A transcriptomic analysis of chrysanthemum nankingense provides insights into the basis of low temperature tolerance

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Ren, Liping ^a,b   Sun, Jing ^a   Chen, Sumei ^a   Gao, Jiaojiao ^a   Dong, Bin ^a   Liu, Yanan ^a   Xia, Xiaolong ^a   Wang, Yinjie ^a   Liao, Yuan ^a   Teng, Nianjun ^a   Fang, Weimin ^a   Guan, Zhiyong ^a   Chen, Fadi ^a,b   Jiang, Jiafu ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b Jiangsu Province Engineering Lab for Modern Facility Agriculture Technology and Equipment   (China)

Author keywords

Low temperature tolerance; Ornamental plant; RNA Sequencing; Transcriptome

Indexed keywords

RNA; TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN SERINE THREONINE KINASE; TRANSCRIPTOME; VEGETABLE PROTEIN;

ARTICLE; CALCIUM SIGNALING; CHRYSANTHEMUM; CHRYSANTHEMUM NANKINGENSE; COLD ACCLIMATIZATION; DOWN REGULATION; FREEZING; LOW TEMPERATURE; NONHUMAN; PHYSICAL TOLERANCE; PLANT LEAF; PLANT STEM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA SEQUENCE; TEMPERATURE TOLERANCE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; UPREGULATION; ADAPTATION; CHROMOSOME MAP; COLD; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; METABOLISM; PLANT GENE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

CHRYSANTHEMUM NANKINGENSE;

ADAPTATION, PHYSIOLOGICAL; CHROMOSOME MAPPING; CHRYSANTHEMUM; COLD TEMPERATURE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENES, PLANT; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PLANT LEAVES; PLANT PROTEINS; PLANT STEMS; PROTEIN-SERINE-THREONINE KINASES; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84908059538     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-844     Document Type: Article

References (73)

1. Liu L, Zhu K, Yang Y, Wu J, Chen F, Yu D. Molecular cloning, expression profiling and trans-activation property studies of a DREB2-like gene from chrysanthemum (Dendranthema vestitum). J Plant Res 2008, 121(2):215-226. 10.1007/s10265-007-0140-x, 18224275.
2. da Silva JA T, Shinoyama H, Aida R, Matsushita Y, Raj SK, Chen F. Chrysanthemum biotechnology: Quo Vadis?. Crit Rev Plant Sci 2013, 32(1):21-52.
3. Cheng X, Chen S, Chen F, Fang W, Deng Y, She L. Interspecific hybrids between Dendranthema morifolium (Ramat.) Kitamura and D. nankingense (Nakai) Tzvel. achieved using ovary rescue and their cold tolerance characteristics. Euphytica 2009, 172(1):101-108.
4. Wang H, Jiang J, Chen S, Qi X, Peng H, Li P, Song A, Guan Z, Fang W, Liao Y. Next-generation sequencing of the Chrysanthemum nankingense (Asteraceae) transcriptome permits large-scale unigene assembly and SSR marker discovery. PLoS One 2013, 8(4):e62293. 10.1371/journal.pone.0062293, 3633874, 23626799.
5. Janská A, Maršík P, Zelenková S, Ovesná J. Cold stress and acclimation-what is important for metabolic adjustment?. Plant Biol 2010, 12(3):395-405. 10.1111/j.1438-8677.2009.00299.x, 20522175.
6. Yang T, Zhang L, Zhang T, Zhang H, Xu S, An L. Transcriptional regulation network of cold-responsive genes in higher plants. Plant Sci 2005, 169(6):987-995.
7. Chinnusamy V, Zhu J, Zhu J-K. Cold stress regulation of gene expression in plants. Trends Plant Sci 2007, 12(10):444-451. 10.1016/j.tplants.2007.07.002, 17855156.
8. Chinnusamy V, Zhu JK, Sunkar R. Gene regulation during cold stress acclimation in plants. Plant Stress Tolerance 2010, 639:39-55.
9. Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 2006, 57:781-803. 10.1146/annurev.arplant.57.032905.105444, 16669782.
10. Heidarvand L, Amiri RM. What happens in plant molecular responses to cold stress?. Acta Physiol Plant 2010, 32(3):419-431.
11. Bohn M, Lüthje S, Sperling P, Heinz E, Dörffling K. Plasma membrane lipid alterations induced by cold acclimation and abscisic acid treatment of winter wheat seedlings differing in frost resistance. J Plant Physiol 2007, 164(2):146-156. 10.1016/j.jplph.2005.12.008, 16500724.
12. Lynch DV, Steponkus PL. Plasma membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiol 1987, 83(4):761-767. 10.1104/pp.83.4.761, 1056446, 16665335.
13. Uemura M, Joseph RA, Steponkus PL. Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol 1995, 109(1):15-30. 157560, 12228580.
14. Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y. Responses of the plasma membrane to low temperatures. Physiol Plant 2006, 126(1):81-89.
15. Komatsu S, Yang G, Khan M, Onodera H, Toki S, Yamaguchi M. Over-expression of calcium-dependent protein kinase 13 and calreticulin interacting protein 1 confers cold tolerance on rice plants. Mol Gen Genomics 2007, 277(6):713-723.
16. 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(3):319-327. 10.1046/j.1365-313x.2000.00787.x, 10929125.
17. Lissarre M, Ohta M, Sato A, Miura K. Cold-responsive gene regulation during cold acclimation in plants. Plant Signal Behav 2010, 5(8):948-952. 10.4161/psb.5.8.12135, 3115169, 20699657.
18. Yang G, Zou H, Wu Y, Liu H, Yuan Y. Identification and characterisation of candidate genes involved in chilling responses in maize (Zea mays L.). Plant Cell, Tissue and Organ Culture (PCTOC) 2011, 106(1):127-141.
19. Thomashow MF. Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 2010, 154(2):571-577. 10.1104/pp.110.161794, 2948992, 20921187.
20. Dong MA, Farré 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 2011, 108(17):7241-7246. 10.1073/pnas.1103741108, 3084081, 21471455.
21. B-h L, Henderson DA, Zhu J-K. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell Online 2005, 17(11):3155-3175.
22. Dong C-H, Agarwal M, Zhang Y, Xie Q, Zhu J-K. 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 2006, 103(21):8281-8286. 10.1073/pnas.0602874103, 1472463, 16702557.
23. Miura K, Ohta M. SIZ1, a small ubiquitin-related modifier ligase, controls cold signaling through regulation of salicylic acid accumulation. J Plant Physiol 2010, 167(7):555-560. 10.1016/j.jplph.2009.11.003, 19959255.
24. Scott IM, Clarke SM, Wood JE, Mur LA. Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 2004, 135(2):1040-1049. 10.1104/pp.104.041293, 514138, 15173571.
25. Zhu J, Dong C-H, Zhu J-K. Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 2007, 10(3):290-295. 10.1016/j.pbi.2007.04.010, 17468037.
26. Ma H, Lu Z, Liu B, Qiu Q, Liu J. Transcriptome analyses of a Chinese hazelnut species Corylus mandshurica. BMC Plant Biol 2013, 13(1):152. 10.1186/1471-2229-13-152, 3819738, 24093758.
27. Hornett EA, Wheat CW. Quantitative RNA-Seq analysis in non-model species: assessing transcriptome assemblies as a scaffold and the utility of evolutionary divergent genomic reference species. BMC Genomics 2012, 13(1):361. 10.1186/1471-2164-13-361, 3469347, 22853326.
28. Wang X-C, Zhao Q-Y, Ma C-L, Zhang Z-H, Cao H-L, Kong Y-M, Yue C, Hao X-Y, Chen L, Ma J-Q. Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC Genomics 2013, 14(1):415. 10.1186/1471-2164-14-415, 3701547, 23799877.
29. Wang H, Zou Z, Wang S, Gong M. Global analysis of transcriptome responses and gene expression profiles to cold stress of Jatropha curcas L. PLoS One 2013, 8(12):e82817. 10.1371/journal.pone.0082817, 3857291, 24349370.
30. Tian D-Q, Pan X-Y, Yu Y-M, Wang W-Y, Zhang F, Ge Y-Y, Shen X-L, Shen F-Q, Liu X-J. De novo characterization of the Anthurium transcriptome and analysis of its digital gene expression under cold stress. BMC Genomics 2013, 14(1):827. 10.1186/1471-2164-14-827, 4046746, 24267953.
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. 10.1038/nmeth.1226, 18516045.
32. Audic S, Claverie J-M. The significance of digital gene expression profiles. Genome Res 1997, 7(10):986-995.
33. Xu L, Zhu L, Tu L, Liu L, Yuan D, Jin L, Long L, Zhang X. Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot 2011, 62(15):5607-5621. 10.1093/jxb/err245, 3223054, 21862479.
34. Reddy AS, Ali GS, Celesnik H, Day IS. Coping with stresses: roles of calcium-and calcium/calmodulin-regulated gene expression. Plant Cell Online 2011, 23(6):2010-2032.
35. Miura K, Furumoto T. Cold signaling and cold response in plants. Int J Mol Sci 2013, 14(3):5312-5337. 10.3390/ijms14035312, 3634503, 23466881.
36. Boudsocq M, Sheen J. CDPKs in immune and stress signaling. Trends Plant Sci 2013, 18(1):30-40. 10.1016/j.tplants.2012.08.008, 3534830, 22974587.
37. Morris ER, Walker JC. Receptor-like protein kinases: the keys to response. Curr Opin Plant Biol 2003, 6(4):339-342. 10.1016/S1369-5266(03)00055-4, 12873528.
38. Lehti-Shiu MD, Zou C, Hanada K, Shiu S-H. Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 2009, 150(1):12-26. 10.1104/pp.108.134353, 2675737, 19321712.
39. McCormack E, Braam J. Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 2003, 159(3):585-598.
40. Xu G-Y, Rocha PS, Wang M-L, Xu M-L, Cui Y-C, Li L-Y, Zhu Y-X, Xia X. A novel rice calmodulin-like gene, OsMSR2, enhances drought and salt tolerance and increases ABA sensitivity in Arabidopsis. Planta 2011, 234(1):47-59. 10.1007/s00425-011-1386-z, 21359958.
41. Hashimoto K, Kudla J. Calcium decoding mechanisms in plants. Biochimie 2011, 93(12):2054-2059. 10.1016/j.biochi.2011.05.019, 21658427.
42. Schulz P, Herde M, Romeis T. Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol 2013, 163(2):523-530. 10.1104/pp.113.222539, 3793034, 24014579.
43. Chen J, Xue B, Xia X, Yin W. A novel calcium-dependent protein kinase gene from Populus euphratica, confers both drought and cold stress tolerance. Biochem Biophys Res Commun 2013, 441(3):630-636. 10.1016/j.bbrc.2013.10.103, 24177011.
44. Singh KB, Foley RC, Oñate-Sánchez L. Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 2002, 5(5):430-436. 10.1016/S1369-5266(02)00289-3, 12183182.
45. Mizoi J, Shinozaki K, Yamaguchi Shinozaki K. AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophysica Acta (BBA)-Gene Regulatory Mechanisms 2012, 1819(2):86-96.
46. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochem Biophys Res Commun 2002, 290(3):998-1009. 10.1006/bbrc.2001.6299, 11798174.
47. Li X, Zhang D, Li H, Wang Y, Zhang Y, Wood AJ. EsDREB2B, a novel truncated DREB2-type transcription factor in the desert legume Eremosparton songoricum, enhances tolerance to multiple abiotic stresses in yeast and transgenic tobacco. BMC Plant Biol 2014, 14(1):44. 10.1186/1471-2229-14-44, 3940028, 24506952.
48. Szabados L, Savouré A. Proline: a multifunctional amino acid. Trends Plant Sci 2010, 15(2):89-97. 10.1016/j.tplants.2009.11.009, 20036181.
49. Kang H-G, Kim J, Kim B, Jeong H, Choi SH, Kim EK, Lee H-Y, Lim PO. Overexpression of FTL1/ DDF1, an AP2 transcription factor, enhances tolerance to cold, drought, and heat stresses in Arabidopsis thaliana. Plant Sci 2011, 180(4):634-641. 10.1016/j.plantsci.2011.01.002, 21421412.
50. Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, Yamane H, Shimono M, Sugano S, Takatsuji H. WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 2013, 64(16):5085-5097. 10.1093/jxb/ert298, 3830488, 24043853.
51. H-h P, Shan W, Kuang J-F, Lu W-J, Chen J-Y. Molecular characterization of cold-responsive basic helix-loop-helix transcription factors MabHLHs that interact with MaICE1 in banana fruit. Planta 2013, 238(5):937-953. 10.1007/s00425-013-1944-7, 23955147.
52. Yang A, Dai X, Zhang W-H. A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 2012, 63(7):2541-2556. 10.1093/jxb/err431, 3346221, 22301384.
53. Kang H, Park SJ, Kwak KJ. Plant RNA chaperones in stress response. Trends Plant Sci 2012, 18(2):100-106.
54. 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 Online 2002, 14(8):1675-1690.
55. Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 2002, 130(4):2129-2141. 10.1104/pp.008532, 166725, 12481097.
56. Lim J, Thomas T, Cavicchioli R. Low temperature regulated DEAD-box RNA helicase from the antarctic archaeon, Methanococcoides burtonii. J Mol Biol 2000, 297(3):553-567. 10.1006/jmbi.2000.3585, 10731411.
57. Chamot D, Owttrim GW. Regulation of cold shock-induced RNA helicase gene expression in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 2000, 182(5):1251-1256. 10.1128/JB.182.5.1251-1256.2000, 94409, 10671444.
58. Kim JS, Kim KA, Oh TR, Park CM, Kang H. Functional characterization of DEAD-box RNA helicases in Arabidopsis thaliana under abiotic stress conditions. Plant Cell Physiol 2008, 49(10):1563-1571. 10.1093/pcp/pcn125, 18725370.
59. Guan Q, Wu J, Zhang Y, Jiang C, Liu R, Chai C, Zhu J. A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell Online 2013, 25(1):342-356.
60. Asakura Y, Galarneau E, Watkins KP, Barkan A, van Wijk KJ. Chloroplast RH3 DEAD box RNA helicases in maize and Arabidopsis function in splicing of specific group II introns and affect chloroplast ribosome biogenesis. Plant Physiol 2012, 159(3):961-974. 10.1104/pp.112.197525, 3387720, 22576849.
61. Karunatilaka KS, Solem A, Pyle AM, Rueda D. Single-molecule analysis of Mss116-mediated group II intron folding. Nature 2010, 467(7318):935-939. 10.1038/nature09422, 20944626.
62. Bhaskaran H, Russell R. Kinetic redistribution of native and misfolded RNAs by a DEAD-box chaperone. Nature 2007, 449(7165):1014-1018. 10.1038/nature06235, 2581903, 17960235.
63. Liu Y, Wang L, Xing X, Sun L, Pan J, Kong X, Zhang M, Li D. ZmLEA3, a multifunctional group 3 LEA protein from maize (Zea mays L.), is involved in biotic and abiotic stresses. Plant Cell Physiol 2013, 54(6):944-959. 10.1093/pcp/pct047, 23543751.
64. Sasaki K, Christov NK, Tsuda S, Imai R. Identification of a novel LEA protein involved in freezing tolerance in wheat. Plant Cell Physiol 2014, 55(1):136-147. 10.1093/pcp/pct164, 24265272.
65. Eriksson SK, Kutzer M, Procek J, Gröbner G, Harryson P. Tunable membrane binding of the intrinsically disordered dehydrin Lti30, a cold-induced plant stress protein. Plant Cell Online 2011, 23(6):2391-2404.
66. Fernández M, Valenzuela S. Isolation, characterization and genes expression analysis of three dehydrin genes during cold acclimation of Eucalyptus globulus. BMC Proceedings 2011, 5(Suppl 7):81.
67. Wang W, Vinocur B, Shoseyov O, Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 2004, 9(5):244-252. 10.1016/j.tplants.2004.03.006, 15130550.
68. Chen B, Zhong D, Monteiro A. Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genomics 2006, 7(1):156. 10.1186/1471-2164-7-156, 1525184, 16780600.
69. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Edgar R, Federhen S, Geer LY, Helmberg W, Kapustin Y, Kenton DL, Khovayko O, Lipman DJ, Madden TL, Maglott DR, Ostell J, Pruitt KD, Schuler GD, Schriml LM, Sequeira E, Sherry ST, Sirotkin K, Souvorov A, Starchenko G, Suzek TO, Tatusov R, Tatusova TA, et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 2008, 36:D13-D21. 2238880, 18045790.
70. Li R, Yu C, Li Y, Lam T-W, Yiu S-M, Kristiansen K, Wang J. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009, 25(15):1966-1967. 10.1093/bioinformatics/btp336, 19497933.
71. 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(18):3674-3676. 10.1093/bioinformatics/bti610, 16081474.
72. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T. KEGG for linking genomes to life and the environment. Nucleic Acids Res 2008, 36(suppl 1):D480-D484. 2238879, 18077471.
73. 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. 10.1006/meth.2001.1262, 11846609.