Plant Molecular Biology Reporter

, Volume 33, Issue 4, pp 1075–1087 | Cite as

Gene Expression Profiles in Jatropha Under Drought Stress and During Recovery

  • Joyce A. CartagenaEmail author
  • Motoaki Seki
  • Maho Tanaka
  • Takaki Yamauchi
  • Shusei Sato
  • Hideki Hirakawa
  • Takashi Tsuge
Original Paper


Jatropha is known for its ability to grow in marginal lands and drought prone areas receiving limited amounts of rainfall. Accordingly, gene discovery in Jatropha will be useful for providing a source of genetic information for the improvement of drought tolerance in crops. In this study, gene expression profiling was performed using a newly developed Jatropha 44 K custom oligomicroarray on Jatropha plants subjected to drought stress and recovery from stress. When the gene expression patterns were compared between those differentially expressed during exposure to drought stress and re-watering, it was possible to identify 332 genes that are involved in the response to dehydration, while 585 genes were found to be significant during recovery, and 374 genes are associated with both dehydration and recovery. Furthermore, representative genes from the three gene categories were compared to those found in other plant species, and a basic understanding on how Jatropha copes with drought and its mechanism for survival in dry conditions is discussed. Taken together, the oligomicroarray that we developed in this study is a useful tool for analyzing expression profiles of Jatropha genes to better understand the molecular mechanism underlying drought stress responses as well as other aspects of molecular studies in Jatropha.


Jatropha Drought Recovery Microarray analysis 



This study was supported in part by Japan Science and Technology Agency (JST), Core Research for Evolutionary Science and Technology (CREST) and grants from the RIKEN Research Institute.

Supplementary material

11105_2014_815_MOESM1_ESM.xlsx (825 kb)
ESM 1 (XLSX 824 kb)


  1. Achten WMJ, Maes WH, Reubens B, Mathijs E, Singh VP, Verchotd L, Muys B (2010) Biomass production and allocation in Jatropha curcas L. seedlings under different levels of drought stress. Biomass Bioenergy 34:667–676CrossRefGoogle Scholar
  2. Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274PubMedCrossRefGoogle Scholar
  3. Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59:469–484PubMedCrossRefGoogle Scholar
  4. Aprile A, Havlickova L, Panna R, Mare C, Borrelli GM, Marone D, Perrotta C, Rampino P, De Bellis L, Curn V, Mastrangelo AM, Rizza F, Cattivelli L (2013) Different stress responsive strategies to drought and heat in two durum wheat cultivars with contrasting water use efficiency. BMC Genomics 14:821–839PubMedCentralPubMedCrossRefGoogle Scholar
  5. Battisti D, Naylor RL (2009) Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323:240–244PubMedCrossRefGoogle Scholar
  6. Caldas T, Demont-Caulet N, Ghazi A, Richarme G (1999) Thermoprotection by glycine betaine and choline. Microbiology 145:2543–2548PubMedGoogle Scholar
  7. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560PubMedCentralPubMedCrossRefGoogle Scholar
  8. Chen Y, Yang J, Wang Z, Zhang H, Mao X, Li C (2013) Gene structures, classification, and expression models of the DREB transcription factor subfamily in Populus trichocarpa. Sci World J. doi: 10.1155/2013/954640 Google Scholar
  9. Cho EK, Choi YJ (2009) A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants. Biotechnol Lett 31:597–606PubMedCrossRefGoogle Scholar
  10. Dos Santos CM, Verissimo V, Filho HCLW, Ferrreira VM, Cavalcante PGS, Rolim EV, Endres L (2013) Seasonal variations of photosynthesis, gas exchange, quantum efficiency of photosystem II and biochemical responses of Jatropha curcas L. grown in semi-humid and semi-arid areas subject to water stress. Ind Crop Prod 41:203–213CrossRefGoogle Scholar
  11. Eswaran N, Parameswaran S, Sathram B, Anantharaman B, Kumar GRK, Tangirala SJ (2010) Yeast functional screen to identify genetic determinants capable of conferring abiotic stress tolerance in Jatropha curcas. BMC Biotechnol 10:23–37PubMedCentralPubMedCrossRefGoogle Scholar
  12. Fornari M, Calvenzani V, Masiero S, Tonelli C, Petroni K (2013) The Arabidopsis NF-YA3 and NF-YA8 genes are functionally redundant and are required in early embryogenesis. PLoS ONE 8:e82043. doi: 10.1371/ journal.pone.0082043 PubMedCentralPubMedCrossRefGoogle Scholar
  13. Georges F, Das S, Ray H, Bock C, Nokhrina K, Kolla VA, Keller W (2009) Over-expression of Brassica napus phosphatidylinositolphospholipase C2 in canola induces significant changes in gene expression and phytohormone distribution patterns, enhances drought tolerance and promotes early flowering and maturation. Plant Cell Environ 32:1664–1681PubMedCrossRefGoogle Scholar
  14. Hackenberg D, Wu Y, Voigt A, Adams R, Schramm P, Grimm B (2012) Studies on differential nuclear translocation mechanism and assembly of the three subunits of the Arabidopsis thaliana transcription factor NF-Y. Mol Plant 5:876–888PubMedCrossRefGoogle Scholar
  15. Hayano-Kanashiro C, Calderón-Vázquez C, Ibarra-Laclette E, Herrera-Estrella L, Simpson J (2009) Analysis of gene expression and physiological responses in three Mexican maize landraces under drought stress and recovery irrigation. PLoS One 4(10):e7531. doi: 10.1371/journal.pone.0007531 PubMedCentralPubMedCrossRefGoogle Scholar
  16. Hu X, Liu R, Li Y, Wang W, Tai F, Xue R, Li C (2010) Heat shock protein 70 regulates the abscisic acid-induced antioxidant response of maize to combined drought and heat stress. Plant Growth Regul 60:225–235CrossRefGoogle Scholar
  17. IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  18. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333PubMedCrossRefGoogle Scholar
  19. Jia H, Zhang S, Ruan M, Wang Y, Wang C (2012) Analysis and application of RD29 genes in abiotic stress response. Acta Physiol Plant 34:1239–1250CrossRefGoogle Scholar
  20. Kakumanu A, Ambavaram MM, Klumas C, Krishnan A, Batlang U, Myers E, Grene R, Pereira A (2012) Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-seq. Plant Physiol 160:846–867PubMedCentralPubMedCrossRefGoogle Scholar
  21. Kheira AAA, Atta NMM (2009) Response of Jatropha curcas L. to water deficits: yield, water use efficiency and oil seed characteristics. Biomass Bioenergy 33:1343–1350CrossRefGoogle Scholar
  22. Krishnamurthy L, Zaman-Allah M, Marimuthu S, Wani SP, Rao AVRK (2012) Root growth in Jatropha and its implications for drought adaptation. Biomass Bioenergy 39:247–252CrossRefGoogle Scholar
  23. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633PubMedCentralPubMedCrossRefGoogle Scholar
  24. Le DT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Ham LH, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2012) Differential gene expression in soybean leaf tissues at late developmental stages under drought stress revealed by genome-wide transcriptome analysis. PLoS ONE 7:e49522. doi: 10.1371/journal.pone.0049522 PubMedCentralPubMedCrossRefGoogle Scholar
  25. Lenka SK, Katiyar A, Chinnusamy V, Bansal KC (2011) Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance. Plant Biotechnol J 9:315–327PubMedCrossRefGoogle Scholar
  26. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251PubMedCentralPubMedCrossRefGoogle Scholar
  27. Li YC, Meng FR, Zhang CY, Zhang N, Sun MS, Ren JP, Niu HB, Wang X, Yin J (2012) Comparative analysis of water stress-responsive transcriptomes in drought-susceptible and -tolerant wheat (Triticum aestivum L.). J Plant Biol 55:349–360CrossRefGoogle Scholar
  28. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45PubMedGoogle Scholar
  29. Minh-Thu P, Hwang D, Jeon J, Nahm BH, Kim Y (2013) Transcriptome analysis of leaf and root of rice seedling to acute dehydration. Rice 6:38–55PubMedCentralPubMedCrossRefGoogle Scholar
  30. Moore JP, Vicré-Gibouin M, Farrant JM, Driouich A (2008) Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plant 134:237–245PubMedCrossRefGoogle Scholar
  31. Moumeni A, Satoh K, Kondoh H, Asano T, Hosaka A, Venuprasad R, Serraj R, Kumar A, Leung H, Kikuchi S (2011) Comparative analysis of root transcriptome profiles of two pairs of drought-tolerant and susceptible rice near-isogenic lines under different drought stress. BMC Plant Biol 11:174–190PubMedCentralPubMedCrossRefGoogle Scholar
  32. Najafabadi MS (2012) Improving rice (Oryza sativa L.) drought tolerance by suppressing a NF-YA transcription factor. Iran J Biotechnol 10:40–48Google Scholar
  33. Nakashima K, Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1997) A nuclear gene, erd1, encoding a chloroplast-targeted Clp protease regulatory subunit homolog is not only induced by water stress but also developmentally up-regulated during senescence in Arabidopsis thaliana. Plant J 12:851–861PubMedCrossRefGoogle Scholar
  34. Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, Anstrom DC, Bensen RJ, Castiglioni PP, Donnarummo MG, Hinchey BS, Kumimoto RW, Maszle DR, Canales RD, Krolikowski KA, Dotson SB, Gutterson N, Ratcliffe OJ, Heard JE (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci U S A 104:16450–16455PubMedCentralPubMedCrossRefGoogle Scholar
  35. Niu G, Rodriguez D, Mendoza M, Jifon J, Ganjegunte G (2012) Responses of Jatropha curcas to salt and drought stresses. Int J Agron. doi: 10.1155/2012/632026 Google Scholar
  36. Oono Y, Seki M, Nanjo T, Narusaka M, Fujita M, Satoh R, Satou M, Sakurai T, Ishida J, Akiyama K, Iida K, Maruyama K, Satoh S, Yamaguchi-Shinozaki K, Shinozaki K (2003) Monitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca 7000 full-length cDNA microarray. Plant J 34:868–887PubMedCrossRefGoogle Scholar
  37. Orfila C, Dal Degan F, Jørgensen B, Scheller HV, Ray PM, Ulvskov P (2012) Expression of mung bean pectin acetyl esterase in potato tubers: effect on acetylation of cell wall polymers and tuber mechanical properties. Planta 236:185–196PubMedCrossRefGoogle Scholar
  38. Perrone I, Pagliarani C, Lovisolo C, Chitarra W, Roman F, Schubert A (2012) Recovery from water stress affects grape leaf petiole transcriptome. Planta 235:1383–1396PubMedCrossRefGoogle Scholar
  39. Pompelli MF, Barata-Luís RM, Vitorino HS, Goncalves ER, Rolim EV, Santosa MG, Almeida-Corteza JS, Ferreirac VM, Lemosc EE, Endres L (2010) Photosynthesis, photoprotection and antioxidant activity of purging nut under drought deficit and recovery. Biomass Bioenergy 34:1207–1215CrossRefGoogle Scholar
  40. Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 25:163–171PubMedCrossRefGoogle Scholar
  41. Sakuma Y, Maruyama K, Osakabe Y, Feng Q, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309PubMedCentralPubMedCrossRefGoogle Scholar
  42. Sampedro J, Cosgrove DJ (2005) The expansin superfamily. Genome Biol 6:242PubMedCentralPubMedCrossRefGoogle Scholar
  43. Sapeta H, Costa JM, Lourenço T, Maroco J, van der Linde P, Oliveira MM (2013) Drought stress response in Jatropha curcas: growth and physiology. Environ Exp Bot 85:76–84CrossRefGoogle Scholar
  44. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292PubMedCrossRefGoogle Scholar
  45. Shan X, Li Y, Jiang Y, Jiang Z, Hao W, Yuan Y (2013) Transcriptome profile analysis of maize seedlings in response to high-salinity, drought and cold stresses by deep sequencing. Plant Mol Biol Rep 31:1485–1491CrossRefGoogle Scholar
  46. Smart LB, Moskal WA, Cameron KD, Bennett AB (2001) MIP genes are down-regulated under drought stress in Nicotiana glauca. Plant Cell Physiol 42:686–693PubMedCrossRefGoogle Scholar
  47. Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426PubMedCrossRefGoogle Scholar
  48. Tang M, Sun J, Liu Y, Chen F, Shen S (2007) Isolation and functional characterization of the JcERF gene, a putative AP2/EREBP domain-containing transcription factor, in the woody oil plant Jatropha curcas. Plant Mol Biol 63:419–428PubMedCrossRefGoogle Scholar
  49. Thao NP, Thu NBA, Hoang XLT, Ha CV, Tran LSP (2013) Differential expression analysis of a subset of drought-responsive GmNAC genes in two soybean cultivars differing in drought tolerance. Int J Mol Sci 14:23828–23841PubMedCentralPubMedCrossRefGoogle Scholar
  50. Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498PubMedCentralPubMedCrossRefGoogle Scholar
  51. Utsumi Y, Tanaka M, Morosawa T, Kurotani A, Yoshida T, Mochida K, Matsui A, Umemura Y, Ishitani M, Shinozaki K, Sakurai T, Seki M (2012) Transcriptome analysis using a high-density oligo microarray under drought stress in various genotypes of cassava, an important tropical crop. DNA Res 19:335–345PubMedCentralPubMedCrossRefGoogle Scholar
  52. Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14PubMedCrossRefGoogle Scholar
  53. Wang XS, Zhu HB, Jin GL, Liu HL, Wu WR, Zhu J (2007) Genome-scale identification and analysis of LEA genes in rice (Oryza sativa L.). Plant Sci 172:414–420CrossRefGoogle Scholar
  54. Wang CR, Yang AF, Yue GD, Gao Q, Yin HY, Zhang JR (2008) Enhanced expression of phospholipase C 1 (ZmPLC1) improves drought tolerance in transgenic maize. Planta 227:1127–1140PubMedCrossRefGoogle Scholar
  55. Xie YJ, Xu S, Han B, Wu MZ, Yuan XX, Han Y, Gu Q, Xu DK, Yang Q, Shen WB (2011) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J 66:280–292PubMedCrossRefGoogle Scholar
  56. Yamaguchi-Shinozaki K, Shinozaki K (1993) Arabidopsis DNA encoding two desiccation-responsive RD29 genes. Plant Physiol 101:1119–1120PubMedCentralPubMedCrossRefGoogle Scholar
  57. Yamauchi T, Watanabe K, Fukazawa A, Mori H, Abe F, Kawaguchi K, Oyanagi A, Nakazono M (2014) Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions. J Exp Bot 65:261–273PubMedCentralPubMedCrossRefGoogle Scholar
  58. Yang ZB, Eticha D, Führs H, Heintz D, Ayoub D, Van Dorsselaer A, Schlingmann B, Rao IM, Braun HP, Horst WJ (2013) Proteomic and phosphoproteomic analysis of polyethylene glycol-induced osmotic stress in root tips of common bean (Phaseolus vulgaris L.). J Exp Bot 64:5569–5586PubMedCentralPubMedCrossRefGoogle Scholar
  59. Zhang Y, Wang Y, Jiang L, Xu Y, Wang Y, Lu D, Chen F (2007) Aquaporin JcPIP2 is involved in drought responses in Jatropha curcas. Acta Biochim Biophys Sin (Shanghai) 39:787–794CrossRefGoogle Scholar
  60. Zhang FL, Niu B, Wang YC, Chen F, Wang SH, Xu Y, Jiang LD, Gao S, Wu J, Tang L, Jia YJA (2008) A novel betaine aldehyde dehydrogenase gene from Jatropha curcas, encoding an enzyme implicated in adaptation to environmental stress. Plant Sci 174:510–518CrossRefGoogle Scholar
  61. Zhang H, Zhang J, Quan R, Pan X, Wan L, Huang R (2013) EAR motif mutation of rice OsERF3 alters the regulation of ethylene biosynthesis and drought tolerance. Planta 237:1443–1451PubMedCrossRefGoogle Scholar
  62. Zheng J, Fu J, Gou M, Huai J, Liu Y, Jian M, Huang Q, Guo X, Dong Z, Wang H, Wang G (2010) Genome-wide transcriptome analysis of two maize inbred lines under drought stress. Plant Mol Biol 72:407–421PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Joyce A. Cartagena
    • 1
    Email author
  • Motoaki Seki
    • 2
    • 3
  • Maho Tanaka
    • 2
  • Takaki Yamauchi
    • 1
  • Shusei Sato
    • 4
    • 5
  • Hideki Hirakawa
    • 5
  • Takashi Tsuge
    • 1
  1. 1.Graduate School of Bioagricultural SciencesNagoya UniversityNagoyaJapan
  2. 2.Plant Genomic Network Research TeamRIKEN Center for Sustainable Resource ScienceYokohamaJapan
  3. 3.Core Research for Evolutional Science and TechnologyJapan Science and TechnologyKawaguchiJapan
  4. 4.Graduate School of Life SciencesTohoku UniversitySendaiJapan
  5. 5.Kazusa DNA Research InstituteKisarazuJapan

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