Polyploidy and the petal transcriptome of Gossypium

Springer Science and Business Media LLC - Tập 14 - Trang 1-14 - 2014
Aditi Rambani1, Justin T Page1, Joshua A Udall1
1Plant and Wildlife Science Department, Brigham Young University, Provo, USA

Tóm tắt

Genes duplicated by polyploidy (homoeologs) may be differentially expressed in plant tissues. Recent research using DNA microarrays and RNAseq data have described a cacophony of complex expression patterns during development of cotton fibers, petals, and leaves. Because of its highly canalized development, petal tissue has been used as a model tissue for gene expression in cotton. Recent advances in cotton genome annotation and assembly now permit an enhanced analysis of duplicate gene deployment in petals from allopolyploid cotton. Homoeologous gene expression levels were quantified in diploid and tetraploid flower petals of Gossypium using the Gossypium raimondii genome sequence as a reference. In the polyploid, most homoeologous genes were expressed at equal levels, though a subset had an expression bias of AT and DT copies. The direction of gene expression bias was conserved in natural and recent polyploids of cotton. Conservation of direction of bias and additional comparisons between the diploids and tetraploids suggested different regulation mechanisms of gene expression. We described three phases in the evolution of cotton genomes that contribute to gene expression in the polyploid nucleus. Compared to previous studies, a surprising level of expression homeostasis was observed in the expression patterns of polyploid genomes. Conserved expression bias in polyploid petals may have resulted from cis-acting modifications that occurred prior to polyploidization. Some duplicated genes were intriguing exceptions to general trends. Mechanisms of gene regulation for these and other genes in the cotton genome warrants further investigation.

Tài liệu tham khảo

Wendel JF, Cronn RC: Polyploidy and the evolutionary history of cotton.In Advances in Agronomy. Volume 78. Edited by Sparks D. Newark, NJ, USA:Academic; 2003:139–186. Krapovickas A, Seijo G: Gossypium ekmanianum (Malvaceae), algodon silvestre de la Republica Dominicana. Bonplandia. 2008, 17: 55-63. Grover CE, Grupp KK, Wanzek RJ, Wendel JF: Assessing the monophyly of polyploid Gossypium species. Plant Syst Evol. 2012, 298: 1177-1183. 10.1007/s00606-012-0615-7. Grover CE, Gallagher JP, Szadkowski EP, Yoo MJ, Flagel LE, Wendel JF: Homoeolog expression bias and expression level dominance in allopolyploids. Plant J. 2012, 196: 966-971. Salmon A, Flagel L, Ying B, Udall JA, Wendel JF: Homoeologous nonreciprocal recombination in polyploid cotton. New Phytol. 2010, 186: 123-134. 10.1111/j.1469-8137.2009.03093.x. Chelaifa H, Monnier A, Ainouche M: Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina × townsendii and Spartina anglica (Poaceae). New Phytol. 2010, 186: 161-174. 10.1111/j.1469-8137.2010.03179.x. Qi B, Huang W, Zhu B, Zhong X, Guo J, Zhao N, Xu C, Zhang H, Pang J, Han F, Liu B: Global transgenerational gene expression dynamics in two newly synthesized allohexaploid wheat (Triticum aestivum) lines. BMC Biol. 2012, 10: 3-10.1186/1741-7007-10-3. 2010 8:139 Adams KL, Cronn R, Percifield R, Wendel JF: Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci U S A. 2003, 100: 4649-4654. 10.1073/pnas.0630618100. Udall JA: A novel approach for characterizing expression levels of genes duplicated by polyploidy. Genetics. 2006, 173: 1823-1827. 10.1534/genetics.106.058271. Hovav R, Udall JA, Hovav E, Rapp R, Flagel L, Wendel JF: A majority of cotton genes are expressed in single-celled fiber. Planta. 2007, 227: 319-329. 10.1007/s00425-007-0619-7. Rapp RA, Haigler CH, Flagel L, Hovav RH, Udall JA, Wendel JF: Gene expression in developing fibres of Upland cotton (Gossypium hirsutum L.) was massively altered by domestication. BMC Biol. 2010, 8: 139-10.1186/1741-7007-8-139. Hovav R, Chaudhary B, Udall JA, Flagel L, Wendel JF: Parallel domestication, convergent evolution and duplicated gene recruitment in allopolyploid cotton. Genetics. 2008, 179: 1725-1733. 10.1534/genetics.108.089656. Flagel LE, Wendel JF: Gene duplication and evolutionary novelty in plants. New Phytol. 2009, 183: 557-564. 10.1111/j.1469-8137.2009.02923.x. Dong S, Adams KL: Differential contributions to the transcriptome of duplicated genes in response to abiotic stresses in natural and synthetic polyploids. New Phytol. 2011, 190: 1045-1057. 10.1111/j.1469-8137.2011.03650.x. Degner JF, Marioni JC, Pai AA, Pickrell JK, Nkadori E, Gilad Y, Pritchard JK: Effect of read-mapping biases on detecting allele-specific expression from RNA-sequencing data. Bioinformatics. 2009, 25: 3207-3212. 10.1093/bioinformatics/btp579. McDaniell R, Lee BK, Song L, Liu Z, Boyle AP, Erdos MR, Scott LJ, Morken MA, Kucera KS, Battenhouse A, Keefe D, Collins FS, Willard HF, Lieb JD, Furey TS, Crawford GE, Iyer VR, Birney E: Heritable individual-specific and allele-specific chromatin signatures in humans. Science. 2010, 328: 235-239. 10.1126/science.1184655. Heap GA, Yang JH, Downes K, Healy BC, Hunt KA, Bockett N, Franke L, Dubois PC, Mein CA, Dobson RJ, Albert TJ, Rodesch MJ, Clayton DG, Todd JA, Van Heel DA, Plagnol V: Genome-wide analysis of allelic expression imbalance in human primary cells by high-throughput transcriptome resequencing. Hum Mol Genet. 2010, 19: 122-134. 10.1093/hmg/ddp473. Flagel LE, Wendel JF: Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol. 2010, 186: 184-193. 10.1111/j.1469-8137.2009.03107.x. Yoo MJ, Szadkowski E, Wendel JF: Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity. 2013, 110: 171-180. 10.1038/hdy.2012.94. Flagel L, Udall J, Nettleton D, Wendel JF: Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol. 2008, 6: 16-10.1186/1741-7007-6-16. 2010 8:139. Bottley A, Xia GM, Koebner RMD: Homoeologous gene silencing in hexaploid wheat. Plant J. 2006, 47: 897-906. 10.1111/j.1365-313X.2006.02841.x. Buggs RJA, Chamala S, Wu W, Gao L, May GD, Schnable PS, Soltis DE, Soltis PS, Barbazuk WB: Characterization of duplicate gene evolution in the recent natural allopolyploidTragopogon miscellusby next-generation sequencing and Sequenom iPLEX MassARRAY genotyping. Mol Ecol. 2010, 19: 132-146. 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: 97-10.1186/1471-2164-11-97. Wang J, Tian L, Madlung A, Lee H-S, Chen M, Lee JJ, Watson B, Kagochi T, Comai L, Chen ZJ: Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics. 2004, 167: 1961-1973. 10.1534/genetics.104.027896. Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC: Genomic changes in resynthesized brassica napus and their effect on gene expression and phenotype. Plant Cell. 2007, 19: 3043-3417. Auger DL, Sheridan WF: Plant Chromosomal Deletions, Insertions, and Rearrangements. Plant Cytogenetics. Edited by: Bass HW, Birchler JA. 2011, New York: Springer, 3-36. Rapp RA, Udall JA, Wendel JF: Genomic expression dominance in allopolyploids. BMC Biol. 2009, 7: 18-10.1186/1741-7007-7-18. 2010 8:139 Bardil A, De Almeida JD, Combes MC, Lashermes P, Bertrand B: Genomic expression dominance in the natural allopolyploid Coffea arabica is massively affected by growth temperature. New Phytol. 2011, 192: 760-774. 10.1111/j.1469-8137.2011.03833.x. Osborn TC, Chris Pires J, Birchler JA, Auger DL, Jeffery Chen Z, Lee H-S, Comai L, Madlung A, Doerge RW, Colot V, Martienssen RA: Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 2003, 19: 141-147. 10.1016/S0168-9525(03)00015-5. Costa V, Angelini C, De Feis I, Ciccodicola A: Uncovering the complexity of transcriptomes with RNA-Seq. J Biomed Biotechnol. 2010, 2010: 853916. Wang Z, Gerstein M, Snyder M: RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009, 10: 57-63. 10.1038/nrg2484. Wan CY, Wilkins TA: A modified hot borate method significantly enhances the yield of high-quality RNA from cotton ( gossypium hirsutum L.). Anal Biochem. 1994, 223: 7-12. 10.1006/abio.1994.1538. Wu TD, Nacu S: Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics. 2010, 26: 873-881. 10.1093/bioinformatics/btq057. Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin D, Llewellyn D, Showmaker KC, Shu S, Udall J, Yoo M-J, Byers R, Chen W, Doron-Faigenboim A, Duke MV, Gong L, Grimwood J, Grover C, Grupp K, Hu G, Lee T-H, Li J, Lin L, Liu T, Marler BS, Page JT, Roberts AW, Romanel E, Sanders WS, Szadkowski E, et al: Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature. 2012, 492: 423-427. 10.1038/nature11798. Page JT, Gingle AR, Udall JA: PolyCat: a resource for genome categorization of sequencing reads from allopolyploid organisms. G3: Genes|Genomes|Genetics. 2013, 3: 517-525. Page JT, Huynh MD, Liechty ZS, Grupp K, Stelly DM, Hulse AM, Ashrafi H, Van Deynze A, Wendel JF, Udall JA: Insights into the evolution of cotton diploids and polyploids from whole-genome re-sequencing. G3: Genes|Genomes|Genetics. 2013, 3: 1809-1818. Piccolo SR, Sun Y, Campbell JD, Lenburg ME, Bild AH, Johnson WE: A single-sample microarray normalization method to facilitate personalized-medicine workflows. Genomics. 2012, 100: 337-344. 10.1016/j.ygeno.2012.08.003. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005, 21: 3674-3676. 10.1093/bioinformatics/bti610. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M: KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 2011, 40: D109-D114. Robinson MD, McCarthy DJ, Smyth GK: EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010, 26: 139-140. 10.1093/bioinformatics/btp616. Flagel LE, Wendel JF, Udall JA: Duplicate gene evolution, homoeologous recombination, and transcriptome characterization in allopolyploid cotton. BMC Genomics. 2012, 13: 1-1. 10.1186/1471-2164-13-1. Tanase K, Nishitani C, Hirakawa H, Isobe S, Tabata S, Ohmiya A, Onozaki T: Transcriptome analysis of carnation (Dianthus caryophyllus L.) based on next-generation sequencing technology. BMC Genomics. 2012, 13: 292-10.1186/1471-2164-13-292. Li H, Dong Y, Yang J, Liu X, Wang Y, Yao N, Guan L, Wang N, Wu J, Li X: De novo transcriptome of safflower and the identification of putative genes for oleosin and the biosynthesis of flavonoids. PLoS ONE. 2012, 7: e30987-10.1371/journal.pone.0030987. Senchina DS, Alverez I, Cronn RC, Liu B, Rong J, Noyes RD, Paterson AH, Wing RA, Wilkins TA, Wendel JF: Rate variation among nuclear genes and the age of polyploidy in gossypium. Mol Biol Evol. 2003, 20: 633-643. 10.1093/molbev/msg065. Madlung A, Wendel JF: Genetic and epigenetic aspects of polyploid evolution in plants. Cytogenet Genome Res. 2013, 140: 270-285. 10.1159/000351430. Udall JA: A global assembly of cotton ESTs. Genome Res. 2006, 16: 441-450. 10.1101/gr.4602906. Studer A, Zhao Q, Ross-Ibarra J, Doebley J: Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Publ Group. 2011, 43: 1160-1163. Hovav R, Udall JA, Chaudhary B, Hovav E, Flagel L, Hu G, Wendel JF: The evolution of spinnable cotton fiber entailed prolonged development and a novel metabolism. PLoS Genet. 2008, 4: e25-10.1371/journal.pgen.0040025. Betancur L, Singh B, Rapp RA, Wendel JF, Marks MD, Roberts AW, Haigler CH: Phylogenetically distinct cellulose synthase genes support secondary wall thickening in arabidopsis shoot trichomes and cotton fiber. J Integr Plant Biol. 2010, 52: 205-220. 10.1111/j.1744-7909.2010.00934.x. Muhlemann JK, Maeda H, Chang CY, San Miguel P, Baxter I, Cooper B, Perera MA, Nikolau BJ, Vitek O, Morgan JA: Developmental changes in the metabolic network of snapdragon flowers. PLoS ONE. 2012, 7: e40381-10.1371/journal.pone.0040381. Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF: Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res. 2006, 16: 1252-1261. 10.1101/gr.5282906. Freeling M, Woodhouse MR, Subramaniam S: Fractionation mutagenesis and similar consequences of mechanisms removing dispensable or less-expressed DNA in plants. Curr Opin Plant Biology. 2012, 15: 131-139. 10.1016/j.pbi.2012.01.015. Hawkins JS, Proulx SR, Rapp RA, Wendel JF: Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants. Proc Natl Acad Sci U S A. 2009, 106: 17811-17816. 10.1073/pnas.0904339106. Tucker S, Vitins A, Pikaard CS: Nucleolar dominance and ribosomal RNA gene silencing. Curr Opin Cell Biol. 2010, 22: 351-356. 10.1016/j.ceb.2010.03.009. Preuss SB, Costa-Nunes P, Tucker S, Pontes O, Lawrence RJ, Mosher R, Kasschau KD, Carrington JC, Baulcombe DC, Viegas W, Pikaard CS: Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol Cell. 2008, 32: 673-684. 10.1016/j.molcel.2008.11.009. Liu B, Brubaker CL, Mergeai G, Cronn RC, Wendel JF: Polyploid formation in cotton is not accompanied by rapid genomic changes. 2001, 44: 321-330.