Global gene expression pattern in a forest tree species, Tectona grandis (Linn. F.), under limited water supply

  • Abhinandan Mani Tripathi
  • Amrita Yadav
  • Siddhartha Proteem Saikia
  • Sribash Roy
Original Article
Part of the following topical collections:
  1. Gene Expression


Global climate change phenomena have led to drought-like situation in many parts of the world. This has major impact on forest growth and development. Among forest tree species, Tectona grandis, commonly known as Teak, is one of the important forest tree species. Limited water availability during early stage of Teak sapling establishment leads to failure in various reforestation programs. Here, we report how global gene expression is affected in Teak sapling during limited water availability (DT) against well watered (DC). The RNA sequencing of combined libraries of DT and DC retrieved 142,539 contigs, assembled in to 110,374 unigenes. Overall, 63,265 unigenes (57%) were annotated against different data bases. Analysis of the most significant gene ontology terms indicated metabolic process, transport process, and response to stress were the important pathways affected during limited water supply. Among the primary metabolic processes, carbohydrate metabolisms related genes were significantly upregulated in DT followed by protein and lipid metabolisms. On the other hand, the major unigenes of secondary metabolic processes upregulated in DT were laccase/diphenol oxidase family protein (8.7-fold), cytochrome P450 family (8.0-fold), and S-adenosyl methionine synthetase family protein (7.4-fold). Further, a total of 34,707 potential simple sequence repeats (SSRs) and 4215 primers were identified from T. grandis transcripts. The differentially expressed transcripts identified in our study provide primary information about key genes in stress response and performing functional analysis to reveal their roles in stress adaptation in plants, especially in forest tree species.


Drought Enrichment Teak Sapling De novo assembly Forest India 



The authors are thankful to Department of Biotechnology (DBT), Government of India for financial support. The project was supported by DBT via project No. BT/PR3544/PBD/16/953/2011. The authors acknowledge University Grant Commission, New Delhi, for fellowship to AMT.

Compliance with ethical standards

Conflict of interest

The authors declared that they have no competing interests.

Supplementary material

11295_2017_1151_MOESM1_ESM.xlsx (15 kb)
Supplementary Table S1 (XLSX 15 kb)
11295_2017_1151_MOESM2_ESM.xlsx (234 kb)
Supplementary Table S2 (XLSX 233 kb)
11295_2017_1151_MOESM3_ESM.xlsx (40 kb)
Supplementary Table S3 (XLSX 39 kb)
11295_2017_1151_MOESM4_ESM.xlsx (16 kb)
Supplementary Table S4 (XLSX 15 kb)
11295_2017_1151_MOESM5_ESM.xlsx (411 kb)
Supplementary Table S5 (XLSX 410 kb)


  1. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought-and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868PubMedPubMedCentralGoogle Scholar
  2. Allen CD, Breshears DD (1998) Drought-induced shift of a forest–woodland ecotone: rapid landscape response to climate variation. Proc Natl Acad Sci 95:14839–14842CrossRefPubMedPubMedCentralGoogle Scholar
  3. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg ET (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684CrossRefGoogle Scholar
  4. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:1CrossRefGoogle Scholar
  5. Backlund P, Janetos A, Schimel D et al (2008) The effects of climate change on agriculture, land resources, water resources, and biodiversity in the United States. In: The effects of climate change on agriculture, land resources, water resources, and biodiversity in the United States. US Climate Change Science Program, Washington, DCGoogle Scholar
  6. Barnett NM, Naylor A (1966) Amino acid and protein metabolism in Bermuda grass during water stress. Plant Physiol 41:1222–1230CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bernstein L, Bosch P, Canziani O, Chen Z, Christ R, Davidson O (2007) Climate change 2007: synthesis report. Summary for policymakers. In: Climate change 2007: synthesis report. Summary for policymakers. IPCC, GenevaGoogle Scholar
  8. Bhat KM et al (2005) Quality timber products of teak from sustainable forest management. In: International Conference on Quality Timber Products of Teak from Sustainable Forest Management (2003: Kerala Forest Research Institute). International Tropical Timber Organization, PeechiGoogle Scholar
  9. Bigler C, Bräker OU, Bugmann H, Dobbertin M, Rigling A (2006) Drought as an inciting mortality factor in scots pine stands of the Valais, Switzerland. Ecosystems 9:330–343CrossRefGoogle Scholar
  10. Bouchabke O, Chang F, Simon M, Voisin R, Pelletier G, Durand-Tardif M (2008) Natural variation in Arabidopsis thaliana as a tool for highlighting differential drought responses. PLoS One 3:e1705CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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 (BBA)-Gene Regulatory Mechanisms 1819:120–128CrossRefGoogle Scholar
  12. Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang H-S, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chini A, Grant JJ, Seki M, Shinozaki K, Loake GJ (2004) Drought tolerance established by enhanced expression of the CC–NBS–LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J 38:810–822CrossRefPubMedGoogle Scholar
  14. Chu X, Wang C, Chen X, Lu W, Li H, Wang X, Hao L, Guo X (2015) The cotton WRKY gene GhWRKY41 positively regulates salt and drought stress tolerance in transgenic Nicotiana Benthamiana. PLoS One 10:e0143022CrossRefPubMedPubMedCentralGoogle Scholar
  15. Engelbrecht BM, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL, Hubbell SP (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–82CrossRefPubMedGoogle Scholar
  16. Ferreira TH, Gentile A, Vilela RD, Costa GGL, Dias LI, Endres L, Menossi M (2012) microRNAs associated with drought response in the bioenergy crop sugarcane (Saccharum spp.) PLoS One 7:e46703CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fofana IJ, Ofori D, Poitel M, Verhaegen D (2009) Diversity and genetic structure of teak (Tectona grandis lf) in its natural range using DNA microsatellite markers. New For 37:175–195CrossRefGoogle Scholar
  18. Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK (2005) Global consequences of land use. Science 309:570–574CrossRefPubMedGoogle Scholar
  19. Galeano E, Vasconcelos TS, Vidal M, Mejia-Guerra MK, Carrer H (2015) Large-scale transcriptional profiling of lignified tissues in Tectona grandis. BMC Plant Biol 15:221CrossRefPubMedPubMedCentralGoogle Scholar
  20. Ghanti SKK, Sujata K, Kumar BV, Karba NN, Janardhan Reddy K, Rao MS, Kishor PK (2011) Heterologous expression of P5CS gene in chickpea enhances salt tolerance without affecting yield. Biol Plant 55:634–640CrossRefGoogle Scholar
  21. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652CrossRefPubMedPubMedCentralGoogle Scholar
  22. Granier C, Aguirrezabal L, Chenu K, Cookson SJ, Dauzat M, Hamard P, Thioux JJ, Rolland G, Bouchier-Combaud S, Lebaudy A (2006) PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytol 169:623–635CrossRefPubMedGoogle Scholar
  23. Hadiarto T, Tran L-SP (2011) Progress studies of drought-responsive genes in rice. Plant Cell Rep 30:297–310CrossRefPubMedGoogle Scholar
  24. Hamanishi ET, Campbell MM (2011) Genome-wide responses to drought in forest trees. Forestry:cpr012Google Scholar
  25. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466CrossRefPubMedPubMedCentralGoogle Scholar
  26. Heath LS, Ramakrishnan N, Sederoff RR, Whetten RW, Chevone BI, Struble CA, Jouenne VY, Chen D, Van Zyl L, Grene R (2002) Studying the functional genomics of stress responses in loblolly pine with the expresso microarray experiment management system. Comparative and Functional Genomics 3:226–243CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hiremath PJ, Farmer A, Cannon SB, Woodward J, Kudapa H, Tuteja R, Kumar A, BhanuPrakash A, Mulaosmanovic B, Gujaria N (2011) Large-scale transcriptome analysis in chickpea (Cicer arietinum L.), an orphan legume crop of the semi-arid tropics of Asia and Africa. Plant Biotechnol J 9:922–931CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hong Y, Zhang H, Huang L, Li D, Song F (2016) Overexpression of a stress-responsive NAC transcription factor Gene ONAC022 improves drought and salt tolerance in Rice. Front Plant Sci 7Google Scholar
  29. Hussain SS, Kayani MA, Amjad M (2011) Transcription factors as tools to engineer enhanced drought stress tolerance in plants. Biotechnol Prog 27:297–306CrossRefPubMedGoogle Scholar
  30. Iordachescu M, Imai R (2008) Trehalose biosynthesis in response to abiotic stresses. J Integr Plant Biol 50:1223–1229CrossRefPubMedGoogle Scholar
  31. Jia H, Wang C, Wang F, Liu S, Li G, Guo X (2015) GhWRKY68 reduces resistance to salt and drought in transgenic Nicotiana Benthamiana. PLoS One 10:e0120646CrossRefPubMedPubMedCentralGoogle Scholar
  32. Jones H, Corlett J (1992) Current topics in drought physiology. J Agric Sci 119:291–296CrossRefGoogle Scholar
  33. Julius S, West J, Joyce LA, Kareiva P, Keller BD, Palmer M, Peterson C (2008) Preliminary review of adaptation options for climate-sensitive ecosystems and resources. National Parks 1Google Scholar
  34. Kaosa-ard A (1981) Teak (Tectona grandis Linn. f) its natural distribution and related factors. Nat His Bulletin Siam Soc 29:55–74Google Scholar
  35. Klute (1986) A physical and mineralogical methods, methods of soil analysis. Am. Soc. of Agronomy, lnc., Soil Sc. Soc. of Am., Inc. Madison, Washington, USAGoogle Scholar
  36. Kollert W, Cherubini L (2012) Teak resources and market assessment 2010. FAO Planted Forests and Trees Working Paper FP/47/E, RomeGoogle Scholar
  37. Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lawlor DW (2013) Genetic engineering to improve plant performance under drought: physiological evaluation of achievements, limitations, and possibilities. J Exp Bot 64:83–108CrossRefPubMedGoogle Scholar
  39. Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain J-L, Laloi M, Coutos-Thévenot P, Maurousset L (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272CrossRefPubMedPubMedCentralGoogle Scholar
  40. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC bioinformatics 12:1CrossRefGoogle Scholar
  41. Lu P-L, Chen N-Z, An R, Su Z, Qi B-S, Ren F, Chen J, Wang X-C (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 63:289–305CrossRefPubMedGoogle Scholar
  42. Ludlow M, Muchow R (1990) A critical evaluation of traits for improving crop yields in water-limited environments. Adv Agron 43:107–153CrossRefGoogle Scholar
  43. Lyngdoh N, Joshi G, Ravikanth G, Shaanker RU, Vasudeva R (2010) Influence of levels of genetic diversity on fruit quality in teak (Tectona grandis lf). Curr Sci 99:639–644Google Scholar
  44. Lyngdoh N, Joshi G, Ravikanth G, Vasudeva R, Shaanker RU (2013) Changes in genetic diversity parameters in unimproved and improved populations of teak (Tectona grandis lf) in Karnataka state, India. J Genet 92:141CrossRefPubMedGoogle Scholar
  45. Ma Y, Qin F, Tran L-SP (2012) Contribution of genomics to gene discovery in plant abiotic stress responses. Mol Plant 5:1176–1178CrossRefPubMedGoogle Scholar
  46. Mizutani M, Ohta D (2010) Diversification of P450 genes during land plant evolution. Annu Rev Plant Biol 61:291–315CrossRefPubMedGoogle Scholar
  47. Mochida K, Shinozaki K (2011) Advances in omics and bioinformatics tools for systems analyses of plant functions. Plant Cell Physiol 52:2017–2038CrossRefPubMedPubMedCentralGoogle Scholar
  48. Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP (2010) Genome-wide analysis of two-component systems and prediction of stress-responsive two-component system members in soybean. DNA Res 17:303–324CrossRefPubMedPubMedCentralGoogle Scholar
  49. Nelson D, Werck-Reichhart D (2011) A P450-centric view of plant evolution. Plant J 66:194–211CrossRefPubMedGoogle Scholar
  50. Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4:248Google Scholar
  51. Oono Y, Seki M, Nanjo T, Narusaka M, Fujita M, Satoh R, Satou M, Sakurai T, Ishida J, Akiyama K (2003) Monitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca. 7000 full-length cDNA microarray. Plant J 34:868–887CrossRefPubMedGoogle Scholar
  52. Palupi E, Owens J, Sadjad S, Sudarsono S, Solihin D (2010) The importance of fruit set, fruit abortion, and pollination success in fruit production of teak (Tectona grandis). Can J For Res 40:2204–2214CrossRefGoogle Scholar
  53. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655CrossRefPubMedPubMedCentralGoogle Scholar
  54. Parvathi M, Nataraja KN, Yashoda B, Ramegowda H, Mamrutha H, Rama N (2013) Expression analysis of stress responsive pathway genes linked to drought hardiness in an adapted crop, finger millet (Eleusine coracana). J Plant Biochem Biotechnol 22:193–201CrossRefGoogle Scholar
  55. Prinz K, Finkeldey R (2014) Genetic variation of teak (Tectona grandis Linn. F.) in Myanmar revealed by microsatellites. Tree Genet Genomes 10:1435–1449CrossRefGoogle Scholar
  56. Reina-Bueno M, Argandoña M, Nieto JJ, Hidalgo-García A, Iglesias-Guerra F, Delgado MJ, Vargas C (2012) Role of trehalose in heat and desiccation tolerance in the soil bacterium rhizobium etli. BMC Microbiol 12:1CrossRefGoogle Scholar
  57. Rodziewicz P, Swarcewicz B, Chmielewska K, Wojakowska A, Stobiecki M (2014) Influence of abiotic stresses on plant proteome and metabolome changes. Acta Physiol Plant 36:1–19CrossRefGoogle Scholar
  58. Roy S (2016) Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome. Plant Signal Behav 11:e1117723CrossRefPubMedGoogle Scholar
  59. Samuel D, Kumar TKS, Ganesh G, Jayaraman G, Yang P-W, Chang M-M, Trivedi VD, Wang S-L, Hwang K-C, Chang D-K (2000) Proline inhibits aggregation during protein refolding. Protein Sci 9:344–352CrossRefPubMedPubMedCentralGoogle Scholar
  60. Saxe H, Cannell MG, Johnsen Ø, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytol 149:369–399CrossRefGoogle Scholar
  61. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108CrossRefPubMedGoogle Scholar
  62. Shaw JD, Steed BE, DeBlander LT (2005) Forest inventory and analysis (FIA) annual inventory answers the question: what is happening to pinyon-juniper woodlands? J For 103:280–285Google Scholar
  63. Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327CrossRefPubMedPubMedCentralGoogle Scholar
  64. Shrestha MK, Volkaert H, Straeten DVD (2005) Assessment of genetic diversity in Tectona grandis using amplified fragment length polymorphism markers. Can J For Res 35:1017–1022CrossRefGoogle Scholar
  65. Solomon EI, Sundaram UM, Machonkin TE (1996) Multicopper oxidases and oxygenases. Chem Rev 96:2563–2606CrossRefPubMedGoogle Scholar
  66. Sreekanth P, Balasundaran M, Nazeem P, Suma T (2012) Genetic diversity of nine natural Tectona grandis lf populations of the western Ghats in southern India. Conserv Genet 13:1409–1419CrossRefGoogle Scholar
  67. Sun TP (2008) Gibberellin metabolism, perception and signaling pathways in Arabidopsis. The Arabidopsis Book 6:e0103Google Scholar
  68. Tamiru M, Undan JR, Takagi H, Abe A, Yoshida K, Undan JQ, Natsume S, Uemura A, Saitoh H, Matsumura H (2015) A cytochrome P450, OsDSS1, is involved in growth and drought stress responses in rice (Oryza sativa L.) Plant Mol Biol 88:85–99CrossRefPubMedGoogle Scholar
  69. Tang S, Dong Y, Liang D, Zhang Z, Ye C-Y, Shuai P, Han X, Zhao Y, Yin W, Xia X (2015) Analysis of the drought stress-responsive transcriptome of black cottonwood (Populus trichocarpa) using deep RNA sequencing. Plant Mol Biol Report 33:424–438CrossRefGoogle Scholar
  70. Tang S, Liang H, Yan D, Zhao Y, Han X, Carlson JE, Xia X, Yin W (2013) Populus Euphratica: the transcriptomic response to drought stress. Plant Mol Biol 83:539–557CrossRefPubMedGoogle Scholar
  71. Tewari DN (1992) A monograph on teak (Tectona grandis Linn. f.). International book distributorsGoogle Scholar
  72. Thiel T, Michalek W, Varshney R, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.) Theor Appl Genet 106:411–422CrossRefPubMedGoogle Scholar
  73. Tran L-SP, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci 104:20623–20628CrossRefPubMedPubMedCentralGoogle Scholar
  74. Trossat C, Rathinasabapathi B, Weretilnyk EA, Shen T-L, Huang Z-H, Gage DA, Hanson AD (1998) Salinity promotes accumulation of 3-dimethylsulfoniopropionate and its precursor S-methylmethionine in chloroplasts. Plant Physiol 116:165–171CrossRefPubMedPubMedCentralGoogle Scholar
  75. Umezawa T, Yoshida R, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proc Natl Acad Sci U S A 101:17306–17311CrossRefPubMedPubMedCentralGoogle Scholar
  76. Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:189–195CrossRefPubMedGoogle Scholar
  77. Van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fulé PZ, Harmon ME, Larson AJ, Smith JM, Taylor AH (2009) Widespread increase of tree mortality rates in the western United States. Science 323:521–524CrossRefPubMedGoogle Scholar
  78. Verhaegen D, Ofori D, Fofana I, Poitel M, Vaillant A (2005) Development and characterization of microsatellite markers in Tectona grandis (Linn. F). Mol Ecol Notes 5:945–947CrossRefGoogle Scholar
  79. Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20CrossRefPubMedGoogle Scholar
  80. Wang KL-C, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151PubMedPubMedCentralGoogle Scholar
  81. Watanabe S, Kojima K, Ide Y, Sasaki S (2000) Effects of saline and osmotic stress on proline and sugar accumulation in Populus Euphratica in vitro. Plant Cell Tissue Organ Cult 63:199–206CrossRefGoogle Scholar
  82. Yamada M, Morishita H, Urano K, Shiozaki N, Yamaguchi-Shinozaki K, Shinozaki K, Yoshiba Y (2005) Effects of free proline accumulation in petunias under drought stress. J Exp Bot 56:1975–1981CrossRefPubMedGoogle Scholar
  83. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803CrossRefPubMedGoogle Scholar
  84. Yang S, Vanderbeld B, Wan J, Huang Y (2010) Narrowing down the targets: towards successful genetic engineering of drought-tolerant crops. Mol Plant 3:469–490CrossRefPubMedGoogle Scholar
  85. Zhao R, Wang X-F, Zhang D-P (2011) CPK12: a Ca2+−dependent protein kinase balancer in abscisic acid signaling. Plant Signal Behav 6:1687–1690CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Abhinandan Mani Tripathi
    • 1
    • 2
  • Amrita Yadav
    • 1
  • Siddhartha Proteem Saikia
    • 3
  • Sribash Roy
    • 1
    • 2
  1. 1.Division of Genetics and Molecular BiologyCSIR-National Botanical Research InstituteLucknowIndia
  2. 2.Academy of Scientific and Innovative Research (AcSIR)New DelhiIndia
  3. 3.Biological Sciences and Technology DivisionCSIR-North East Institute of Science & TechnologyJorhatIndia

Personalised recommendations