Deep-sequencing transcriptome analysis of chilling tolerance mechanisms of a subnival alpine plant, Chorispora bungeana

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Zhao, Zhiguang ^a,b   Tan, Lingling ^a   Dang, Chunyan ^a   Zhang, Hua ^a   Wu, Qingbai ^b   An, Lizhe ^a  

^a LANZHOU UNIVERSITY   (China)

^b Chinese Academy of Sciences ^*  (China)

Author keywords

Alpine plant; Chilling tolerance; Chorispora bungeana; Cold acclimation; Transcriptome

Indexed keywords

ARABIDOPSIS; CHORISPORA BUNGEANA;

TRANSCRIPTOME;

ADAPTATION; ARABIDOPSIS; ARTICLE; BRASSICACEAE; COLD; COMPARATIVE STUDY; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENE REGULATORY NETWORK; GENETICS; HIGH THROUGHPUT SEQUENCING;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; BRASSICACEAE; COLD TEMPERATURE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENE REGULATORY NETWORKS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME;

MLCS; MLOWN;

EID: 84869234101     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-222     Document Type: Article

References (88)

1. Fu XY, Chang JF, An LZ, Zhang MX, Xu SJ, Chen T, Liu YH, Xin H, Wang JH. Association of the cold-hardiness of Chorispora bungeana with the distribution and accumulation of calcium in the cells and tissues. Environ Exp Bot 2006, 55:282-293.
2. Liu YJ, Zhao ZG, Si J, Di CX, Han J, An LZ. Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. Plant Growth Regul 2009, 59:207-214.
3. Shi Y, An L, Zhang M, Huang C, Zhang H, Xu S. Regulation of the plasma membrane during exposure to low temperatures in suspension-cultured cells from a cryophyte (Chorispora bungeana). Protoplasma 2008, 232:173-181. 10.1007/s00709-008-0291-1, 18421547.
4. Guo FX, Zhang MX, Chen Y, Zhang WH, Xu SJ, Wang JH, An LZ. Relation of several antioxidant enzymes to rapid freezing resistance in suspension cultured cells from alpine Chorispora bungeana. Cryobiology 2006, 52:241-250. 10.1016/j.cryobiol.2005.12.001, 16426599.
5. Ding S, Huang CL, Sheng HM, Song CL, Li YB, An LZ. Effect of inoculation with the endophyte Clavibacter sp. strain Enf12 on chilling tolerance in Chorispora bungeana. Physiol Plant 2011, 141:141-151. 10.1111/j.1399-3054.2010.01428.x, 21044086.
6. Wu JM, Zhao ZG, Xing H, Guo HP, Li WX, An LZ, Xu SJ, Chen T. Effects of freezing on plasma membrane H + -ATPase of the callus from Chorispora bungeana. Biol Plant 2007, 51:229-234.
7. Guy CL. Cold accelimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Biol 1990, 41:187-223.
8. Thomashow MF. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Ann Rev Plant Physiol Plant Mol Biol 1999, 50:571-599.
9. Steponkus PL. Cold acclimation of hedera helix: evidence for a two phase process. Plant Physiol 1971, 47:175-180. 10.1104/pp.47.2.175, 365835, 16657589.
10. Koster KL, Lynch DV. Solute accumulation and compartmentation during the cold acclimation of puma rye. Plant Physiol 1992, 98:108-113. 10.1104/pp.98.1.108, 1080156, 16668599.
11. Kamata T, Uemura M. Solute accumulation in heat seedlings during cold acclimation: contribution to increased freezing tolerance. Cryo Letters 2004, 25:311-322.
12. Kushad MM, Yelenosky G. Evaluation of polyamine and proline levels during low temperature acclimation of citrus. Plant Physiol 1987, 84:692-695. 10.1104/pp.84.3.692, 1056652, 16665504.
13. Evert DR, Weiser CJ. Relationship of electrical conductance at two frequencies to cold injury and acclimation in cornus stolonifera Michx. Plant Physiol 1971, 47:204-208. 10.1104/pp.47.2.204, 365842, 16657596.
14. Miller RW, de la Roche I, Pomeroy MK. Structural and functional responses of wheat mitochondrial membranes to growth at low temperatures. Plant Physiol 1974, 53:426-433. 10.1104/pp.53.3.426, 543240, 16658718.
15. Pomeroy MK, Raison JK. Maintenance of membrane fluidity during development of freezing tolerance of winter wheat seedlings. Plant Physiol 1981, 68:382-385. 10.1104/pp.68.2.382, 427495, 16661921.
16. Toivio-Kinnucan MA, Chen HH, Li PH, Stushnoff C. Plasma membrane alterations in callus tissues of tuber-bearing solanum species during cold acclimation. Plant Physiol 1981, 67:478-483. 10.1104/pp.67.3.478, 425709, 16661698.
17. Taulavuori E, Tahkokorpi M, Taulavuori K, Laine K. Anthocyanins and glutathione S-transferase activities in response to low temperature and frost hardening in Vaccinium myrtillus (L.). J Plant Physiol 2004, 161:903-911. 10.1016/j.jplph.2003.12.001, 15384401.
18. Korn M, Peterek S, Mock HP, Heyer AG, Hincha DK. Heterosis in the freezing tolerance, and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance. Plant Cell Environ 2008, 31:813-827. 10.1111/j.1365-3040.2008.01800.x, 2440548, 18284584.
19. Carvallo MA, Pino MT, Jeknic Z, Zou C, Doherty CJ, Shiu SH, Chen TH, Thomashow MF. A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana. J Exp Bot 2011, 62:3807-3819. 10.1093/jxb/err066, 3134341, 21511909.
20. Stockinger EJ, Gilmour SJ, Thomashow MF. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci U S A 1997, 94:1035-1040. 10.1073/pnas.94.3.1035, 19635, 9023378.
21. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 1998, 280:104-106. 10.1126/science.280.5360.104, 9525853.
22. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 1998, 10:1391-1406. 144379, 9707537.
23. Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J. The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression Is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 1999, 119:463-470. 10.1104/pp.119.2.463, 32122, 9952441.
24. Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K. An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem Biophys Res Commun 1998, 250:161-170. 10.1006/bbrc.1998.9267, 9735350.
25. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF. Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 2000, 124:1854-1865. 10.1104/pp.124.4.1854, 59880, 11115899.
26. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF. Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 2009, 21:972-984. 10.1105/tpc.108.063958, 2671710, 19270186.
27. Franklin KA, Whitelam GC. Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 2007, 39:1410-1413. 10.1038/ng.2007.3, 17965713.
28. Dong MA, Farre EM, Thomashow MF. Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc Natl Acad Sci U S A 2011, 108:7241-7246. 10.1073/pnas.1103741108, 3084081, 21471455.
29. Pino MT, Skinner JS, Park EJ, Jeknic Z, Hayes PM, Thomashow MF, Chen TH. Use of a stress inducible promoter to drive ectopic AtCBF expression improves potato freezing tolerance while minimizing negative effects on tuber yield. Plant Biotechnol J 2007, 5:591-604. 10.1111/j.1467-7652.2007.00269.x, 17559519.
30. Benedict C, Skinner JS, Meng R, Chang Y, Bhalerao R, Huner NP, Finn CE, Chen TH, Hurry V. The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant Cell Environ 2006, 29:1259-1272. 10.1111/j.1365-3040.2006.01505.x, 17080948.
31. Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT. Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 2002, 129:1086-1094. 10.1104/pp.003442, 166503, 12114563.
32. Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 2003, 33:751-763. 10.1046/j.1365-313X.2003.01661.x, 12609047.
33. Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 2005, 41:195-211.
34. Fowler S, Thomashow MF. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 2002, 14:1675-1690. 10.1105/tpc.003483, 151458, 12172015.
35. Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF. Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 2001, 127:910-917. 10.1104/pp.010548, 129262, 11706173.
36. Yun KY, Park MR, Mohanty B, Herath V, Xu F, Mauleon R, Wijaya E, Bajic VB, Bruskiewich R, de Los Reyes BG. Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress. BMC Plant Biol 2010, 10:16. 10.1186/1471-2229-10-16, 2826336, 20100339.
37. Greenup AG, Sasani S, Oliver SN, Walford SA, Millar AA, Trevaskis B. Transcriptome analysis of the vernalization response in barley (Hordeum vulgare) seedlings. PLoS One 2011, 6:e17900. 10.1371/journal.pone.0017900, 3052371, 21408015.
38. Zhou D, Zhou J, Meng L, Wang Q, Xie H, Guan Y, Ma Z, Zhong Y, Chen F, Liu J. Duplication and adaptive evolution of the COR15 genes within the highly cold-tolerant Draba lineage (Brassicaceae). Gene 2009, 441:36-44. 10.1016/j.gene.2008.06.024, 18640249.
39. von Meijenfeldt N. Unraveling the cold response in Draba. PhD thesis 2010, The Netherlands: Universiteit van Amsterdam, The Institute for Biodiversity and Ecosystem Dynamics (IBED) and the Swammerdam Institute for Life Sciences (SILS).
40. Archambault A, Stromvik MV. PR-10, defensin and cold dehydrin genes are among those over expressed in Oxytropis (Fabaceae) species adapted to the arctic. Funct Integr Genomics 2011, 11:497-505. 10.1007/s10142-011-0223-6, 3156302, 21499864.
41. Blanc G, Agarkova I, Grimwood J, Kuo A, Brueggeman A, Dunigan DD, Gurnon J, Ladunga I, Lindquist E, Lucas S, et al. The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 2012, 13:R39. 10.1186/gb-2012-13-5-r39, 3446292, 22630137.
42. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29:644-652. 10.1038/nbt.1883, 21572440.
43. Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, et al. TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 2003, 19:651-652. 10.1093/bioinformatics/btg034, 12651724.
44. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009, 25:1966-1967. 10.1093/bioinformatics/btp336, 19497933.
45. Xu DL, Long H, Liang JJ, Zhang J, Chen X, Li JL, Pan ZF, Deng GB, Yu MQ. De novo assembly and characterization of the root transcriptome of Aegilops variabilis during an interaction with the cereal cyst nematode. BMC Genomics 2012, 13:133. 10.1186/1471-2164-13-133, 3439707, 22494814.
46. Nakayama K, Okawa K, Kakizaki T, Honma T, Itoh H, Inaba T. Arabidopsis Cor15am is a chloroplast stromal protein that has cryoprotective activity and forms oligomers. Plant Physiol 2007, 144:513-523. 10.1104/pp.106.094581, 1913801, 17384167.
47. Qiu Q, Ma T, Hu Q, Liu B, Wu Y, Zhou H, Wang Q, Wang J, Liu J. Genome-scale transcriptome analysis of the desert poplar, Populus euphratica. Tree Physiology 2011, 31:452-461. 10.1093/treephys/tpr015, 21427158.
48. Wong MM, Cannon CH, Wickneswari R. Identification of lignin genes and regulatory sequences involved in secondary cell wall formation in Acacia auriculiformis and Acacia mangium via de novo transcriptome sequencing. BMC Genomics 2011, 12:342. 10.1186/1471-2164-12-342, 3161972, 21729267.
49. Maere S, Heymans K, Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 2005, 21:3448-3449. 10.1093/bioinformatics/bti551, 15972284.
50. Ishitani M, Xiong L, Stevenson B, Zhu JK. Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 1997, 9:1935-1949. 157048, 9401119.
51. Yeh S, Moffatt BA, Griffith M, Xiong F, Yang DS, Wiseman SB, Sarhan F, Danyluk J, Xue YQ, Hew CL, et al. Chitinase genes responsive to cold encode antifreeze proteins in winter cereals. Plant Physiol 2000, 124:1251-1264. 10.1104/pp.124.3.1251, 59223, 11080301.
52. Nelson DC, Riseborough JA, Flematti GR, Stevens J, Ghisalberti EL, Dixon KW, Smith SM. Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiol 2009, 149:863-873. 2633839, 19074625.
53. Scott IM, Clarke SM, Wood JE, Mur LA. Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 2004, 135:1040-1049. 10.1104/pp.104.041293, 514138, 15173571.
54. Ding CK, Wang CY, Gross KC, Smith DL. Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 2002, 214:895-901. 10.1007/s00425-001-0698-9, 11941466.
55. Huang X, Li J, Bao F, Zhang X, Yang S. A gain-of-function mutation in the Arabidopsis disease resistance gene RPP4 confers sensitivity to low temperature. Plant Physiol 2010, 154:796-809. 10.1104/pp.110.157610, 2949010, 20699401.
56. Monroy AF, Sangwan V, Dhindsa RS. Low temperature signal transduction during cold acclimation: protein phosphatase 2A as an early target for cold-inactivation. Plant J 1998, 13:653-660.
57. Monroy AF, Sarhan F, Dhindsa RS. Cold-Induced Changes in Freezing Tolerance, Protein Phosphorylation, and Gene Expression (Evidence for a Role of Calcium). Plant Physiol 1993, 102:1227-1235. 158909, 12231898.
58. Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 2004, 15:141-152. 10.1016/j.molcel.2004.06.023, 15225555.
59. Wen JQ, Oono K, Imai R. Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice. Plant Physiol 2002, 129:1880-1891. 10.1104/pp.006072, 166777, 12177502.
60. Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K. Over-expression of a single Ca2 + -dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 2000, 23:319-327. 10.1046/j.1365-313x.2000.00787.x, 10929125.
61. Saijo Y, Kinoshita N, Ishiyama K, Hata S, Kyozuka J, Hayakawa T, Nakamura T, Shimamoto K, Yamaya T, Izui K. A Ca(2+)-dependent protein kinase that endows rice plants with cold- and salt-stress tolerance functions in vascular bundles. Plant Cell Physiol 2001, 42:1228-1233. 10.1093/pcp/pce158, 11726707.
62. Abbasi F, Onodera H, Toki S, Tanaka H, Komatsu S. OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced by cold and gibberellin in rice leaf sheath. Plant Mol Biol 2004, 55:541-552. 10.1007/s11103-004-1178-y, 15604699.
63. Tsai TM, Chen YR, Kao TW, Tsay WS, Wu CP, Huang DD, Chen WH, Chang CC, Huang HJ. PaCDPK1, a gene encoding calcium-dependent protein kinase from orchid, Phalaenopsis amabilis, is induced by cold, wounding, and pathogen challenge. Plant Cell Rep 2007, 26:1899-1908. 10.1007/s00299-007-0389-5, 17593367.
64. Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S. CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 2003, 15:411-423. 10.1105/tpc.006858, 141210, 12566581.
65. Huang C, Ding S, Zhang H, Du H, An L. CIPK7 is involved in cold response by interacting with CBL1 in Arabidopsis thaliana. Plant Sci 2011, 181:57-64. 10.1016/j.plantsci.2011.03.011, 21600398.
66. Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK. The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci U S A 2006, 103:8281-8286. 10.1073/pnas.0602874103, 1472463, 16702557.
67. Michael TP, Salome PA, McClung CR. Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proc Natl Acad Sci U S A 2003, 100:6878-6883. 10.1073/pnas.1131995100, 164540, 12736379.
68. Mikkelsen MD, Thomashow MF. A role for circadian evening elements in cold-regulated gene expression in Arabidopsis. Plant J 2009, 60:328-339. 10.1111/j.1365-313X.2009.03957.x, 19566593.
69. Fowler SG, Cook D, Thomashow MF. Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 2005, 137:961-968. 10.1104/pp.104.058354, 1065397, 15728337.
70. Gerloff ED, Richardson T, Stahmann MA. Changes in Fatty acids of alfalfa roots during cold hardening. Plant Physiol 1966, 41:1280-1284. 10.1104/pp.41.8.1280, 550518, 16656398.
71. Palta JP, Whitaker BD, Weiss LS. Plasma Membrane Lipids Associated with Genetic Variability in Freezing Tolerance and Cold Acclimation of Solanum Species. Plant Physiol 1993, 103:793-803. 159049, 12231980.
72. Williams JP, Khan MU, Mitchell K, Johnson G. The effect of temperature on the level and biosynthesis of unsaturated fatty acids in diacylglycerols of Brassica napus leaves. Plant Physiol 1988, 87:904-910. 10.1104/pp.87.4.904, 1054867, 16666243.
73. Kodama H, Hamada T, Horiguchi G, Nishimura M, Iba K. Genetic enhancement of cold tolerance by expression of a gene for chloroplast [omega]-3 fatty acid desaturase in transgenic tobacco. Plant Physiol 1994, 105:601-605. 159399, 12232227.
74. Nishida I, Murata N. Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 1996, 47:541-568. 10.1146/annurev.arplant.47.1.541, 15012300.
75. Wu J, Zhao Z, An L, Liu Y, Xu S, Gao D, Zhang Y. Inhibition of glutathione synthesis decreases chilling tolerance in Chorispora bungeana callus. Cryobiology 2008, 57:9-17. 10.1016/j.cryobiol.2008.04.001, 18486938.
76. Wang J, An L, Wang R, Yang D, Si J, Fu X, Chang J, Xu S. Plant regeneration of Chorispora bungeana via somatic embryogenesis. In Vitro Cell Dev Biol Plant 2006, 42:148-151.
77. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5:621-628. 10.1038/nmeth.1226, 18516045.
78. Wang L, Feng Z, Wang X, Zhang X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 2010, 26:136-138. 10.1093/bioinformatics/btp612, 19855105.
79. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995, 57:289-300.
80. 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, 20:45-58. 10.1101/gr.093302.109, 2798830, 19858364.
81. Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D'Angelo C, Bornberg-Bauer E, Kudla J, Harter K. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 2007, 50:347-363. 10.1111/j.1365-313X.2007.03052.x, 17376166.
82. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 2004, 20:307-315. 10.1093/bioinformatics/btg405, 14960456.
83. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon 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, 16081474.
84. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L. WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 2006, 34:W293-297. 10.1093/nar/gkl031, 1538768, 16845012.
85. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003, 13:2498-2504. 10.1101/gr.1239303, 403769, 14597658.
86. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3:RESEARCH0034. 126239, 12184808.
87. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 2005, 139:5-17. 10.1104/pp.105.063743, 1203353, 16166256.
88. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45. 10.1093/nar/29.9.e45, 55695, 11328886.