Skip to main content
SpringerLink
Log in

Genetic mapping of sulfur assimilation genes reveals a QTL for onion bulb pungency

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Onion exhibits wide genetic and environmental variation in bioactive organosulfur compounds that impart pungency and health benefits. A PCR-based molecular marker map that included candidate genes for sulfur assimilation was used to identify genomic regions affecting pungency in the cross 'W202A' × 'Texas Grano 438'. Linkage mapping revealed that genes encoding plastidic ferredoxin-sulfite reductase (SiR) and plastidic ATP sulfurylase (ATPS) are closely linked (1–2 cM) on chromosome 3. Inbred F3 families derived from the F2 population used to construct the genetic map were grown in replicated trials in two environments and bulb pungency was evaluated as pyruvic acid or lachrymatory factor. Broad-sense heritability of pungency was estimated to be 0.78–0.80. QTL analysis revealed significant associations of both pungency and bulb soluble solids content with marker intervals on chromosomes 3 and 5, which have previously been reported to condition pleiotropic effects on bulb carbohydrate composition. Highly significant associations (LOD 3.7–8.7) were observed between ATPS and SiR Loci and bulb pungency but not with bulb solids content. This association was confirmed in two larger, independently derived F2 families from the same cross. Single-locus models suggested that the partially dominant locus associated with these candidate genes controls 30–50% of genetic variation in pungency in these pedigrees. These markers may provide a practical means to select for lower pungency without correlated selection for lowered solids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

EPA:

Enzymatically produced pyruvic acid

SSC:

Soluble solids content

SSCP:

Single-stranded conformation polymorphism

HDX:

Heteroduplex

LF:

Onion lachrymatory factor

CAPS:

Cleaved amplified polymorphic sequence

ACSO:

Alk(en)yl cysteine sulfoxide

References

  • Ali M, Bordia T, Mustafa T (1999) Effect of raw versus boiled aqueous extract of garlic and onion on platelet aggregation. Prostaglandins Leukot Essent Fatty Acids 60:43–47

    Article  PubMed  CAS  Google Scholar 

  • Block E (1992) The organosulfur chemistry of the genus Allium—implications for the organic chemistry of sulfur. Agnew Chem Int Ed Engl 31:1135–1178

    Article  Google Scholar 

  • Crowther T, Collin HA, Smith B, Tomsett AB, O’Connor D, Jones MG (2005) Assessment of the flavour of fresh uncooked onions by taste-panels and analysis of flavour precursors, pyruvate and sugars. J Sci Food Agric 85:112–120

    Article  CAS  Google Scholar 

  • Freeman GG, Mossadeghi N (1970) Effect of sulphate nutrition on flavour components of onion (Allium cepa). J Sci Food Agric 21:610–615

    Article  CAS  Google Scholar 

  • Galmarini CR, Goldman IL, Havey MJ (2001) Genetic analyses of correlated solids, flavor, and health-enhancing traits in onion (Allium cepa L.). Mol Genet Genomics 265:543–551

    Article  PubMed  CAS  Google Scholar 

  • Griffiths G, Trueman L, Crowther T, Thomas B, Smith B (2002) Onions-a global benefit to health. Phytother Res 16:603–615

    Article  PubMed  CAS  Google Scholar 

  • Imai S, Tsuge N, Tomotake M, Nagatome Y, Sawada H, Nagata T, Kumagai H (2002) Plant biochemistry: an onion enzyme that makes the eyes water. Nature 419:685

    Article  PubMed  CAS  Google Scholar 

  • Kuhl JC, Cheung F, Yuan Q, Martin W, Zewdie Y, McCallum J, Catanach A, Rutherford P, Sink KC, Jenderek M, Prince JP, Town CD, Havey MJ (2004) A unique set of 11,008 onion expressed sequence tags reveals expressed sequence and genomic differences between the monocot orders Asparagales and Poales. Plant Cell 16:114–125

    Article  PubMed  Google Scholar 

  • Kyung KH, Lee YC (2001) Antimicrobial activities of sulfur compounds derived from S-alk(en)yl-L-cysteine sulfoxides in Allium and Brassica. Food Rev Int 17:183–198

    Article  CAS  Google Scholar 

  • Leustek T, Martin MN, Bick JA, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol 51:141–165

    Article  PubMed  CAS  Google Scholar 

  • Lin M, Watson JF, Baggett JR (1995) Inheritance of soluble solids and pyruvic acid content of bulb onions. J Am Soc Hortic Sci 120:119–122

    CAS  Google Scholar 

  • Martin W, McCallum J, Shigyo M, Jakse J, Kuhl J, Yamane N, Pither-Joyce M, Gokce A, Sink K, Town C, Havey M (2005) Genetic mapping of expressed sequences in onion and in silico comparisons with rice show scant colinearity. Mol Genet Genomics 274:197–204

    Article  PubMed  CAS  Google Scholar 

  • McCallum JA, Grant DG, McCartney EP, Scheffer J, Shaw ML, Butler RC (2001a) Genotypic and environmental variation in bulb composition of New Zealand adapted onion (Allium cepa) germplasm. N Z J Crop Hortic Sci 29:149–158

    Google Scholar 

  • McCallum JA, Leite D, Pither-Joyce MD, Havey MJ (2001b) Expressed sequence markers for genetic analysis of bulb onion (Allium cepa. L.). Theor Appl Genet 103:979–991

    Article  CAS  Google Scholar 

  • McCallum JA, Pither-Joyce MD, Shaw ML (2002) Sulfur deprivation and genotype affect gene expression and metabolism of onion roots. J Am Soc Hortic Sci 127:583–589

    CAS  Google Scholar 

  • McCallum J, Porter N, Searle B, Shaw M, Bettjeman B, McManus M (2005) Sulfur and nitrogen fertility affects flavour of field-grown onions. Plant Soil 274:151–158

    Article  CAS  Google Scholar 

  • McCallum J, Clarke A, Pither-Joyce M, Shaw M, Butler R, Brash D, Scheffer J, Sims I, van Heusden S, Shigyo M, Havey M (2006) Genetic mapping of a major gene affecting onion bulb fructan content. Theor Appl Genet 112:958–967

    Article  PubMed  CAS  Google Scholar 

  • McManus MT, Leung S, Lambert A, Scott RW, Pither-Joyce M, Chen B, McCallum J (2005) Molecular and biochemical characterisation of a serine acetyltransferase of onion, Allium cepa (L.). Phytochemistry 66:1407–1416

    Article  PubMed  CAS  Google Scholar 

  • Payne RW, Baird DB, Cherry M, Gilmour AR, Harding SA, Kane AF, Lane PW, Murray DA, Soutar DM, Thompson R, Todd AD, Tunnicliffe Wilson G, Webster R, Welham SJ (2005) GenStat 8.2. Lawes Agricultural Trust

  • Randle WM (1992) Onion germplasm interacts with sulfur fertility for plant sulfur utilization and bulb pungency. Euphytica 59:151–156

    Article  CAS  Google Scholar 

  • Randle WM (2000) Increasing nitrogen concentration in hydroponic solutions affects onion flavor and bulb quality. J Am Soc Hortic Sci 125:254–259

    CAS  Google Scholar 

  • Randle WM, Lancaster JE (2002) Sulphur compounds in Alliums in relation to flavour quality. In: Rabinowitch H, Currah L (eds) Allium crop science—Recent advances. CABI Publishing, Oxford, pp 1–62

    Google Scholar 

  • Randle WM, Kopsell DE, Kopsell DA, Snyder RL (1999) Total sulfur and sulfate accumulation in onion is affected by sulfur fertility. J Plant Nutr 22:45–51

    Article  CAS  Google Scholar 

  • Rendu F, Brohard-Bohn B, Pain S, Bachelot-Loza C, Auger J (2001) Thiosulfinates inhibit platelet aggregation and microparticle shedding at a calpain-dependent step. Thromb Haemost 86:1284–1291

    PubMed  CAS  Google Scholar 

  • Ricroch A, Yockteng R, Brown SC, Nadot S (2005) Evolution of genome size across some cultivated Allium species. Genome 48:511–520

    Article  PubMed  CAS  Google Scholar 

  • Rose P, Whiteman M, Moore PK, Zhu YZ (2005) Bioactive S-alk(en)yl cysteine sulfoxide metabolites in the genus Allium: the chemistry of potential therapeutic agents. Nat Prod Rep 22:351–368

    Article  PubMed  CAS  Google Scholar 

  • Schmidt NE, Santiago LM, Eason HD, Dafford KA, Grooms CA, Link TE, Manning DT, Cooper SD, Keith RC, Chance WO, Walla MD, Cotham WE (1996) Rapid extraction method of quantitating the lachrymatory factor of onion using gas chromatography. J Agric Food Chem 44:2690–2693

    Article  CAS  Google Scholar 

  • Schwimmer S, Guadagni D (1962) Relation between olefactory threshold concentration and pyruvic acid content of onion juice. J Food Sci 27:94–97

    Article  CAS  Google Scholar 

  • Schwimmer S, Weston WJ (1961) Enzymatic development of pyruvic acid in onion as a measure of pungency. J Agric Food Chem 9:301–304

    Article  Google Scholar 

  • Simon PW (1995) Genetic analysis of pungency and soluble solids in long-storage onions. Euphytica 82:1–8

    Article  CAS  Google Scholar 

  • Sinclair PJ, Blakeney AB, Barlow EWR (1995) Relationships between bulb dry matter content, soluble solids concentration and non-structural carbohydrate composition in the onion (Allium cepa). J Sci Food Agric 69:203–209

    Article  CAS  Google Scholar 

  • Wall MM, Mohammad A, Corgan JN (1996) Heritability estimates and response to selection for the pungency and single center traits in onion. Euphytica 87:133–139

    Article  Google Scholar 

Download references

Acknowledgments

We acknowledge significant contributions of the following: Bodhi Bettjeman, Paul McCartney and Winston Fahey for technical support; David and Judy MacMillan and Enza Zaden NZ Ltd for field trial support. This work was funded by the New Zealand Foundation for Research, Science and Technology.

Author information

Authors and Affiliations

  1. New Zealand Institute for Crop & Food Research Limited, Private Bag 4704, Christchurch, New Zealand

    John McCallum, Meeghan Pither-Joyce, Martin Shaw, Fernand Kenel, Sheree Davis & Ruth Butler

  2. New Zealand Institute for Crop & Food Research Limited, Cronin Rd, RD1, Pukekohe, New Zealand

    John Scheffer

  3. Agricultural Research Service, USDA, Department of Horticulture, University of Wisconsin, 1575 Linden Drive, Madison, WI, 53706, USA

    Jernej Jakse & Michael J. Havey

Authors
  1. John McCallum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Meeghan Pither-Joyce
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin Shaw
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fernand Kenel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sheree Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ruth Butler
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. John Scheffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jernej Jakse
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Michael J. Havey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John McCallum.

Additional information

Communicated by C. F. Quiros.

Rights and permissions

Reprints and permissions

About this article

Cite this article

McCallum, J., Pither-Joyce, M., Shaw, M. et al. Genetic mapping of sulfur assimilation genes reveals a QTL for onion bulb pungency. Theor Appl Genet 114, 815–822 (2007). https://doi.org/10.1007/s00122-006-0479-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-006-0479-8

Keywords

Search

Navigation