Integrated RNA-Seq and sRNA-Seq analysis identifies chilling and freezing responsive key molecular players and pathways in tea plant (Camellia sinensis)

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Zheng, Chao ^a,b   Zhao, Lei ^a,b   Wang, Yu ^a,b   Shen, Jiazhi ^a,b   Zhang, Yinfei ^a,b   Jia, Sisi ^a,b   Li, Yusheng ^c   Ding, Zhaotang ^a,b  

^a QINGDAO AGRICULTURAL UNIVERSITY   (China)

^b Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural Plant   (China)

^c Fruit and Tea Technology Extension Station   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA PRIMEVEROSIDASE; BUTENOLIDE; ENZYME; KARRIKIN; MESSENGER RNA; MICRORNA; PROTEIN CBF1; PROTEIN DREB1B; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BETA-PRIMEVEROSIDASE; GLYCOSIDASE; PHYTOHORMONE; PLANT RNA; TEA;

ARTICLE; CAMELLIA SINENSIS; COLD STRESS; CONTROLLED STUDY; FREEZING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; NEXT GENERATION SEQUENCING; NONHUMAN; PHOTOSYNTHESIS; PLANT RESPONSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; SRNA SEQUENCING; GENE REGULATORY NETWORK; GENETICS; HIGH THROUGHPUT SEQUENCING; PROCEDURES; TEA;

CAMELLIA SINENSIS; THEACEAE;

CAMELLIA SINENSIS; FREEZING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GLYCOSIDE HYDROLASES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; PLANT GROWTH REGULATORS; RNA, MESSENGER; RNA, PLANT; TEA;

EID: 84930631843     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125031     Document Type: Article

References (107)

1. Chen L, Zhou Z-X, Yang Y-J (2007) Genetic improvement and breeding of tea plant (Camellia sinensis) in China: from individual selection to hybridization and molecular breeding. Euphytica 154: 239-248.
2. Wang Y, Jiang CJ, Li YY, Wei CL, Deng WW (2012) CsICE1 and CsCBF1: two transcription factors involved in cold responses in Camellia sinensis. Plant cell reports 31: 27-34. doi: 10.1007/s00299-011-1136-5 PMID: 21850593
3. Huang L, Ye Z, Bell RW, Dell B (2005) Boron nutrition and chilling tolerance of warm climate crop species. Annals of botany 96: 755-767. PMID: 16033777
4. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Current opinion in plant biology 14: 290-295. doi: 10.1016/j.pbi.2011.02.001 PMID: 21377404
5. Lynch DV, Steponkus PL (1987) Plasma membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiology 83: 761-767. PMID: 16665335
6. Hare PD, Cress WA, Staden JV (1998) Dissecting the roles of osmolyte accumulation during stress. Plant, cell & environment 21: 535-553.
7. Pennycooke JC, Cox S, Stushnoff C (2005) Relationship of cold acclimation, total phenolic content and antioxidant capacity with chilling tolerance in petunia (Petunia x hybrida). Environmental and Experimental Botany 53: 225-232.
8. Chinnusamy V, Zhu J, Zhu J-K (2007) Cold stress regulation of gene expression in plants. Trends in plant science 12: 444-451. PMID: 17855156
9. Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118: 1-8. PMID: 9733520
10. Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends in plant science 9: 399-405. PMID: 15358271
11. Provart NJ, Gil P, Chen W, Han B, Chang H-S, Wang X, et al. (2003) Gene expression phenotypes of Arabidopsis associated with sensitivity to low temperatures. Plant Physiology 132: 893-906. PMID: 12805619
12. Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. The Plant Journal 41: 195-211. PMID: 15634197
13. Pang T, Ye C-Y, Xia X, Yin W (2013) De novo sequencing and transcriptome analysis of the desert shrub, Ammopiptanthus mongolicus, during cold acclimation using Illumina/Solexa. BMC genomics 14: 488. doi: 10.1186/1471-2164-14-488 PMID: 23865740
14. Wang H, Zou Z, Wang S, Gong M (2013) Global analysis of transcriptome responses and gene expression profiles to cold stress of Jatropha curcas L. PloS one 8: e82817. doi: 10.1371/journal.pone.0082817 PMID: 24349370
15. Li X-W, Feng Z-G, Yang H-M, Zhu X-P, Liu J, Yuan H-Y (2010) A novel cold-regulated gene from Camellia sinensis, CsCOR1, enhances salt-and dehydration-tolerance in tobacco. Biochemical and biophysical research communications 394: 354-359. doi: 10.1016/j.bbrc.2010.03.011 PMID: 20206599
16. Wang L, Li X, Zhao Q, Jing S, Chen S, Yuan H (2009) Identification of genes induced in response to low-temperature treatment in tea leaves. Plant molecular biology reporter 27: 257-265.
17. Wang X-C, Zhao Q-Y, Ma C-L, Zhang Z-H, Cao H-L, Kong Y-M, et al. (2013) Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC genomics 14: 415. doi: 10.1186/1471-2164-14-415 PMID: 23799877
18. Renaut J, Lutts S, Hoffmann L, Hausman JF (2004) Responses of poplar to chilling temperatures: proteomic and physiological aspects. Plant Biology 6: 81-90. PMID: 15095138
19. Changsong Z, Diqiu Y (2010) Analysis of the cold-responsive transcriptome in the mature pollen of Arabidopsis. Journal of Plant Biology 53: 400-416.
20. Chen J, Tian Q, Pang T, Jiang L, Wu R, Xia X, et al. (2014) Deep-sequencing transcriptome analysis of low temperature perception in a desert tree, Populus euphratica. BMC genomics 15: 326. doi: 10.1186/1471-2164-15-326 PMID: 24884892
21. Barrero-Gil J, Salinas J (2013) Post-translational regulation of cold acclimation response. Plant Science 205-206: 48-54. doi: 10.1016/j.plantsci.2013.01.013 PMID: 23498868
22. He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nature Reviews Genetics 5: 522-531. PMID: 15211354
23. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. cell 116: 281-297. PMID: 14744438
24. Li B, Qin Y, Duan H, Yin W, Xia X (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. Journal of experimental botany 62: 3765-3779. doi: 10.1093/jxb/err051 PMID: 21511902
25. Liu H-H, Tian X, Li Y-J, Wu C-A, Zheng C-C (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. Rna 14: 836-843. doi: 10.1261/rna.895308 PMID: 18356539
26. Yang C, Li D, Mao D, Liu X, Ji C, Li X, et al. (2013) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant, cell & environment 36: 2207-2218.
27. Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. The Plant Journal 74: 840-851. doi: 10.1111/tpj.12169 PMID: 23480361
28. Kuo H-F, Chiou T-J (2011) The role of microRNAs in phosphorus deficiency signaling. Plant physiology 156: 1016-1024. doi: 10.1104/pp.111.175265 PMID: 21562333
29. Li X, Wang X, Zhang S, Liu D, Duan Y, Dong W (2012) Identification of soybean microRNAs involved in soybean cyst nematode infection by deep sequencing. PloS one 7: e39650. doi: 10.1371/journal.pone.0039650 PMID: 22802924
30. Kozomara A and Griffiths-Jones S (2013) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic acids research: gkt1181.
31. Mohanpuria P, Yadav SK (2012) Characterization of novel small RNAs from tea (Camellia sinensis L.). Molecular biology reports 39: 3977-3986. doi: 10.1007/s11033-011-1178-3 PMID: 21744261
32. Das A (2010) Computational Identification of Conserved microRNAs and Their Targets in Tea (Camellia sinensis). American Journal of Plant Sciences 01: 77-86.
33. Prabu GR, Mandal AKA (2010) Computational Identification of miRNAs and Their Target Genes from Expressed Sequence Tags of Tea (Camellia sinensis). Genomics, Proteomics & Bioinformatics 8: 113-121.
34. Zhu QW, Luo YP (2013) Identification of miRNAs and their targets in tea (Camellia sinensis). Journal of Zhejiang University Science B 14: 916-923. doi: 10.1631/jzus.B1300006 PMID: 24101208
35. Jeyaraj A, Chandran V, Gajjeraman P (2014) Differential expression of microRNAs in dormant bud of tea [Camellia sinensis (L.) O. Kuntze]. Plant cell reports.
36. Le TD, Liu L, Liu B, Tsykin A, Goodall GJ, Satou K, et al. (2013) Inferring microRNA and transcription factor regulatory networks in heterogeneous data. BMC bioinformatics 14: 92. doi: 10.1186/1471-2105-14-92 PMID: 23497388
37. Xia J, Zeng C, Chen Z, Zhang K, Chen X, Zhou Y, et al. (2014) Endogenous small-noncoding RNAs and their roles in chilling response and stress acclimation in Cassava. BMC genomics 15: 634. doi: 10.1186/1471-2164-15-634 PMID: 25070534
38. Jeong D-H, Green PJ (2013) The role of rice microRNAs in abiotic stress responses. Journal of Plant Biology 56: 187-197.
39. Haas BJ, Zody MC (2010) Advancing RNA-seq analysis. Nature biotechnology 28: 421. doi: 10.1038/nbt0510-421 PMID: 20458303
40. Tian DQ, Pan XY, Yu YM, Wang WY, Zhang F, Ge YY, et al. (2013) De novo characterization of the Anthurium transcriptome and analysis of its digital gene expression under cold stress. BMC genomics 14: 827. doi: 10.1186/1471-2164-14-827 PMID: 24267953
41. Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, et al. (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PloS one 2: e219. PMID: 17299599
42. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nature Reviews Genetics 10: 57-63. doi: 10.1038/nrg2484 PMID: 19015660
43. Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, et al. (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome biology 8: R96. PMID: 17543110
44. Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, et al. (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PloS one 2.
45. Wang C, Wang X, Kibet NK, Song C, Zhang C, Li X, et al. (2011) Deep sequencing of grapevine flower and berry short RNA library for discovery of novel microRNAs and validation of precise sequences of grapevine microRNAs deposited in miRBase. Physiologia plantarum 143: 64-81. doi: 10.1111/j.1399-3054.2011.01481.x PMID: 21496033
46. Morin RD, Aksay G, Dolgosheina E, Ebhardt HA, Magrini V, Mardis ER, et al. (2008) Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome research 18: 571-584. doi: 10.1101/gr.6897308 PMID: 18323537
47. Vasudevan S (2012) Posttranscriptional upregulation by microRNAs. Wiley Interdiscip Rev RNA 3: 311-330. doi: 10.1002/wrna.121 PMID: 22072587
48. Vaucheret H, Mallory AC, Bartel DP (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Molecular cell 22: 129-136. PMID: 16600876
49. Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. The Plant journal: for cell and molecular biology 55: 131-151. doi: 10.1111/j.1365-313X.2008.03497.x PMID: 18363789
50. Barakat A, Sriram A, Park J, Zhebentyayeva T, Main D, Abbott A (2012) Genome wide identification of chilling responsive microRNAs in Prunus persica. BMC genomics 13: 481. doi: 10.1186/1471-2164-13-481 PMID: 22978558
51. Svensson JT, Crosatti C, Campoli C, Bassi R, Stanca AM, Close TJ, et al. (2006) Transcriptome analysis of cold acclimation in barley Albina and Xantha mutants. Plant physiology 141: 257-270. PMID: 16603669
52. Catalá R, Medina J, Salinas J (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proceedings of the National Academy of Sciences 108: 16475-16480. doi: 10.1073/pnas.1107161108 PMID: 21930922
53. Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, et al. (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant molecular biology 55: 327-342. PMID: 15604685
54. Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiologia plantarum 126: 45-51.
55. Song Y, Chen Q, Ci D, Zhang D (2013) Transcriptome profiling reveals differential transcript abundance in response to chilling stress in Populus simonii. Plant cell reports 32: 1407-1425. doi: 10.1007/s00299-013-1454-x PMID: 23652820
56. Monroy AF, Sangwan V, Dhindsa RS (1998) Low temperature signal transduction during cold acclimation: protein phosphatase 2A as an early target for cold-inactivation. The Plant Journal 13: 653-660.
57. Jeon J, Kim NY, Kim S, Kang NY, Novak O, Ku SJ, et al. (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. The Journal of biological chemistry 285: 23371-23386. doi: 10.1074/jbc.M109.096644 PMID: 20463025
58. Ren L, Sun J, Chen S, Gao J, Dong B, Liu Y, et al. (2014) A transcriptomic analysis of Chrysanthemum nankingense provides insights into the basis of low temperature tolerance. BMC genomics 15.
59. Ligterink W, Hirt H (2001) Mitogen-activated protein (MAP) kinase pathways in plants: versatile signaling tools. International review of cytology 201: 209-275. PMID: 11057833
60. Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. Journal of experimental botany 55: 225-236. PMID: 14673035
61. Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. Journal of Plant Biology 51: 167-173.
62. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proceedings of the National Academy of Sciences of the United States of America 97: 2940-2945. PMID: 10717008
63. Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. The Plant cell 17: 3155-3175. PMID: 16214899
64. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. The Plant journal: for cell and molecular biology 16: 433-442. PMID: 9881163
65. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 101: 15243-15248. PMID: 15383661
66. Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, et al. (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt-and cold-responsive gene expression. The Plant Journal 33: 751-763. PMID: 12609047
67. Chen L, Song Y, Li S, Zhang L, Zou C, Yu D (2012) The role of WRKY transcription factors in plant abiotic stresses. Biochimica et biophysica acta 1819: 120-128. doi: 10.1016/j.bbagrm.2011.09.002 PMID: 21964328
68. Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant molecular biology 51: 21-37. PMID: 12602888
69. Yanhui C, Xiaoyuan Y, Kun H, Meihua L, Jigang L, Zhaofeng G, et al. (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant molecular biology 60: 107-124. PMID: 16463103
70. Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Molecular biology and evolution 20: 735-747. PMID: 12679534
71. Ramsay NA, Glover BJ (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends in plant science 10: 63-70. PMID: 15708343
72. Taoka K, Yanagimoto Y, Daimon Y, Hibara K, Aida M, Tasaka M (2004) The NAC domain mediates functional specificity of CUP-SHAPED COTYLEDON proteins. The Plant journal: for cell and molecular biology 40: 462-473. PMID: 15500463
73. Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Frontiers in microbiology 4: 248. doi: 10.3389/fmicb.2013.00248 PMID: 24058359
74. Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, et al. (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323: 1053-1057. doi: 10.1126/science.1166386 PMID: 19229035
75. Fang Y, Xie K, Xiong L (2014) Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice. Journal of experimental botany 65: 2119-2135. doi: 10.1093/jxb/eru072 PMID: 24604734
76. Wu MF, Tian Q and Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development (Cambridge, England) 133: 4211-4218. PMID: 17021043
77. Smekalova V, Doskocilova A, Komis G, Samaj J (2014) Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnology advances 32: 2-11. doi: 10.1016/j.biotechadv.2013.07.009 PMID: 23911976
78. Du H, Liu H, Xiong L (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Frontiers in plant science 4: 397. doi: 10.3389/fpls.2013.00397 PMID: 24130566
79. Bhardwaj AR, Joshi G, Pandey R, Kukreja B, Goel S, Jagannath A, et al. (2014) A Genome-Wide Perspective of miRNAome in Response to High Temperature, Salinity and Drought Stresses in Brassica juncea (Czern) L. PloS one 9.
80. Curaba J, Spriggs A, Taylor J, Li Z, Helliwell C (2012) miRNA regulation in the early development of barley seed. BMC plant biology 12.
81. Fan G, Zhai X, Niu S, Ren Y (2014) Dynamic expression of novel and conserved microRNAs and their targets in diploid and tetraploid of Paulownia tomentosa. Biochimie 102: 68-77. doi: 10.1016/j.biochi.2014.02.008 PMID: 24565810
82. Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, et al. (2004) Plastidial alpha-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135: 849-858. PMID: 15173560
83. Kaplan F (2004) Amylase Induction and the Protective Role of Maltose during Temperature Shock. Plant Physiology 135: 1674-1684. PMID: 15247404
84. Gomez-Anduro G, Ceniceros-Ojeda EA, Casados-Vazquez LE, Bencivenni C, Sierra-Beltran A, Murillo-Amador B, et al. (2011) Genome-wide analysis of the beta-glucosidase gene family in maize (Zea mays L. var B73). Plant molecular biology 77: 159-183. doi: 10.1007/s11103-011-9800-2 PMID: 21695572
85. Mizutani M, Nakanishi H, Ema J, Ma SJ, Noguchi E, Inohara-Ochiai M, et al. (2002) Cloning of beta-primeverosidase from tea leaves, a key enzyme in tea aroma formation. Plant Physiol 130: 2164-2176. PMID: 12481100
86. Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. The FEBS journal 276: 3148-3162. doi: 10.1111/j.1742-4658.2009.07033.x PMID: 19490115
87. Chitnis VR, Gao F, Yao Z, Jordan MC, Park S, Ayele BT (2014) After-ripening induced transcriptional changes of hormonal genes in wheat seeds: the cases of brassinosteroids, ethylene, cytokinin and salicylic acid. PloS one 9: e87543. doi: 10.1371/journal.pone.0087543 PMID: 24498132
88. Rae L, Lao NT, Kavanagh TA (2011) Regulation of multiple aquaporin genes in Arabidopsis by a pair of recently duplicated DREB transcription factors. Planta 234: 429-444. doi: 10.1007/s00425-011-1414-z PMID: 21509693
89. Lim CW, Kim JH, Baek W, Kim BS, Lee SC (2012) Functional roles of the protein phosphatase 2C, AtAIP1, in abscisic acid signaling and sugar tolerance in Arabidopsis. Plant science: an international journal of experimental plant biology 187: 83-88.
90. Ye H, Du H, Tang N, Li X, Xiong L (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant molecular biology 71: 291-305. doi: 10.1007/s11103-009-9524-8 PMID: 19618278
91. Nelson DC, Flematti GR, Riseborough JA, Ghisalberti EL, Dixon KW, Smith SM (2010) Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 107: 7095-7100. doi: 10.1073/pnas.0911635107 PMID: 20351290
92. Soos V, Sebestyen E, Juhasz A, Light ME, Kohout L, Szalai G, et al. (2010) Transcriptome analysis of germinating maize kernels exposed to smoke-water and the active compound KAR1. BMC plant biology 10: 236. doi: 10.1186/1471-2229-10-236 PMID: 21044315
93. Smith SM, Li J (2014) Signalling and responses to strigolactones and karrikins. Current opinion in plant biology 21: 23-29. doi: 10.1016/j.pbi.2014.06.003 PMID: 24996032
94. Zhao Z, Tan L, Dang C, Zhang H, Wu Q, An L (2012) Deep-sequencing transcriptome analysis of chilling tolerance mechanisms of a subnival alpine plant, Chorispora bungeana. BMC plant biology 12: 222. doi: 10.1186/1471-2229-12-222 PMID: 23171377
95. Thomashow MF (1999) PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. Annual review of plant physiology and plant molecular biology 50: 571-599. PMID: 15012220
96. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature biotechnology 29: 644-652. doi: 10.1038/nbt.1883 PMID: 21572440
97. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological): 289-300.
98. Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, et al. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic acids research 36: 3420-3435. doi: 10.1093/nar/gkn176 PMID: 18445632
99. Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proceedings / International Conference on Intelligent Systems for Molecular Biology; ISMB International Conference on Intelligent Systems for Molecular Biology: 138-148.
100. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449. PMID: 15972284
101. Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21: 3787-3793. PMID: 15817693
102. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome biology 10: R25. doi: 10.1186/gb-2009-10-3-r25 PMID: 19261174
103. Wen M, Shen Y, Shi S, Tang T (2012) miREvo: an integrative microRNA evolutionary analysis platform for next-generation sequencing experiments. BMC Bioinformatics 13: 140. doi: 10.1186/1471-2105-13-140 PMID: 22720726
104. Friedlander MR, Mackowiak SD, Li N, Chen W, Rajewsky N (2012) miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic acids research 40: 37-52. doi: 10.1093/nar/gkr688 PMID: 21911355
105. Wu HJ, Ma YK, Chen T, Wang M, Wang XJ (2012) PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic acids research 40: W22-28. doi: 10.1093/nar/gks554 PMID: 22693224
106. Storey JD (2003) The positive false discovery rate: A Bayesian interpretation and the q-value. Annals of statistics: 2013-2035.
107. Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-ΔΔCT Method. Methods 25: 402-408. PMID: 11846609