The low-recombining pericentromeric region of barley restricts gene diversity and evolution but not gene expression

Plant Journal

Volumn 79, Issue 6, 2014, Pages 981-992

  Baker, Katie ^a   Bayer, Micha ^b   Cook, Nicola ^a,e   Dreißig, Steven ^c   Dhillon, Taniya ^a   Russell, Joanne ^b   Hedley, Pete E ^b   Morris, Jenny ^b   Ramsay, Luke ^b   Colas, Isabelle ^b   Waugh, Robbie ^a,b   Steffenson, Brian ^d   Milne, Iain ^b   Stephen, Gordon ^b   Marshall, David ^b   Flavell, Andrew J ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

barley; genome evolution; heterochromatin; Hordeum vulgare; pericentromeric

Indexed keywords

NUCLEIC ACIDS;

BARLEY; GENOME EVOLUTION; HETEROCHROMATIN; HORDEUM VULGARE; PERICENTROMERIC;

GENE EXPRESSION;

HETEROCHROMATIN;

GENE DUPLICATION; GENE EXPRESSION; GENE ONTOLOGY; GENETIC RECOMBINATION; GENETIC VARIATION; GENETICS; HETEROCHROMATIN; HORDEUM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT GENOME; SEQUENCE ANALYSIS;

BASE SEQUENCE; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION; GENE ONTOLOGY; GENETIC VARIATION; GENOME, PLANT; HETEROCHROMATIN; HORDEUM; MOLECULAR SEQUENCE DATA; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, RNA;

EID: 84907018247     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12600     Document Type: Article

References (62)

1. Begun, D.J., and, Aquadro, C.F., (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature, 356, 519-520.
2. Berchowitz, L.E., Hanlon, S.E., Lieb, J.D., and, Copehnaver, G.P., (2009) A positive but complex association between meiotic double-strand break hotspots and open chromatin in Saccharomyces cerevisiae. Genome Res. 19, 2245-2257.
3. Carchilan, M., Delgado, M., Ribeiro, T., Costa-Nunes, P., Caperta, A., Morais-Cecílio, L., Jones, R.N., Viegas, W., and, Houben, A., (2007) Transcriptionally active heterochromatin in rye B chromosomes. Plant Cell, 19, 1738-1749.
4. Charlesworth, B., Betancourt, A.J., Kaiser, V.B., and, Gordo, I., (2009) Genetic recombination and molecular evolution. Cold Spring Harbor Symp. Quant. Biol. 74, 1-10.
5. Chen, J., Huang, Q., Gao, D., et al. (2013) Whole-genome sequencing of Oryza brachyantha reveals mechanisms underlying Oryza genome evolution. Nat. Commun. 4, 1595.
6. Choo, K.H.A., (1998) Why is the centromere so cold? Genome Res. 8, 81-82.
7. Close, T.J., Bhat, P.R., Lonardi, S., et al. (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics, 10, 582.
8. Comadran, J., Kilian, B., Russell, J., et al. (2012) Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat. Genet. 44, 1388-1392.
9. Conesa, A., Götz, S., García-Gõmez, J.M., Terol, J., Talõn, M., and, Robles, M., (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674-3676.
10. Druka, A., Muehlbauer, G., Druka, I., et al. (2006) An atlas of gene expression from seed to seed through barley development. Funct. Integr. Genomics, 6, 202-211.
11. Drummond, A.J., Ashton, B., Buxton, S., et al. (2011). Geneious v6.1.6 created by Biomatters. Available from http://www.geneious.com/
12. Du, Z., Zhou, X., Ling, Y., Zhang, Z., and, Su, Z., (2010) AgriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64-W70.
13. Du, J., Zhixi, T., Sui, Y., Zhao, M., Song, Q., Cannon, S.B., Cregan, P., and, Ma, J., (2012) Pericentromeric effects shape the patterns of divergence, retention, and expression of duplicated genes in the paleopolyploid soybean. Plant Cell, 24, 21-32.
14. Fu, H., Zheng, Z., and, Dooner, H.K., (2002) Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude. Proc. Natl Acad. Sci. USA, 99, 1082-1087.
15. Gent, J.I., Dong, Y., Jiang, J., and, Dawe, R.K., (2012) Strong epigenetic similarity between maize centromeric and pericentromeric regions at the level of small RNAs, DNA methylation and H3 chromatin modifications. Nucleic Acids Res. 40, 1550-1560.
16. Hall, L.E., Mitchell, S.E., and, O'Neill, R.J., (2012) Pericentric and centromeric transcription: a perfect balance required. Chromosome Res. 20, 535-546.
17. Hammer, Ø., Harper, D.A.T., and, Ryan, P.D., (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4, 9.
18. Higgins, J.D., Perry, R.M., Barakate, A., Ramsay, L., Waugh, R., Halpin, C., Armstrong, S.J., and, Franklin, F.C.H., (2012) Spatiotemporal asymmetry of the meiotic program underlies the predominantly distal distribution of meiotic crossovers in barley. Plant Cell, 24, 4096-4109.
19. Houben, A., Demidov, D., Gernand, D., Meister, A., Leach, C.R., and, Schubert, I., (2003) Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. Plant J. 33, 967-973.
20. Hudson, R.R., (1994) How can the low levels of DNA sequence variation in regions of the Drosophila genome with low recombination be explained? Proc. Natl Acad. Sci. USA, 91, 6815-6818.
21. Huo, N., Garvin, D.F., You, F.M., McMahon, S., Luo, M.-C., Gu, Y.Q., Lazo, G.R., and, Vogel, J.P., (2011) Comparison of a high-density genetic linkage map to genome features in the model grass Brachypodium distachyon. Theor. Appl. Genet. 123, 455-464.
22. IBM Corp. (2012) IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY: IBM Corp.
23. International Barley Genome Sequencing Consortium (IBGSC) (2012) A physical, genetic, and functional sequence assembly of the barley genome. Nature, 491, 711-716.
24. Jost, K.L., Bertulat, B., and, Cardoso, M.C., (2012) Heterochromatin and gene positioning: inside, outside, any side? Chromosoma, 121, 555-563.
25. Kim, J.S., Islam-Faridi, M.N., Klein, P.E., Stelly, D.M., Price, H.J., Klein, R.R., and, Mullet, J.E., (2005) Comprehensive molecular cytogenetic analysis of sorghum genome architecture: distribution of euchromatin, heterochromatin, genes and recombination in comparison to rice. Genetics, 171, 1963-1976.
26. Krzywinski, M.I., Schein, J.E., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S.J., and, Marra, M.A., (2009) Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645.
27. Langmead, B., Trapnell, C., Pop, M., and, Salzberg, S.L., (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25.
28. Lippman, Z., Gendrel, A.V., Black, M., et al. (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature, 430, 471-476.
29. Luo, M.C., Deal, K.R., Akhunov, E.D., et al. (2009) Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae. Proc. Natl Acad. Sci. USA, 106, 15780-15785.
30. Lynch, M., and, Conery, J.S., (2000) The evolutionary fate and consequences of duplicate genes. Science, 290, 1151-1155.
31. Matsumoto, T., Tanaka, T., Sakai, H., et al. (2011) Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol. 156, 20-28.
32. Mayer, K.F.X., Martis, M., Hedley, P.E., et al. (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell, 23, 1249-1263.
33. Milne, I., Stephen, G., Bayer, M., Cock, P.J.A., Pritchard, L., Cardle, L., Shaw, P.D., and, Marshall, D., (2013) Using Tablet for visual exploration of second-generation sequencing data. Brief. Bioinform. 142, 193-202.
34. Nordborg, M., Hu, T.T., Ishino, Y., et al. (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, e196.
35. Okonechnikov, K., Golosova, O., and, Fursov, M., (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics, 28, 1166-1167.
36. Paterson, A.H., Bowers, J.E., Bruggman, R., et al. (2009) The Sorghum bicolor genome and the diversification of the grasses. Nature, 457, 551-556.
37. Prlic, A., Yates, A., Bliven, S.E., et al. (2012) BioJava: an open- source framework for bioinformatics. Bioinformatics, 28, 2693-2695.
38. Rizzon, C., Ponger, L., and, Gaut, B.S., (2006) Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Comput. Biol. 2, e115.
39. Salse, J., Bolot, S., Throude, M., Jouffe, V., Piegu, B., Quraishi, U.M., Calcagno, T., Cooke, R., Delseny, M., and, Feuillet, C., (2008) Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell, 20, 11-24.
40. Sato, K., Shin, I.T., Shinozaki, K., Takeda, Y., Yamazaki, Y., Conte, M., and, Kohara, Y., (2009) Development of 5006 full-length cDNAs in barley: a tool for accessing cereal genomics resources. DNA Res. 16, 81-89.
41. Schmutz, J., Cannon, S.B., Schlueter, J., et al. (2010) Genome sequence of the paleopolyploid soybean. Nature, 463, 178-183.
42. Schnable, P.S., Ware, D., Fulton, R.S., et al. (2009) The B73 Maize genome: complexity, diversity and dynamics. Science, 326, 1112-1115.
43. Schnable, J.C., Springer, N.M., and, Freeling, M., (2011) Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc. Natl Acad. Sci. USA, 108, 4069-4074.
44. Schnable, J.C., Freeling, M., and, Lyons, E., (2012) Genome-wide analysis of syntenic gene deletion in the grasses. Genome Biol. Evol. 4, 265-277.
45. Shi, J., and, Dawe, R.K., (2006) Partitioning of the maize epigenome by the number of methyl groups on histone H3 lysines 9 and 27. Genetics, 173, 1571-1583.
46. Steffenson, B.J., Olivera, P., Roy, J.K., Yue, A., Jin, B., Smith, K.P., and, Muehlbauer, G.J., (2007) A walk on the wild side: mining wild wheat and barley collections for rust resistance genes. Aust. J. Agric. Res. 58, 532-544.
47. Thiel, T., Graner, A., Waugh, R., Grosse, I., Close, T.J., and, Stein, N., (2009) Evidence and evolutionary analysis of ancient whole-genome duplication in barley predating the divergence from rice. BMC Evol. Biol. 9, 209.
48. Thomas, B.C., Pederson, B.S., and, Freeling, M., (2006) Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res. 16, 934-946.
49. Tian, Z., Rizzon, C., Du, J., Zhu, L., Bennetzen, J.L., Jackson, S.A., Gaut, B.S., and, Ma, J., (2009) Do genetic recombination and gene density shape the pattern of DNA elimination in rice long terminal repeat retrotransposons? Genome Res. 19, 2221-2230.
50. Wang, Y., Tang, H., DeBarry, J.D., et al. (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 407, e49.
51. Wicker, T., Buchmann, J.P., and, Keller, B., (2010) Patching gaps in plant genomes results in gene movement and erosion of colinearity. Genome Res. 20, 1229-1237.
52. Wicker, T., Mayer, K.F.X., Gundlach, H., et al. (2011) Frequent gene movement and pseudogene evolution is common to the large and complex genomes of wheat, barley and their relatives. Plant Cell, 23, 1706-1718.
53. Wolfe, K.H., (2000) Robustness-it's not where you think it is. Nat. Genet. 25, 3-4.
54. Wolfe, K.H., (2001) Yesterday's polyploids and the mystery of diploidization. Nat. Rev. Genet. 2, 333-341.
55. Woodhouse, M.R., Schnable, J.C., Pederson, B.S., Lyons, E., Lisch, D., Subramaniam, S., and, Freeling, M., (2010) Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of two homeologs. PLoS Biol. 8, e10000409.
56. Wright, S.I., Foxe, J.P., DeRose-Wilson, L., Kawabe, A., Looseley, M., Gaut, B.S., and, Charlesworth, D., (2006) Testing for effects of recombination rate on nucleotide diversity in natural populations of Arabidopsis lyrata. Genetics, 174, 1421-1430.
57. Wu, Y., Kikuchi, S., Yan, H., Zhang, W., Rosenbaum, H., Iniguez, L., and, Jiang, J., (2011) Euchromatic subdomains in rice centromeres are associated with genes and transcription. Plant Cell, 23, 4054-4064.
58. Yang, Z., (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591.
59. Yang, L., and, Gaut, B.S., (2011) Factors that contribute to variation in evolutionary rate among Arabidopsis genes. Mol. Biol. Evol. 28, 2359-2369.
60. Yang, J., Gu, Z., and, Li, W.H., (2003) Rate of protein evolution versus fitness effect of gene deletion. Mol. Biol. Evol. 20, 772-774.
61. Yin, B.L., Guo, L., Zhan, D.F., Terzaghi, W., Wang, X.F., Liu, T.T., Hea, H., Cheng, Z.K., and, Deng, X.W., (2008) Integration of cytological features with molecular and epigenetic properties of rice chromosome 4. Mol. Plant, 1, 816-829.
62. Zhang, L., and, Gaut, B.S., (2003) Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome? Genome Res. 13, 2533-2540.