Intraspecific sequence comparisons reveal similar rates of non-collinear gene insertion in the B and D genomes of bread wheat

. 2012 Aug 30 ; 12 () : 155. [epub] 20120830

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu srovnávací studie, časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid22935214

BACKGROUND: Polyploidization is considered one of the main mechanisms of plant genome evolution. The presence of multiple copies of the same gene reduces selection pressure and permits sub-functionalization and neo-functionalization leading to plant diversification, adaptation and speciation. In bread wheat, polyploidization and the prevalence of transposable elements resulted in massive gene duplication and movement. As a result, the number of genes which are non-collinear to genomes of related species seems markedly increased in wheat. RESULTS: We used new-generation sequencing (NGS) to generate sequence of a Mb-sized region from wheat chromosome arm 3DS. Sequence assembly of 24 BAC clones resulted in two scaffolds of 1,264,820 and 333,768 bases. The sequence was annotated and compared to the homoeologous region on wheat chromosome 3B and orthologous loci of Brachypodium distachyon and rice. Among 39 coding sequences in the 3DS scaffolds, 32 have a homoeolog on chromosome 3B. In contrast, only fifteen and fourteen orthologs were identified in the corresponding regions in rice and Brachypodium, respectively. Interestingly, five pseudogenes were identified among the non-collinear coding sequences at the 3B locus, while none was found at the 3DS locus. CONCLUSION: Direct comparison of two Mb-sized regions of the B and D genomes of bread wheat revealed similar rates of non-collinear gene insertion in both genomes with a majority of gene duplications occurring before their divergence. Relatively low proportion of pseudogenes was identified among non-collinear coding sequences. Our data suggest that the pseudogenes did not originate from insertion of non-functional copies, but were formed later during the evolution of hexaploid wheat. Some evidence was found for gene erosion along the B genome locus.

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Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408:796–815. doi: 10.1038/35048692. PubMed DOI

International Brachypodium Initiative. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature. 2010;463:763–768. doi: 10.1038/nature08747. PubMed DOI

Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Ri AD, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S. et al.The genome of the domesticated apple (Malus x domestica Borkh.) Nat Genet. 2010;42:833–839. doi: 10.1038/ng.654. PubMed DOI

Devos KM, Dubcovsky J, Dvorak J, Chinoy CN, Gale MD. Structural evolution of wheat chromosomes 4A, 5A, and 7B and its impact on recombination. Theor Appl Genet. 1995;91:282–288. doi: 10.1007/BF00220890. PubMed DOI

Dvorak J, Akhunov ED. Tempos of gene locus deletions and duplications and their relationship to rRecombination rate during diploid and polyploid evolution in the Aegilops-Triticum alliance. Genetics. 2005;171:323–332. doi: 10.1534/genetics.105.041632. PubMed DOI PMC

Feldman M. In: The world wheat book: a history of wheat breeding. Bonjean AP, Angus WJ, editor. Lavoisier Publishing, Paris; 2001. Origin of cultivated wheat; pp. 3–56.

Hanada K, Vallejo V, Nobuta K, Slotkin RK, Lisch D, Meyers BC, Shiu S-H, Jiang N. The functional role of Pack-MULEs in rice inferred from purifying selection and expression profile. Plant Cell. 2009;21:25–38. doi: 10.1105/tpc.108.063206. PubMed DOI PMC

Yang L, Bennetzen JL. Distribution, diversity, evolution, and survival of Helitrons in the maize genome. PNAS. 2009;106:19922–19927. PubMed PMC

Wicker T, Buchmann JP, Keller B. Patching gaps in plant genomes results in gene movement and erosion of colinearity. Genome Res. 2010;20:1229–1237. doi: 10.1101/gr.107284.110. PubMed DOI PMC

Choulet F, Wicker T, Rustenholz C, Paux E, Salse J, Leroy P, Schlub S, Le Paslier M-C, Magdelenat G, Gonthier C, Couloux A, Budak H, Breen J, Pumphrey M, Liu S, Kong X, Jia J, Gut M, Brunel D, Anderson JA, Gill BS, Appels R, Keller B, Feuillet C. Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable elements spaces. Plant Cell. 2010;22:1686–1701. doi: 10.1105/tpc.110.074187. PubMed DOI PMC

Wicker T, Mayer KFX, Gundlach H, Martis M, Steuernagel B, Scholz U, Šimková H, Kubaláková M, Choulet F, Taudien S, Platzer M, Feuillet C, Fahima T, Budak H, Doležel J, Keller B, Stein N. Frequent gene movement and pseudogene evolution is common to the large and complex genomes of wheat, barley, and their relatives. Plant Cell. 2011;23:1706–1718. doi: 10.1105/tpc.111.086629. PubMed DOI PMC

Proost S, Pattyn P, Gerats T, Van de Peer Y. Journey through the past: 150 million years of plant genome evolution. Plant J. 2011;66:58–65. doi: 10.1111/j.1365-313X.2011.04521.x. PubMed DOI

Lai J, Ma J, Swigoňová Z, Ramakrishna W, Linton E, Llaca V, Tanyolac B, Park Y-J, Jeong O-Y, Bennetzen JL, Messing J. Gene loss and movement in the maize genome. Genome Res. 2004;14:1924–1931. doi: 10.1101/gr.2701104. PubMed DOI PMC

Chang PL, Dilkes BP, McMahon M, Comai L, Nuzhdin SV. Homoeolog-specific retention and use in allotetraploid Arabidopsis suecica depends on parent of origin and network partners. Genome Biol. 2010;11:R125. doi: 10.1186/gb-2010-11-12-r125. PubMed DOI PMC

Koh J, Soltis PS, Soltis DE. Homeolog loss and expression changes in natural populations of the recently and repeatedly formed allotetraploid Tragopogon mirus (Asteraceae) BMC Genomics. 2010;11:97. doi: 10.1186/1471-2164-11-97. PubMed DOI PMC

Doležel J, Kubaláková M, Paux E, Bartoš J, Feuillet C. Chromosome-based genomics in the cereals. Chromosome Res. 2007;15:51–66. doi: 10.1007/s10577-006-1106-x. PubMed DOI

Vrána J, Kubaláková M, Simková H, Cíhalíková J, Lysák MA, Dolezel J. Flow sorting of mitotic chromosomes in common wheat (Triticum aestivum L.) Genetics. 2000;156:2033–2041. PubMed PMC

Kubaláková M, Vrána J, Číhalíková J, Šimková H, Doležel J. Flow karyotyping and chromosome sorting in bread wheat ( Triticum aestivum L.) Theor Appl Genet. 2002;104:1362–1372. doi: 10.1007/s00122-002-0888-2. PubMed DOI

Šafář J, Šimková H, Kubaláková M, Číhalíková J, Suchánková P, Bartoš J, Doležel J. Development of chromosome-specific BAC resources for genomics of bread wheat. Cytogenet Genome Res. 2010;129:211–223. doi: 10.1159/000313072. PubMed DOI

Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kianian S, Spielmeyer W, Lagudah E, Somers D, Kilian A, Alaux M, Vautrin S, Bergès H, Eversole K, Appels R, Safar J, Simkova H, Dolezel J, Bernard M, Feuillet C. A physical map of the 1-gigabase bread wheat chromosome 3B. Science. 2008;322:101–104. doi: 10.1126/science.1161847. PubMed DOI

Paux E, Legeai F, Guilhot N, Adam-Blondon A-F, Alaux M, Salse J, Sourdille P, Leroy P, Feuillet C. Physical mapping in large genomes: accelerating anchoring of BAC contigs to genetic maps through in silico analysis. Funct Integr Genomics. 2007;8:29–32. PubMed

Sambrook J, Fritsch E, Maniatis T. Molecular Cloning: A Laboratory Manual. 2. Cold Spring Harbor Laboratory Press, NY; 1989.

Leroy P, Guilhot N, Choulet F, Theil S, Flutre T, Seidel M, Alaux M, Tanaka T, Itoh T, Feuillet C. TriAnnot: a versatile and high performance pipeline for the automated annotation of plant genomes. Front. 2012;3:5. PubMed PMC

Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream M-A, Barrell B. Artemis: sequence visualization and annotation. Bioinformatics. 2000;16:944–945. doi: 10.1093/bioinformatics/16.10.944. PubMed DOI

Sonnhammer ELL, Durbin R. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene. 1995;167:GC1–GC10. doi: 10.1016/0378-1119(95)00714-8. PubMed DOI

Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8:973–982. doi: 10.1038/nrg2165. PubMed DOI

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res. 1997;25:3389–3402. doi: 10.1093/nar/25.17.3389. PubMed DOI PMC

Wu TD, Watanabe CK. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics. 2005;21:1859–1875. doi: 10.1093/bioinformatics/bti310. PubMed DOI

Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR. The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res. 2007;35:D883–D887. doi: 10.1093/nar/gkl976. PubMed DOI PMC

Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG, Parkhill J. ACT: the Artemis comparison tool. Bioinformatics. 2005;21:3422–3423. doi: 10.1093/bioinformatics/bti553. PubMed DOI

Shahmuradov IA, Solovyev VV, Gammerman AJ. Plant promoter prediction with confidence estimation. Nucl. 2005;33:1069–1076. doi: 10.1093/nar/gki247. PubMed DOI PMC

González VM, Benjak A, Hénaff EM, Mir G, Casacuberta JM, Garcia-Mas J, Puigdomènech P. Sequencing of 6.7 Mb of the melon genome using a BAC pooling strategy. BMC Plant Biol. 2010;10:246. doi: 10.1186/1471-2229-10-246. PubMed DOI PMC

Rounsley S, Marri PR, Yu Y, He R, Sisneros N, Goicoechea JL, Lee SJ, Angelova A, Kudrna D, Luo M, Affourtit J, Desany B, Knight J, Niazi F, Egholm M, Wing RA. De novo next generation sequencing of plant genomes. Rice. 2009;2:35–43. doi: 10.1007/s12284-009-9025-z. DOI

Akhunov E, Akhunova A, Dvorak J. BAC libraries of Triticum urartu, Aegilops speltoides and Ae. tauschii, the diploid ancestors of polyploid wheat. Theor Appl Genet. 2005;111:1617–1622. doi: 10.1007/s00122-005-0093-1. PubMed DOI

You FM, Huo N, Deal KR, Gu YQ, Luo M-C, McGuire PE, Dvorak J, Anderson OD. Annotation-based genome-wide SNP discovery in the large and complex Aegilops tauschii genome using next-generation sequencing without a reference genome sequence. BMC Genomics. 2011;12:59. doi: 10.1186/1471-2164-12-59. PubMed DOI PMC

Rustenholz C, Choulet F, Laugier C, Safar J, Simkova H, Dolezel J, Magni F, Scalabrin S, Cattonaro F, Vautrin S, Bellec A, Berges H, Feuillet C, Paux E. A 3,000-loci transcription map of chromosome 3B unravels the structural and functional features of gene islands in hexaploid wheat. Plant Physiol. 2011;157:1596–1608. doi: 10.1104/pp.111.183921. PubMed DOI PMC

Bolot S, Abrouk M, Masood-Quraishi U, Stein N, Messing J, Feuillet C, Salse J. The “inner circle” of the cereal genomes. Curr Opin Plant Biol. 2009;12:119–125. doi: 10.1016/j.pbi.2008.10.011. PubMed DOI

Massa AN, Wanjugi H, Deal KR, O’Brien K, You FM, Maiti R, Chan AP, Gu YQ, Luo MC, Anderson OD, Rabinowicz PD, Dvorak J, Devos KM. Gene space dynamics during the evolution of Aegilops tauschii, Brachypodium distachyon, Oryza sativa, and Sorghum bicolor genomes. Mol Biol Evol. 2011;28:2537–2547. doi: 10.1093/molbev/msr080. PubMed DOI PMC

Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC. et al.The Sorghum bicolor genome and the diversification of grasses. Nature. 2009;457:551–556. doi: 10.1038/nature07723. PubMed DOI

Vogel JP, Garvin DF, Mockler TC. et al.Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature. 2010;463:763–768. doi: 10.1038/nature08747. PubMed DOI

Baucom RS, Estill JC, Chaparro C, Upshaw N, Jogi A, Deragon J-M, Westerman RP, SanMiguel PJ, Bennetzen JL. Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet. 2009;5:e1000732. doi: 10.1371/journal.pgen.1000732. PubMed DOI PMC

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. PNAS. 2002;99:8133–8138. doi: 10.1073/pnas.072223799. PubMed DOI PMC

Brunner S, Keller B, Feuillet C. A large rearrangement involving genes and low-copy DNA interrupts the microcollinearity between rice and barley at the Rph7 locus. Genetics. 2003;164:673–683. PubMed PMC

Kumar S, Mohan A, Balyan HS, Gupta PK. Orthology between genomes of Brachypodium, wheat and rice. BMC Research Notes. 2009;2:93. doi: 10.1186/1756-0500-2-93. PubMed DOI PMC

Flagel L, Udall J, Nettleton D, Wendel J. Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol. 2008;6:16. doi: 10.1186/1741-7007-6-16. PubMed DOI PMC

Yang L, Takuno S, Waters ER, Gaut BS. Lowly expressed genes in Arabidopsis thaliana bear the signature of possible pseudogenization by promoter degradation. Mol Biol Evol. 2011;28:1193–1203. doi: 10.1093/molbev/msq298. PubMed DOI

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