A step towards understanding plant responses to multiple environmental stresses: A genome-wide study

Plant, Cell and Environment

Volumn 37, Issue 9, 2014, Pages 2024-2035

  Sewelam, Nasser ^a,b   Oshima, Yoshimi ^a   Mitsuda, Nobutaka ^a   Ohme Takagi, Masaru ^a,c  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b Tanta University   (Egypt)

^c SAITAMA UNIVERSITY   (Japan)

Author keywords

Abiotic stress; Arabidopsis; Heat; High salinity; Microarray; Multiple stresses; Osmotic stress

Indexed keywords

ARABIDOPSIS;

TRANSCRIPTOME;

ARABIDOPSIS; DESERT CLIMATE; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETICS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENE; PLANT GENOME; REGULATORY SEQUENCE; UPREGULATION;

ARABIDOPSIS; DESERT CLIMATE; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC ASSOCIATION STUDIES; GENOME, PLANT; REGULATORY SEQUENCES, NUCLEIC ACID; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME; UP-REGULATION;

EID: 84905002128     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12274     Document Type: Article

References (51)

1. Abe H., Urao T., Ito T., Seki M., Shinozaki K. & Yamaguchi-Shinozaki K. (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. The Plant Cell 15, 63-78.
2. Anderson J.P., Badruzsaufari E., Schenk P.M., Manners J.M., Desmond O.J., Ehlert C., ... Kazan K. (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. The Plant Cell 16, 3460-3479.
3. Benedict C., Geisler M., Trygg J., Huner N. & Hurry V. (2006) Consensus by democracy. Using meta-analyses of microarray and genomic data to model the cold acclimation signaling pathway in Arabidopsis. Plant Physiology 141, 1219-1232.
4. Benjamini Y. & Hochberg Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B 57, 289-300.
5. Bray E.A., Bailey-Serres J. & Weretilnyk E. (2000) Responses to abiotic stress. In Biochemistry and Molecular Biology of Plants (eds B.B. Buchanan, W. Gruissem & R.L. Jones ) pp. 1158-1203. American Society of Plant Biologists, Rockville, MD.
6. Cheong Y.H., Chang H.S., Gupta R., Wang X., Zhu T. & Luan S. (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiology 129, 661-677.
7. Feder M.E. & Hofmann G.E. (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61, 243-282.
8. Goyal K., Walton L.J. & Tunnacliffe A. (2005) LEA proteins prevent protein aggregation due to water stress. The Biochemical Journal 388, 151-157.
9. 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. Journal of Experimental Botany 64, 1755-1767.
10. de Hoon M.J.L., Imoto S., Nolan J. & Miyano S. (2004) Open source clustering software. Bioinformatics (Oxford, England) 20, 1453-1454.
11. Huang J., Minnis P., Yan H., Yi Y., Chen B., Zhang L. & Ayers J.K. (2010) Dust aerosol effect on semi-arid climate over Northwest China detected from A-Train satellite measurements. Atmospheric Chemistry and Physics 10, 6863-6872.
12. Ikeda M., Mitsuda N. & Ohme-Takagi M. (2011) Arabidopsis hsfB1 and hsfB2b act as repressors of the expression of heat-inducible hsfs but positively regulate the acquired thermotolerance. Plant Physiology 157, 1243-1254.
13. Kilian J., Whitehead D., Horak J., Wanke D., Weinl S., Batistic O., ... Harter K. (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. The Plant Journal 50, 347-363.
14. Kishor P., Hong Z., Miao G.H., Hu C. & Verma D. (1995) Overexpression of [delta]-pyrroline-5-Carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiology 108, 1387-1394.
15. Kreps J.A., Wu Y., Chang H.S., Zhu T., Wang X. & Harper J.F. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology 130, 2129-2141.
16. Krishnaswamy S., Verma S., Rahman M.H. & Kav N.N. (2011) Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis. Plant Molecular Biology 75, 107-127.
17. Kuhl N.M. & Rensing L. (2000) Heat shock effects on cell cycle progression. Cellular and Molecular Life Sciences 57, 450-463.
18. Kumar S.V. & Wigge P.A. (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136-147.
19. Lang V. & Palva E.T. (1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) heynh. Plant Molecular Biology 20, 951-962.
20. Larkindale J. & Vierling E. (2008) Core genome responses involved in acclimation to high temperature. Plant Physiology 146, 748-761.
21. Lee K.H., Piao H.L., Kim H.Y., Choi S.M., Jiang F., Hartun W., ... Hwang I. (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126, 1109-1120.
22. Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K. & Shinozaki K. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell 10, 1391-1406.
23. Matsui A., Ishida J., Morosawa T., Mochizuki Y., Kaminuma E., Endo T.A., ... Seki M. (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant and Cell Physiology 49, 1135-1149.
24. Nishizawa A., Yabuta Y., Yoshida E., Maruta T., Yoshimura K. & Shigeoka S. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. The Plant Journal 48, 535-547.
25. Prasch C.M. & Sonnewald U. (2013) Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiology 162, 1849-1866.
26. R Development Core Team (2008) R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria. Retrieved from http://www.R-project.org.
27. Rasmussen S., Barah P., Suarez-Rodriguez M.C., Bressendorff S., Friis P., Costantino P., ... Mundy J. (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiology 161, 1783-1794.
28. Rizhsky L., Liang H. & Mittler R. (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology 130, 1143-1151.
29. Rizhsky L., Liang H., Shuman J., Shulaev V., Davletova S. & Mittler R. (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology 134, 1683-1696.
30. Schenk P.M., Kazan K., Wilson I., Anderson J.P., Richmond T., Somerville S.C. & Manners J.M. (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Sciences of the United States of America 97, 11655-11660.
31. Schoffl F., Rieping M., Baumann G., Bevan M. & Angermuller S. (1989) The function of plant heat shock promoter elements in the regulated expression of chimaeric genes in transgenic tobacco. Molecular & General Genetics 217, 246-253.
32. Seki M., Narusaka M., Ishida J., Nanjo T., Fujita M., Oono 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. The Plant Journal 31, 279-292.
33. Shahnejat-Bushehri S., Mueller-Roeber B. & Balazadeh S. (2012) Arabidopsis NAC transcription factor JUNGBRUNNEN1 affects thermomemory-associated genes and enhances heat stress tolerance in primed and unprimed conditions. Plant Signaling & Behavior 7, 1518-1521.
34. Sharma S. & Verslues P.E. (2010) Mechanisms independent of abscisic acid (ABA) or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery. Plant, Cell & Environment 33, 1838-1851.
35. Sharma S., Villamor J.G. & Verslues P.E. (2011) Essential role of tissue-specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiology 157, 292-304.
36. Skirycz A., Claeys H., De Bodt S., Oikawa A., Shinoda S., Andriankaja M., ... Inze D. (2011) Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. The Plant Cell 23, 1876-1888.
37. Skriver K., Olsen F.L., Rogers J.C. & Mundy J. (1991) Cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. Proceedings of the National Academy of Sciences of the United States of America 88, 7266-7270.
38. Sun Y. & MacRae T.H. (2005) Small heat shock proteins: molecular structure and chaperone function. Cellular and Molecular Life Sciences 62, 2460-2476.
39. Tolleter D., Hincha D.K. & Macherel D. (2010) A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state. Biochimica et Biophysica Acta 1798, 1926-1933.
40. Tunnacliffe A. & Wise M.J. (2007) The continuing conundrum of the LEA proteins. Die Naturwissenschaften 94, 791-812.
41. Uknes S., Mauch-Mani B., Moyer M., Potter S., Williams S., Dincher S., ... Ryals J. (1992) Acquired resistance in Arabidopsis. The Plant Cell 4, 645-656.
42. Uno Y., Furihata T., Abe H., Yoshida R., Shinozaki K. & Yamaguchi-Shinozaki K. (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proceedings of the National Academy of Sciences of the United States of America 97, 11632-11637.
43. Vierling E. (1991) The roles of heat shock proteins in plants. Annual Review of Plant Physiology 42, 579-620.
44. Wang Z.Y., Xiong L., Li W., Zhu J.K. & Zhu J. (2011) The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in Arabidopsis. The Plant Cell 23, 1971-1984.
45. Xiong L., Ishitani M. & Zhu J.K. (1999) Interaction of osmotic stress, temperature, and abscisic acid in the regulation of gene expression in Arabidopsis. Plant Physiology 119, 205-212.
46. Xu Z.Y., Lee K.H., Dong T., Jeong J.C., Jin J.B., Kanno Y., ... Hwang I. (2012) A vacuolar β-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. The Plant Cell 24, 2184-2199.
47. Yamaguchi-Shinozaki K. & Shinozaki K. (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. The Plant Cell 6, 251-264.
48. Yasuda M., Ishikawa A., Jikumaru Y., Seki M., Umezawa T., Asami T., ... Nakashita H. (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. The Plant Cell 20, 1678-1692.
49. Zeller G., Henz S.R., Widmer C.K., Sachsenberg T., Rätsch G., Weigel D. & Laubinger S. (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. The Plant Journal 58, 1068-1082.
50. Zhong L., Zhou W., Wang H., Ding S., Lu Q., Wen X., ... Lu C. (2013) Chloroplast small heat shock protein HSP21 interacts with plastid nucleoid protein pTAC5 and is essential for chloroplast development in Arabidopsis under heat stress. The Plant Cell 25, 2925-2943.
51. Zhu J., Shi H., Lee B.H., Damsz B., Cheng S., Stirm V., ... Bressan R.A. (2004) An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proceedings of the National Academy of Sciences of the United States of America 101, 9873-9878.