Comparative transcriptomics analysis reveals difference of key gene expression between banana and plantain in response to cold stress

BMC Genomics

Gan-Jun Yi²  Sheng Zhang⁴  Xin-Xiang Peng¹  Chun-Yu Li²  Jun-Hua Wu¹  Li-Jie Ding¹  Tong-Xin Dou¹  Wei-Di He³  Jie Gao¹  Qiao-Song Yang² 

[1]State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, South China Agricultural University, Guangzhou 510640, China

[2]Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Ministry of Agriculture, Guangzhou 510640, China

[3]National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China

[4]Institute of Biotechnology, Cornell University, Ithaca 14853-2703, NY, USA

关键词: MYBS3 pathways;    ICE1;    Plantain;    Banana;    Cold tolerance;    Comparative transcriptome analysis;   

Others  :  1211963
DOI  :  10.1186/s12864-015-1551-z

 received in 2015-01-07, accepted in 2015-04-17,  发布年份 2015

【 摘 要 】

Background

Banana and plantain (Musa spp.) comprise an important part of diets for millions of people around the globe. Low temperature is one of the key environmental stresses which greatly affects the global banana production. To understand the molecular mechanism of the cold-tolerance in plantain we used RNA-Seq based comparative transcriptomics analyses for both cold-sensitive banana and cold-tolerant plantain subjected to the cold stress for 0, 3 and 6 h.

Results

The cold-response genes at early stage are identified and grouped in both species by GO analysis. The results show that 10 and 68 differentially expressed genes (DEGs) are identified for 3 and 6 h of cold stress respectively in plantain, while 40 and 238 DEGs are identified respectively in banana. GO classification analyses show that the majority of DEGs identified in both banana and plantain belong to 11 categories including regulation of transcription, response to stress signal transduction, etc. A similar profile for 28 DEGs was found in both banana and plantain for 6 h of cold stress, suggesting both share some common adaptation processes in response to cold stress. There are 17 DEGs found uniquely in cold-tolerance plantain, which were involved in signal transduction, abiotic stress, copper ion equilibrium, photosynthesis and photorespiration, sugar stimulation, protein modifications etc. Twelve early responsive genes including ICE1 and MYBS3 were selected and further assessed and confirmed by qPCR in the extended time course experiments (0, 3, 6, 24 and 48 h), which revealed significant expression difference of key genes in response to cold stress, especially ICE1 and MYBS3 between cold-sensitive banana and cold-tolerant plantain.

Conclusions

We found that the cold-tolerance pathway appears selectively activated by regulation of ICE1 and MYBS3 expression in plantain under different stages of cold stress. We conclude that the rapid activation and selective induction of ICE1 and MYBS3 cold tolerance pathways in plantain, along with expression of other cold-specific genes, may be one of the main reasons that plantain has higher cold resistance than banana.

【 授权许可】

   
2015 Yang et al.

【 图 表 】

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【 参考文献 】

• [1]Zhou MQ, Shen C, Wu LH, Tang KX, Lin J. CBF-dependent signaling pathway: A key responder to low temperature stress in plants. Crit Rev Biotechnol. 2011; 31(2):186-92.
• [2]Sanghera GS, Wani SH, Hussain W, Singh NB. Engineering cold stress tolerance in crop plants. Curr Genomics. 2011; 12(1):30-43.
• [3]Nakashima K, Yamaguchi-Shinozaki K. Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant. 2006; 126(1):62-71.
• [4]Chinnusamy V, Zhu J, Zhu J. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007; 12(10):444-51.
• [5]Zhang T, Zhao X, Wang W, Pan Y, Huang L, Liu X et al.. Comparative Transcriptome Profiling of Chilling Stress Responsiveness in Two Contrasting Rice Genotypes. PLoS One. 2012; 7(8):e43274.
• [6]Liu H, Ouyang B, Zhang J, Wang T, Li H, Zhang Y et al.. Differential Modulation of Photosynthesis, Signaling, and Transcriptional Regulation between Tolerant and Sensitive Tomato Genotypes under Cold Stress. PLoS One. 2012; 7(11):e50785.
• [7]Xin H, Zhu W, Wang L, Xiang Y, Fang L, Li J et al.. Genome Wide Transcriptional Profile Analysis of Vitis amurensis and Vitis vinifera in Response to Cold Stress. PLoS One. 2013; 8(3):e58740.
• [8]Zhang JZ, Creelman RA, Zhu JK. From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol. 2004; 135(2):615-21.
• [9]D Hont A, Denoeud F, Aury J, Baurens F, Carreel F, Garsmeur O et al.. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature. 2012; 488(7410):213-7.
• [10]Yang QS, Wu JH, Li CY, Wei YR, Sheng O, Hu CH et al.. Quantitative proteomic analysis reveals that antioxidation mechanisms contribute to cold tolerance in plantain (Musa paradisiaca L.; ABB Group) seedlings. Mol Cell Proteomics. 2012; 11(12):1853-69.
• [11]Israeli Y, Lahav E. Injuries to banana caused by adverse climate and weather. Diseases of Banana, Abacá Enset. CABI Publishing, Wallingford, Oxon, UK.2000, 351-379.
• [12]Lü Q F, Feng F, Zhang X Z. Cold tolerance of banana in relation to cell structure in leaf tissue. J. Zhanjiang Ocean Univ, 2000, 20:48-51.
• [13]Kai L, Chun-hua HU, DU Fa-xiu, Yu-e Z, Yue-rong W, Gan-jun YI. Over-Expression of the Arabidopsis CBF1 Gene in Dongguandajiao (Musa spp. ABB group) and Detection of Its Cold Resistance. Scientia Agricultura Sinica. 2012, 45(8):1653-1660.
• [14]Su CF, Wang YC, Hsieh TH, Lu CA, Tseng TH, Yu SM. A Novel MYBS3-Dependent Pathway Confers Cold Tolerance in Rice. Plant Physiol. 2010; 153(1):145-58.
• [15]Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, et al. COLD1 Confers Chilling Tolerance in Rice. Cell. 2015, 160(6):1209-1221.
• [16]Zhang Q, Zhang JZ, Chow WS, Sun LL, Chen JW, Chen YJ et al.. The influence of low temperature on photosynthesis and antioxidant enzymes in sensitive banana and tolerant plantain (Musa sp.) cultivars. Photosynthetica. 2011; 49(2):201-8.
• [17]Feng D, Liu B, Li W, He Y, Qi K, Wang JWH. Over-expression of a cold-induced plasma membrane protein gene ( MpRCI) from plantain enhances low temperature-resistance in transgenic tobacco. Environ Exp Bot. 2009; 65(2):395-402.
• [18]Zhang G, Guo G, Hu X, Zhang Y, Li Q, Li R et al.. Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Res. 2010; 20(5):646-54.
• [19]Li W, Wu J, Zhang H, Shi S, Liu L, Shu B et al.. De Novo Assembly and Characterization of Pericarp Transcriptome and Identification of Candidate Genes Mediating Fruit Cracking in Litchi chinensis Sonn. Int J Mol Sci. 2014; 15(10):17667-85.
• [20]Lu X, Kim H, Zhong S, Chen H, Hu Z, Zhou B. De novo transcriptome assembly for rudimentary leaves in Litchi chinesis Sonn. and identification of differentially expressed genes in response to reactive oxygen species. BMC Genomics. 2014, 15(1):805.
• [21]Luria N, Sela N, Yaari M, Feygenberg O, Kobiler I, Lers A et al.. De-novo assembly of mango fruit peel transcriptome reveals mechanisms of mango response to hot water treatment. BMC Genomics. 2014; 15(1):957. BioMed Central Full Text
• [22]Urasaki N, Tarora K, Shudo A, Ueno H, Tamaki M, Miyagi N et al.. Digital Transcriptome Analysis of Putative Sex-Determination Genes in Papaya (Carica papaya). PLoS One. 2012; 7(7):e40904.
• [23]Crifò T, Puglisi I, Petrone G, Recupero GR, Lo Piero AR. Expression analysis in response to low temperature stress in blood oranges: Implication of the flavonoid biosynthetic pathway. Gene. 2011; 476(1–2):1-9.
• [24]Perrone I, Pagliarani C, Lovisolo C, Chitarra W, Roman F, Schubert A. Recovery from water stress affects grape leaf petiole transcriptome. Planta. 2012; 235(6):1383-96.
• [25]VAN DEN, BERG N, BERGER DK, HEIN I, BIRCH PRJ, WINGFIELD MJ et al.. Tolerance in banana to Fusarium wilt is associated with early up-regulation of cell wall-strengthening genes in the roots. Mol Plant Pathol. 2007; 8(3):333-41.
• [26]Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M et al.. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 2003; 17(8):1043-54.
• [27]Lu CA, Ho TH, Ho SL, Yu SM. Three novel MYB proteins with one DNA binding repeat mediate sugar and hormone regulation of alpha-amylase gene expression. Plant Cell. 2002; 14(8):1963-80.
• [28]Ruelland E, Vaultier M, Zachowski A, Hurry V. Cold Signaling and Cold Acclimation in Plants. Advances in Botanical Research. 2009, 49:35-150.
• [29]Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S. OST1 Kinase Modulates Freezing Tolerance by Enhancing ICE1 Stability in Arabidopsis. Dev Cell. 2015; 32(3):278-89.
• [30]Miura K, Ohta M, Nakazawa M, Ono M, Hasegawa PM. ICE1 Ser403 is necessary for protein stabilization and regulation of cold signaling and tolerance. Plant J. 2011; 67(2):269-79.
• [31]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):319-27.
• [32]Xu G, Rocha PSCF, Wang M, Xu M, Cui Y, Li L et al.. A novel rice calmodulin-like gene, OsMSR2, enhances drought and salt tolerance and increases ABA sensitivity in Arabidopsis. Planta. 2011; 234(1):47-59.
• [33]Du H, Liu H, Xiong L. Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci. 2013; 4:397.
• [34]Neuteboom LW, Ng JM, Kuyper M, Clijdesdale OR, Hooykaas PJ, van der Zaal BJ. Isolation and characterization of cDNA clones corresponding with mRNAs that accumulate during auxin-induced lateral root formation. Plant Mol Biol. 1999; 39(2):273-87.
• [35]Rohde P, Hincha DK, Heyer AG. Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance. Plant J. 2004; 38(5):790-9.
• [36]Lo Piero AR, Lo Cicero L, Puglisi I. The metabolic fate of citric acid as affected by cold storage in blood oranges. J Plant Biochem Biot. 2014; 23(2):161-6.
• [37]Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L. Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol. 2008; 67(1–2):169-81.
• [38]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(3):241-9.
• [39]Zhang Y, Chen C, Jin XF, Xiong AS, Peng RH, Hong YH et al.. Expression of a rice DREB1 gene, OsDREB1D, enhances cold and high-salt tolerance in transgenic Arabidopsis. BMB Rep. 2009; 42(8):486-92.
• [40]Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X 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(49):37636-45.
• [41]Peng Y, Bartley LE, Canlas P, Ronald PC. OsWRKY IIa Transcription Factors Modulate Rice Innate Immunity. Rice. 2010; 3(1):36-42.
• [42]Wang Q, Wang M, Zhang X, Hao B, Kaushik SK, Pan Y. WRKY gene family evolution in Arabidopsis thaliana. Genetica. 2011; 139(8):973-83.
• [43]Jakoby M, Weisshaar B, Dr Ge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj TPF. bZIP transcription factors in Arabidopsis. Trends Plant Sci. 2002; 7(3):106-11.
• [44]Yu G, Jiang L, Ma X, Xu Z, Liu M, Shan S et al.. A Soybean C2H2-Type Zinc Finger Gene GmZF1 Enhanced Cold Tolerance in Transgenic Arabidopsis. PLoS One. 2014; 9(10):e109399.
• [45]Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C et al.. Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci U S A. 2010; 107(32):14502-7.
• [46]Peng Y, Lin W, Wei H, Krebs SL, Arora R. Phylogenetic analysis and seasonal cold acclimation-associated expression of early light-induced protein genes of Rhododendron catawbiense. Physiol Plant. 2007; 132(1):44-52.
• [47]Hermans C, Porco S, Verbruggen N, Bush DR. Chitinase-Like Protein CTL1 Plays a Role in Altering Root System Architecture in Response to Multiple Environmental Conditions. Plant Physiol. 2010; 152(2):904-17.
• [48]Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NHT, Zhu S et al.. The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J. 2005; 24(14):2579-89.
• [49]Zhang M, Takano T, Liu S, Zhang X. Abiotic stress response in yeast and metal-binding ability of a type 2 metallothionein-like protein (PutMT2) from Puccinellia tenuiflora. Mol Biol Rep. 2014; 41(9):5839-49.
• [50]Izumi M, Tsunoda H, Suzuki Y, Makino A, Ishida H. RBCS1A and RBCS3B, two major members within the Arabidopsis RBCS multigene family, function to yield sufficient Rubisco content for leaf photosynthetic capacity. J Exp Bot. 2012; 63(5):2159-70.
• [51]Marri L, Pesaresi A, Valerio C, Lamba D, Pupillo P, Trost P et al.. In vitro characterization of Arabidopsis CP12 isoforms reveals common biochemical and molecular properties. J Plant Physiol. 2010; 167(12):939-50.
• [52]von Kampen J, Nieländer U, Wettern M. Expression of ubiquitin genes in Chlamydomonas reinhardtii: involvement in stress response and cell cycle. Planta. 1995; 197(3):528-34.
• [53]Ai-kui C, Rui-hong H, Dong-yang LI, Lian-lian L, Hui-xia L, Shang-jian T. A Comparison of Two Methods for Electrical Conductivity about Plant Leaves. J Guangdong Educ Inst. 2010, 5:018.