On the genome constitution and evolution of intermediate wheatgrass (Thinopyrum intermedium: Poaceae, Triticeae)
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
21592357
PubMed Central
PMC3123223
DOI
10.1186/1471-2148-11-127
PII: 1471-2148-11-127
Knihovny.cz E-zdroje
- MeSH
- fylogeneze MeSH
- genom rostlinný * MeSH
- polyploidie MeSH
- pšenice genetika MeSH
- rostlinné proteiny genetika MeSH
- synthasa škrobu genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- granule-bound starch synthase I MeSH Prohlížeč
- rostlinné proteiny MeSH
- synthasa škrobu MeSH
BACKGROUND: The wheat tribe Triticeae (Poaceae) is a diverse group of grasses representing a textbook example of reticulate evolution. Apart from globally important grain crops, there are also wild grasses which are of great practical value. Allohexaploid intermediate wheatgrass, Thinopyrum intermedium (2n = 6x = 42), possesses many desirable agronomic traits that make it an invaluable source of genetic material useful in wheat improvement. Although the identification of its genomic components has been the object of considerable investigation, the complete genomic constitution and its potential variability are still being unravelled. To identify the genomic constitution of this allohexaploid, four accessions of intermediate wheatgrass from its native area were analysed by sequencing of chloroplast trnL-F and partial nuclear GBSSI, and genomic in situ hybridization. RESULTS: The results confirmed the allopolyploid origin of Thinopyrum intermedium and revealed new aspects in its genomic composition. Genomic heterogeneity suggests a more complex origin of the species than would be expected if it originated through allohexaploidy alone. While Pseudoroegneria is the most probable maternal parent of the accessions analysed, nuclear GBSSI sequences suggested the contribution of distinct lineages corresponding to the following present-day genera: Pseudoroegneria, Dasypyrum, Taeniatherum, Aegilops and Thinopyrum. Two subgenomes of the hexaploid have most probably been contributed by Pseudoroegneria and Dasypyrum, but the identity of the third subgenome remains unresolved satisfactorily. Possibly it is of hybridogenous origin, with contributions from Thinopyrum and Aegilops. Surprising diversity of GBSSI copies corresponding to a Dasypyrum-like progenitor indicates either multiple contributions from different sources close to Dasypyrum and maintenance of divergent copies or the presence of divergent paralogs, or a combination of both. Taeniatherum-like GBSSI copies are most probably pseudogenic, and the mode of their acquisition by Th. intermedium remains unclear. CONCLUSIONS: Hybridization has played a key role in the evolution of the Triticeae. Transfer of genetic material via extensive interspecific hybridization and/or introgression could have enriched the species' gene pools significantly. We have shown that the genomic heterogeneity of intermediate wheatgrass is higher than has been previously assumed, which is of particular concern to wheat breeders, who frequently use it as a source of desirable traits in wheat improvement.
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Vogel KP, Jensen KJ. Adaptation of perennial triticeae to the eastern Central Great Plains. J Range Manag. 2001;54:674–679. doi: 10.2307/4003670. DOI
Tsitsin NV. Novyi vid i novye raznovidnosti pshenitsy. (New species and varieties of wheats) Byul Gl Bot Sada AN SSSR. 1960;38:38–41.
Tsvelev NN. Conspectus specierum tribus Triticeae Dum. familiae Poaceae in flora URSS. Nov Sist Vyssh Rast. 1973;10:19–59.
Sharma H, Ohm H, Goulart L, Lister R, Appels R, Benlhabib O. Introgression and characterization of barley yellow dwarf virus resistance from Thinopyrum intermedium into wheat. Genome. 1995;38:406–413. doi: 10.1139/g95-052. PubMed DOI
Friebe B, Gill KS, Tuleen NA, Gill BS. Transfer of wheat streak mosaic virus resistance from Agropyron intermedium into wheat. Crop Sci. 1996;36:857–861. doi: 10.2135/cropsci1996.0011183X003600040006x. DOI
Tang S, Li Z, Jia X, Larkin PJ. Genomic in situ hybridization (GISH) analyses of Thinopyrum intermedium, its partial amphiploid Zhong 5, and disease-resistant derivatives in wheat. Theor Appl Genet. 2000;100:344–352. doi: 10.1007/s001220050045. DOI
Fedak G, Han F. Characterization of derivatives from wheat-Thinopyrum wide crosses. Cytogenet Genome Res. 2005;109:360–367. doi: 10.1159/000082420. PubMed DOI
Li HJ, Wang XM. Thinopyrum ponticum and Th. intermedium: the promising source of resistance to fungal and viral diseases of wheat. J Genet Genomics. 2009;36:557–565. doi: 10.1016/S1673-8527(08)60147-2. PubMed DOI
Peto FH. Hybridization of Triticum and Agropyron. II. Cytology of the male parents and F1 generation. Can J Res C Bot Sci. 1936;14:203–214.
Vakar BA. A cytological study of F1 - F6 Triticum vulgare × Agropyron intermedium hybrids. Bull Acad Sci USSR. 1938. pp. 627–641.
Matsumura S. Hybrids between wheat and Agropyron. Jpn J Genet. 1952;23:27–29.
Stebbins GL, Pun FT. Artificial and natural hybrids in the Gramineae, tribe Hordeae. VI. Chromosome pairing in Secale cereale × Agropyron intermedium and the problem of genome homologies in the Triticinae. Genetics. 1953;38:600–608. PubMed PMC
Dewey DR. The genome structure of intermediate wheatgrass. J Hered. 1962;53:282–290.
Dewey DR. In: Gene manipulation in plant improvement. Gustafson JP, editor. New York: Plenum; 1984. The genomic system of classification as a guide to intergeneric hybridization with the perennial Triticeae; pp. 209–279.
Dvořák J. Genome relationships among Elytrigia (= Agropyron) elongata, E. stipifolia, 'E. elongata 4x', E. caespitosa, E. intermedia, and 'E. elongata 10x'. Can J Genet Cytol. 1981;23:481–492.
Löve Á. Conspectus of the Triticeae. Feddes Repert. 1984;95:425–521.
Liu ZW, Wang RRC. Genome analysis of Elytrigia caespitosa, Lophopyrum nodosum, Pseudoroegneria geniculata ssp. scythica, and Thinopyrum intermedium (Triticeae: Gramineae) Genome. 1993;36:102–111. doi: 10.1139/g93-014. PubMed DOI
Assadi M, Runemark H. Hybridisation, genomic constitution and generic delimitation in Elymus s. l. (Poaceae: Triticeae) Plant Syst Evol. 1995;194:189–205. doi: 10.1007/BF00982855. DOI
Chen Q, Conner RL, Laroche A, Thomas JB. Genome analysis of Thinopyrum intermedium and Thinopyrum ponticum using genomic in situ hybridization. Genome. 1998;41:580–586. PubMed
Kishii M, Wang RRC, Tsujimoto H. GISH analysis revealed new aspect of genomic constitution of Thinopyrum intermedium. Czech J Genet Plant Breed. 2005;41(Special issue):91–95.
Wang RRC, von Bothmer R, Dvořák J, Fedak G, Linde-Laursen I, Muramatsu M. In: Proceedings of the 2nd International Triticeae Symposium. Wang RRC, Jensen KB, Jaussi C, editor. Logan, USA: Utah State University; 1995. Genomic symbols in the Triticeae (Poaceae) pp. 29–34.
Aizatulina KhS, Yachevskaya GL, Pereladova TP. Study of the genome structure of Agropyron intermedium (Host) Beauv. Tsitol Genet. 1989;23:15–22. PubMed
Friebe B, Mukai Y, Gill BS, Cauderon Y. C-banding and in situ hybridization analyses of Agropyron intermedium, a partial wheat × Ag. intermedium amphiploid, and 6 derived chromosome addition lines. Theor Appl Genet. 1992;84:899–905. PubMed
Xu J, Conner RL. Intravarietal variation in satellites and C-banded chromosomes of Agropyron intermedium ssp. trichophorum cv. Greenleaf. Genome. 1994;37:305–310. doi: 10.1139/g94-042. PubMed DOI
Mason-Gamer RJ. Reticulate evolution, introgression, and intertribal gene capture in an allohexaploid grass. Syst Biol. 2004;53:25–37. doi: 10.1080/10635150490424402. PubMed DOI
Mason-Gamer RJ. Allohexaploidy, introgression, and the complex phylogenetic history of Elymus repens (Poaceae) Mol Phylogenet Evol. 2008;47:598–611. doi: 10.1016/j.ympev.2008.02.008. PubMed DOI
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. doi: 10.1016/j.ympev.2006.01.023. PubMed DOI
Fortune PM, Schierenbeck KA, Ainouche AK, Jacquemin J, Wendel JF, Ainouche ML. Evolutionary dynamics of waxy and the origin of hexaploid Spartina species (Poaceae) Mol Phylogenet Evol. 2007;43:1040–1055. doi: 10.1016/j.ympev.2006.11.018. PubMed DOI
Fortune PM, Pourtau N, Viron N, Ainouche ML. Molecular phylogeny and reticulate origins of the polyploid Bromus species from section Genea (Poaceae) Am J Bot. 2008;95:454–464. doi: 10.3732/ajb.95.4.454. PubMed DOI
Mason-Gamer RJ, Weil CF, Kellogg EA. Granule-bound starch synthase: structure, function, and phylogenetic utility. Mol Biol Evol. 1998;15:1658–1673. PubMed
Ingram AL, Doyle JJ. The origin and evolution of Eragrostis tef (Poaceae) and related polyploids: Evidence from nuclear waxy and plastid rps16. Am J Bot. 2003;90:116–122. doi: 10.3732/ajb.90.1.116. PubMed DOI
Evans RC, Alice LA, Campbell CS, Kellogg EA, Dickinson TA. The granule-bound starch synthase (GBSSI) gene in the Rosaceae: multiple loci and phylogenetic utility. Mol Phylogenet Evol. 2000;17:388–400. doi: 10.1006/mpev.2000.0828. PubMed DOI
Mitchell A, Wen J. Phylogenetic utility and evidence for multiple copies of granule-bound starch synthase I (GBSSI) in Araliaceae. Taxon. 2004;53:29–41. doi: 10.2307/4135486. DOI
Winkworth RC, Donoghue MJ. Viburnum phylogeny: evidence from the duplicated nuclear gene GBSSI. Mol Phylogenet Evol. 2004;33:109–126. doi: 10.1016/j.ympev.2004.05.006. PubMed DOI
Mahelka V, Kopecký D. Gene capture from across the grass family in the allohexaploid Elymus repens (L.) Gould (Poaceae, Triticeae) as evidenced by ITS, GBSSI, and molecular cytogenetics. Mol Biol Evol. 2010;27:1370–1390. doi: 10.1093/molbev/msq021. PubMed DOI
Mason-Gamer RJ, Orme NL, Anderson CM. Phylogenetic analysis of North American Elymus and the monogenomic Triticeae (Poaceae) using three chloroplast DNA data sets. Genome. 2002;45:991–1002. doi: 10.1139/g02-065. PubMed DOI
Jakob SS, Blattner FR. A chloroplast genealogy of Hordeum (Poaceae): long-term persisting haplotypes, incomplete lineage sorting, regional extinction, and the consequences for phylogenetic inference. Mol Biol Evol. 2006;23:1602–1612. doi: 10.1093/molbev/msl018. PubMed DOI
Liu Q, Ge S, Tang H, Zhang X, Zhu G, Lu BR. Phylogenetic relationships in Elymus (Poaceae: Triticeae) based on the nuclear ribosomal internal transcribed spacer and chloroplast trnL-F sequences. New Phytol. 2006;170:411–420. doi: 10.1111/j.1469-8137.2006.01665.x. PubMed DOI
Fehrer J, Krak K, Chrtek J Jr. Intra-individual polymorphism in diploid and apomictic polyploid hawkweeds (Hieracium, Lactuceae, Asteraceae): disentangling phylogenetic signal, reticulation, and noise. BMC Evol Biol. 2009;9:239. doi: 10.1186/1471-2148-9-239. PubMed DOI PMC
Redinbaugh MG, Jones TA, Zhang Y. Ubiquity of the St chloroplast genome in St-containing Triticeae polyploids. Genome. 2000;43:846–852. doi: 10.1139/g00-053. PubMed DOI
McMillan E, Sun G. Genetic relationships of tetraploid Elymus species and their genomic donor species inferred from polymerase chain reaction-restriction length polymorphism analysis of chloroplast gene regions. Theor Appl Genet. 2004;108:535–542. doi: 10.1007/s00122-003-1453-3. PubMed DOI
Xu DH, Ban T. Phylogenetic and evolutionary relationships between Elymus humidus and other Elymus species based on sequencing of non-coding regions of cpDNA and AFLP of nuclear DNA. Theor Appl Genet. 2004;108:1443–1448. doi: 10.1007/s00122-004-1588-x. PubMed DOI
Zhang C, Fan X, Yu HQ, Zhang L, Wang XL, Zhou YH. Different maternal genome donor to Kengyilia species inferred from chloroplast trnL-F sequences. Biol Plant. 2009;53:759–763. doi: 10.1007/s10535-009-0139-3. DOI
Mahelka V, Suda J, Jarolímová V, Trávníček P, Krahulec F. Genome size discriminates between closely related taxa Elytrigia repens and E. intermedia (Poaceae: Triticeae) and their hybrid. Folia Geobot. 2005;40:367–384. doi: 10.1007/BF02804286. DOI
Mahelka V, Fehrer J, Krahulec F, Jarolímová V. Recent natural hybridization between two allopolyploid wheatgrasses (Elytrigia, Poaceae): ecological and evolutionary implications. Ann Bot. 2007;100:249–260. doi: 10.1093/aob/mcm093. PubMed DOI PMC
Štorchová H, Hrdličková R, Chrtek J Jr, Tetera M, Fitze D, Fehrer J. An improved method for DNA isolation from plants collected in the field and conserved in saturated NaCl/CTAB solution. Taxon. 2000;49:79–84. doi: 10.2307/1223934. DOI
Taberlet P, Gielly L, Pautou G, Bouvet J. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol. 1991;17:1105–1109. doi: 10.1007/BF00037152. PubMed DOI
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25:4876–4882. doi: 10.1093/nar/25.24.4876. PubMed DOI PMC
Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–98.
Müller K. Incorporating information from length-mutational events into phylogenetic analysis. Mol Phylogenet Evol. 2006;38:667–676. doi: 10.1016/j.ympev.2005.07.011. PubMed DOI
Müller K. SeqState - primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinformatics. 2005;4:65–69. doi: 10.2165/00822942-200504010-00008. PubMed DOI
Swofford DL. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates; 2003.
Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. doi: 10.1093/bioinformatics/17.8.754. PubMed DOI
Ronquist F, Huelsenbeck JP. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. doi: 10.1093/bioinformatics/btg180. PubMed DOI
Nylander JAA. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University; 2004.
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. doi: 10.1093/molbev/msm092. PubMed DOI
Yang Z, Bielawski JP. Statistical methods for detecting molecular adaptation. Trends Ecol Evol. 2000;15:496–503. doi: 10.1016/S0169-5347(00)01994-7. PubMed DOI PMC
Liberles DA. Evaluation of methods for determination of a reconstructed history of gene sequence evolution. Mol Biol Evol. 2001;18:2040–2047. PubMed
Bergen Center for Computational Science Ka/Ks Calculation tool. http://services.cbu.uib.no/tools/kaks/
Tajima F. Simple methods for testing molecular clock hypothesis. Genetics. 1993;135:599–607. PubMed PMC
Schwarzacher T, Heslop-Harrison P. Practical In Situ Hybridization. Oxford: BIOS Scientific Publishers; 2002.
Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV. Selection in the evolution of gene duplications. Genome Biol. 2002;3:research0008.1–0008.9. doi: 10.1186/gb-2002-3-2-research0008. PubMed DOI PMC
Mason-Gamer RJ, Burns MM, Naum M. Reticulate Evolutionary History of a Complex Group of Grasses: Phylogeny of Elymus StStHH Allotetraploids Based on Three Nuclear Genes. PLoS ONE. 2010;5:e10989. doi: 10.1371/journal.pone.0010989. PubMed DOI PMC
Small RL, Cronn RC, Wendel JF. Use of nuclear genes for phylogeny reconstruction in plants. Aust Syst Bot. 2004;17:145–170. doi: 10.1071/SB03015. DOI
Gradzielewska A. The genus Dasypyrum - part 1. The taxonomy and relationships within Dasypyrum and with Triticeae species. Euphytica. 2006;152:429–440. doi: 10.1007/s10681-006-9232-2. DOI
Galasso I, Blanco A, Katsiotis A, Pignone D, Heslop-Harrison JS. Genomic organization and phylogenetic relationships in the genus Dasypyrum analysed by Southern and in situ hybridization of total genomic and cloned DNA probes. Chromosoma. 1997;106:53–61. doi: 10.1007/s004120050224. PubMed DOI
Ohta S, Morishita M. Genome relationships in the genus Dasypyrum (Gramineae) Hereditas. 2001;135:101–110. PubMed
Yang ZJ, Liu C, Feng J, Li GR, Zhou JP, Deng KJ, Ren ZL. Studies on genome relationship and species-specific PCR marker for Dasypyrum breviaristatum in Triticeae. Hereditas. 2006;143:47–54. doi: 10.1111/j.2006.0018-0661.01930.x. PubMed DOI
Uslu E, Reader SM, Miller TE. Characterization of Dasypyrum villosum (L.) Candargy chromosomes by fluorescent in situ hybridization. Hereditas. 1999;131:129–134.
Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science. 2000;290:1151–1155. doi: 10.1126/science.290.5494.1151. PubMed DOI
Szczepaniak M, Cieślak E, Bednarek PT. Natural hybridization between Elymus repens and Elymus hispidus assessed by AFLP analysis. Acta Soc Bot Pol. 2007;76:225–234.
Wang RRC. Genome analysis of Thinopyrum bessarabicum and T. elongatum. Can J Genet Cytol. 1985;27:722–728.
Wang RRC, Hsiao C. Genome relationship between Thinopymm bessarabicum and T. elongatum: revisited. Genome. 1989;32:802–809. doi: 10.1139/g89-514. DOI
Jauhar PP. Dilemma of genome relationship in the diploid species Thinopyrum bessarabicum and Thinopyrum elongatum (Triticeae: Poaceae) Genome. 1990;33:944–946. doi: 10.1139/g90-143. PubMed DOI
Mason-Gamer RJ. Origin of North American species of Elymus (Poaceae: Triticeae) allotetraploids based on granule-bound starch synthase gene sequences. Syst Bot. 2001;26:757–768.
Sharma HC, Gill BS. New hybrids between Agropyron and wheat. 2. Production, morphology and cytogenetic analysis of F1 hybrids and backcross derivatives. Theor Appl Genet. 1983;66:111–121. PubMed
Sharma H, Ohm H, Goulart L, Lister R, Appels R, Benlhabib O. Introgression and characterization of barley yellow dwarf virus resistance from Thinopyrum intermedium into wheat. Genome. 1995;38:406–413. doi: 10.1139/g95-052. PubMed DOI
Franke R, Nestrowicz R, Senula A, Staat B. Intergeneric hybrids between Triticum aestivum L. and wild Triticeae. Hereditas. 1992;116:225–231.
Chen Q, Conner RL, Laroche A, Ahmad F. Molecular cytogenetic evidence for a high level of chromosome pairing among different genomes in Triticum aestivum-Thinopyrum intermedium hybrids. Theor Appl Genet. 2001;102:847–852. doi: 10.1007/s001220000496. DOI
Hegde SG, Waines JG. Hybridization and introgression between bread wheat and wild and weedy relatives in North America. Crop Sci. 2004;44:1145–1155. doi: 10.2135/cropsci2004.1145. DOI
Mahelka V. Response to flooding intensity in Elytrigia repens, E. intermedia (Poaceae: Triticeae) and their hybrid. Weed Res. 2006;46:82–90. doi: 10.1111/j.1365-3180.2006.00490.x. DOI
Stebbins GL. Taxonomy and the evolution of genera, with special reference to the family Gramineae. Evolution. 1956;10:235–245. doi: 10.2307/2406009. DOI
Kellogg EA, Appels R, Mason-Gamer RJ. When gene trees tell different stories: the diploid genera of Triticeae. Syst Bot. 1996;21:312–347.
Morrell PL, Lundy KE, Clegg MT. Distinct geographic patterns of genetic diversity are maintained in wild barley (Hordeum vulgare ssp. spontaneum) despite migration. Proc Natl Acad Sci USA. 2003;100:10812–10817. doi: 10.1073/pnas.1633708100. PubMed DOI PMC
Domon E, Saito A, Takeda K. Comparison of the waxy locus sequence from a non-waxy strain and two waxy mutants of spontaneous and artificial origins in barley. Genes Genet Syst. 2002;77:351–359. doi: 10.1266/ggs.77.351. PubMed DOI
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. doi: 10.3732/ajb.0800345. PubMed DOI
Jakob SS, Martinez-Meyer E, Blattner FR. Phylogeographic analyses and paleodistribution modeling indicate pleistocene in situ survival of Hordeum species (Poaceae) in southern Patagonia without genetic or spatial restriction. Mol Biol Evol. 2009;26:907–923. doi: 10.1093/molbev/msp012. PubMed DOI