RNA-seq analyses of multiple meristems of soybean: Novel and alternative transcripts, evolutionary and functional implications

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Wang, Lei ^a   Cao, Chenlong ^a   Ma, Qibin ^b   Zeng, Qiaoying ^b   Wang, Haifeng ^a   Cheng, Zhihao ^a   Zhu, Genfeng ^a   Qi, Ji ^a   Ma, Hong ^a   Nian, Hai ^b   Wang, Yingxiang ^a  

^a FUDAN UNIVERSITY   (China)

^b SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Alternative splicing; Meristem; Novel transcriptional regions; RNA seq; Soybean; Transcription factors; Transcriptome

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ALTERNATIVE RNA SPLICING; ANTIBODY SPECIFICITY; DNA MICROARRAY; DUPLICATE GENE; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MERISTEM; METABOLISM; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PLANT GENE; PROCEDURES; SEQUENCE ANALYSIS; SOYBEAN;

ALTERNATIVE SPLICING; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, DUPLICATE; GENES, PLANT; MERISTEM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; SOYBEANS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84902301794     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-169     Document Type: Article

References (88)

1. Shoemaker RC, Schlueter J, Doyle JJ. Paleopolyploidy and gene duplication in soybean and other legumes. Curr Opin Plant Biol 2006, 9(2):104-109.
2. Lam HM, Xu X, Liu X, Chen W, Yang G, Wong FL, Li MW, He W, Qin N, Wang B, Li J, Jian M, Wang J, Shao G, Wang J, Sun SS, Zhang G. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 2010, 42(12):1053-1059.
3. Findley SD, Cannon S, Varala K, Du J, Ma J, Hudson ME, Birchler JA, Stacey G. A fluorescence in situ hybridization system for karyotyping soybean. Genetics 2010, 185(3):727-744.
4. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, et al. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463(7278):178-183.
5. Libault M, Farmer A, Joshi T, Takahashi K, Langley RJ, Franklin LD, He J, Xu D, May G, Stacey G. An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J 2010, 63(1):86-99.
6. Schlueter JA, Lin JY, Schlueter SD, Vasylenko-Sanders IF, Deshpande S, Yi J, O'Bleness M, Roe BA, Nelson RT, Scheffler BE, Jackson SA, Shoemaker RC. Gene duplication and paleopolyploidy in soybean and the implications for whole genome sequencing. BMC Genomics 2007, 8:330.
7. Gill N, Findley S, Walling JG, Hans C, Ma J, Doyle J, Stacey G, Jackson SA. Molecular and chromosomal evidence for allopolyploidy in soybean. Plant Physiol 2009, 151(3):1167-1174.
8. Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, Stacey G, Doerge RW, Jackson SA. The fate of duplicated genes in a polyploid plant genome. Plant J 2012, 73(1):143-153.
9. Du J, Tian Z, Hans CS, Laten HM, Cannon SB, Jackson SA, Shoemaker RC, Ma J. Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J 2010, 63(4):584-598.
10. Sultan M, Schulz MH, Richard H, Magen A, Klingenhoff A, Scherf M, Seifert M, Borodina T, Soldatov A, Parkhomchuk D, Schmidt D, O'Keeffe S, Haas S, Vingron M, Lehrach H, Yaspo ML. A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 2008, 321(5891):956-960.
11. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009, 10(1):57-63.
12. Martin JA, Wang Z. Next-generation transcriptome assembly. Nat Rev Genet 2011, 12(10):671-682.
13. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 2008, 320(5881):1344-1349.
14. Aanes H, Winata CL, Lin CH, Chen JP, Srinivasan KG, Lee SG, Lim AY, Hajan HS, Collas P, Bourque G, Gong Z, Korzh V, Alestrom P, Mathavan S. Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition. Genome Res 2011, 21(8):1328-1338.
15. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, Brown JB, Cherbas L, Davis CA, Dobin A, Li R, Lin W, Malone JH, Mattiuzzo NR, Miller D, Sturgill D, Tuch BB, Zaleski C, Zhang D, Blanchette M, Dudoit S, Eads B, Green RE, Hammonds A, Jiang L, Kapranov P, et al. The developmental transcriptome of Drosophila melanogaster. Nature 2011, 471(7339):473-479.
16. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456(7221):470-476.
17. Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong WK, Mockler TC. Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 2010, 20(1):45-58.
18. Jiao Y, Tausta SL, Gandotra N, Sun N, Liu T, Clay NK, Ceserani T, Chen M, Ma L, Holford M, Zhang HY, Zhao H, Deng XW, Nelson T. A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies. Nat Genet 2009, 41(2):258-263.
19. Lu T, Lu G, Fan D, Zhu C, Li W, Zhao Q, Feng Q, Zhao Y, Guo Y, Li W, Huang X, Han B. Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res 2010, 20(9):1238-1249.
20. Marquez Y, Brown JWS, Simpson C, Barta A, Kalyna M. Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 2012, 22(6):1184-1195.
21. Yang H, Lu P, Wang Y, Ma H. The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J 2011, 65(4):503-516.
22. Zhang GJ, Guo GW, Hu XD, Zhang Y, Li QY, Li RQ, Zhuang RH, Lu ZK, He ZQ, Fang XD, Chen L, Tian W, Tao Y, Kristiansen K, Zhang XQ, Li SG, Yang HM, Wang J, Wang J. Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Res 2010, 20(5):646-654.
23. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, Reidel EJ, Turgeon R, Liu P, Sun Q, Nelson T, Brutnell TP. The developmental dynamics of the maize leaf transcriptome. Nat Genet 2010, 42(12):1060-1067.
24. Krasileva KV, Buffalo V, Bailey P, Pearce S, Ayling S, Tabbita F, Soria M, Wang S, Akhunov E, Uauy C, Dubcovsky J. Separating homeologs by phasing in the tetraploid wheat transcriptome. Genome Biol 2013, 14(6):R66.
25. Kang C, Darwish O, Geretz A, Shahan R, Alkharouf N, Liu Z. Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. Plant Cell 2013, 25(6):1960-1978.
26. Liew LC, Singh MB, Bhalla PL. An RNA-seq transcriptome analysis of histone modifiers and RNA silencing genes in soybean during floral initiation process. PLoS One 2013, 8(10):e77502.
27. Severin AJ, Woody JL, Bolon YT, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE, Graham MA, Cannon SB, May GD, Vance CP, Shoemaker RC. RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 2010, 10:160.
28. Yang H, Zhou Y, Gu J, Xie S, Xu Y, Zhu G, Wang L, Huang J, Ma H, Yao J. Deep mRNA sequencing analysis to capture the transcriptome landscape of zebrafish embryos and larvae. PLoS One 2013, 8(5):e64058.
29. Wang Y, Xiao R, Wang H, Cheng Z, Li W, Zhu G, Ma H. The Arabidopsis RAD51 paralogs RAD51B, RAD51D and XRCC2 play partially redundant roles in somatic DNA repair and gene regulation. New Phytol 2014, 201(1):292-304.
30. Libault M, Farmer A, Brechenmacher L, Drnevich J, Langley RJ, Bilgin DD, Radwan O, Neece DJ, Clough SJ, May GD, Stacey G. Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiol 2010, 152(2):541-552.
31. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5(7):621-628.
32. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 2008, 18(9):1509-1517.
33. Taylor JS, Raes J. Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 2004, 38:615-643.
34. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I, Penkett CJ, Rogers J, Bahler J. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 2008, 453(7199):1239-1243.
35. Lister R, O'Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 2008, 133(3):523-536.
36. Cloonan N, Forrest ARR, Kolle G, Gardiner BBA, Faulkner GJ, Brown MK, Taylor DF, Steptoe AL, Wani S, Bethel G, Robertson AJ, Perkins AC, Bruce SJ, Lee CC, Ranade SS, Peckham HE, Manning JM, McKernan KJ, Grimmond SM. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods 2008, 5(7):613-619.
37. Morin R, Bainbridge M, Fejes A, Hirst M, Krzywinski M, Pugh T, McDonald H, Varhol R, Jones S, Marra M. Profiling the HeLa S3 transcriptome using randomly primed cDNA and massively parallel short-read sequencing. Biotechniques 2008, 45(1):81-94.
38. Durbak AR, Tax FE. CLAVATA signaling pathway receptors of Arabidopsis regulate cell proliferation in fruit organ formation as well as in meristems. Genetics 2011, 189(1):177-194.
39. Su Z, Wang J, Yu J, Huang X, Gu X. Evolution of alternative splicing after gene duplication. Genome Res 2006, 16(2):182-189.
40. Shen Y, Zhou Z, Wang Z, Li W, Fang C, Wu M, Ma Y, Liu T, Kong L-A, Peng DL. Global dissection of alternative splicing in paleopolyploid soybean. Plant Cell 2014, 26(3):996-1008.
41. Katz Y, Wang ET, Airoldi EM, Burge CB. Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nat Methods 2010, 7(12):1009-1015.
42. Sugimoto K, Jiao Y, Meyerowitz EM. Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 2010, 18(3):463-471.
43. He C, Chen X, Huang H, Xu L. Reprogramming of H3K27me3 is critical for acquisition of pluripotency from cultured Arabidopsis tissues. PLoS Genet 2012, 8(8):e1002911.
44. Rogers ED, Jackson T, Moussaieff A, Aharoni A, Benfey PN. Cell type-specific transcriptional profiling: implications for metabolite profiling. Plant J 2012, 70(1):5-17.
45. Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Maree AF, Scheres B. Root system architecture from coupling cell shape to auxin transport. PLoS Biol 2008, 6(12):e307.
46. Zhao Y. Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 2010, 61:49-64.
47. Mravec J, Skupa P, Bailly A, Hoyerova K, Krecek P, Bielach A, Petrasek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerova K, Rolcik J, Seifertova D, Luschnig C, Benkova E, Zazimalova E, Geisler M, Friml J. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 2009, 459(7250):1136-1140.
48. Ding Z, Wang B, Moreno I, Duplakova N, Simon S, Carraro N, Reemmer J, Pencik A, Chen X, Tejos R, Skupa P, Pollmann S, Mravec J, Petrasek J, Zazimalova E, Honys D, Rolcik J, Murphy A, Orellana A, Geisler M, Friml J. ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat Commun 2012, 3:941.
49. Motchoulski A, Liscum E. Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. Science 1999, 286(5441):961-964.
50. Haerizadeh F, Wong CE, Singh MB, Bhalla PL. Genome-wide analysis of gene expression in soybean shoot apical meristem. Plant Mol Biol 2009, 69(6):711-727.
51. Jung C-H, Wong CE, Singh MB, Bhalla PL. Comparative genomic analysis of soybean flowering genes. PLoS One 2012, 7(6):e38250.
52. Dreni L, Pilatone A, Yun D, Erreni S, Pajoro A, Caporali E, Zhang D, Kater MM. Functional analysis of all AGAMOUS subfamily members in rice reveals their roles in reproductive organ identity determination and meristem determinacy. Plant Cell 2011, 23(8):2850-2863.
53. Dorca-Fornell C, Gregis V, Grandi V, Coupland G, Colombo L, Kater MM. The Arabidopsis SOC1-like genes AGL42, AGL71 and AGL72 promote flowering in the shoot apical and axillary meristems. Plant J 2011, 67(6):1006-1017.
54. Shani E, Yanai O, Ori N. The role of hormones in shoot apical meristem function. Curr Opin Plant Biol 2006, 9(5):484-489.
55. Cheng Y, Dai X, Zhao Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 2006, 20(13):1790-1799.
56. Vanneste S, Friml J. Auxin: a trigger for change in plant development. Cell 2009, 136(6):1005-1016.
57. Yang X, Makaroff CA, Ma H. The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell 2003, 15(6):1281-1295.
58. Novillo F, Alonso JM, Ecker JR, Salinas J. CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci U S A 2004, 101(11):3985-3990.
59. Su Z, Ma X, Guo H, Sukiran NL, Guo B, Assmann SM, Ma H. Flower development under drought stress: morphological and transcriptomic analyses reveal acute responses and long-term acclimation in Arabidopsis. Plant Cell 2013, 25(10):3785-3807.
60. Blackmore S, Wortley AH, Skvarla JJ, Rowley JR. Pollen wall development in flowering plants. New Phytol 2007, 174(3):483-498.
61. Yang WC, Shi DQ, Chen YH. Female gametophyte development in flowering plants. Annu Rev Plant Biol 2010, 61:89-108.
62. Spencer WC, Zeller G, Watson JD, Henz SR, Watkins KL, McWhirter RD, Petersen S, Sreedharan VT, Widmer C, Jo J, Reinke V, Petrella L, Strome S, Von Stetina SE, Katz M, Shaham S, Ratsch G, Miller DM. A spatial and temporal map of C. elegans gene expression. Genome Res 2011, 21(2):325-341.
63. Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C. Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 2008, 407(1):1-11.
64. Salinas M, Xing S, Höhmann S, Berndtgen R, Huijser P. Genomic organization, phylogenetic comparison and differential expression of the SBP-box family of transcription factors in tomato. Planta 2012, 235(6):1171-1184.
65. Preston JC, Hileman LC. Functional evolution in the plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family. Front Plant Sci 2013, 4:80.
66. Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ. Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 2008, 18(10):758-762.
67. Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T. SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 2009, 21(1):347-361.
68. Unte US, Sorensen A-M, Pesaresi P, Gandikota M, Leister D, Saedler H, Huijser P. SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 2003, 15(4):1009-1019.
69. Cho SH, Coruh C, Axtell MJ. miR156 and miR390 regulate tasiRNA accumulation and developmental timing in Physcomitrella patens. Plant Cell 2012, 24(12):4837-4849.
70. Stone JM, Liang X, Nekl ER, Stiers JJ. Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 2005, 41(5):744-754.
71. Bäurle I, Dean C. The timing of developmental transitions in plants. Cell 2006, 125(4):655-664.
72. Martin RC, Asahina M, Liu P-P, Kristof JR, Coppersmith JL, Pluskota WE, Bassel GW, Goloviznina NA, Nguyen TT, Martínez-Andújar C. The regulation of post-germinative transition from the cotyledon-to vegetative-leaf stages by microRNA-targeted SQUAMOSA PROMOTERNNNBINDING PROTEIN LIKE13 in Arabidopsis. Seed Sci Res 2010, 20(02):89-96.
73. Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P. The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 2008, 67(1-2):183-195.
74. Alvarez-Buylla ER, Benítez M, Corvera-Poiré A, Cador T, De Folter S, Gamboa de Buen A, Garay-Arroyo A, García-Ponce B, Jaimes-Miranda F, V R, Pérez-Ruiz RV, Piñeyro-Nelson A, Sánchez-Corralesa YE. Flower development. Arabidopsis Book 2010, 8:e0127.
75. Reed JW. Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci 2001, 6(9):420-425.
76. Sundberg E, Ostergaard L. Distinct and dynamic auxin activities during reproductive development. Cold Spring Harb Perspect Biol 2009, 1(6):a001628.
77. Paz MM, Shou H, Guo Z, Zhang Z, Banerjee AK, Wang K. Assessment of conditions affecting Agrobacterium-mediated soybean transformation using the cotyledonary node explant. Euphytica 2004, 136(2):167-179.
78. Wang Y, Suo H, Zheng Y, Liu K, Zhuang C, Kahle KT, Ma H, Yan X. The soybean root-specific protein kinase GmWNK1 regulates stress-responsive ABA signaling on the root system architecture. Plant J 2010, 64(2):230-242.
79. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 2001, 25(4):402-408.
80. Feng J, Meyer CA, Wang Q, Liu JS, Liu XS, Zhang Y. GFOLD: a generalized fold change for ranking differentially expressed genes from RNA-seq data. Bioinformatics 2012, 28(21):2782-2788.
81. Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, Lee T-H, Jin H, Marler B, Guo H. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 2012, 40(7):e49-e49.
82. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012, 7(3):562-578.
83. Qi J, Zhao F. inGAP-sv: a novel scheme to identify and visualize structural variation from paired end mapping data. Nucleic Acids Res 2011, 39:W567-W575.
84. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215(3):403-410.
85. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 2005, 33:D121-D124.
86. Kohonen T. Self-organized formation of topologically correct feature maps. Biol Cybern 1982, 43(1):59-69.
87. Du Z, Zhou X, Ling Y, Zhang Z, Su Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 2010, 38:W64-W70.
88. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M. Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004, 37(6):914-939.