Seed and floret size parameters of sunflower are determined by partially overlapping sets of quantitative trait loci with epistatic interactions
Floret and seed traits are moderately correlated phenotypically in modern sunflower cultivars, but the underlying genetics are mostly independent. Seed traits in particular are governed in part by epistatic effects among quantitative trait loci.
Seed size is an important quality component in marketing commercial sunflower (Helianthus annuus L.), particularly for the in-shell confectionery market, where long and broad seed types are preferred as a directly consumed snack food globally. Floret size is also important because corolla tube length was previously shown to be inversely correlated with pollinator visitation, impacting bee foraging potential and pollinator services to the plant. Commercial sunflower production benefits from pollinator visits, despite being self-compatible, and bees are required in hybrid seed production, where “female” and “male” inbred lines are crossed at field scale. Issues with pollination of long-seed confectionery sunflower suggest that there may be an unfavorable correlation between seed and floret traits; thus, our objective was to determine the strength of the correlation between seed and floret traits, and confirm any co-localization of seed and floret trait loci using genome-wide association analysis in the SAM diversity panel of sunflower. Our results indicate that phenotypic correlations between seed and floret traits are generally low to moderate, regardless of market class, a component of population substructure. Association mapping results mirror the correlations: while a few loci overlap, many loci for the two traits are not overlapping or even adjacent. The genetics of these traits, while modestly quantitative and influenced by epistatic effects, are not a barrier to simultaneous improvement of seed length and pollinator-friendly floret traits. We conclude that breeding for large seed size, which is required for the confectionery seed market, is possible without producing florets too long for efficient use by pollinators, which promotes bee foraging and associated pollination services.
KeywordsSunflower Helianthus annuus L. Seed size Corolla Floret Pollinator Confectionery
The authors acknowledge the assistance of Jonathan Tetlie, Brady Koehler, and Michael Grove in the maintenance and collection of field samples for this work. The assistance of Brian Smart and Cloe Pogoda to the development of figures is also greatly appreciated. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.
JRP and BSH developed the experimental design; JRP, BF, and ZMP conducted and validated the phenotypic experiments; QMG, SR, and BSH developed the statistical design, conducted the association mapping and epistasis work, and wrote the manuscript; and all authors contributed to final review and acceptance of the manuscript.
This work was supported by funds from the USDA-Agricultural Research Service (project number 3060-21000-043-00D).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights
This work did not involve human participants or research on animals.
- Bachlava E, Tang S, Pizarro G, Schuppert GF, Brunick RK, Draeger D, Leon A, Hahn V, Knapp SJ (2010) Pleiotropy of the branching locus (B) masks linked and unlinked quantitative trait loci affecting seed traits in sunflower. Theor Appl Genet 120:829–842. https://doi.org/10.1007/s00122-009-1212-1 CrossRefPubMedGoogle Scholar
- Cakmak I, Song DS, Mixson TA, Serrano E, Clement ML, Savitski A, Johnson G, Giray T, Abramson CI, Barthell JF, Wells H (2010) Foraging response of turkish honey bee subspecies to flower color choices and reward consistency. J Insect Behav 23:100–116. https://doi.org/10.1007/s10905-009-9199-7 CrossRefGoogle Scholar
- DeBolt S, Scheible W-R, Schrick K, Auer M, Beisson F, Bischoff V, Bouvier-Navé P, Carroll A, Hematy K, Li Y, Milne J, Nair M, Schaller H, Zemla M, Somerville C (2009) Mutations in UDP-glucose: sterol glucosyltransferase in arabidopsis cause transparent testa phenotype and suberization defect in seeds. Plant Physiol 151:78–87. https://doi.org/10.1104/pp.109.140582 CrossRefPubMedPubMedCentralGoogle Scholar
- Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, Higgins J, DeFelice M, Lochner A, Faggart M, Liu-Cordero SN, Rotimi C, Adeyemo A, Cooper R, Ward R, Lander ES, Daly MJ, Altshuler D (2002) The structure of haplotype blocks in the human genome. Science 296:2225–2229. https://doi.org/10.1126/science.1069424 CrossRefPubMedGoogle Scholar
- Garrison E, Marth G (2012) Haplotype-based variant detection from short-read sequencing. arXiv:1207.3907 [q-bio.GN]
- INRA (2018) INRA sunflower bioinformatics resources. https://www.heliagene.org. Accessed 7 Mar 2019
- Kamerling JP, Boons G-J, Lee YC, Suzuki A, Taniguchi N, and Voragen AGJ. (2007) Comprehensive glycoscience. From chemistry to systems biology. In: Kamerling JP (ed) Elsevier Science, Amsterdam, The NetherlandsGoogle Scholar
- Nambeesan SU, Mandel JR, Bowers JE, Marek LF, Ebert D, Corbi J, Rieseberg LH, Knapp SJ, and Burke JM. (2015) Association mapping in sunflower (Helianthus annuus L.) reveals independent control of apical vs. basal branching. BMC Plant Biol. https://doi.org/10.1186/s12870-015-0458-9
- R Core Team (2013) R: A language and environment for statistical computing. R Found. Stat. Comput. Vienna, Austria 0: ISBN:3-900051-07-0Google Scholar
- SAS Institute (2013) The SAS system for Windows. Release 9.4. SAS Inst., Cary, NCGoogle Scholar
- USDA-NASS. (2018). Census of Agriculture, Ag Census Web MapsGoogle Scholar
- Zuber H, Davidian J-C, Aubert G, Aimé D, Belghazi M, Lugan R, Heintz D, Wirtz M, Hell R, Thompson R, Gallardo K (2010) The seed composition of arabidopsis mutants for the group 3 sulfate transporters indicates a role in sulfate translocation within developing seeds. Plant Physiol 154:913–926. https://doi.org/10.1104/pp.110.162123 CrossRefPubMedPubMedCentralGoogle Scholar