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Allelic variation in genes contributing to glycoalkaloid biosynthesis in a diploid interspecific population of potato

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Variation for allelic state within genes of both primary and secondary metabolism influences the quantity and quality of steroidal glycoalkaloids produced in potato leaves.

Abstract

Genetic factors associated with the biosynthesis and accumulation of steroidal glycoalkaloids (SGAs) in potato were addressed by a candidate gene approach and whole genome single nucleotide polymorphism (SNP) genotyping. Allelic sequences spanning coding regions of four candidate genes [3-hydroxy-3-methylglutaryl coenzyme A reductase 2 (HMG2); 2,3-squalene epoxidase; solanidine galactosyltransferase; and solanidine glucosyltransferase (SGT2)] were obtained from two potato species differing in SGA composition: Solanum chacoense (chc 80-1) and Solanum tuberosum group Phureja (phu DH). An F2 population was genotyped and foliar SGAs quantified. The concentrations of α-solanine, α-chaconine, leptine I, leptine II and total SGAs varied broadly among F2 individuals. F2 plants with chc 80-1 alleles for HMG2 or SGT2 accumulated significantly greater leptines and total SGAs compared to plants with phu DH alleles. Plants with chc 80-1 alleles at both loci expressed the greatest levels of total SGAs, α-solanine and α-chaconine. A significant positive correlation was found between α-solanine and α-chaconine accumulation as well as between leptine I and leptine II. A whole genome SNP genotyping analysis of an F2 subsample verified the importance of chc 80-1 alleles at HMG2 and SGT2 for SGA synthesis and accumulation and suggested additional candidate genes including some previously associated with SGA production. Loci on five and seven potato pseudochromosomes were associated with synthesis and accumulation of SGAs, respectively. Two loci, on pseudochromosomes 1 and 6, explained phenotypic segregation of α-solanine and α-chaconine synthesis. Knowledge of the genetic factors influencing SGA production in potato may assist breeding for pest resistance.

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References

  • Arnqvist L (2007) Plant sterol metabolism with emphasis on glycoalkaloid biosynthesis in potato. Dept of plant biology and forest genetics. Swedish University of Agricultural Sciences, Uppsala, p 50

    Google Scholar 

  • Benveniste P (2004) Biosynthesis and accumulation of sterols. Annu Rev Plant Biol 55:429–457

    Article  CAS  PubMed  Google Scholar 

  • Boluarte-Medina T, Fogelman E, Chani E, Miller AR, Levin I, Levy D, Veilleux RE (2002) Identification of molecular markers associated with leptine in reciprocal backcross families of diploid potato. Theor Appl Genet 105:1010–1018

    Article  Google Scholar 

  • Choi D, Ward BL, Bostock RM (1992) Differential induction and suppression of potato 3-hydroxy-3-methylglutaryl coenzyme A reductase genes in response to Phytophthora infestans and to its elicitor arachidonic acid. Plant Cell 4:1333–1344

    CAS  PubMed Central  PubMed  Google Scholar 

  • Choi D, Bostock RM, Avdiushko S, Hildebrand DF (1994) Lipid-derived signals that discriminate wound- and pathogen-responsive isoprenoid pathways in plants: methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes and antimicrobial isoprenoids in Solanum tuberosum L. Proc Nat Acad Sci USA 91:2329–2333

    Article  CAS  PubMed  Google Scholar 

  • Distl M, Wink M (2009) Identification and quantification of steroidal alkaloids from wild tuber-bearing Solanum species by HPLC and LC-ESI-MS. Potato Res 52:79–104

    Article  CAS  Google Scholar 

  • Edwards EJ, Cobb AH (1996) Improved high performance liquid chromatographic method for the analysis of potato (Solanum tuberosum) glycoalkaloids. J Agr Food Chem 44:2705–2709

    Article  CAS  Google Scholar 

  • FAO (2008) Potato pest and disease management. International year of the Potato 2008. http://www.potato2008.org/en/potato/pests.html

  • Felcher KJ, Coombs JJ, Massa AN, Hansey CN, Hamilton JP, Veilleux RE, Buell CR, Douches DS (2012) Integration of two diploid potato linkage maps with the potato genome sequence. PLoS ONE 7:e36347

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Friedman M (2006) Potato glycoalkaloids and metabolites: roles in the plant and in the diet. J Agr Food Chem 54:8655–8681

    Article  CAS  Google Scholar 

  • Friedman M, Dao L (1992) Distribution of glycoalkaloids in potato plants and commercial potato products. J Agr Food Chem 40:419–423

    Article  CAS  Google Scholar 

  • Friedman M, McDonald GM (1997) Potato glycoalkaloids: chemistry, analysis, safety, and plant physiology. Crit Rev Plant 16:55–132

    CAS  Google Scholar 

  • Ginzberg I, Tokuhisa JG, Veilleux RE (2009) Potato steroidal glycoalkaloids: biosynthesis and genetic manipulation. Potato Res 52:1–15

    Article  CAS  Google Scholar 

  • Ginzberg I, Thippeswamy M, Fogelman E, Demirel U, Mweetwa A, Tokuhisa J, Veilleux R (2012) Induction of potato steroidal glycoalkaloid biosynthetic pathway by overexpression of cDNA encoding primary metabolism HMG-CoA reductase and squalene synthase. Planta 235:1341–1353

    Google Scholar 

  • Hamilton JP, Hansey CN, Whitty BR, Stoffel K, Massa AN, Van Deynze A, De Jong WS, Douches DS, Buell CR (2011) Single nucleotide polymorphism discovery in elite North American potato germplasm. BMC Genomics 12:302

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Haynes FL (1972) The use of cultivated diploid Solanum species in potato breeding. In: Prospects for the potato in the developing world. International Potato Center (CIP), Lima, Peru

  • Heftmann E (1983) Biogenesis of steroids in Solanaceae. Phytochemistry 22:1843–1860

    Article  CAS  Google Scholar 

  • Hutvágner G, Bánfalvi Z, Milánkovics I, Silhavy D, Polgár Z, Horváth S, Wolters P, Nap JP (2001) Molecular markers associated with leptinine production are located on chromosome 1 in Solanum chacoense. Theor Appl Genet 102:1065–1071

    Article  Google Scholar 

  • Itkin M, Heinig U, Tzfadia O, Bhide AJ, Shinde B, Cardenas PD, Bocobza SE, Unger T, Malitsky S, Finkers R, Tikunov Y, Bovy A, Chikate Y, Singh P, Rogachev I, Beekwilder J, Giri AP, Aharoni A (2013) Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science 341:175–179

    Article  CAS  PubMed  Google Scholar 

  • Johnson AAT, Piovano SM, Ravichandran V, Veilleux RE (2001) Selection of monoploids for protoplast fusion and generation of intermonoploid somatic hybrids of potato. Am J Potato Res 78:19–29

    Article  CAS  Google Scholar 

  • Judo MS, Wedel AB, Wilson C (1998) Stimulation and suppression of PCR-mediated recombination. Nucleic Acids Res 26:1819–1825

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaneko K, Tanaka MW, Mitsuhashi H (1976) Origin of nitrogen in the biosynthesis of solanidine by Veratrum grandiflorum. Phytochemistry 15:1391–1393

    Article  CAS  Google Scholar 

  • Kaneko K, Tanaka MW, Mitsuhashi H (1977) Dormantinol, a possible precursor in solanidine biosynthesis, from budding Veratrum grandiflorum. Phytochemistry 16:1247–1251

    Article  CAS  Google Scholar 

  • Kolbe H, Stephan-Beckmann S (1997) Development, growth and chemical composition of the potato crop (Solanum tuberosum L.). II. Tuber and whole plant. Potato Res 40:135–153

    Article  CAS  Google Scholar 

  • Krits P, Fogelman E, Ginzberg I (2007) Potato steroidal glycoalkaloid levels and the expression of key isoprenoid metabolic genes. Planta 227:143–150

    Article  CAS  PubMed  Google Scholar 

  • Laurila J, Laakso I, Valkonen JPT, Hiltunen R, Pehu E (1996) Formation of parental-type and novel glycoalkaloids in somatic hybrids between Solanum brevidens and S. tuberosum. Plant Sci 118:145–155

    Article  CAS  Google Scholar 

  • Lenz TL, Becker S (2008) Simple approach to reduce PCR artefact formation leads to reliable genotyping of MHC and other highly polymorphic loci–implications for evolutionary analysis. Gene 427:117–123

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lightbourn GJ, Veilleux RE (2007) Production and evaluation of somatic hybrids derived from monoploid potato. Am J Potato Res 84:425–435

    Article  Google Scholar 

  • Liu YG, Chen Y (2007) High-efficiency thermal asymmetric interlaced PCR for amplification of unknown flanking sequences. Biotechniques 43:649–656

    Article  CAS  PubMed  Google Scholar 

  • Manrique-Carpintero NC, Tokuhisa JG, Ginzberg I, Holliday JA, Veilleux RE (2013) Sequence diversity in coding regions of candidate genes in the glycoalkaloid biosynthetic pathway of wild potato species. G3:g3.113.007146 Early Online

  • McCue KF, Shepherd LVT, Allen PV, Maccree MM, Rockhold DR, Corsini DL, Davies HV, Belknap WR (2005) Metabolic compensation of steroidal glycoalkaloid biosynthesis in transgenic potato tubers: using reverse genetics to confirm the in vivo enzyme function of a steroidal alkaloid galactosyltransferase. Plant Sci 168:267–273

    Article  CAS  Google Scholar 

  • McCue KF, Allen PV, Shepherd LV, Blake A, Maccree MM, Rockhold DR, Novy RG, Stewart D, Davies HV, Belknap WR (2007a) Potato glycosterol rhamnosyltransferase, the terminal step in triose side-chain biosynthesis. Phytochemistry 68:327–334

    Article  CAS  PubMed  Google Scholar 

  • McCue KF, Allen PV, Shepherd LVT, Blake A, Rockhold DR, Novy RG, Stewart D, Davies HV, Belknap WR (2007b) Manipulation and compensation of steroidal glycoalkaloid biosynthesis in potatoes. Acta Hort 745:343–349

    CAS  Google Scholar 

  • Moehs CP, Allen PV, Friedman M, Belknap WR (1997) Cloning and expression of solanidine UDP-glucose glucosyltransferase from potato. Plant J 11:227–236

    Article  CAS  PubMed  Google Scholar 

  • Morris SC, Lee TH (1984) The toxicity and teratogenicity of Solanaceae glycoalkaloids, particularly those of the potato (Solanum tuberosum): a review. Food Technol Aust 36:118–124

    CAS  Google Scholar 

  • Mweetwa MA (2009) Biosynthesis of steroidal glycoalkaloids in Solanum chacoense Bitter. Virginia Polytechnic Institute and State University, Blacksburg, p 118

    Google Scholar 

  • Mweetwa AM, Hunter D, Poe R, Harich KC, Ginzberg I, Veilleux RE, Tokuhisa JG (2012) Steroidal glycoalkaloids in Solanum chacoense. Phytochemistry 75:32–40

    Article  CAS  PubMed  Google Scholar 

  • Nahar N (2011) Regulation of sterol and glycoalkaloid biosynthesis in potato (Solanum tuberosum L.)—Identification of key genes and enzymatic steps. Department of plant biology and forest genetics. Swedish University of Agricultural Sciences, Uppsala, p 66

    Google Scholar 

  • Nema PK, Ramayya N, Duncan E, Niranjan K (2008) Potato glycoalkaloids: formation and strategies for mitigation. J Sci Food Agr 88:1869–1881

    Article  CAS  Google Scholar 

  • Osbourn A (2010) Gene clusters for secondary metabolic pathways: an emerging theme in plant biology. Plant Physiol 154:531–535

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pichersky E, Gang DR (2000) Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective. Trends Plant Sci 5:439–445

    Article  CAS  PubMed  Google Scholar 

  • Ramkumar G, Sivaranjani AKP, Pandey MK, Sakthivel K, Rani NS, Sudarshan I, Prasad GSV, Neeraja CN, Sundaram RM, Viraktamath BC, Madhav MS (2010) Development of a PCR-based SNP marker system for effective selection of kernel length and kernel elongation in rice. Mol Breeding 26:735–740

    Article  Google Scholar 

  • Ronning CM, Stommel JR, Kowalski SP, Sanford LL, Kobayashi RS, Pineada O (1999) Identification of molecular markers associated with leptine production in a population of Solanum chacoense bitter. Theor Appl Genet 98:39–46

    Article  CAS  Google Scholar 

  • Sagredo B, Lafta A, Casper H, Lorenzen J (2006) Mapping of genes associated with leptine content of tetraploid potato. Theor Appl Genet 114:131–142

    Article  CAS  PubMed  Google Scholar 

  • Sagredo B, Lorenzen J, Casper H, Lafta A (2011) Linkage analysis of a rare alkaloid present in a tetraploid potato with Solanum chacoense background. Theor Appl Genet 122:471–478

    Article  CAS  PubMed  Google Scholar 

  • Sanford L, Kobayashi R, Deahl K, Sinden S (1996) Segregation of leptines and other glycoalkaloids in Solanum tuberosum (4x) × Solanum chacoense (4x) crosses. Am J Potato Res 73:21–33

    Article  CAS  Google Scholar 

  • Schaller H (2004) New aspects of sterol biosynthesis in growth and development of higher plants. Plant Physiol Biochem 42:465–476

    Article  CAS  PubMed  Google Scholar 

  • Sinden SL, Sanford LL, Osman SF (1980) Glycoalkaloids and resistance to the Colorado potato beetle in Solanum chacoense Bitter. Am Potato J 57:331–343

    Article  CAS  Google Scholar 

  • Sinden SL, Sanford LL, Cantelo WW, Deahl KL (1986) Leptine glycoalkaloids and resistance to the Colorado potato beetle (Coleoptera: Chrysomelidae) in Solanum chacoense. Environ Entomol 15:1057–1062

    CAS  Google Scholar 

  • Sørensen K, Kirk H, Olsson K, Labouriau R, Christiansen J (2008) A major QTL and an SSR marker associated with glycoalkaloid content in potato tubers from Solanum tuberosum × S. sparsipilum located on chromosome I. Theor Appl Genet 117:1–9

    Article  PubMed  Google Scholar 

  • Strickberger MW (1968) Genetics. Macmillan, New York

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195

    Article  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thompson JR, Marcelino LA, Polz MF (2002) Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by ‘reconditioning PCR’. Nucleic Acids Res 30:2083–2088

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Todd AE, Orengo CA, Thornton JM (1999) Evolution of protein function, from a structural perspective. Curr Opin Chem Biol 3:548–556

    Article  CAS  PubMed  Google Scholar 

  • Väänänen T, Ikonen T, Rokka VM, Kuronen P, Serimaa R, Ollilainen V (2005) Influence of incorporated wild Solanum genomes on potato properties in terms of starch nanostructure and glycoalkaloid content. J Agr Food Chem 53:5313–5325

    Article  Google Scholar 

  • Valkonen JPT, Keskitalo M, Vasara T, Pietilä L (1996) Potato glycoalkaloids: a burden or a blessing? Crit Rev Plant 15:1–20

    CAS  Google Scholar 

  • Van Dam J, Levin I, Struik PC, Levy D (1999) Genetic characterisation of tetraploid potato (Solanum tuberosum L.) emphasising genetic control of total glycoalkaloid content in the tubers. Euphytica 110:67–76

    Article  Google Scholar 

  • Van Dam J, Levin I, Struik PC, Levy D (2003) Identification of epistatic interaction affecting glycoalkaloid content in tubers of tetraploid potato (Solanum tuberosum L.). Euphytica 134:353–360

    Article  Google Scholar 

  • Veilleux RE (1990) Solanum phureja: anther culture and the induction of haploids in a cultivated diploid potato species. Bajaj YPS edn. Springer-Verlag, New York

  • Waxman D, Peck JR (1998) Pleiotropy and the preservation of perfection. Science 279:1210–1213

    Article  CAS  Google Scholar 

  • Wentzinger LF, Bach TJ, Hartmann MA (2002) Inhibition of squalene synthase and squalene epoxidase in tobacco cells triggers an up-regulation of 3-hydroxy-3-methylglutaryl coenzyme a reductase. Plant Physiol 130:334–346

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yencho GC, Kowalski SP, Kobayashi RS, Sinden SL, Bonierbale MW, Deahl KL (1998) QTL mapping of foliar glycoalkaloid aglycones in Solanum tuberosum x S. berthaultii potato progenies: quantitative variation and plant secondary metabolism. Theor Appl Genet 97:563–574

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by Research Grant No. IS-4134-08 R from BARD, The United States—Israel Binational Agricultural Research and Development Fund. We thank Suzanne Piovano for technical assistance, Maichel Miguel Aguayo Bustos for programming help, Anne Ryan of the Laboratory for Interdisciplinary Statistical Analysis LISA for statistical consultation.

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Correspondence to Richard E. Veilleux.

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Communicated by G. Bryan.

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Manrique-Carpintero, N.C., Tokuhisa, J.G., Ginzberg, I. et al. Allelic variation in genes contributing to glycoalkaloid biosynthesis in a diploid interspecific population of potato. Theor Appl Genet 127, 391–405 (2014). https://doi.org/10.1007/s00122-013-2226-2

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