Comparative transcriptome profiling of Pyropia yezoensis (Ueda) M.S. Hwang & H.G. Choi in response to temperature stresses

BMC Genomics

Guiqi Bi³  Li Wang¹  Fanna Kong³  Min Cao³  Guiyang Li²  Yunxiang Mao³  Peipei Sun³ 

[1] Institute of Plant Resources, Dalian Nationalities University, Dalian 116600, China;Key Laboratory for Sustainable Utilization of Marine Fisheries Resources, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China;Key Laboratory of Marine Genetics and Breeding (MOE), College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China

关键词: Transcriptome;    DGE;    Freezing stress;    Chilling stress;    High temperature stress;    RNA-seq;    Pyropia yezoensis;   

Others  :  1216171
DOI  :  10.1186/s12864-015-1586-1

 received in 2014-08-28, accepted in 2015-04-27,  发布年份 2015

【 摘 要 】

Background

Pyropia yezoensis is a model organism often used to investigate the mechanisms underlying stress tolerance in intertidal zones. The digital gene expression (DGE) approach was used to characterize a genome-wide comparative analysis of differentially expressed genes (DEGs) that influence the physiological, developmental or biochemical processes in samples subjected to 4 treatments: high-temperature stress (HT), chilling stress (CS), freezing stress (FS) and normal temperature (NT).

Results

Equal amounts of total RNAs collected from 8 samples (two biological replicates per treatment) were sequenced using the Illumina/Solexa platform. Compared with NT, a total of 2202, 1334 and 592 differentially expressed unigenes were detected in HT, CS and FS respectively. Clustering analysis suggested P. yezoensis acclimates to low and high-temperature stress condition using different mechanisms: In heat stress, the unigenes related to replication and repair of DNA and protein processing in endoplasmic reticulum were active; however at low temperature stresses, unigenes related to carbohydrate metabolism and energy metabolism were active. Analysis of gene differential expression showed that four categories of DEGs functioning as temperature sensors were found, including heat shock proteins, H2A, histone deacetylase complex and transcription factors. Heat stress caused chloroplast genes down-regulated and unigenes encoding metacaspases up-regulated, which is an important regulator of PCD. Cold stress caused an increase in the expression of FAD to improve the proportion of polyunsaturated fatty acids. An up-regulated unigene encoding farnesyl pyrophosphate synthase was found in cold stress, indicating that the plant hormone ABA also played an important role in responding to temperature stress in P. yezoensis.

Conclusion

The variation of amount of unigenes and different gene expression pattern under different temperature stresses indicated the complicated and diverse regulation mechanism in response to temperature stress in P. yezoensis. Several common metabolism pathways were found both in P. yezoensis and in higher plants, such as FAD in low-temperature stress and HSP in heat stress. Meanwhile, many chloroplast genes and unigene related to the synthesis of abscisic acid were detected, revealing its unique temperature-regulation mechanism in this intertidal species. This sequencing dataset and analysis may serve as a valuable resource to study the mechanisms involved in abiotic stress tolerance in intertidal seaweeds.

【 授权许可】

   
2015 Sun et al.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】

• [1]Iba K. Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu Rev Plant Biol. 2002; 53(1):225-245.
• [2]Larcher W. Physiological plant ecology: ecophysiology and stress physiology of functional groups: Springer Science and Business Media 2003.
• [3]Wei W, Qi X, Wang L, Zhang Y, Hua W, Li D, Lv H, Zhang X. Characterization of the sesame (Sesamum indicum L.) global transcriptome using Illumina paired-end sequencing and development of EST-SSR markers. BMC Genomics. 2011; 12(1):451. BioMed Central Full Text
• [4]Feng C, Chen M, Xu C-j, Bai L, Yin X-r, Li X, Allan AC, Ferguson IB, Chen K-s. Transcriptomic analysis of Chinese bayberry (Myrica rubra) fruit development and ripening using RNA-Seq. BMC Genomics. 2012; 13(1):19. BioMed Central Full Text
• [5]Chang L, Xia Y-p, Chen J-j, Xiao Y-m. Application of digital gene expression tag profiling on differential gene expression of two developmental stages in bulbs of Lycoris sprengeri. Indian J Horticulture. 2011; 68(4):522-528.
• [6]Zenoni S, Ferrarini A, Giacomelli E, Xumerle L, Fasoli M, Malerba G, Bellin D, Pezzotti M, Delledonne M. Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-Seq. Plant Physiol. 2010; 152(4):1787-1795.
• [7]Collén J, Guisle‐Marsollier I, Léger JJ, Boyen C. Response of the transcriptome of the intertidal red seaweed Chondrus crispus to controlled and natural stresses. New Phytol. 2007; 176(1):45-55.
• [8]Dawes C, Orduna-Rojas J, Robledo D. Response of the tropical red seaweed Gracilaria cornea to temperature, salinity and irradiance. J Appl Phycol. 1998; 10(5):419-425.
• [9]Kayama M, Iijima N, Kuwahara M, Sado T, Araki S, Sakurai T. Effect of water temperature on the fatty acid composition of Porphyra. Bulletin of the Japanese Society of Scientific Fisheries 1985, 51(4):687-691.
• [10]Choi S, Hwang MS, Im S, Kim N, Jeong W-J, Park E-J, Gong Y-G, Choi D-W. Transcriptome sequencing and comparative analysis of the gametophyte thalli of Pyropia tenera under normal and high temperature conditions. J Appl Phycol 2013,25(4):1237-1246.
• [11]Xu Y, Chen C, Ji D, Hang N, Xie C. Proteomic profile analysis of Pyropia haitanensis in response to high-temperature stress. J Appl Phycol 2014,26(1):607-618.
• [12]Storey JD. The positive false discovery rate: A Bayesian interpretation and the q-value. Ann Stat 2003,31(6):2013-2035.
• [13]Murata N, Los DA. Membrane fluidity and temperature perception. Plant Physiol. 1997; 115(3):875.
• [14]Nishida I, Murata N. Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Biol. 1996; 47(1):541-568.
• [15]Tocher D, Leaver M, Hodgson P. Recent advances in the biochemistry and molecular biology of fatty acyl desaturases. Prog Lipid Res. 1998; 37(2–3):73-117.
• [16]Bossie MA, Martin CE. Nutritional regulation of yeast delta-9 fatty acid desaturase activity. J Bacteriol. 1989; 171(12):6409-6413.
• [17]Sakamoto T, Los DA, Higashi S, Wada H, Nishida I, Ohmori M, Murata N. Cloning of ω3 desaturase from cyanobacteria and its use in altering the degree of membrane-lipid unsaturation. Plant Mol Biol. 1994; 26(1):249-263.
• [18]Bray EA, Bailey-Serres J, Weretilnyk E. Responses to abiotic stresses. Biochemistry and molecular biology of plants 2000, 1158: e1203.
• [19]Feder ME, Hofmann GE. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol. 1999; 61(1):243-282.
• [20]Nelson RJ, Ziegelhoffer T, Nicolet C, Werner-Washburne M, Craig EA. The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell. 1992; 71(1):97-105.
• [21]Schroda M, Vallon O. Chaperones and proteases. Chlamydomonas Sourcebook, Ed. 2008; 2:671-729.
• [22]Mayer M, Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci. 2005; 62(6):670-684.
• [23]Cheng MY, Hartl F-U, Martin J, Pollock RA, Kalousek F, Neupert W, Hallberg EM, Hallberg RL, Horwich A. Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature. 1989; 6208:585-674.
• [24]Sanchez MdlP, Caro E, Desvoyes B, Ramirez-Parra E, Gutierrez C. Chromatin dynamics during the plant cell cycle. In: Semin Cell Dev Biol 2008,19(6): 537-546.
• [25]Steward N, Kusano T, Sano H. Expression of ZmMET1, a gene encoding a DNA methyltransferase from maize, is associated not only with DNA replication in actively proliferating cells, but also with altered DNA methylation status in cold-stressed quiescent cells. Nucleic Acids Res. 2000; 28(17):3250-3259.
• [26]Franklin KA. Plant chromatin feels the heat. Cell. 2010; 140(1):26-28.
• [27]Takemaru K-I, Li F-Q, Ueda H, Hirose S. Multiprotein bridging factor 1 (MBF1) is an evolutionarily conserved transcriptional coactivator that connects a regulatory factor and TATA element-binding protein. Proc Natl Acad Sci. 1997; 94(14):7251-7256.
• [28]Brendel C, Gelman L, Auwerx J. Multiprotein bridging factor-1 (MBF-1) is a cofactor for nuclear receptors that regulate lipid metabolism. Mol Endocrinol. 2002; 16(6):1367-1377.
• [29]Liu Q-X, Jindra M, Ueda H, Hiromi Y, Hirose S. Drosophila MBF1 is a co-activator for Tracheae Defective and contributes to the formation of tracheal and nervous systems. Development. 2003; 130(4):719-728.
• [30]Grover A, Mittal D, Negi M, Lavania D. Generating high temperature tolerant transgenic plants: achievements and challenges. Plant Sci. 2013; 205:38-47.
• [31]Uji T, Sato R, Mizuta H, Saga N. Changes in membrane fluidity and phospholipase D activity are required for heat activation of PyMBF1 in Pyropia yezoensis (Rhodophyta). J Appl Phycol. 2013; 25(6):1887-1893.
• [32]Suzuki N, Sejima H, Tam R, Schlauch K, Mittler R. Identification of the MBF1 heat‐response regulon of Arabidopsis thaliana. Plant J. 2011; 66(5):844-851.
• [33]Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta. 2003; 218(1):1-14.
• [34]Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L. MYB transcription factors in < i> Arabidopsis. Trends Plant Sci. 2010; 15(10):573-581.
• [35]Agarwal M, Hao Y, Kapoor A, Dong C-H, Fujii H, Zheng X, Zhu J-K. 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(49):37636-37645.
• [36]Koonin E, Aravind L. Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ. 2002; 9(4):394-404.
• [37]Saheb E, Trzyna W, Bush J. Caspase-like proteins: Acanthamoeba castellanii metacaspase and Dictyostelium discoideum paracaspase, what are their functions? J Biosciences 2014,39(5):909-916.
• [38]Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inzé D, Delledonne M, Van Breusegem F. Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J Biol Chem. 2007; 282(2):1352-1358.
• [39]Coll NS, Vercammen D, Smidler A, Clover C, Van Breusegem F, Dangl JL, Epple P. Arabidopsis type I metacaspases control cell death. Science. 2010; 330(6009):1393-1397.
• [40]Flower TR, Chesnokova LS, Froelich CA, Dixon C, Witt SN. Heat shock prevents alpha-synuclein-induced apoptosis in a yeast model of Parkinson's disease. J Mol Biol. 2005; 351(5):1081-1100.
• [41]Bouchard JN, Yamasaki H. Implication of nitric oxide in the heat-stress-induced cell death of the symbiotic alga Symbiodinium microadriaticum. Mar Biol. 2009; 156(11):2209-2220.
• [42]Olvera-Carrillo Y, Salanenka Y, Nowack MK. Control of programmed cell death during plant reproductive development. In: Biocommunication of Plants. Springer 2012,14:171-196.
• [43]Pang SJ, Liu F, Shan TF, Gao SQ, Zhang ZH. Cultivation of the brown alga Sargassum horneri: sexual reproduction and seedling production in tank culture under reduced solar irradiance in ambient temperature. J Appl Phycol. 2009; 21(4):413-422.
• [44]Mathur S, Agrawal D, Jajoo A. Photosynthesis: Response to high temperature stress. J Photoch Photobio B 2014,137:116-126.
• [45]Watanabe Y, Nishihara GN, Tokunaga S, Terada R. Effect of irradiance and temperature on the photosynthesis of a cultivated red alga, Pyropia tenera (= Porphyra tenera), at the southern limit of distribution in Japan. Phycol Res 2014,62(3):187-196.
• [46]Penfield S. Temperature perception and signal transduction in plants. New Phytol. 2008; 179(3):615-628.
• [47]Zeevaart J, Creelman R. Metabolism and physiology of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol. 1988; 39(1):439-473.
• [48]Wang X, Zhao P, Liu X, Chen J, Xu J, Chen H, et al. Quantitative profiling method for phytohormones and betaines in algae by liquid chromatography electrospray ionization tandem mass spectrometry. Biomedical Chromatography. 2013.
• [49]Chernys JT, Zeevaart JA. Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol. 2000; 124(1):343-354.
• [50]Bopp-Buhler M, Wabra P, Hartung W, Gimmler H. Evidence for direct ABA synthesis in Dunaliella (Volvocales). Cryptogamic botany 1991,2(2):192-200.
• [51]Yamamoto H, Inomata M, Tsuchiya S, Nakamura M, Uchiyama T, Oritani T. Early biosynthetic pathway to abscisic acid in Cercospora cruenta. Biosci Biotechnol Biochem. 2000; 64(10):2075-2082.
• [52]Hirai N, Yoshida R, Todoroki Y, OHIGASHI H. Biosynthesis of abscisic acid by the non-mevalonate pathway in plants, and by the mevalonate pathway in fungi. Biosci Biotechnol Biochem. 2000; 64(7):1448-1458.
• [53]Gilmour SJ, Thomashow MF. Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol. 1991; 17(6):1233-1240.
• [54]Tamminen I, Mäkelä P, Heino P, Palva ET. Ectopic expression of ABI3 gene enhances freezing tolerance in response to abscisic acid and low temperature in Arabidopsis thaliana. Plant J. 2001; 25(1):1-8.
• [55]Yang H, Mao Y, Kong F, Yang G, Ma F, Wang L. Profiling of the transcriptome of Porphyra yezoensis with Solexa sequencing technology. Chin Sci Bull. 2011; 56(20):2119-2130.
• [56]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29(7):644-652.
• [57]Conesa A, Götz S. Blast2GO. A comprehensive suite for functional analysis in plant genomics. International journal of plant genomics 2008, 619832.
• [58]Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007; 35(suppl 2):W182-W185.
• [59]Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12(1):323. BioMed Central Full Text
• [60]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.
• [61]Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010; 11(10):R106. BioMed Central Full Text
• [62]Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 1995,57(1):289-300.
• [63]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.