Physiology and Molecular Biology of Plants

, Volume 25, Issue 1, pp 31–45 | Cite as

Enriched networks ‘nucleoside/nucleotide and ribonucleoside/ribonucleotide metabolic processes’ and ‘response to stimulus’ potentially conferred to drought adaptation of the epiphytic orchid Dendrobium wangliangii

  • Dake Zhao
  • Yana Shi
  • Harini Anandhi Senthilkumar
  • Qin Qiao
  • Qiuxia Wang
  • Yong ShenEmail author
  • Guangwan HuEmail author
Research Article


Dendrobium wangliangii is an endangered and epiphytic orchid with tolerance to seasonally extreme arid conditions and occurs exclusively in the hot-dry valley area of southwestern China. To reveal its molecular basis responsible for ecological adaptation, large-scale transcriptome sequencing was performed using Illumina sequencing with pooled mRNA extracted from whole plants and pseudobulbs during drought and rainy seasons. Based on the target transcript selection, the differentially expressed genes were related to 8 well-known drought-tolerant categories, and to morphological traits in resistance to water stress including pseudobulbs and roots. Further gene ontology enrichment analysis revealed that ‘nucleoside/nucleotide and ribonucleoside/ribonucleotide metabolic processes’ and ‘response to stimulus’ were the two most important aspects in resistance to drought stress with respect to the whole plant. In addition, the difference in the number and category of differentially expressed genes in whole plant and stem suggested the involvement of genes specifically localized in the stem, such as GTP-binding protein, lipases, signaling related transcripts and those involved in the ATP metabolic process. The comprehensive analysis of the epiphytic orchid in response to water deprivation indicates that integral tactics lead to active adaptation as a basal defense response to drought stress by the endangered epiphyte, including the collaboration of metabolic processes, responses to a various stimulus and other candidate genes contribute to its extreme drought tolerance. Insights from this study can be further utilized to understand stress-responsive genes in other medicinally important species and to improve the drought tolerance of food crops.


Dendrobium wangliangii Drought adaptation Dry-hot valley Gene annotation Orchid Transcriptome 



This work was supported financially by the National Natural Science Foundation of China (31270244; 21362045; 81560622).

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  1. Alexa A, Rahnenfuhrer J (2016) topGO: enrichment analysis for gene ontology. R package version 2.27.0Google Scholar
  2. Asano T, Hayashi N, Kikuchi S, Ohsugi R (2012) CDPK-mediated abiotic stress signaling. Plant Signal Behav 7:817–821CrossRefGoogle Scholar
  3. Baldoni E, Genga A, Cominelli E (2015) Plant MYB transcription factors: their role in drought response mechanisms. Int J Mol Sci 16:15811–15851CrossRefGoogle Scholar
  4. Basu S, Ramegowda V, Kumar A, Pereira A (2016) Plant adaptation to drought stress. F1000 Res 5:1554CrossRefGoogle Scholar
  5. Bhardwaj J, Chauhan R, Swarnkar MK, Chahota RK, Singh AK, Shankar R, Yadav SK (2013) Comprehensive transcriptomic study on horse gram (Macrotyloma uniflorum): de novo assembly functional characterization and comparative analysis in relation to drought stress. BMC Genom 14:647CrossRefGoogle Scholar
  6. Bhardwaj AR, Joshi G, Kukreja B, Malik V, Arora P, Pandey R, Shukla RN, Bankar KG, Katiyar-Agarwal S, Goel S (2015) Global insights into high temperature and drought stress regulated genes by RNA-Seq in economically important oilseed crop Brassica juncea. BMC Plant Biol 15:9CrossRefGoogle Scholar
  7. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinform 10:421CrossRefGoogle Scholar
  8. Chaves MM, Oliveira MM (2014) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384CrossRefGoogle Scholar
  9. Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15:1196–1200CrossRefGoogle Scholar
  10. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676CrossRefGoogle Scholar
  11. Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626CrossRefGoogle Scholar
  12. Dixit S, Biswal AK, Min A, Henry A, Oane RH, Raorane ML, Longkumer T, Pabuayon IM, Mutte SK, Vardarajan AR, Miro B, Govindan G, Albano-Enriquez B, Pueffeld M, Sreenivasulu N, Slamet-Loedin I, Sundarvelpandian K, Tsai YC, Raghuvanshi S, Hsing YI, Kumar A, Kohli A (2015) Action of multiple intra-QTL genes concerted around a co-localized transcription factor underpins a large effect QTL. Sci Rep 5:15183CrossRefGoogle Scholar
  13. Dong Y, Wang C, Han X, Tang S, Liu S, Xia X, Yin W (2014) A novel bHLH transcription factor PebHLH35 from Populus euphratica confers drought tolerance through regulating stomatal development photosynthesis and growth in Arabidopsis. Biochem Biophys Res Commun 450:453–458CrossRefGoogle Scholar
  14. Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H, Brearley C, Hell R, Marin E, Pogson BJ (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012CrossRefGoogle Scholar
  15. Fan QJ, Yan FX, Qiao G, Zhang BX, Wen XP (2014) Identification of differentially-expressed genes potentially implicated in drought response in pitaya (Hylocereus undatus) by suppression subtractive hybridization and cDNA microarray analysis. Gene 533:322–331CrossRefGoogle Scholar
  16. Fang Y, Liao K, Du H, Xu Y, Song H, Li X, Xiong L (2015) A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J Exp Bot 66:6803–6817CrossRefGoogle Scholar
  17. Franco-Zorrilla JM, López-Vidriero I, Carrasco JL, Godoy M, Vera P, Solano R (2014) DNA-binding specificities of plant transcription factors and their potential to define target genes. Proc Natl Acad Sci 111:2367–2372CrossRefGoogle Scholar
  18. Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151CrossRefGoogle Scholar
  19. Gong X, Zhang J, Hu J, Wang W, Wu H, Zhang Q, Liu JH (2015) FcWRKY70 a WRKY protein of Fortunella crassifolia functions in drought tolerance and modulates putrescine synthesis by regulating arginine decarboxylase gene. Plant Cell Environ 38:2248–2262CrossRefGoogle Scholar
  20. Guo L, Yang H, Zhang X, Yang S (2013) Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Exp Bot 64:1755–1767CrossRefGoogle Scholar
  21. Guo H, Li Z, Zhou M, Cheng H (2014) cDNA-AFLP analysis reveals heat shock proteins play important roles in mediating cold heat and drought tolerance in Ammopiptanthus mongolicus. Funct Integr Genom 14:127–133CrossRefGoogle Scholar
  22. Ha S, Vankova R, Yamaguchishinozaki K, Shinozaki K, Tran LS (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17:172–179CrossRefGoogle Scholar
  23. He J, Norhafis H, Qin L (2013) Responses of green leaves and green pseudobulbs of CAM orchid Cattleya laeliocattleya Aloha case to drought stress. J Bot 2013:1–9CrossRefGoogle Scholar
  24. Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM ATAF and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci 103:12987–12992CrossRefGoogle Scholar
  25. Hu GW, Long CL, Jin XH (2008) Dendrobium wangliangii (Orchidaceae) a new species belonging to section Dendrobium from Yunnan China. Bot J Linn Soc 157:217–221CrossRefGoogle Scholar
  26. Huang L, Zhang F, Wang W, Zhou Y, Fu B, Li Z (2014) Comparative transcriptome sequencing of tolerant rice introgression line and its parents in response to drought stress. BMC Genom 15:1026CrossRefGoogle Scholar
  27. Joshi R, Wani SH, Singh B, Bohra A, Dar ZA, Lone AA, Pareek A, Singla-Pareek SL (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029CrossRefGoogle Scholar
  28. Komatsu K, Suzuki N, Kuwamura M, Nishikawa Y, Nakatani M, Ohtawa H, Takezawa D, Seki M, Tanaka M, Taji T, Hayashi T, Sakata Y (2013) Group A PP2Cs evolved in land plants as key regulators of intrinsic desiccation tolerance. Nat Commun 4:375–381Google Scholar
  29. Le DT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2012) Differential gene expression in soybean leaf tissues at late developmental stages under drought stress revealed by genome-wide transcriptome analysis. PLoS ONE 7:e49522CrossRefGoogle Scholar
  30. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323CrossRefGoogle Scholar
  31. Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260CrossRefGoogle Scholar
  32. Li H, Yao W, Fu Y, Li S, Guo Q (2015) De novo assembly and discovery of genes that are involved in drought tolerance in Tibetan Sophora moorcroftiana. PLoS ONE 10:e111054CrossRefGoogle Scholar
  33. Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6 a stress-responsive mitogen-activated protein kinase induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386–3399CrossRefGoogle Scholar
  34. Liu H, Sultan MARF, Liu X, Zhang J, Yu F, Zhao H (2015) Physiological and comparative proteomic analysis reveals different drought responses in roots and leaves of drought-tolerant wild wheat (Triticum boeoticum). PLoS ONE 10:e0121852CrossRefGoogle Scholar
  35. Magalhães AP, Verde N, Reis F, Martins I, Costa D, Lino-Neto T, Castro PH, Tavares RM, Azevedo H (2016) RNA-seq and gene network analysis uncover activation of an ABA-dependent signalosome during the cork oak root response to drought. Front Plant Sci 6:1195CrossRefGoogle Scholar
  36. Mittler R, Kim Y, Song L, Coutu J, Coutu A, Ciftci-Yilmaz S, Lee H, Stevenson B, Zhu JK (2006) Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett 580:6537–6542CrossRefGoogle Scholar
  37. Mizoi J, Ohori T, Moriwaki T, Kidokoro S, Todaka D, Maruyama K, Kusakabe K, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2013) GmDREB2A; 2 a canonical DEHYDRATION-RESPONSIVE ELEMENT-BINDING PROTEIN2-type transcription factor in soybean is post-translationally regulated and mediates dehydration-responsive element-dependent gene expression. Plant Physiol 161:346–361CrossRefGoogle Scholar
  38. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628CrossRefGoogle Scholar
  39. Müller T, Ensminger I, Schmid KJ (2012) A catalogue of putative unique transcripts from Douglas-fir (Pseudotsuga menziesii) based on 454 transcriptome sequencing of genetically diverse drought stressed seedlings. BMC Genom 13:673CrossRefGoogle Scholar
  40. Nakashima K, Jan A, Todaka D, Maruyama K, Goto S, Shinozaki K, Yamaguchi-Shinozaki K (2014) Comparative functional analysis of six drought-responsive promoters in transgenic rice. Planta 239:47–60CrossRefGoogle Scholar
  41. Ng CKY, Hew CS (2000) Orchid pseudobulbs- ‘false’ bulbs with a genuine importance in orchid growth and survival! Sci Hortic 83:165–172CrossRefGoogle Scholar
  42. Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought salt and abscisic acid responses and abscisic acid biosynthesis. Plant Cell 23:2169–2183CrossRefGoogle Scholar
  43. Osakabe Y, Osakabe K, Shinozaki K, Tran LSP (2014) Response of plants to water stress. Front Plant Sci 5:86CrossRefGoogle Scholar
  44. Padmalatha KV, Dhandapani G, Kanakachari M, Kumar S, Dass A, Patil DP, Rajamani V, Kumar K, Pathak R, Rawat B (2012) Genome-wide transcriptomic analysis of cotton under drought stress reveal significant down-regulation of genes and pathways involved in fibre elongation and up-regulation of defense responsive genes. Plant Mol Biol 78:223–246CrossRefGoogle Scholar
  45. Park SH, Jeong JS, Lee KH, Kim YS, Do Choi Y, Kim JK (2015) OsbZIP23 and OsbZIP45 members of the rice basic leucine zipper transcription factor family are involved in drought tolerance. Plant Biotech Rep 9:89–96CrossRefGoogle Scholar
  46. Robinson MD, McCarthy DJ, Smyth GK (2010) EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140CrossRefGoogle Scholar
  47. Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571CrossRefGoogle Scholar
  48. Seo PJ, Park C (2009) Auxin homeostasis during lateral root development under drought condition. Plant Signal Behav 4:1002–1004CrossRefGoogle Scholar
  49. Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 6:902CrossRefGoogle Scholar
  50. Shen H, Liu C, Zhang Y, Meng X, Zhou X, Chu C, Wang X (2012) OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol Biol 180:241–253CrossRefGoogle Scholar
  51. Singh D, Laxmi A (2015) Transcriptional regulation of drought response: a tortuous network of transcriptional factors. Front Plant Sci 6:895Google Scholar
  52. Stancato GC, Mazzafera P, Buckeridge MS (2001) Effect of a drought period on the mobilisation of non-structural carbohydrates photosynthetic efficiency and water status in an epiphytic orchid. Plant Physiol Biochem 39:1009–1016CrossRefGoogle Scholar
  53. Tian XJ, Long Y, Wang J, Zhang JW, Wang YY, Li WM, Peng YF, Yuan QH, Pei XW (2015) De novo transcriptome assembly of common wild rice (Oryza rufipogon Griff.) and discovery of drought-response genes in root tissue based on transcriptomic data. PLoS ONE 10:e0131455CrossRefGoogle Scholar
  54. Tognetti VB, Mühlenbock P, Van Breusegem F (2012) Stress homeostasis-the redox and auxin perspective. Plant Cell Environ 35:321–333CrossRefGoogle Scholar
  55. Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45:1097–1102CrossRefGoogle Scholar
  56. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing signaling and transport. Plant Cell Physiol 51:1821–1839CrossRefGoogle Scholar
  57. Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292:2070–2072CrossRefGoogle Scholar
  58. Weinl S, Kudla J (2009) The CBL-CIPK Ca2+ decoding signaling network: function and perspectives. New Phytol 184:517–528CrossRefGoogle Scholar
  59. Weng L, Zhao F, Li R, Xu C, Chen K, Xiao H (2015) The zinc finger transcription factor SlZFP2 negatively regulates abscisic acid biosynthesis and fruit ripening in tomato. Plant Physiol 167:931–949CrossRefGoogle Scholar
  60. Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322CrossRefGoogle Scholar
  61. Xiong L, Zhu J (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139CrossRefGoogle Scholar
  62. Xu Y, Gao S, Yang Y, Huang M, Cheng L, Wei Q, Fei Z, Gao J, Hong B (2013) Transcriptome sequencing and whole genome expression profiling of chrysanthemum under dehydration stress. BMC Genom 14:662CrossRefGoogle Scholar
  63. Yu S, Zhang F, Yu Y, Zhang D, Zhao X, Wang W (2012) Transcriptome profiling of dehydration stress in the Chinese cabbage (Brassica rapa L. ssp. pekinensis) by tag sequencing. Plant Mol Biol Rep 30:17–28CrossRefGoogle Scholar
  64. Zhang L, Zhao G, Xia C, Jia J, Liu X, Kong X (2012) A wheat R2R3-MYB gene TaMYB30-B improves drought stress tolerance in transgenic Arabidopsis. J Exp Bot 63:5873–5885CrossRefGoogle Scholar
  65. Zhang N, Liu B, Ma C, Zhang G, Chang J, Si H, Wang D (2014) Transcriptome characterization and sequencing-based identification of drought-responsive genes in potato. Mol Biol Rep 41:505–517CrossRefGoogle Scholar
  66. Zhao D, Hu G, Chen Z, Shi Y, Zheng L, Tang A, Long C (2013) Micropropagation and in vitro flowering of Dendrobium wangliangii: a critically endangered medicinal orchid. J Med Plants Res 7:2098–2110CrossRefGoogle Scholar
  67. Zhou S, Palmer M, Zhou J, Bhatti S, Howe KJ, Fish T, Thannhauser TW (2013) Differential root proteome expression in tomato genotypes with contrasting drought tolerance exposed to dehydration. J Am Soc Hortic 138:131–141Google Scholar
  68. Zotz G, Tyree MT (1996) Water stress in the epiphytic orchid Dimerandra emarginata (G. Meyer) Hoehne. Oecologia 107:151–159CrossRefGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2018

Authors and Affiliations

  1. 1.Biocontrol Engineering Research Center of Plant Disease and PestYunnan UniversityKunmingChina
  2. 2.Institute of Medicinal Plants, Yunnan Academy of Agricultural SciencesKunmingChina
  3. 3.Department of Biological Sciences, Lehman CollegeCity University of New YorkNew YorkUSA
  4. 4.School of AgricultureYunnan UniversityKunmingChina
  5. 5.Key Laboratory of Special Biological Resource Development and Utilization of Universities in Yunnan ProvinceKunming UniversityKunmingChina
  6. 6.College of Agriculture and Biotechnology, Yunnan Agricultural UniversityKunmingChina
  7. 7.Wuhan Botanical Garden, Chinese Academy of SciencesWuhanChina
  8. 8.Sino-Africa Joint Research Center, Chinese Academy of SciencesWuhanChina

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