Differential gene expression and alternative splicing between diploid and tetraploid watermelon

Journal of Experimental Botany

Volumn 66, Issue 5, 2015, Pages 1369-1385

  Saminathan, Thangasamy ^a   Nimmakayala, Padma ^a   Manohar, Sumanth ^a   Malkaram, Sridhar ^a   Almeida, Aldo ^a   Cantrell, Robert ^a   Tomason, Yan ^a   Abburi, Lavanya ^a   Rahman, Mohammad A ^a   Vajja, Venkata G ^a   Khachane, Amit ^b   Kumar, Brajendra ^b   Rajasimha, Harsha K ^b   Levi, Amnon ^c   Wehner, Todd ^d   Reddy, Umesh K ^a  

^a WEST VIRGINIA STATE UNIVERSITY   (United States)

^b Genome International Corporation   (United States)

^c USDA ARS US Vegetable Laboratory   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Alternative splicing; Gene expression; Genome duplication; RACE PCR; RNA seq; Tetraploid; Watermelon (Citrullus lanatus)

Indexed keywords

CITRULLUS LANATUS; CITRULLUS LANATUS VAR. LANATUS;

PLANT PROTEIN;

ALTERNATIVE RNA SPLICING; CITRULLUS; COMPARATIVE STUDY; DIPLOIDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; TETRAPLOIDY;

ALTERNATIVE SPLICING; CITRULLUS; DIPLOIDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; PLANT PROTEINS; TETRAPLOIDY;

EID: 84924368511     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru486     Document Type: Article

References (75)

1. Ahmad I, Hussain T, Nafees M, et al. 2013. Morphological dissimilarity between tetraploid and diploid watermelon (Citrullus lanatus Thunb.). World Applied Sciences Journal 21, 858-861.
2. Albertin W, Brabant P, Catrice O, Eber F, Jenczewski E, Chevre AM, Thiellement H. 2005. Autopolyploidy in cabbage (Brassica oleracea L.) does not alter significantly the proteomes of green tissues. Proteomics 5, 2131-2139.
3. Andrus CF, Seshadri VS, Grimball PC. 1971. Production of seedless watermelons. Agricultural Research Service, Technical Bulletin , Vol. 1425: US Department of Agriculture.
4. Barbazuk WB, Fu Y, McGinnis KM. 2008. Genome-wide analyses of alternative splicing in plants: opportunities and challenges. Genome Research 18, 1381-1392.
5. Bennett MD. 1977. The time and duration of meiosis. Philosophical Transactions of the Royal Society B: Biological Sciences 277, 201-226.
6. Berget SM, Moore C, Sharp PA. 1977. Spliced segments at the 5' terminus of adenovirus 2 late mRNA. Proceedings of the National Academy of Sciences, USA 74, 3171-3175.
7. Buggs RJA, Doust AN, Tate JA, Koh J, Soltis K, Feltus FA, Paterson AH, Soltis PS, Soltis DE. 2009. Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids. Heredity (Edinburgh) 103, 73-81.
8. Cavalier-Smith T. 2005. Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Annals of Botany 95, 147-175.
9. Chapple C. 1998. Molecular-genetic analysis of plant cytochrome P450-dependent monooxygenases. Annual Review of Plant Physiology and Plant Molecular Biology 49, 311-343.
10. Chen ZJ, Ni Z. 2006. Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. Bioessays 28, 240-252.
11. Chen ZJ. 2007. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review of Plant Biology 58, 377-406.
12. Chettoor A, Givan S, Cole R, Coker C, Unger-Wallace E, Vejlupkova Z, Vollbrecht E, Fowler J, Evans M. 2014. Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes. Genome Biol 15, 414.
13. Coate JE, Bar H, Doyle JJ. 2014. Extensive translational regulation of gene expression in an allopolyploid (Glycine dolichocarpa). Plant Cell 26, 136-150.
14. Coate JE, Doyle JJ. 2010. Quantifying whole transcriptome size, a prerequisite for understanding transcriptome evolution across species: an example from a plant allopolyploid. Genome Biology and Evolution 2, 534-546.
15. Comai L. 2000. Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12, 1551-1568.
16. Comai L. 2005. The advantages and disadvantages of being polyploid. Nature Reviews Genetics 6, 836-846.
17. de Hoon MJ, Imoto S, Nolan J, Miyano S. 2004. Open source clustering software. Bioinformatics 20, 1453-1454.
18. Dinesh-Kumar SP, Baker BJ. 2000. Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proceedings of the National Academy of Sciences, USA 97, 1908-1913.
19. Dolezel J, Bartos J. 2005. Plant DNA flow cytometry and estimation of nuclear genome size. Annals of Botany 95, 99-110.
20. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF. 2008. Evolutionary genetics of genome merger and doubling in plants. Annual Review of Genetics 42, 443-461.
21. Feldman M, Levy AA. 2009. Genome evolution in allopolyploid wheat-a revolutionary reprogramming followed by gradual changes. Journal of Genetics and Genomics 36, 511-518.
22. Flagel L, Udall J, Nettleton D, Wendel J. 2008. Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biology 6, 16.
23. Gaeta RT, Yoo SY, Pires JC, Doerge RW, Chen ZJ, Osborn TC. 2009. Analysis of gene expression in resynthesized Brassica napus allopolyploids using Arabidopsis 70mer oligo microarrays. PLoS One 4, e4760.
24. Grabowski P. 2002. Alternative splicing in parallel. Nature Biotechnology 20, 346-347.
25. Gu Z, Rifkin SA, White KP, Li WH. 2004. Duplicate genes increase gene expression diversity within and between species. Nature Genetics 36, 577-579.
26. Guo M, Davis D, Birchler JA. 1996. Dosage effects on gene expression in a maize ploidy series. Genetics 142, 1349-1355.
27. Guo S, Zhang J, Sun H, et al. 2013. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nature Genetics 45, 51-58.
28. Hu Z-L, Bao J, Reecy JM. 2008. CateGOrizer: A web-based program to batch analyze gene ontology classification categories. Online Journal of Bioinformatics 9, 108-112.
29. Ilut DC, Coate JE, Luciano AK, Owens TG, May GD, Farmer A, Doyle JJ. 2012. A comparative transcriptomic study of an allotetraploid and its diploid progenitors illustrates the unique advantages and challenges of RNA-seq in plant species. American Journal of Botany 99, 383-396.
30. Jackson S, Chen ZJ. 2010. Genomic and expression plasticity of polyploidy. Current Opinion in Plant Biology 13, 153-159.
31. Jegu T, Latrasse D, Delarue M, Hirt H, Domenichini S, Ariel F, Crespi M, Bergounioux C, Raynaud C, Benhamed M. 2014. The BAF60 subunit of the SWI/SNF chromatin-remodeling complex directly controls the formation of a gene loop at FLOWERING LOCUS C in Arabidopsis. Plant Cell 26, 538-551.
32. Kashkush K, Feldman M, Levy AA. 2002. Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160, 1651-1659.
33. Keren H, Lev-Maor G, Ast G. 2010. Alternative splicing and evolution: diversification, exon definition and function. Nature Reviews Genetics 11, 345-355.
34. Kirhara H. 1951. Triploid watermelons. Proceedings of the American Society for Horticultural Science 58, 217-230.
35. Koh J, Chen S, Zhu N, Yu F, Soltis PS, Soltis DE. 2012. Comparative proteomics of the recently and recurrently formed natural allopolyploid Tragopogon mirus (Asteraceae) and its parents. New Phytologist 196, 292-305.
36. Krishnaswami R, Andal R. 1978. Stomatal chloroplast number in diploids and polyploids of Gossypium. Proceedings of the Indian Academy of Sciences 87, 109-112.
37. Langham RJ, Walsh J, Dunn M, Ko C, Goff SA, Freeling M. 2004. Genomic duplication, fractionation and the origin of regulatory novelty. Genetics 166, 935-945.
38. Liu L, Missirian V, Zinkgraf M, Groover A, Filkov V. 2014. Evaluation of experimental design and computational parameter choices affecting analyses of ChIP-seq and RNA-seq data in undomesticated poplar trees. BMC Genomics 15, S3.
39. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-C T method. Methods 25, 402-408.
40. Madlung A, Masuelli RW, Watson B, Reynolds SH, Davison J, Comai L. 2002. Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids. Plant Physiology 129, 733-746.
41. Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y. 2005. Modeling gene and genome duplications in eukaryotes. Proceedings of the National Academy of Sciences, USA 102, 5454-5459.
42. Mittelsten Scheid O, Jakovleva L, Afsar K, Maluszynska J, Paszkowski J. 1996. A change of ploidy can modify epigenetic silencing. Proceedings of the National Academy of Sciences, USA 93, 7114-7119.
43. Nam J, Kaufmann K, Theissen G, Nei M. 2005. A simple method for predicting the functional differentiation of duplicate genes and its application to MIKC-type MADS-box genes. Nucleic Acids Research 33, e12.
44. Ng DW, Zhang C, Miller M, Shen Z, Briggs SP, Chen ZJ. 2012. Proteomic divergence in Arabidopsis autopolyploids and allopolyploids and their progenitors. Heredity (Edinb) 108, 419-430.
45. Noh J, Sheikh S, Chon HG, Seong MH, Lim JH, Lee SG, Jung GT, Kim JM, Ju H-J, Huh YC. 2012. Screening different methods of tetraploid induction in watermelon [Citrullus lanatus (thunb.) Manst. and Nakai]. Horticulture, Environment, and Biotechnology 53, 521-529.
46. Rastogi S, Liberles DA. 2005. Subfunctionalization of duplicated genes as a transition state to neofunctionalization. BMC Evolutionary Biology 5, 28.
47. Reddy AS, Marquez Y, Kalyna M, Barta A. 2013. Complexity of the alternative splicing landscape in plants. Plant Cell 25, 3657-3683.
48. Reddy UK, Nimmakayala P, Levi A, et al. 2014. High-resolution genetic map for understanding the effect of genome-wide recombination rate on nucleotide diversity in watermelon. G3 (Bethesda) pii: g3.114.012815.
49. Remy E, Cabrito TR, Baster P, Batista RA, Teixeira MC, Friml J, Sa-Correia I, Duque P. 2013. A major facilitator superfamily transporter plays a dual role in polar auxin transport and drought stress tolerance in Arabidopsis. Plant Cell 25, 901-926.
50. Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, Stacey G, Doerge RW, Jackson SA. 2013. The fate of duplicated genes in a polyploid plant genome. Plant Journal 73, 143-153.
51. Saldanha AJ. 2004. Java Treeview-extensible visualization of microarray data. Bioinformatics 20, 3246-3248.
52. Severin A, Woody J, Bolon Y-T, et al. 2010. RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10, 160.
53. Staiger D, Brown JW. 2013. Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell 25, 3640-3656.
54. Syed NH, Kalyna M, Marquez Y, Barta A, Brown JWS. 2012. Alternative splicing in plants-coming of age. Trends in Plant Science 17, 616-623.
55. Tack D, Darracq A, Adams KL. 2014. Abstract W629: Reshaped patterns of alternative splicing after allopolyploidy in Brassica napus. In Plant and Animal Genome XXII , 11-15 January, San Diego, CA, USA.
56. Thakare D, Yang R, Steffen JG, Zhan J, Wang D, Clark RM, Wang X, Yadegari R. 2014. RNA-Seq analysis of laser-capture microdissected cells of the developing central starchy endosperm of maize. Genomics Data 2, 242-245.
57. Thangasamy S, Chen PW, Lai MH, Chen J, Jauh GY. 2012. Rice LGD1 containing RNA binding activity affects growth and development through alternative promoters. Plant Journal 71, 288-302.
58. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111.
59. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28, 511-515.
60. Udall JA, Swanson JM, Nettleton D, Percifield RJ, Wendel JF. 2006. A novel approach for characterizing expression levels of genes duplicated by polyploidy. Genetics 173, 1823-1827.
61. Veron AS, Kaufmann K, Bornberg-Bauer E. 2007. Evidence of interaction network evolution by whole-genome duplications: a case study in MADS-box proteins. Molecular Biology and Evolution 24, 670-678.
62. Vitulo N, Forcato C, Carpinelli EC, et al. 2014. A deep survey of alternative splicing in grape reveals changes in the splicing machinery related to tissue, stress condition and genotype. BMC Plant Biology 14, 99.
63. Walters B, Lum G, Sablok G, Min XJ. 2013. Genome-wide landscape of alternative splicing events in Brachypodium distachyon. DNA Research 20, 163-171.
64. Wang J, Tian L, Lee HS, et al. 2006. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172, 507-517.
65. Wang L, Cao C, Ma Q, et al. 2014. RNA-seq analyses of multiple meristems of soybean: novel and alternative transcripts, evolutionary and functional implications. BMC Plant Biology 14, 169.
66. Wang Y, Wang X, Paterson AH. 2012. Genome and gene duplications and gene expression divergence: a view from plants. Annals of the New York Academy of Sciences 1256, 1-14.
67. Wang Z, Gerstein M, Snyder M. 2009. RNA-Seq: a revolutionary tool for transcriptomics. Nature Reviews Genetics 10, 57-63.
68. Wu HP, Su YS, Chen HC, Chen YR, Wu CC, Lin WD, Tu SL. 2014. Genome-wide analysis of light-regulated alternative splicing mediated by photoreceptors in Physcomitrella patens. Genome Biology 15, R10.
69. Yang X, Zhang H, Li L. 2012. Alternative mRNA processing increases the complexity of microRNA-based gene regulation in Arabidopsis. Plant Journal 70, 421-431.
70. Yao H, Kato A, Mooney B, Birchler J. 2011. Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43. Plant Molecular Biology 75, 237-251.
71. Zahn LM, Kong H, Leebens-Mack JH, Kim S, Soltis PS, Landherr LL, Soltis DE, Depamphilis CW, Ma H. 2005. The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. Genetics 169, 2209-2223.
72. Zhang X, Deng M, Fan G. 2014. Differential transcriptome analysis between Paulownia fortunei and its synthesized autopolyploid. International Journal of Molecular Sciences 15, 5079-5093.
73. Zhang Z, Kishino H. 2004. Genomic background predicts the fate of duplicated genes: evidence from the yeast genome. Genetics 166, 1995-1999.
74. Zhou J, Lemos B, Dopman EB, Hartl DL. 2011a. Copy-number variation: the balance between gene dosage and expression in Drosophila melanogaster. Genome Biology and Evolution 3, 1014-1024.
75. Zhou R, Moshgabadi N, Adams KL. 2011b. Extensive changes to alternative splicing patterns following allopolyploidy in natural and resynthesized polyploids. Proceedings of the National Academy of Sciences, USA 108, 16122-16127.