trait loci (QTL) for self-incompatibility (SI), SP, and seed dormancy in a backcross population produced from a cross between an elite, self-pollinated, nondormant inbred line (NMS373) and a wild, self-incompatible, dormant population (ANN1811). A population consisting of 212 BC1 progeny was subsequently produced by backcrossing a single hybrid individual to NMS373. BC1 progeny produced 0–838 seeds per primary capitula when naturally selfed and 0–518 seeds per secondary capitula when manually selfed and segregated for a single S locus. The S locus mapped to linkage group 17 and was tightly linked to a cluster of previously identified QTL for several domestication and postdomestication traits. Two synergistically interacting QTL were identified for SP among self-compatible (ss) BC1 progeny (R2=34.6%). NMS373 homozygotes produced 271.5 more seeds per secondary capitulum than heterozygotes. Germination percentages of seeds after-ripened for 4 weeks ranged from 0% to 100% among self-compatible BC1S1 families. Three QTL for seed dormancy were identified (R2=38.3%). QTL effects were in the predicted direction (wild alleles decreased self-pollination and seed germination). The present analysis differentiated between loci governing SI and SP and identified DNA markers for bypassing SI and seed dormancy in elite × wild crosses through marker-assisted selection.

Keywords

Quantitative Trait Locus Linkage Group Seed Dormancy Composite Interval Mapping Quantitative Trait Locus Effect 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This research was funded by grants to S.J. Knapp from the United States Department of Agriculture (USDA) National Research Initiative Competitive Grants Program Plant Genome Program (no. 98-35300-6166) and the USDA Cooperative State Research Education and Extension Service Initiative for Future Agricultural and Food Systems Plant Genome Program (no. 2000-04292).

Supplementary material

122_2005_1934_ESM_supp.pdf (155 kb)
(PDF 156 KB)

References

  1. Alissa A, Jonard R, Serieys H, Vincourt P (1986) La culture d’embryons isoles dans un programme d’amelioration du tournesol. C R Acad Sci Paris 302:161–164Google Scholar
  2. Basten CJ, Weir BS, Zeng ZB (2002) qtl cartographer. Department of Statistics, North Carolina State University, Raleigh, N.C.Google Scholar
  3. Berry ST, Leon AJ, Peerbolte R, Challis C, Livini C, Jones R, Feingold S (1997) Presentation of the Advanta sunflower RFLP linkage map for public research. In: Proc 19th Sunflower Res Workshop. Fargo, N.D., pp 113–118Google Scholar
  4. Borevitz JO, Chory J (2004) Genomics tools for QTL analysis and gene discovery. Curr Opin Plant Biol 7:132–136CrossRefPubMedGoogle Scholar
  5. Boyes DC, Nasrallah JB (1993) Physical linkage of the SLG and SRK genes at the self-incompatibility locus of Brassica oleracea. Mol Gen Genet 236:369–373CrossRefPubMedGoogle Scholar
  6. Boyes DC, Nasrallah ME, Vrebalov J, Nasrallah JB (1997) The self-incompatibility (S) haplotypes of Brassica contain highly divergent and rearranged sequences of ancient origin. Plant Cell 9:237–247CrossRefPubMedGoogle Scholar
  7. Burke JM, Tang S, Knapp SJ, Rieseberg LH (2002) Genetic analysis of sunflower domestication. Genetics 161:1257–1267PubMedGoogle Scholar
  8. Burke JM, Lai Z, Salmaso M, Nakazato T, Tang S, Heesacker A, Knapp SJ, Rieseberg LH (2004) Comparative mapping and rapid karyotypic evolution in the genus Helianthus. Genetics 167:449–457CrossRefPubMedGoogle Scholar
  9. Cabrillac D, Delorme V, Garin J, Ruffio-Chable V et al (1999) The S15 self-incompatibility haplotype in Brassica oleracea includes three S gene family members expressed in stigmas. Plant Cell 11:971–986CrossRefPubMedGoogle Scholar
  10. Cai HW, Morishima H (2000) Genomic regions affecting seed shattering and seed dormancy in rice. Theor Appl Genet 100:840–846CrossRefGoogle Scholar
  11. Chandler JM, Jan CC (1985) Comparison of germination techniques for wild Helianthus seeds. Crop Sci 25:356–358Google Scholar
  12. Clerkx EJM, El-Lithy ME, Veirling E, Ruys GJ, Blankestijn-De Vries et al (2004) Analysis of natural allelic variation of Arabidopsis seed germination and seed longevity traits between the accessions Landsberg erecta and Shakdara, using a new recombinant inbred line population. Plant Physiol 135:432–443CrossRefPubMedGoogle Scholar
  13. Conneally PM, Edwards JH, Kidd KK, Lalouel JM, Morton NE, Ott J, White R (1985) Report of the committee on methods of linkage analysis and reporting. Cytogenet Cell Genet 40:356–359PubMedGoogle Scholar
  14. Connor DJ, Hall AJ (1997) Sunflower physiology. In: Schneiter AA (ed) Sunflower technology and production. Crop Science Society of America, Madison, pp 113–182Google Scholar
  15. Corbineau F, Baginol S, Come D (1990) Sunflower (Helianthus annuus L.) seed dormancy and its regulation by ethylene. Isr J Bot 39:313–325Google Scholar
  16. Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative trait. Genetics 142:285–294PubMedGoogle Scholar
  17. Fennimore SA, Nyquist WE, Shaner GE, Doerge RW, Foley ME (1999) A genetic model and molecular markers for wild oat (Avena fatua L.) seed dormancy. Theor Appl Genet 99:711–718CrossRefGoogle Scholar
  18. Fernandez-Martinez J, Knowles PF (1978) Inheritance of self incompatibility in wild sunflower. In: Proc 8th Int Sunflower Conf. Minneapolis, Int Sunflower Assoc, Paris, pp 484–489Google Scholar
  19. Fick GN (1978) Selection for self-fertility and oil percentage in development of sunflower hybrids. In: Proc 8th Int Sunflower Conf. Int Sunflower Assoc, Paris, pp 418–422Google Scholar
  20. Fick GN, Rehder D (1977) Selection criteria in development of high oil sunflower hybrids. In: Proc 2nd Sunflower Forum, Fargo, Natl Sunflower Assoc, Paris, pp 26–27Google Scholar
  21. Fick GN, Zimmer DE (1976) Yield stability of sunflower hybrids and open pollinated varieties. In: Proc 7th Int Sunflower Conf. Int Sunflower Assoc, Paris, pp 253–258Google Scholar
  22. Gedil MA, Wye C, Berry S, Segers B, Peleman J et al (2001) An integrated restriction fragment length polymorphism-amplified fragment length polymorphism linkage map for cultivated sunflower. Genome 44:213–221CrossRefPubMedGoogle Scholar
  23. Habura ECH (1957) Parasterilitat bei sonnenblumen. Z Pflanzenzuecht 37:280–298Google Scholar
  24. Heiser CB (1951) The sunflower among North American Indians. Proc Am Philos Soc 95:432–448Google Scholar
  25. Heiser CB (1954) Variation and subspeciation in the common sunflower, Helianthus annuus. Am Midl Nat 51:287–305Google Scholar
  26. Heiser CB (1976) The sunflower. University of Oklahoma Press, NormanGoogle Scholar
  27. Heiser CB, Smith DM, Clevenger SB, Martin WC (1969) The North American sunflowers (Helianthus). Mem Torr Bot Club 22:1–218Google Scholar
  28. Hiscock SJ, McInnis SM (2003) Pollen recognition and rejection during the sporophytic self-incompatibility response: Brassica and beyond. Trends Plant Sci 8:1360–1385CrossRefGoogle Scholar
  29. Hongtrakul V, Slabaugh MB, Knapp SJ (1998) DFLP, SSCP, and SSR markers for Δ 9-stearoyl-acyl carrier protein desaturases strongly expressed in developing seeds of sunflower: intron lengths are hypervariable among elite inbred lines. Mol Breed 4:195–203CrossRefGoogle Scholar
  30. Ivanov IG (1975) Study on compatibility and incompatibility display in crossing selfed sunflower lines. Rastenievud Nauk 12:36–40Google Scholar
  31. Kolkman J, Slabaugh MB, Bruniard J, Berry S, Bushman SB, Olungu C, Maes N, Abratti G, Zambelli A, Miller JF, Leon A, Knapp SJ (2004) Acetohydroxyacid synthase mutations conferring resistance to imidazolinone or sulfonylurea herbicides in sunflower. Theor Appl Genet 109:1147–1155CrossRefPubMedGoogle Scholar
  32. Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36CrossRefPubMedGoogle Scholar
  33. Kovacik A, Skaloud (1990) Results of inheritance evaluation of agronomically important traits in sunflower. Helia 13:41–46Google Scholar
  34. Kozik A, Michelmore RW, Knapp SJ, Matvienko MS, Rieseberg LH et al (2002) Lettuce and sunflower expressed sequences tags (ESTs) (http://cgpdb.ucdavis.edu).
  35. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg F (1987) mapmaker: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181CrossRefPubMedGoogle Scholar
  36. LeClercq P (1980) Etudes genetiques sur l’autosterilite chez le tournesol. Ann Amelior Plant 30:499–501Google Scholar
  37. Littel RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. Statistical Analysis System, Cary, N.C.Google Scholar
  38. Lofgren JR, Nelson L (1977) Breeding for self incompatibility in sunflowers. In: Proc 2nd Sunflower Res Workshop. Fargo, Natl Sunflower Assoc, Paris, pp 2–4Google Scholar
  39. Luciano A, Kinman ML, Smith JD (1965) Heritability of self-incompatibility in the sunflower (Helianthus annuus). Crop Sci 5:529–532Google Scholar
  40. Lynch M, Walsh B (1997) Genetics and analysis of quantitative traits. Sinauer, SunderlandGoogle Scholar
  41. Miller JF (1997) Registration of cmsHA89 (PEF1) cytoplasmic male-sterile, RPEF1 restorer, and two nuclear male-sterile (NMS 373 and 377) sunflower genetic stocks. Crop Sci 37:1984Google Scholar
  42. Miller JF, Fick GN (1997) The genetics of sunflower. In: Schneiter AA (ed) Sunflower technology and production. Crop Science Society of America, Madison, pp 441–495Google Scholar
  43. Nasrallah JB (2002) Recognition and rejection of self in plant reproduction. Science 296:305–308CrossRefPubMedGoogle Scholar
  44. Nasrallah JB, Nasrallah ME (1993) Pollen-stigma signalling in the sporophytic self-incompatibility response. Plant Cell 5:1325–1335CrossRefPubMedGoogle Scholar
  45. Nettancourt D de (1977) Incompatibility in angiosperms. Springer, Berlin Heidelberg New YorkGoogle Scholar
  46. Nou IS, Watanabe M, Isogai A, Hinata K (1993) Comparison of S-alleles and S-glycoproteins between two wild populations of Brassica campestris in Turkey and Japan. Sex Plant Reprod 6:79–86CrossRefGoogle Scholar
  47. Ockendon DJ (2000) The S-allele collection of Brassica oleracea. Acta Hortic 539:25–30Google Scholar
  48. Olivieri AM, Lucchin M, Parrini P (1988) Self-sterility and incompatibility in sunflower. In: Proc 12th Int Sunflower Conf. Int Sunflower Assoc, Paris, pp 339–343Google Scholar
  49. Rieseberg LH (1998) Genetic mapping as a tool for studying speciation. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, New York, pp 459–487Google Scholar
  50. Rieseberg LH, Choi H, Chan R, Spore C (1993) Genomic map of a diploid hybrid species. Heredity 70:285–293Google Scholar
  51. Rieseberg LH, Van Fossen C, Desrochers A (1995) Hybrid speciation accompanied by genomic reorganization in wild sunflowers. Nature 375:313–316CrossRefGoogle Scholar
  52. Ruffio-Chable V, Gaude T (2001) S-haplotype polymorphism in Brassica oleracea. Acta Hort 546:257–261Google Scholar
  53. Russell WA (1952) A study of the relationships of seed yield, oil content, and other agronomic characters with sunflower inbred lines and their topcrosses. Can J Agric Sci 33:291–314Google Scholar
  54. Segala A, Segala M, Piquemal G (1980) Recherches en vue d’ameliorer le degre d’autogamie des cultivars de tournesol. I. L’autogamie et l’autocompatibilite pollinique. Ann Amelior Plant 30:151–159Google Scholar
  55. Seiler G (1988) Influence of pH, storage temperature, and maturity on germination of four wild annual sunflower species (Helianthus spp.). In: Proc 12th Int Sunflower Conf. Int Sunflower Assoc, Paris, pp 269–270Google Scholar
  56. Seiler GJ (1992) Utilization of wild sunflower species for the improvement of cultivated sunflower. Field Crops Res 30:195–230CrossRefGoogle Scholar
  57. Seiler GJ (1996) Dormancy and germination of wild Helianthus species. In: Caligari PDS, Hind DJN (eds) Compositae: biology and utilitzation. Proc Int Compositae Conf. Kew Gardens, UK, pp 213–222Google Scholar
  58. Seiler GJ (1997) Anatomy and morphology of sunflower. In: Schneiter AA (ed) Sunflower technology and production. Crop Science Society of America, Madison, pp 67–111Google Scholar
  59. Seiler GJ (1998) Seed maturity, storage time and temperature, and media treatment effects on germination of two wild sunflowers. Agron J 90:221–226Google Scholar
  60. Sokal RR, Rohlf FJ (1981) Biometry. WH Freeman and Co, New YorkGoogle Scholar
  61. Tang S, Yu JK, Slabaugh MB, Shintani DK, Knapp SJ (2002) Simple sequence repeat map of the sunflower genome. Theor Appl Genet 105:1124–1136CrossRefPubMedGoogle Scholar
  62. Tang S, Kishore VK, Knapp SJ (2003) PCR-multiplexes for a genome-wide framework of simple sequence repeat marker loci in cultivated sunflower. Theor Appl Genet 107:6–19PubMedGoogle Scholar
  63. Tang S, Leon A, Bridges WC, Knapp SJ (2005) Quantitative trait loci for genetically correlated seed traits epistatically interact and are tightly linked to branching and pericarp pigment loci in sunflower. Crop Sci (in press)Google Scholar
  64. Vranceanu AV, Stoenescu FM, Scarlat A (1978) The influence of different genetic and environmental factors on pollen self-compatibility in sunflower. In: Proc 8th Int Sunflower Conf. Int Sunflower Assoc, Paris, pp 453–465Google Scholar
  65. Vranceanu AV, Iuoras M, Stoenescu FM (1988) Genetic study of short petiole trait and its use in sunflower breeding. In: Proc 12th Int Sunflower Conf. Int Sunflower Assoc, Paris, pp 429–434Google Scholar
  66. Yu JK, Mangor J, Thompson L, Edwards KJ, Slabaugh MB, Knapp SJ (2002) Allelic diversity of simple sequence repeat markers among elite inbred lines in cultivated sunflower. Genome 45:652–660CrossRefPubMedGoogle Scholar
  67. Yu JK, Tang S, Slabaugh MB, Heesacker A, Cole G, Herring M, Soper JJ, Han F, Chu WC, Webb DM, Thompson L, Edwards KJ, Berry S, Leon A, Olungu C, Maes N, Knapp SJ (2003) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci 43:367–387Google Scholar
  68. Zeng ZB (1993) Theoretical basis of separation of multiple linked gene effects on mapping quantitative trait loci. Proc Natl Acad Sci USA 90:10972–10976PubMedGoogle Scholar
  69. Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Sonali D. Gandhi
    • 1
  • Adam F. Heesacker
    • 1
  • Carrie A. Freeman
    • 1
  • Jason Argyris
    • 2
  • Kent Bradford
    • 2
  • Steven J. Knapp
    • 3
    Email author
  1. 1.Department of Crop and Soil ScienceOregon State UniversityCorvallisUSA
  2. 2.Department of Vegetable CropsUniversity of CaliforniaDavisUSA
  3. 3.Center for Applied Genetic TechnologiesThe University of GeorgiaAthensUSA

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