Skip to main content
Log in

Retrotransposon-related genetic distance and hybrid performance in sunflower (Helianthus annuus L.)

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Heterosis is a main force leading the development of the hybrid seed industry in sunflower. The purpose of this study is to evaluate if heterosis effects for morphological traits among sunflower hybrids can be related to differences in the repetitive component of the genome of parental lines. The assumption is that, at least for certain traits, heterosis results from mutations in the cis-regulatory elements of genes, largely related to retrotransposon insertions and/or removals. Our experimental approach consists of a correlation study between hybrid performance and retrotransposon-related genetic distances between inbreds. Six sunflower inbred lines of different origin were crossed in a half diallel fashion; comparing parental lines and hybrids, mid parent heterosis of F1 hybrids was evaluated for six traits. We estimated the parental genetic distances between the six inbreds on data gathered by the inter-retrotransposon-amplified-polymorphism (IRAP) protocol. Different retrotransposons previously isolated in sunflower were targeted by 11 primer pairs designed on conserved LTR domains. As a control, genetic distances were also calculated using 86 genic SNPs. We analysed the correlation between the mid-parent heterosis for each of the six traits analysed and the genetic distance (calculated on data obtained by SNP or IRAP analyses) between the parental lines. Differences between parents showed to be largely related to variations in the retrotransposon component of the genome. Retrotransposon-related genetic distance between parents resulted to be larger than that related to genic SNPs, and significantly correlated to seed yield and, at a lesser extent, to plant height and stem diameter in hybrids. The hypothesis that variations in the repetitive component of the genome, especially LTR-retrotransposons, affect the displaying of heterosis is discussed.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahmad S, Khan MS, Swati MS, Shah GS, Khalil IH (2005) A study on heterosis and inbreeding depression in sunflower (Helianthus annuus L.). Songklanakarin J Sci Technol 27:1–8

    Google Scholar 

  • Boppenmaier J, Melchinger AE, Brunklaus-Jung E, Geiger HH, Herrmann RG (1992) Genetic distance for RFLPs in European maize inbreds: I. Relation to performance of flint dent crosses for forage traits. Crop Sci 32:895–902

    Article  Google Scholar 

  • Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17:343–360

    Article  PubMed  CAS  Google Scholar 

  • Buckler ES, Gaut BS, McMullen MD (2006) Molecular and functional diversity of maize. Curr Opin Plant Biol 9:172–176

    Article  PubMed  CAS  Google Scholar 

  • Buti M, Giordani T, Vukich M, Gentzbittel L, Pistelli L, Cattonaro F, Morgante M, Cavallini A, Natali L (2009) HACRE1, a recently inserted copia-like retrotransposon of sunflower (Helianthus annuus L.). Genome 52:904–911

    Article  PubMed  CAS  Google Scholar 

  • Buti M, Giordani T, Cattonaro F, Cossu RM, Pistelli L, Vukich M, Morgante M, Cavallini A, Natali L (2011) Temporal dynamics in the evolution of the sunflower genome as revealed by sequencing and annotation of three large genomic regions. Theor Appl Genet 123:779–791

    Article  PubMed  CAS  Google Scholar 

  • Cavallini A, Natali L, Zuccolo A, Giordani T, Jurman I, Ferrillo V, Vitacolonna N, Sarri V, Cattonaro F, Ceccarelli M, Cionini PG, Morgante M (2010) Analysis of genome composition and organization in sunflower (Helianthus annuus L.) and related species. Theor Appl Genet 120:491–508

    Article  PubMed  CAS  Google Scholar 

  • Charcosset A, Gallais A (2003) Application of markers in selection. In: de Vienne D (ed) Molecular markers in plants genetics and biotechnology. Science Publishers, Enfield, pp 53–176

    Google Scholar 

  • Charcosset AM, Lefort-Buson M, Gallais A (1991) Relationship between heterosis and heterozygosity at marker loci: a theoretical computation. Theor Appl Genet 81:571–575

    Article  Google Scholar 

  • Cheres MT, Knapp SJ (1998) Ancestral origins and genetic diversity of cultivated sunflower: analysis of the pedigrees of public germplasm. Crop Sci 38:1476–1482

    Article  Google Scholar 

  • Cheres MT, Miller JF, Crane JM, Knapp SJ (2000) Genetic distance as a predictor of heterosis and hybrid performance within and between heterotic groups in sunflower. Theor Appl Genet 100:889–894

    Article  Google Scholar 

  • Ching A, Caldwell KS, Jung M, Dolan M, Smith OS, Tingey S, Morgante M, Rafalski AJ (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 3:19

    Article  PubMed  Google Scholar 

  • Clark RM, Wagler TN, Quijada P, Doebley J (2006) A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat Genet 38:594–597

    Article  PubMed  CAS  Google Scholar 

  • Darvishzadeh R (2012) Phenotypic and molecular marker distance as a tool for prediction of heterosis and F1 performance in sunflower (Helianthus annuus L.) under well-watered and water-stressed conditions. Aust J Crop Sci 6:732–738

    CAS  Google Scholar 

  • Davenport CB (1908) Degeneration, albinism and inbreeding. Science 28:454–455

    Article  PubMed  CAS  Google Scholar 

  • Diers BW, Mac Vetty PBE, Osborn TC (1996) Relationship between heterosis and genetic distance based on restriction fragment length polymorphism markers in oilseed rape (Brassica napus L.). Crop Sci 36:79–83

    Article  Google Scholar 

  • Dubreuil P, Dufour P, Krejci E, Causse M, de Vienne D, Gallais A, Charcosset A (1996) Organization of RFLP diversity among inbred lines of maize representing the most significant heterotic groups. Crop Sci 36:790–799

    Article  Google Scholar 

  • Duvick DN (1999) Heterosis: feeding people and protecting natural resources. In: Coors JG, Pandey S (eds) The genetics and exploitation of heterosis in crops. Crop Science Society of America, Madison, pp 19–30

    Google Scholar 

  • East EM (1908) Inbreeding in corn. Rep Conn Agric Exp Stn 1907:419–429

    Google Scholar 

  • Felsenstein J (1989) PHYLIP—Phylogeny Inference Package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Frascaroli E, Canè MA, Landi P, Pea G, Gianfranceschi L, Villa M, Morgante M, Pè ME (2007) Classical genetic and quantitative trait loci analyses of heterosis in a maize hybrid between two elite inbred lines. Genetics 176:625–644

    Article  PubMed  CAS  Google Scholar 

  • Giordani T, Natali L, D’Ercole A, Pugliesi C, Fambrini M, Vernieri P, Vitagliano C, Cavallini A (1999) Expression of a dehydrin gene during embryo development and drought stress in ABA-deficient mutants of sunflower (Helianthus annuus L.). Plant Mol Biol 39:739–748

    Article  PubMed  CAS  Google Scholar 

  • Giordani T, Buti M, Natali L, Pugliesi C, Cattonaro F, Morgante M, Cavallini A (2010) An analysis of sequence variability in eight genes putatively involved in drought response in sunflower (Helianthus annuus L.). Theor Appl Genet 122:1039–1049

    Article  PubMed  Google Scholar 

  • Godshalk EB, Lee M, Lamkey KR (1990) Relationship of restriction fragment length polymorphisms to single-cross hybrid performance in maize. Theor Appl Genet 80:273–280

    Article  CAS  Google Scholar 

  • Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS (2004) Allelic variation of gene expression in maize hybrids. Plant Cell 16:1707–1716

    Article  PubMed  CAS  Google Scholar 

  • Guo M, Rupe MA, Yang X, Crasta O, Zinselmeier C, Smith OS, Bowen B (2006) Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theor Appl Genet 113:831–845

    Article  PubMed  CAS  Google Scholar 

  • Hongtrakul V, Huestis GM, Knapp SJ (1997) Amplified fragment length polymorphisms as a tool for DNA fingerprinting sunflower germplasm: genetic diversity among oilseed inbred lines. Theor Appl Genet 95:400–407

    Article  CAS  Google Scholar 

  • Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bull Soc Vaud Sci Nat 44:223–270

    Google Scholar 

  • Janick J (1998) Hybrids in horticultural crops. In: Lamkey KR, Staub JE (eds) Concepts and breeding of heterosis in crop plants. Crop Science Society of America, Madison, pp 45–56

    Google Scholar 

  • Jones DF (1917) Dominance of linked factors as a means of accounting for heterosis. Genetics 2:466–479

    PubMed  CAS  Google Scholar 

  • Kalendar R, Grob T, Regina M, Suoniemi A, Schulman A (1999) IRAP and REMAP: two new retrotransposon-based DNA fingerprinting techniques. Theor Appl Genet 98:704–711

    Article  CAS  Google Scholar 

  • Kaya Y (2005) Hybrid vigor in sunflower (Helianthus annuus L.). Helia 28:77–86

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982

    Article  PubMed  Google Scholar 

  • Krystkowiak K, Adamski T, Surma M, Kaczmarek Z (2009) Relationship between phenotypic and genetic diversity of parental genotypes and the specific combining ability and heterosis effects in wheat (Triticum aestivum L.). Euphytica 165:419–434

    Article  Google Scholar 

  • Lai J, Li R, Xu X, Jin W, Xu M, Zhao H et al (2010) Genome-wide patterns of genetic variation among elite maize inbred lines. Nature Genet 42:1027–1030

    Article  PubMed  CAS  Google Scholar 

  • Martin JM, Talbort LE, Lanning SP, Blake NK (1995) Hybrid performance in wheat as related to parental diversity. Crop Sci 35:104–108

    Article  Google Scholar 

  • Melchinger AE (1999) Genetic diversity and heterosis. In: Coors JG, Pandey S (eds) The genetics and exploitation of heterosis in crops. Crop Science Society of America, Madison, pp 99–118

    Google Scholar 

  • Melchinger AE, Gumber RK (1998) Overview of heterosis and heterotic groups in agronomic crops. In: Lamkey KR, Staub JE (eds) Concepts and breeding of heterosis in crop plants. Crop Science Society of America, Madison, pp 29–44

    Google Scholar 

  • Melchinger AE, Lee M, Lamkey KR, Woodman WW (1990) Genetic diversity for restriction fragment length polymorphisms: relation to genetic effects in maize inbreds. Crop Sci 30:1033–1040

    Article  CAS  Google Scholar 

  • Melchinger AE, Utz HF, Piepho HP, Zeng ZB, Schön CC (2007) The role of epistasis in the manifestation of heterosis: a systems-oriented approach. Genetics 177:1815–1825

    Article  PubMed  CAS  Google Scholar 

  • Messing J, Dooner HK (2006) Organization and variability of the maize genome. Curr Opin Plant Biol 9:157–163

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Scalabrin S, Morgante M (2004) Mapping and sequencing complex genomes: let’s get physical. Nat Rev Genet 5:578–588

    Article  PubMed  CAS  Google Scholar 

  • Miller JF (1992) Registration of five oilseed sunflower germplasm restorer lines (RHA 373 to 377) and two nuclear male sterile populations (NMS 274 and 801). Crop Sci 32:1298

    Article  Google Scholar 

  • Moll RH, Salhuana WS, Robinson HF (1962) Heterosis and genetic diversity in variety crosses of maize. Crop Sci 2:197–198

    Article  Google Scholar 

  • Morgante M, De Paoli E, Radovic S (2007) Transposable elements and the plant pan-genomes. Curr Opin Plant Biol 10:149–155

    Article  PubMed  CAS  Google Scholar 

  • Moser H, Lee M (1994) RFLP variation and genealogical distance, multivariate distance, heterosis, and genetic variance in oats. Theor Appl Genet 87:947–956

    Article  CAS  Google Scholar 

  • Natali L, Giordani T, Cavallini A (2003) Sequence variability of a dehydrin gene within Helianthus annuus. Theor Appl Genet 106:811–818

    PubMed  CAS  Google Scholar 

  • Natali L, Santini S, Giordani T, Minelli S, Maestrini P, Cionini PG, Cavallini A (2006) Distribution of Ty3-gypsy- and Ty1-copia-like DNA sequences in the genus Helianthus and other Asteraceae. Genome 49:64–72

    Article  PubMed  CAS  Google Scholar 

  • Ouvrard O, Cellier F, Ferrare K, Tousch D, Lamaze T, Dupuis J-M, Casse-Delbart F (1996) Identification and expression of water stress- and abscisic acid-regulated genes in a drought-tolerant sunflower genotype. Plant Mol Biol 31:819–829

    Article  PubMed  CAS  Google Scholar 

  • Paschold A, Jia Y, Marcon C, Lund S, Larson NB, Yeh CT, Ossowski S, Lanz C, Nettleton D, Schnable PS, Hochholdinger F (2012) Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents. Genome Res 22(12):2445–2454. doi:10.1101/gr.138461.112

    Article  PubMed  CAS  Google Scholar 

  • Rohlf FJ (2008) NTSYSpc: numerical taxonomy system, ver. 2.00. Exeter Publishing Ltd., Setauket

  • Rychlik W, Rhoads RE (1989) A computer program for choosing optimal oligonucleotides for filter hybridization, sequencing and in vitro amplification of DNA. Nucl Acids Res 17:8543–8551

    Article  PubMed  CAS  Google Scholar 

  • Sheng JX, Lu GY, Fu TD, Yang GS (2002) Relationships between genetic diversity and hybrid performance in oilseed rape (Brassica napus). Acta Agron Sin 28:622–627

    Google Scholar 

  • Shull GH (1908) The composition of a field of maize. Am Breed Assoc Rep 4:296–301

    Google Scholar 

  • Sokal RR, Michener CD (1958) A statistical method for evaluating systematic relationships. Univ Kans Sci Bull 38:1409–1438

    Google Scholar 

  • Springer NM, Stupar RM (2007) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res 17:264–275

    Article  PubMed  CAS  Google Scholar 

  • Springer NM, Ying K, Fu Y, Ji T, Yeh CT, Jia Y, Wu W, Richmond T et al (2009) Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet 5:e1000734

    Article  PubMed  Google Scholar 

  • Stam M, Belele C, Dorweiler JE, Chandler VL (2002) Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev 16:1906–1918

    Article  PubMed  CAS  Google Scholar 

  • Staton SE, Bakken BH, Blackman BK, Chapman MA, Kane NC, Tang S, Ungerer MC, Knapp SJ, Rieseberg LH, Burke JM (2012) The sunflower (Helianthus annuus L.) genome reflects a recent history of biased accumulation of transposable elements. Plant J 72:142–153

    Article  PubMed  CAS  Google Scholar 

  • Stupar RM, Springer NM (2006) Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics 173:2199–2210

    Article  PubMed  CAS  Google Scholar 

  • Tersac M, Blanchard P, Brunel D, Vancourt P (1994) Relations between heterosis and enzymatic polymorphisms in populations of cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 88:49–55

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Vukich M, Schulman AH, Giordani T, Natali L, Kalendar R, Cavallini A (2009a) Genetic variability in sunflower (Helianthus annuus L.) and in the Helianthus genus as assessed by retrotransposon-based molecular markers. Theor Appl Genet 119:1027–1038

    Article  PubMed  CAS  Google Scholar 

  • Vukich M, Giordani T, Natali L, Cavallini A (2009b) Copia and Gypsy retrotransposons activity in sunflower (Helianthus annuus L.). BMC Plant Biol 9:150

    Article  PubMed  Google Scholar 

  • Zanoni U, Dudley JW (1989) Comparison of different methods of identifying inbreds useful for improving elite maize hybrids. Crop Sci 29:577–582

    Article  Google Scholar 

  • Zhang Q, Gao YJ, Saghai Maroof MA, Yang SH, Li JX (1995) Molecular divergence and hybrid performance in rice. Mol Breed 1:133–142

    Article  Google Scholar 

  • Zhang G, Angeles ER, Abenes MLP, Khush GS, Huang N (1996) RAPD and RFLP mapping for the bacterial blight resistance gene xa-13 in rice. Theor Appl Genet 93:65–70

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Thanks are due to Dr. Elisabetta Frascaroli (University of Bologna) for her useful suggestions during the investigation and to Dr. Andrea Cini (Kayser Italia) for revising the manuscript. This work was supported by PRIN-MIUR, Projects “Variabilità di sequenza ed eterosi in piante coltivate” and “SUNREP: caratterizzazione molecolare della componente ripetitiva del genoma di girasole”.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Cavallini.

Additional information

M. Buti and T. Giordani contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 74 kb)

Supplementary material 2 (PDF 49 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buti, M., Giordani, T., Vukich, M. et al. Retrotransposon-related genetic distance and hybrid performance in sunflower (Helianthus annuus L.). Euphytica 192, 289–303 (2013). https://doi.org/10.1007/s10681-013-0883-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10681-013-0883-5

Keywords

Navigation