Plant Molecular Biology

, Volume 80, Issue 3, pp 299–314 | Cite as

Clusters of genes encoding fructan biosynthesizing enzymes in wheat and barley

  • Bao-Lam Huynh
  • Diane E. Mather
  • Andreas W. Schreiber
  • John Toubia
  • Ute Baumann
  • Zahra Shoaei
  • Nils Stein
  • Ruvini Ariyadasa
  • James C. R. Stangoulis
  • James Edwards
  • Neil Shirley
  • Peter Langridge
  • Delphine Fleury
Article

Abstract

Fructans are soluble carbohydrates with health benefits and possible roles in plant adaptation. Fructan biosynthetic genes were isolated using comparative genomics and physical mapping followed by BAC sequencing in barley. Genes encoding sucrose:sucrose 1-fructosyltransferase (1-SST), fructan:fructan 1-fructosyltransferase (1-FFT) and sucrose:fructan 6-fructosyltransferase (6-SFT) were clustered together with multiple copies of vacuolar invertase genes and a transposable element on two barley BAC. Intron–exon structures of the genes were similar. Phylogenetic analysis of the fructosyltransferases and invertases in the Poaceae showed that the fructan biosynthetic genes may have evolved from vacuolar invertases. Quantitative real-time PCR was performed using leaf RNA extracted from three wheat cultivars grown under different conditions. The 1-SST, 1-FFT and 6-SFT genes had correlated expression patterns in our wheat experiment and in existing barley transcriptome database. Single nucleotide polymorphism (SNP) markers were developed and successfully mapped to a major QTL region affecting wheat grain fructan accumulation in two independent wheat populations. The alleles controlling high- and low- fructan in parental lines were also found to be associated in fructan production in a diverse set of 128 wheat lines. To the authors’ knowledge, this is the first report on the mapping and sequencing of a fructan biosynthetic gene cluster and in particular, the isolation of a novel 1-FFT gene from barley.

Keywords

Cereals Polysaccharides Physical map Quantitative trait locus Invertase 

Notes

Acknowledgments

Research funding from International Science Linkages (CG120174), German Ministry of Education and Research (0314000A) and International Barley Sequencing Consortium is gratefully acknowledged. We thank Prof Robert Henry for providing grain samples from which an international collection of wheat accessions had been grown in a common environment, Dr Michael Francki for kindly providing gene primers and primer sequences, Dr Tim Sutton for organising BAC sequencing, Mr Jim Lewis, Ms Margaret Pallotta, Dr Genet Mekuria, Ms Elise Tucker, Ms Vivienne Le, Ms Marija Knez and Mr Lachlan Palmer for technical assistance, Prof Stanley Miklavcic, Prof Robin Graham, Dr Hugh Wallwork, Dr Bu-Jun Shi, Dr Ryan Whitford and Dr Nicholas Collins for advice. Constructive comments from two anonymous reviewers are also gratefully acknowledged.

Supplementary material

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References

  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  2. Bruno WJ, Socci ND, Halpern AL (2000) Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol Biol Evol 17:189–197PubMedCrossRefGoogle Scholar
  3. Burton RA, Jobling SA, Harvey AJ, Shirley NJ, Mather DE, Bacic A, Fincher GB (2008) The genetics and transcriptional profiles of the cellulose synthase-like HvCslF gene family in barley. Plant Physiol 146:1821–1833PubMedCrossRefGoogle Scholar
  4. Chalmers J, Johnson X, Lidgett A, Spangenberg G (2003) Isolation and characterisation of a sucrose:sucrose 1-fructosyltransferase gene from perennial ryegrass (Lolium perenne). J Plant Physiol 160:1385–1391PubMedCrossRefGoogle Scholar
  5. Chevreux B, Wetter T, Suhai S (1999) Genome sequence assembly using trace signals and additional sequence information. In: Computer science and biology: proceedings of the German conference on bioinformatics (GCB), pp 45–56Google Scholar
  6. Close TJ, Bhat PR, Lonardi S, Wu YH, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao SAM, Varshney RK, Szucs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, DeYoung J, Marshall DF, Madishetty K, Fenton RD, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genom 10:582–595CrossRefGoogle Scholar
  7. Druka A, Muehlbauer G, Druka I, Caldo R, Baumann U, Rostoks N, Schreiber A, Wise R, Close T, Kleinhofs A, Graner A, Schulman A, Langridge P, Sato K, Hayes P, McNicol J, Marshall D, Waugh R (2006) An atlas of gene expression from seed to seed through barley development. Funct Integr Genom 6:202–211CrossRefGoogle Scholar
  8. Edelman J, Jefford TG (1968) The mechanism of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus. New Phytol 67:517–531CrossRefGoogle Scholar
  9. Edwards J (2011) A genetic analysis of drought related traits in hexaploid wheat. PhD thesis, University of AdelaideGoogle Scholar
  10. Feuillet C, Keller B (1999) High gene density is conserved at syntenic loci of small and large grass genomes. Proc Nat Acad Sci 96:8265–8270PubMedCrossRefGoogle Scholar
  11. Francki MG, Walker E, Forster JW, Spangenberg G, Appels R (2006) Fructosyltransferase and invertase genes evolved by gene duplication and rearrangements: rice, perennial ryegrass, and wheat gene families. Genome 49:1081–1091PubMedCrossRefGoogle Scholar
  12. Gibson GR, Probert HM, Van Loo J, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17:259–275PubMedCrossRefGoogle Scholar
  13. Henry RJ, Saini HS (1989) Characterization of cereal sugars and oligosaccharides. Cereal Chem 66:362–365Google Scholar
  14. Hohmann U, Graner A, Endo TR, Gill BS, Herrmann RG (1995) Comparison of wheat physical maps with barley linkage maps for group 7 chromosomes. Theor Appl Genet 91:618–626Google Scholar
  15. Hossain KG, Kalavacharla V, Lazo GR, Hegstad J, Wentz MJ, Kianian PMA, Simons K, Gehlhar S, Rust JL, Syamala RR, Obeori K, Bhamidimarri S, Karunadharma P, Chao S, Anderson OD, Qi LL, Echalier B, Gill BS, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Akhunov ED, Dvorak J, Miftahudin M, Ross K, Gustafson JP, Radhawa HS, Dilbirligi M, Gill KS, Peng JH, Lapitan NLV, Greene RA, Bermudez-Kandianis CE, Sorrells ME, Feril O, Pathan MS, Nguyen HT, Gonzalez-Hernandez JL, Conley EJ, Anderson JA, Choi DW, Fenton D, Close TJ, McGuire PE, Qualset CO, Kianian SF (2004) A chromosome bin map of 2148 expressed sequence tag loci of wheat homoeologous group 7. Genetics 168:687–699PubMedCrossRefGoogle Scholar
  16. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinf:1–5. http://www.hindawi.com/journals/abi/2008/420747/.
  17. Huang Y, Niu B, Gao Y, Fu L, Li W (2010) CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics 26:680–682PubMedCrossRefGoogle Scholar
  18. Huynh BL, Palmer L, Mather DE, Wallwork H, Graham RD, Welch RM, Stangoulis JCR (2008a) Genotypic variation in wheat grain fructan content revealed by a simplified HPLC method. J Cereal Sci 48:369–378CrossRefGoogle Scholar
  19. Huynh BL, Wallwork H, Stangoulis JCR, Graham RD, Willsmore KL, Olson S, Mather DE (2008b) Quantitative trait loci for grain fructan concentration in wheat (Triticum aestivum L.). Theor Appl Genet 117:701–709PubMedCrossRefGoogle Scholar
  20. Innan H, Kondrashov F (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11:97–108PubMedCrossRefGoogle Scholar
  21. Izanloo A, Condon AG, Langridge P, Tester M, Schnurbusch T (2008) Different mechanisms of adaptation to cyclic water stress in two South Australian bread wheat cultivars. J Exp Bot 59:3327–3346PubMedCrossRefGoogle Scholar
  22. Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinf 9:286–298CrossRefGoogle Scholar
  23. Kawakami A, Yoshida M (2002) Molecular characterization of sucrose:sucrose 1-fructosyltransferase and sucrose: fructan 6-fructosyltransferase associated with fructan accumulation in winter wheat during cold hardening. Biosci Biotechnol Biochem 66:2297–2305PubMedCrossRefGoogle Scholar
  24. Kawakami A, Yoshida M (2005) Fructan:fructan 1-fructosyltransferase, a key enzyme for biosynthesis of graminan oligomers in hardened wheat. Planta 223:90–104PubMedCrossRefGoogle Scholar
  25. Kleessen B, Schwarz S, Boehm A, Fuhrmann H, Richter A, Henle T, Krueger M (2007) Jerusalem artichoke and chicory inulin in bakery products affect faecal microbiota of healthy volunteers. Br J Nutr 98:540–549PubMedCrossRefGoogle Scholar
  26. Lasseur B, Schroeven L, Lammens W, Le Roy K, Spangenberg G, Manduzio H, Vergauwen R, Lothier J, Prud’homme M-P, Van den Ende W (2009) Transforming a fructan:fructan 6G-fructosyltransferase from perennial ryegrass into a sucrose:sucrose 1-fructosyltransferase. Plant Physiol 149:327–339PubMedCrossRefGoogle Scholar
  27. Linde-Laursen I, Heslop-Harrison JS, Shepherd KW, Taketa S (1997) The barley genome and its relationship with the wheat genomes. A survey with an internationally agreed recommendation for barley chromosome nomenclature. Hereditas 126:1–16CrossRefGoogle Scholar
  28. Manly KF, Cudmore RH, Meer JM (2001) Map manager QTX, cross-platform software for genetic mapping. Mamm Genome 12:930–932PubMedCrossRefGoogle Scholar
  29. Marshall DJ, Hayward A, Eales D, Imelfort M, Stiller J, Berkman PJ, Clark T, McKenzie M, Lai KT, Duran C, Batley J, Edwards D (2010) Targeted identification of genomic regions using TAGdb. Plant Methods 6:19–25PubMedCrossRefGoogle Scholar
  30. Mayer KFX, Martis M, Hedley PE, Šimková H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubaláková M, Suchánková P, Murat F, Felder M, Nussbaumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto T, Scholz U, Doležel J, Waugh R, Stein N (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell Online 23:1249–1263CrossRefGoogle Scholar
  31. Moshfegh AJ, Friday JE, Goldman JP, Chug Ahuja JK (1999) Presence of inulin and oligofructose in the diets of Americans. J Nutr 129:1407S–1411SPubMedGoogle Scholar
  32. Mutwil M, Øbro J, Willats WGT, Persson S (2008) GeneCAT—novel webtools that combine BLAST and co-expression analyses. Nucleic Acids Res 36:W320–W326PubMedCrossRefGoogle Scholar
  33. Nagaraj VJ, Altenbach D, Galati V, Lüscher M, Meyer AD, Boller T, Wiemken A (2004) Distinct regulation of sucrose:sucrose-1-fructosyltransferase (1-SST) and sucrose:fructan-6-fructosyltransferase (6-SFT), the key enzymes of fructan synthesis in barley leaves: 1-SST as the pacemaker. New Phytol 161:735–748CrossRefGoogle Scholar
  34. Nilsson U, Dahlqvist A, Nilsson B (1986) Cereal fructosans: part 2-characterization and structure of wheat fructosans. Food Chem 22:95–106CrossRefGoogle Scholar
  35. Ning Z, Cox AJ, Mullikin JC (2001) SSAHA: a fast search method for large DNA databases. Genome Res 11:1725–1729PubMedCrossRefGoogle Scholar
  36. Probert HM, Gibson GR (2002) Investigating the prebiotic and gas-generating effects of selected carbohydrates on the human colonic microflora. Lett Appl Microbiol 35:473–480PubMedCrossRefGoogle Scholar
  37. Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Akhunov ED, Dvorak J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Kantety R, La Rota CM, Munkvold JD, Sorrells SF, Sorrells ME, Dilbirligi M, Sidhu D, Erayman M, Randhawa HS, Sandhu D, Bondareva SN, Gill KS, Mahmoud AA, Ma XF, Miftahudin M, Gustafson JP, Conley EJ, Nduati V, Gonzalez-Hernandez JL, Anderson JA, Peng JH, Lapitan NLV, Hossain KG, Kalavacharla V, Kianian SF, Pathan MS, Zhang DS, Nguyen HT, Choi DW, Fenton RD, Close TJ, McGuire PE, Qualset CO, Gill BS (2004) A chromosome bin map of 16,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712PubMedCrossRefGoogle Scholar
  38. Roberfroid MB, Delzenne NM (1998) Dietary fructans. Annu Rev Nutr 18:117–143Google Scholar
  39. Rustenholz C, Choulet F, Laugier C, Safár J, Simková H, Dolezel J, Magni F, Scalabrin S, Cattonaro F, Vautrin S, Bellec A, Bergès H, Feuillet C, Paux E (2011) A 3,000-loci transcription map of chromosome 3B unravels the structural and functional features of gene islands in hexaploid wheat. Plant Physiol 157:1596–1608PubMedCrossRefGoogle Scholar
  40. Ruuska SA, Rebetzke GJ, van Herwaarden AF, Richards RA, Fettell NA, Tabe L, Jenkins CLD (2006) Genotypic variation in water-soluble carbohydrate accumulation in wheat. Funct Plant Biol 33:799–809CrossRefGoogle Scholar
  41. Sabot F, Guyot R, Wicker T, Chantret N, Laubin B, Chalhoub B, Leroy P, Sourdille P, Bernard M (2005) Updating of transposable element annotations from large wheat genomic sequences reveals diverse activities and gene associations. Mol Genet Genom 274:119–130CrossRefGoogle Scholar
  42. Sakata K, Nagamura Y, Numa H, Antonio BA, Nagasaki H, Idonuma A, Watanabe W, Shimizu Y, Horiuchi I, Matsumoto T, Sasaki T, Higo K (2002) RiceGAAS: an automated annotation system and database for rice genome sequence. Nucleic Acids Res 30:98–102PubMedCrossRefGoogle Scholar
  43. Salamov AA, Solovyev VV (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10:516–522PubMedCrossRefGoogle Scholar
  44. Schnyder H, Gillenberg C, Hinz J (1993) Fructan contents and dry matter deposition in different tissues of the wheat grain during development. Plant, Cell Environ 16:179–187CrossRefGoogle Scholar
  45. Schreiber AW, Sutton T, Caldo RA, Kalashyan E, Lovell B, Mayo G, Muehlbauer GJ, Druka A, Waugh R, Wise RP, Langridge P, Baumann U (2009) Comparative transcriptomics in the Triticeae. BMC Genom 10:285–302CrossRefGoogle Scholar
  46. Schroeven L, Lammens W, Van Laere A, Van den Ende W (2008) Transforming wheat vacuolar invertase into a high affinity sucrose:sucrose 1-fructosyltransferase. New Phytol 180:822–831PubMedCrossRefGoogle Scholar
  47. Schulte D, Close TJ, Graner A, Langridge P, Matsumoto T, Muehlbauer G, Sato K, Schulman AH, Waugh R, Wise RP, Stein N (2009) The international barley sequencing consortium-at the threshold of efficient access to the barley genome. Plant Physiol 149:142–147PubMedCrossRefGoogle Scholar
  48. Schulte D, Ariyadasa R, Shi B, Fleury D, Saski C, Atkins M, deJong P, Wu C–C, Graner A, Langridge P, Stein N (2011) BAC library resources for map-based cloning and physical map construction in barley (Hordeum vulgare L.). BMC Genom 12:247–258CrossRefGoogle Scholar
  49. Setter TL, Anderson WK, Asseng S, Barclay I (1998) Review of the impact of high shoot carbohydrate concentrations on maintenance of high yields in cereals exposed to environmental stress during grain filling. In: Nagarajan S, Singh G, Tyagi BS (eds) Wheat research needs beyond 2000 AD. Publishing House, New Delhi, pp 237–255Google Scholar
  50. Stanke M, Diekhans M, Baertsch R, Haussler D (2008) Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24:637–644PubMedCrossRefGoogle Scholar
  51. Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–7PubMedCrossRefGoogle Scholar
  52. 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 28:2731–2739PubMedCrossRefGoogle Scholar
  53. Van den Ende W, Clerens S, Vergauwen R, Boogaerts D, Le Roy K, Arckens L, Van Laere A (2006) Cloning and functional analysis of a high DP fructan:fructan 1-fructosyl transferase from Echinops ritro (Asteraceae): comparison of the native and recombinant enzymes. J Exp Bot 57:775–789PubMedCrossRefGoogle Scholar
  54. Van Der Meer IM, Koops AJ, Hakkert JC, Van Tunen AJ (1998) Cloning of the fructan biosynthesis pathway of Jerusalem artichoke. Plant J 15:489–500PubMedCrossRefGoogle Scholar
  55. Van Loo J, Coussement P, De Leenheer L, Hoebregs H, Smits G (1995) On the presence of inulin and oligofructose as natural ingredients in the western diet. Crit Rev Food Sci Nutr 35:525–552PubMedCrossRefGoogle Scholar
  56. Van Os H, Stam P, Visser RGF, Van Eck HJ (2005) RECORD: a novel method for ordering loci on a genetic linkage map. Theor Appl Genet 112:30–40PubMedCrossRefGoogle Scholar
  57. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:research0034.0031–research0034.0011Google Scholar
  58. Veerassamy S, Smith A, Tillier ERM (2003) A transition probability model for amino acid substitutions from blocks. J Comput Biol 10:997–1010PubMedCrossRefGoogle Scholar
  59. Vijn I, Smeekens S (1999) Fructan: more than a reserve carbohydrate? Plant Physiol 120:351–359PubMedCrossRefGoogle Scholar
  60. Wei J-Z, Chatterton NJ (2001) Fructan biosynthesis and fructosyltransferase evolution: expression of the 6-SFT (sucrose:fructan 6-fructosyltransferase) gene in crested wheatgrass (Agropyron cristatum). J Plant Physiol 158:1203–1213CrossRefGoogle Scholar
  61. Wei J-Z, Chatterton NJ, Larson SR, Wang RRC (2000) Linkage mapping and nucleotide polymorphisms of the 6-SFT gene of cool-season grasses. Genome 43:931–938PubMedCrossRefGoogle Scholar
  62. Wei J-Z, Chatterton NJ, Harrison PA, Wang RRC, Larson SR (2002) Characterization of fructan biosynthesis in big bluegrass (Poa secunda). J Plant Physiol 159:705–715CrossRefGoogle Scholar
  63. Weng Y, Lazar MD (2002) Comparison of homoeologous group-6 short arm physical maps of wheat and barley reveals a similar distribution of recombinogenic and gene-rich regions. Theor Appl Genet 104:1078–1085PubMedCrossRefGoogle Scholar
  64. Xue G-P, McIntyre CL, Jenkins CLD, Glassop D, van Herwaarden AF, Shorter R (2008) Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiol 146:441–454PubMedCrossRefGoogle Scholar
  65. Xue G-P, Kooiker M, Drenth J, McIntyre CL (2011) TaMYB13 is a transcriptional activator of fructosyltransferase genes involved in β-2,6-linked fructan synthesis in wheat. Plant J 68:857–870PubMedCrossRefGoogle Scholar
  66. Yang J, Zhang J, Wang Z, Zhu Q, Liu L (2004) Activities of fructan- and sucrose-metabolizing enzymes in wheat stems subjected to water stress during grain filling. Planta 220:331–343PubMedCrossRefGoogle Scholar
  67. Yu Y, Tomkins JP, Waugh R, Frisch DA, Kudrna D, Kleinhofs A, Brueggeman RS, Muehlbauer GJ, Wise RP, Wing RA (2000) A bacterial artificial chromosome library for barley (Hordeum vulgare L.) and the identification of clones containing putative resistance genes. Theor Appl Genet 101:1093–1099CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Bao-Lam Huynh
    • 1
    • 2
    • 3
    • 4
  • Diane E. Mather
    • 1
  • Andreas W. Schreiber
    • 1
  • John Toubia
    • 1
  • Ute Baumann
    • 1
  • Zahra Shoaei
    • 1
  • Nils Stein
    • 5
  • Ruvini Ariyadasa
    • 5
  • James C. R. Stangoulis
    • 6
  • James Edwards
    • 1
    • 7
  • Neil Shirley
    • 1
  • Peter Langridge
    • 1
  • Delphine Fleury
    • 1
  1. 1.Australian Centre for Plant Functional Genomics and School of Agriculture, Food and Wine, Waite Research InstituteThe University of AdelaideGlen OsmondSouth Australia
  2. 2.Phenomics and Bioinformatics Research Centre, School of Mathematics and StatisticsUniversity of South AustraliaMawson LakesSouth Australia
  3. 3.Breeding DivisionRubber Research Institute of VietnamHo Chi MinhVietnam
  4. 4.Department of Nematology University of CaliforniaRiversideUSA
  5. 5.Leibniz Institute of Plant Genetics and Crop Plant Research (IPK)GaterslebenGermany
  6. 6.School of Biological SciencesFlinders UniversityAdelaideSouth Australia
  7. 7.Australian Grain TechnologiesGlen OsmondSouth Australia

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