期刊论文详细信息
BMC Evolutionary Biology
Expansion of the gamma-gliadin gene family in Aegilops and Triticum
Marinus JM Smulders5  Luud JWJ Gilissen5  Ingrid M van der Meer5  Elena Z Kochieva2  Nadejda N Chikida3  Elma MJ Salentijn1  Svetlana V Goryunova4 
[1] Plant Research International, Wageningen UR, P.O. Box 16, Wageningen, NL-6700 AA, The Netherlands;Bioengineering Center, Moscow, 117312, Russia;All-Russian Institute of Plant Industry, St. Petersburg, 190000, Russia;Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, 119991, Russia;Allergy Consortium, Wageningen, The Netherlands
关键词: Evolution;    Multigene family;    Aegilops;    Triticum;    Wheat;    Gamma-gliadin;   
Others  :  1140104
DOI  :  10.1186/1471-2148-12-215
 received in 2012-04-28, accepted in 2012-10-31,  发布年份 2012
PDF
【 摘 要 】

Background

The gamma-gliadins are considered to be the oldest of the gliadin family of storage proteins in Aegilops/Triticum. However, the expansion of this multigene family has not been studied in an evolutionary perspective.

Results

We have cloned 59 gamma-gliadin genes from Aegilops and Triticum species (Aegilops caudata L., Aegilops comosa Sm. in Sibth. & Sm., Aegilops mutica Boiss., Aegilops speltoides Tausch, Aegilops tauschii Coss., Aegilops umbellulata Zhuk., Aegilops uniaristata Vis., and Triticum monococcum L.) representing eight different genomes: Am, B/S, C, D, M, N, T and U. Overall, 15% of the sequences contained internal stop codons resulting in pseudogenes, but this percentage was variable among genomes, up to over 50% in Ae. umbellulata. The most common length of the deduced protein, including the signal peptide, was 302 amino acids, but the length varied from 215 to 362 amino acids, both obtained from Ae. speltoides. Most genes encoded proteins with eight cysteines. However, all Aegilops species had genes that encoded a gamma-gliadin protein of 302 amino acids with an additional cysteine. These conserved nine-cysteine gamma-gliadins may perform a specific function, possibly as chain terminators in gluten network formation in protein bodies during endosperm development. A phylogenetic analysis of gamma-gliadins derived from Aegilops and Triticum species and the related genera Lophopyrum, Crithopsis, and Dasypyrum showed six groups of genes. Most Aegilops species contained gamma-gliadin genes from several of these groups, which also included sequences from the genera Lophopyrum, Crithopsis, and Dasypyrum. Hordein and secalin sequences formed separate groups.

Conclusions

We present a model for the evolution of the gamma-gliadins from which we deduce that the most recent common ancestor (MRCA) of Aegilops/Triticum-Dasypyrum-Lophopyrum-Crithopsis already had four groups of gamma-gliadin sequences, presumably the result of two rounds of duplication of the locus.

【 授权许可】

   
2012 Goryunova et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150324093431617.pdf 938KB PDF download
Figure 4. 96KB Image download
Figure 3. 42KB Image download
Figure 2. 150KB Image download
Figure 1. 22KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】
  • [1]Harberd NP, Bartels D, Thompson RD: Analysis of the gliadin multigene loci in bread wheat using nullisomic-tetrasomic lines. Mol Gen Genet 1985, 198:234-242.
  • [2]Okita TW, Cheesbrough V, Reeves CD: Evolution and heterogeneity of the α-/β-type and γ-type gliadin DNA sequences. J Biol Chem 1985, 260:8203-8213.
  • [3]Anderson OD, Litts JC, Greene FC: The α-gliadin gene family. I. Characterization of ten new wheat α-gliadin genomic clones, evidence for limited sequence conservation of flanking DNA, and southern analysis of the gene family. Theor Appl Genet 1997, 95:50-58.
  • [4]Van Herpen TWJM, Goryunova SV, Van der Schoot J, et al.: Alpha-gliadin genes from the A, B, and D genomes of wheat contain different sets of celiac disease epitopes. BMC Genom 2006, 7:1.
  • [5]Shewry PR, Tatham AS: The prolamin storage proteins of cereal seeds: structure and evolution. Biochem J 1990, 267:1-12.
  • [6]Payne PI, Holt LM, Jackson EA, Law CN: Wheat storage proteins: their genetics and their potential for manipulation by plant breeding. Phil Trans R Soc Lond B 1984, 304:359-371.
  • [7]Payne PI, Jackson EA, Holt LM, Law CN: Genetic linkage between endosperm storage protein genes on each of the short arms of chromosomes 1A and 1B in wheat. Theor Appl Genet 1984, 67:235-243.
  • [8]Sabelli P, Shewry PR: Characterization and organization of gene families at the Gli-1 loci of bread and durum wheat by restriction fragment analysis. Theor Appl Genet 1991, 83:209-216.
  • [9]Anderson OD, Hsia CC, Torres V: The wheat γ-gliadin genes: characterization of ten new sequences and further understanding of γ-gliadin gene family structure. Theor Appl Genet 2001, 103:323-330.
  • [10]Qi PF, Wei YM, Ouellet T, Chen Q, Tan X, Zheng YL: The γ-gliadin multigene family in common wheat (Triticum aestivum) and its closely related species. BMC Genom 2009, 10:168. BioMed Central Full Text
  • [11]Petersen G, Seberg O, Yde M, Berthelsen K: Phylogenetic relationships of Triticum and Aegilops and evidence for the origin of the A, B, and D genomes of common wheat (Triticum aestivum). Mol Phylogenet Evol 2006, 39:70-82.
  • [12]Kilian B, Ozkan H, Deusch O, Effgen S, Brandolini A, Kohl J, Martin W, Salamini F: Independent wheat B and G genome origins in outcrossing Aegilops progenitor haplotypes. Mol Biol Evol 2007, 24:217-227.
  • [13]Shewry PR, Tatham AS: Disulphide bonds in wheat gluten proteins. J Cereal Sci 1997, 25:207-227.
  • [14]Wang S, Shen X, Ge P, Li J, Subburaj S, Li X, Zeller FJ, Hsam SL, Yan Y: Molecular characterization and dynamic expression patterns of two types of γ-gliadin genes from Aegilops and Triticum species. Theor Appl Genet 2012, 125:1371-1384.
  • [15]Zhang Q, Donga Y, An X, Wang A, Zhang Y, Li X, Gao L, Xi X, He Z, Yan Y: Characterization of HMW glutenin subunits in common wheat and related species by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF-MS). J Cereal Sci 2008, 47:252-261.
  • [16]Li XH, Zhang YZ, Gao LY, Wang AL, Ji KM, He ZH: Molecular cloning, heterologous expression, and phylogenetic analysis of a novel y-type HMW glutenin subunit gene from the G genome of Triticum timopheevi. Genome 2007, 50:1130-1140.
  • [17]Zhang MY, Wang K, Wang SL, Li XH, Zeller FJ, Hsam SLK, Yan YM: Molecular cloning, function prediction and phylogenetic analysis of LMW glutenin subunit genes in Triticum timopheevii (Zhuk.). Plant Breed 2010, 129:622-629.
  • [18]Wang S, Li X, Wang K, Wang X, Li S, Zhang Y, Guo G, Zeller FJ, Hsam SLK, Yan Y: Phylogenetic analysis of C, M, N, and U genomes and their relationships with Triticum and other related genomes as revealed by LMW-GS genes at Glu-3 loci. Genome 2011, 54:273-284.
  • [19]Van Slageren MW: Wild wheats: a monograph of Aegilops L. and Amblyopyrum (Jaub. & Spach) Eig (Poaceae). Wag Ag Un P 1994, 7:513.
  • [20]Edwards K, Johnstone C, Thompson C: A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 1991, 19:1349.
  • [21]Dorokhov DB, Klocke EA: Rapid and economic technique for RAPD analysis of plant genomes. Russ J Genet 1997, 33:358-365.
  • [22]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
  • [23]Dereeper A, Guignon V, Blanc G, et al.: (12 co-authors): Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008, 36:W465-W469.
  • [24]Dereeper A, Audic S, Claverie JM, Blanc G: BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 2010, 10:8. BioMed Central Full Text
  • [25]Anisimova M, Gascuel O: Approximate likelihood ratio test for branchs: A fast, accurate and powerful alternative. Syst Biol 2006, 55:539-52.
  • [26]Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.
  • [27]Salentijn EMJ, Mitea DC, Goryunova SV, Van der Meer IM, Padioleau I, Gilissen LJWJ, Koning F, Smulders MJM: Celiac disease T cell epitopes from gamma-gliadins: immunoreactivity depends on the genome of origin, transcript frequency, and flanking protein variation. BMC Genomics 2012, 13:277. BioMed Central Full Text
  • [28]Bowden WM: The taxonomy and nomenclature of the wheats, barleys, and ryes and their wild relatives. Can J Bot 1959, 37:657-684.
  • [29]Kimber G, Sears ER: Evolution in the genusTriticumand the origin of cultivated wheat. In Wheat and Wheat Improvement. 2nd edition. Edited by Heyne EG. Madison, WI: Am. Soc. Agron; 1987:154-164.
  • [30]Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P: Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc Natl Acad Sci USA 2002, 99:8133-8138.
  • [31]Clegg MT, Cummings MP, Durbin ML: The evolution of plant nuclear genes. Proc Natl Acad Sci USA 1997, 94:7791-7798.
  • [32]Pan Q, Wendel J, Fluhr R: Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 2000, 50:203-213.
  • [33]Gao S, Gu YQ, Wu J, Coleman-Derr D, Huo N, Crossman C, Jia J, Zuo Q, Ren Z, Anderson OD, Kong X: Rapid evolution and complex structural organization in genomic regions harboring multiple prolamin genes in the polyploid wheat genome. Plant Mol Biol 2007, 65:189-203.
  • [34]Nei M, Gu X, Sitnikova T: Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci USA 1997, 94:7799-7806.
  • [35]Escobar JS, Scornavacca C, Cenci A, Guilhaumon C, Santoni S, Douzery EJP, Ranwez V, Glémin S, David J: Multigenic phylogeny and analysis of tree incongruences in Triticeae (Poaceae). BMC Evol Biol 2011, 11:181. BioMed Central Full Text
  • [36]Zhukovsky PM: A critical systematic survey of the species of the genus Aegilops L. B Appl Botany, Genet Plant Breeding 1928, 18:497-609.
  • [37]Eig A: Monographisch-kritische Übersicht der Gattung Aegilops. Feddes Repertorium Specierum novarum regni vegetabilis Beih 1929, 55:1-228.
  • [38]Kihara H: Fertility and morphological variation in the substitution backcrosses of the hybrid Triticum vulgare × Aegilops caudata. Proc X Int Congr Genet 1959, 1:142-171.
  • [39]Hammer K: Vorarbeiten zur monographischen Darstellung von Wildpflanzensortimenten: Aegilops L. Kulturpflanze 1980, 28:33-180.
  • [40]Whitcombe JR: A guide to the species of Aegilops L.: their taxonomy, morphology, and distribution. Rome, Italy: International Board for Plant Genetic Resources (IPGRI); 1983:74.
  • [41]Eig A: Amblyopyrum Eig. A new genus separated from the genus Aegilops. PZE Ins Agr Nat Hist Agr Res 1929, 2:199-204.
  • [42]Badaeva E, Friebe B, Gill B: Genome differentiation in Aegilops. 1. Distribution of highly repetitive DNA sequences on chromosomes of diploid species. Genome 1996, 39:293-306.
  • [43]Kihara H: Considerations on the evolution and distribution of Aegilops species based on the analyser-method. Cytologia 1954, 19:336-357.
  • [44]Dvorak J, Zhang HB: Reconstruction of the phylogeny of the genus Triticum from variation in repeated nucleotide sequences. Theor Appl Genet 1992, 84:419-429.
  • [45]Dvorak J, Luo M-C, Yang Z-L: Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 1998, 148:423-434.
  • [46]Dvorak J, Luo M-C, Yang Z-L, Zhang H-B: The structure of the Aegilops tauschii genepool and the evolution of hexaploid wheat. Theor Appl Genet 1998, 97:657-670.
  • [47]Ogihara Y, Tsunewaki K: Diversity and evolution of chloroplast DNA in Triticum and Aegilops as revealed by restriction fragment analysis. Theor Appl Genet 1988, 76:321-332.
  • [48]Dvorak J, Zhang HB: Variation in repeated nucleotide sequences sheds light on the phylogeny of the wheat B and G genomes. Proc Natl Acad Sci USA 1990, 87:9640-9644.
  • [49]Miyashita NT, Monri N, Tsunewaki K: Molecular variation in chloroplast DNA regions in ancestral species of wheat. Genetics 1994, 137:883-889.
  • [50]Sasanuma T, Miyashita NT, Tsunewaki K: Wheat phylogeny determined by RFLP analysis of nuclear DNA. 3. Intra- and interspecific variations of five Aegilops Sitopsis species. Theor Appl Genet 1996, 92:928-934.
  • [51]Dvorak J, Luo M-C, Yang Z-L: Genetic evidence on the origin of T. aestivum L. In The origins of agriculture and the domestication of crop plants in the Near East. Edited by Damania A. Aleppo, Syria, ICARDA: ICARDA; 1998:235-251.
  • [52]Giorgi D, D'Ovidio R, Tanzarella OA, Porceddu E: RFLP analysis of Aegilops species belonging to the Sitopsis section. Genet Resour Crop Evol 2002, 49:145-151.
  • [53]Goryunova SV, Kochieva EZ, Chikida NN, Pukhalskyi VA: Phylogenetic relationships and intraspecific variation of D-genome Aegilops L. as revealed by RAPD analysis. Russ J Genet 2004, 40:515-523.
  • [54]Chennaveeraiah MA: Karyomorphologic and Cytotaxonomic Studies in Aegilops. Acta Horti Gotoburgensis 1960, 23:85-178.
  • [55]Zhukovskii PM: Kul’turnye rasteniya i ikh sorodichi (Cultivated Plants and Their Relatives). Kolos, Leningrad; 1971:122-130. in Russian
  • [56]Lucas H, Jahier J: Phylogenetic relationships in some diploid species of Triticineae: cytogenetic analysis of interspecific hybrids. Theor Appl Genet 1988, 75:498-502.
  • [57]Meimberg H, Rice KJ, Milan NF, Njoku CC, Mckay JK: Multiple origins promote the ecological amplitude of allopolyploid Aegilops (Poaceae). Am J Bot 2009, 96:1262-1273.
  • [58]Altenbach SB, Vensel WH, DuPont FM: Analysis of expressed sequence tags from a single wheat cultivar facilitates interpretation of tandem mass spectrometry data and discrimination of gamma gliadin proteins that may play different functional roles in flour. BMC Plant Biol 2010, 10:7. BioMed Central Full Text
  • [59]Gianibelli MC, Larroque OR, MacRitchie F, Wrigley CW: Biochemical, genetic, and molecular characterization of wheat endosperm proteins. St. Paul, Minnesota, USA: American Association of Cereal Chemists, Inc; 2001:1-20. [Online review] Publication no. C-2001-0926-01O
  • [60]Upelniek VP, Brezhneva TA, Dadashev SY, Novozhilova OA, Molkanova OI, Semikhov VF: On the use of alleles of gliadin-coding loci as possible adaptability markers in the spring wheat (Triticum aestivum L.) cultivars during seed germination. Russ J Genet 2003, 39:1426-1431.
  • [61]Gil-Humanes J, Pistón F, Hernando A, Alvarez JB, Shewry PR, Barro F: Silencing of γ-gliadins by RNA interference (RNAi) in bread wheat. J Cereal Sci 2008, 48:565-568.
  • [62]Gil-Humanes J, Pistón F, Tollefsen S, Sollid LM, Barro F: Effective shutdown in the expression of celiac disease-related wheat gliadin T-cell epitopes by RNA interference. Proc Natl Acad Sci USA 2010, 107:17023-17028.
  • [63]Gil-Humanes J, Pistón F, Shewry PR, Tosi P, Barro F: Suppression of gliadins results in altered protein body morphology in wheat. J Exp Bot 2011, 62:4203-4213.
  • [64]Pistón F, Gil-Humanes J, Rodríguez-Quijano M, Barro F: Down-regulating γ-gliadins in bread wheat leads to non-specific increases in other gluten proteins and has no major effect on dough gluten strength. PLoS ONE 2011, 6:e24754.
  • [65]Gil-Humanes J, Pistón F, Giménez MJ, Martín A, Barro F: The Introgression of RNAi Silencing of γ-Gliadins into Commercial Lines of Bread Wheat Changes the Mixing and Technological Properties of the Dough. PLoS ONE 2012, 7:e45937.
  • [66]Van den Broeck HC, Van Herpen TWJM, Schuit C, Salentijn EMJ, Dekking L, Bosch D, Hamer RJ, Smulders MJM, Gilissen LJWJ, Van der Meer IM IM: Removing celiac disease-related gluten proteins from bread wheat while retaining technological properties: a study with Chinese Spring deletion lines. BMC Plant Biol 2009, 9:41. BioMed Central Full Text
  文献评价指标  
  下载次数:49次 浏览次数:10次