BMC Genomics | |
Deep sequencing-based characterization of transcriptome of trifoliate orange (Poncirus trifoliata (L.) Raf.) in response to cold stress | |
Ji-Hong Liu1  Xiaona Zhang1  Min Wang1  | |
[1] Key Laboratory of Horticultural Plant Biology (MOE), College of Horticulture and Forestry Science, Huazhong Agricultural University, Wuhan, 430070, China | |
关键词: Citrus; Digital gene expression; Transcriptome profiling; Cold stress; RNA-seq; Poncirus trifoliata; | |
Others : 1221848 DOI : 10.1186/s12864-015-1629-7 |
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received in 2015-02-12, accepted in 2015-05-12, 发布年份 2015 | |
【 摘 要 】
Background
Trifoliate orange (Poncirus trifoliata (L.) Raf.) is extremely cold hardy after a full acclimation; however the underlying molecular mechanisms underlying this economically valuable trait remain poorly understood. In this study, global transcriptome profiles of trifoliate orange under cold conditions (4 °C) over a time course were generated by high-throughput sequencing.
Results
More than 68 million high-quality reads were produced and assembled into a non-redundant data of 77,292 unigenes with an average length of 1112 bp (N50 = 1778 bp). Of these, 23,846 had significant sequence similarity to known genes and these were assigned to 61 gene ontology (GO) categories and 25 clusters of orthologous groups (COG) involved in 128 KEGG pathways. Sequences derived from cold-treated and control plants were mapped to the assembled transcriptome, resulting in the identification of 5549 differentially expressed genes (DEGs). These comprised 600 (462 up-regulated, 138 down-regulated), 2346 (1631 up-regulated, 715 down-regulated), and 5177 (2702 up-regulated, 2475 down-regulated) genes from the cold-treated samples at 6, 24 and 72 h, respectively. The accuracy of the RNA-seq derived transcript expression data was validated by analyzing the expression patterns of 17 DEGs by qPCR. Plant hormone signal transduction, plant-pathogen interaction, and secondary metabolism were the most significantly enriched GO categories amongst in the DEGs. A total of 60 transcription factors were shown to be cold responsive. In addition, a number of genes involved in the catabolism and signaling of hormones, such as abscisic acid, ethylene and gibberellin, were affected by the cold stress. Meanwhile, levels of putrescine progressively increased under cold, which was consistent with up-regulation of an arginine decarboxylase gene.
Conclusions
This dataset provides valuable information regarding the trifoliate orange transcriptome changes in response to cold stress and may help guide future identification and functional analysis of genes that are importnatn for enhancing cold hardiness.
【 授权许可】
2015 Wang et al.
【 预 览 】
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【 参考文献 】
- [1]Chinnusamy V, Zhu JH, Zhu JK. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007; 12:444-51.
- [2]Michael MF. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol. 1999; 50:571-99.
- [3]Zhu JH, Dong CH, Zhu JK. Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol. 2007; 10:290-5.
- [4]Medina J, Catalá R, Salinas J. The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci. 2011; 180:3-11.
- [5]Nakashima K, Ito Y, Yamaguchi-Shinozaki K. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol. 2009; 149:88-95.
- [6]Chinnusamy V, Ohta M, Kanrar S, Lee B, Hong XH, Agarwal M et al.. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Gene Dev. 2003; 17:1043-54.
- [7]Dong CH, Agarwal M, Zhang YY, 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; 103:8281-6.
- [8]Agarwal M, Hao YJ, Kapoor A, Dong CH, Fujii H, Zheng XY et al.. A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem. 2006; 281:37636-45.
- [9]Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA et al.. Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol. 2008; 49:1135-49.
- [10]Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ. Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J. 2010; 8:749-71.
- [11]Tian DQ, Pan XY, Yu YM, Wang WY, Zhang F, Ge YY et al.. De novo characterization of the Anthurium transcriptome and analysis of its digital gene expression under cold stress. BMC Genomics. 2013; 14:827. BioMed Central Full Text
- [12]Wang XC, Zhao QY, Ma CL, Zhang ZH, Cao HL, Kong YM et al.. Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC Genomics. 2013; 14:415. BioMed Central Full Text
- [13]Wang JM, Yang Y, Liu XH, Huang J, Wang Q, Gu JH et al.. Transcriptome profiling of the cold response and signaling pathways in Lilium lancifolium. BMC Genomics. 2014; 15:203. BioMed Central Full Text
- [14]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; 14:1675-90.
- [15]Martin JA, Wang Z. Next-generation transcriptome assembly. Nat Rev Genet. 2011; 12:671-82.
- [16]Huang JZ, Lu X, Yan H, Chen SY, Zhang WK, Huang RF et al.. Transcriptome characterization and sequencing-based identification of salt-responsive genes in Millettia pinnata, a semi-mangrove plant. DNA Res. 2012; 19:195-207.
- [17]Shi Y, Yan X, Zhao PS, Yin HX, Zhao X, Xiao HL et al.. Transcriptomic analysis of a tertiary relict plant, extreme xerophyte Reaumuria soongorica to identify genes related to drought adaptation. PLoS One. 2013; 8:e63993.
- [18]Chen J, Tian Q, Pang T, Jiang LB, Wu RL, Xia XL et al.. Deep-sequencing transcriptome analysis of low temperature perception in a desert tree, Populus euphratica. BMC Genomics. 2014; 15:326. BioMed Central Full Text
- [19]Kakumanu A, Ambavaram MMR, Klumas C, Krishnan A, Batlang U, Myers E et al.. Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol. 2012; 160:846-67.
- [20]Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U, Murat F et al.. Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol. 2014; 32:656-62.
- [21]Zhang CK, Lang P, Dane F, Ebel RC, Singh NK, Locy RD et al.. Cold acclimation induced genes of trifoliate orange (Poncirus trifoliata). Plant Cell Rep. 2005; 23:764-9.
- [22]Peng T, Zhu XF, Fan QJ, Sun PP, Liu JH. Identification and characterization of low temperature stress responsive genes in Poncirus trifoliata by suppression subtractive hybridization. Gene. 2012; 492:220-8.
- [23]Sahin-Çevik M, Moore GA. Identification and expression analysis of cold-regulated genes from the cold-hardy Citrus relative Poncirus trifoliata (L.) Raf. Plant Mol Biol. 2006; 62:83-97.
- [24]Wang J, Sun PP, Chen CL, Wang Y, Fu XZ, Liu JH. An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. J Exp Bot. 2011; 62:2899-914.
- [25]Huang XS, Wang W, Zhang Q, Liu JH. A basic helix-loop-helix transcription factor, PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiol. 2013; 162:1178-94.
- [26]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I et al.. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29:644-52.
- [27]Ye J, Fang L, Zheng HK, Zhang Y, Chen J, Zhang ZJ et al.. WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 2006; 34:293-7.
- [28]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; 21:3674-6.
- [29]Iseli C, Jongeneel CV, Bucher P. ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol. 1999; 7:138-48.
- [30]Li RQ, Yu C, Li YR, Lam TW, Yiu SM, Kristianse K et al.. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics. 2009; 25:1966-7.
- [31]Kim YO, Kim JS, Kang H. Cold-inducible zinc finger-containing glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis thaliana. Plant J. 2005; 42:890-900.
- [32]Kim JY, Park SJ, Kwak KJ, Jung CH, Ahn SJ, Goh CH et al.. Cold shock domain proteins and glycine-rich RNA-binding proteins from Arabidopsis thaliana can promote the cold adaptation process in Escherichia coli. Nucleic Acids Res. 2007; 35:506-16.
- [33]Kovtun Y, Chiu WL, Tena G, Sheen J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A. 2000; 97:2940-5.
- [34]Jaspers P, Kangasjärvi J. Reactive oxygen species in abiotic stress signaling. Physiol Plant. 2010; 138:405-13.
- [35]Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH. Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot. 2002; 89:841-50.
- [36]Shinozaki K, Yamaguchi-Shinozaki K, Seki M. Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol. 2003; 6:410-7.
- [37]Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W. Calmodulins and calcineurin B–like proteins calcium sensors for specific signal response coupling in plants. Plant Cell. 2002; 14:389-400.
- [38]Valmonte GR, Arthur K, Higgins CM, MacDiarmid RM. Calcium-dependent protein kinases in plants: evolution, expression and function. Plant Cell Physiol. 2014; 55:551-69.
- [39]Franza S, Ehlerta B, Liesea A, Kurtha J, Cazalé AC, Romeisa T. Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol Plant. 2011; 4:83-96.
- [40]Xu YJ, Gao S, Yang YJ, Huang NY, Cheng LN, Wei Q et al.. Transcriptome sequencing and whole genome expression profiling of chrysanthemum under dehydration stress. BMC Genomics. 2013; 14:662. BioMed Central Full Text
- [41]Janská A, Maršík P, Zelenková S, Ovesná J. Cold stress and acclimation–what is important for metabolic adjustment? Plant Biol. 2010; 12:395-405.
- [42]Lee B, Henderson DA, Zhu JK. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell. 2005;17:3155–75
- [43]Peleg Z, Blumwald E. Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol. 2011; 14:290-5.
- [44]Tuteja N. Abscisic acid and abiotic stress signaling. Plant Signal Behav. 2007; 2:135-8.
- [45]Heino P, Sandman G, Lång V, Nordin K, Palva ET. Abscisic acid deficiency prevents development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Theor Appl Genet. 1990; 79:801-6.
- [46]Lang V, Mantyla E, Welin B, Palva ET. Alterations in water status, endogenous abscisic acid content, and expression of rab18 gene during the development of freezing tolerance in Arabidopsis thaliana. Plant Physiol. 1994; 104:1341-9.
- [47]Espasandin FD, Maiale SJ, Calzadilla P, Ruiz OA, Sansberro PA. Transcriptional regulation of 9-cis-epoxycarotenoid dioxygenase (NCED) gene by putrescine accumulation positively modulates ABA synthesis and drought tolerance in Lotus tenuis plants. Plant Physiol Biochem. 2014; 76:29-35.
- [48]Tähtiharju S, Palva T. Antisense inhibition of protein phosphatase 2C accelerates cold acclimation in Arabidopsis thaliana. Plant J. 2001; 26:461-70.
- [49]Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY et al.. Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol. 2007; 143:707-19.
- [50]Jung JY, Shin R, Schachtman DP. Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. Plant Cell. 2009; 21:607-21.
- [51]Kendrick MD, Chang C. Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Boil. 2008; 11:479-85.
- [52]Chu C, Lee TM. The relationship between ethylene biosynthesis and chilling tolerance in seedlings of rice (Oryza sativa L.). Bot Bull Acad Sin. 1989; 30:263-73.
- [53]Ciardi JA, Deikman J, Orzolek MD. Increased ethylene synthesis enhances chilling tolerance in tomato. Physiol Plant. 1997; 101:333-40.
- [54]Yu XM, Griffith M, Wiseman SB. Ethylene induces antifreeze activity in winter rye leaves. Plant Physiol. 2001; 126:1232-40.
- [55]Zhang Z, Huang R. Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis. Plant Mol Biol. 2010; 73:241-9.
- [56]Catalá R, López-Cobollo R, Castellano MM, Angostob T, Alonsoc JM, Eckerc JR et al.. The Arabidopsis 14-3-3 protein RARE COLD INDUCIBLE 1A links low-temperature response and ethylene biosynthesis to regulate freezing tolerance and cold acclimation. Plant Cell. 2014; 26:3326-42.
- [57]Shi Y, Tian S, Hou L, Huang XZ, Zhang XY, Guo HW et al.. Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell. 2012; 24:2578-95.
- [58]Colebrook EH, Thomas SG, Phillips AL, Hedden P. The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol. 2014; 217:67-75.
- [59]Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K et al.. Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell. 2007; 19:3037-57.
- [60]Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P. The cold-inducible CBF1 factor–dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell. 2008; 20:2117-29.
- [61]Miller GAD, Mittler R. Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot. 2006; 98:279-88.
- [62]Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R. The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J Biol Chem. 2008; 283:9269-75.
- [63]Agarwal PK, Jha B. Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol Plant. 2010; 54:201-12.
- [64]Liu JH, Peng T, Dai W. Critical cis-acting elements and interacting transcription factors: key players associated with abiotic stress responses in plants. Plant Mol Biol Rep. 2014; 32:303-17.
- [65]Chinnusamy V, Zhu JK, Sunkar R. Gene regulation during cold stress acclimation in plants. Plant Stress Tolerance. 2010;639:39–55.
- [66]Zhang LC, Liu GX, Zhao GY, Xia C, Jia JZ, Liu X et al.. Characterization of a wheat R2R3-MYB transcription factor gene, TaMYB19, involved in enhanced abiotic stresses in Arabidopsis. Plant Cell Physiol. 2014; 55:1802-12.
- [67]Tiburcio AF, Altabella T, Bitrián M, Alcázar R. The roles of polyamines during the lifespan of plants: from development to stress. Planta. 2014; 240:1-18.
- [68]Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S et al.. TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics. 2003; 19:651-2.
- [69]Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000; 28:27-30.
- [70]Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008; 5:621-8.
- [71]Fu XZ, Chen CW, Wang Y, Liu JH, Moriguchi T. Ectopic expression of MdSPDS1 in sweet orange (Citrus sinensis Osbeck) reduces canker susceptibility: involvement of H 2 O 2 production and transcriptional alteration. BMC Plant Biol. 2011; 11:55. BioMed Central Full Text