Microarray analysis and scale-free gene networks identify candidate regulators in drought-stressed roots of loblolly pine (P. taeda L.)

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Lorenz, W Walter ^a   Alba, Rob ^b   Yu, Yuan Sheng ^a   Bordeaux, John M ^a   Simões, Marta ^c   Dean, Jeffrey F D ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b MONSANTO COMPANY   (United States)

^c INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; PHYTOHORMONE; REACTIVE OXYGEN METABOLITE; MESSENGER RNA;

ABIOTIC STRESS; ARTICLE; BIOTIC STRESS; CONTROLLED STUDY; DNA MICROARRAY; DROUGHT STRESS; DROUGHT TOLERANCE; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC CORRELATION; GENOTYPE; LOBLOLLY PINE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC STRESS; PLANT GENE; PLANT ROOT; PROPAGULE; REGULATOR GENE; UPREGULATION; DROUGHT; EXPRESSED SEQUENCE TAG; GENE REGULATORY NETWORK; GENETICS; GENOMICS; METABOLISM; METHODOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REPRODUCIBILITY;

PINUS TAEDA;

DROUGHTS; EXPRESSED SEQUENCE TAGS; GENE REGULATORY NETWORKS; GENOMICS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PINUS TAEDA; PLANT ROOTS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; STRESS, PHYSIOLOGICAL;

EID: 79956283627     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-264     Document Type: Article

References (123)

1. Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J Exp Bot 2007, 58(2):221-227.
2. Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 2003, 218:1. Springer Science & Business Media B.V, 10.1007/s00425-003-1105-5, 14513379.
3. Bartels D, Sunkar R. Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 2005, 24(1):23-58.
4. Chaves MM, Maroco JP, Pereira JS. Understanding plant responses to drought - from genes to the whole plant. Funct Plant Biol 2003, 30(3):239-264.
5. Davies WJ, Zhang J. Root signals and the regulation of growth and development of plants in drying soil. Annual Review of Plant Physiology and Plant Molecular Biology 1991, 42(1):55-76.
6. Schachtman DP, Goodger JQD. Chemical root to shoot signaling under drought. Trends in Plant Science 2008, 13(6):281-287. 10.1016/j.tplants.2008.04.003, 18467158.
7. Davies W, Kudoyarova G, Hartung W. Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant's response to drought. Journal of Plant Growth Regulation 2005, 24(4):285-295.
8. Hartung W, Schraut D, Jiang F. Physiology of abscisic acid (ABA) in roots under stress - a review of the relationship between root ABA and radial water and ABA flows. Australian Journal of Agricultural Research 2005, 56:1253-1259.
9. Sharp RE, LeNoble ME. ABA, ethylene and the control of shoot and root growth under water stress. J Exp Bot 2002, 53(366):33-37. 10.1093/jexbot/53.366.33, 11741038.
10. Alvarez S, Marsh EL, Schroeder SG, Schachtman DP. Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ 2008, 31(3):325-340. 10.1111/j.1365-3040.2007.01770.x, 18088330.
11. De Smet I, Zhang H, Inzé D, Beeckman T. A novel role for abscisic acid emerges from underground. 2006, 11(9):434-439.
12. Vartanian N, Marcotte L, Giraudat J. Drought rhizogenesis in Arabidopsis thaliana (differential responses of hormonal mutants). Plant Physiol 1994, 104(2):761-767. 159256, 12232124.
13. Hose E, Steudle E, Hartung W. Abscisic acid and hydraulic conductivity of maize roots: a study using cell- and root-pressure probes. Planta 2000, 211(6):874-882. 10.1007/s004250000412, 11144273.
14. Deyholos MK. Making the most of drought and salinity transcriptomics. Plant Cell Environ 2010, 33(4):648-654. 10.1111/j.1365-3040.2009.02092.x, 20002333.
15. Kreps JA, Wu YJ, Chang HS, Zhu T, Wang X, Harper JF. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology 2002, 130(4):2129-2141. 10.1104/pp.008532, 166725, 12481097.
16. Yang L, Zheng B, Mao C, Qi X, Liu F, Wu P. Analysis of transcripts that are differentially expressed in three sectors of the rice root system under water deficit. Molecular Genetics and Genomics 2004, 272(4):433-442. 10.1007/s00438-004-1066-9, 15480789.
17. Mohammadi M, Kav HNV, Deyholos MK. Transcript expression profile of water-limited roots of hexaploid wheat (Triticum aestivum 'Opata'). Genome 2008, 51(5):357-367. 10.1139/G08-020, 18438439.
18. Spollen WG, Tao W, Valliyodan B, Chen K, Hejlek LG, Kim JJ, LeNoble ME, Zhu J, Bohnert HJ, Henderson D, Schachtman DP, Davis GE, Springer GK, Sharp RE, Nguyen HT. Spatial distribution of transcript changes in the maize primary root elongation zone at low water potential. BMC Plant Biology 2008, 8:15. 10.1186/1471-2229-8-15, 2262081, 18234103.
19. Micheletto S, Rodriguez-Uribe L, Hernandez R, Richins RD, Curry J, O'Connell MA. Comparative transcript profiling in roots of Phaseolus acutifolius and P-vulgaris under water deficit stress. Plant Science 2007, 173(5):510-520.
20. Buchanan CD, Lim SY, Salzman RA, Kagiampakis L, Morishige DT, Weers BD, Klein RR, Pratt LH, Cordonnier-Pratt MM, Klein PE, Mullet JE. Sorghum bicolor's transcriptome response to dehydration, high salinity and ABA. Plant Molecular Biology 2005, 58(5):699-720. 10.1007/s11103-005-7876-2, 16158244.
21. Chen D, Liang MX, DeWald D, Weimer B, Peel MD, Bugbee B, Michaelson J, Davis E, Wu Y. Identification of dehydration responsive genes from two non-nodulated alfalfa cultivars using Medicago truncatula microarrays. Acta Physiol Plant 2008, 30(2):183-199.
22. Street NR, Skogstrom O, Sjodin A, Tucker J, Rodriguez-Acosta M, Nilsson P, Jansson S, Taylor G. The genetics and genomics of the drought response in Populus. Plant J 2006, 48(3):321-341. 10.1111/j.1365-313X.2006.02864.x, 17005011.
23. Caruso A, Chefdor F, Carpin S, Depierreux C, Delmotte FM, Kahlem G, Morabito D. Physiological characterization and identification of genes differentially expressed in response to drought induced by PEG 6000 in Populus canadensis leaves. Journal of Plant Physiology 2008, 165(9):932-941. 10.1016/j.jplph.2007.04.006, 17928100.
24. Berta M, Giovannelli A, Sebastiani F, Camussi A, Racchi ML. Transcriptome changes in the cambial region of poplar (Populus alba L.) in response to water deficit. Plant Biol 2010, 12(2):341-354. 10.1111/j.1438-8677.2009.00320.x, 20398240.
25. Wilkins O, Waldron L, Nahal H, Provart NJ, Campbell MM. Genotype and time of day shape the Populus drought response. Plant J 2009, 60(4):703-715. 10.1111/j.1365-313X.2009.03993.x, 19682285.
26. Bogeat-Triboulot MB, Brosche M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, Laukens K, Teichmann T, Altman A, Hausman JF, Polle A, Kangasjarvi J, Dreyer E. Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiol 2007, 143(2):876-892. 1803728, 17158588.
27. Chang SJ, Puryear JD, Dias M, Funkhouser EA, Newton RJ, Cairney J. Gene expression under water deficit in loblolly pine (Pinus taeda): Isolation and characterization of cDNA clones. Physiologia Plantarum 1996, 97(1):139-148.
28. Heath LS, Ramakrishnan N, Sederoff RR, Whetten RW, Chevone BI, Struble CA, Jouenne VY, Chen D, Zyl L, Grene R. Studying the functional genomics of stress responses in loblolly pine with the expresso microarray experiment management system. Comparative and Functional Genomics 2002, 3:226-243. 10.1002/cfg.169, 2447276, 18628855.
29. Watkinson JI, Sioson AA, Vasquez-Robinet C, Shukla M, Kumar D, Ellis M, Heath LS, Ramakrishnan N, Chevone B, Watson LT, van Zyl L, Egertsdotter U, Sederoff RR, Grene R. Photosynthetic acclimation is reflected in specific patterns of gene expression in drought-stressed loblolly pine. Plant Physiol 2003, 133(4):1702-1716. 10.1104/pp.103.026914, 300725, 14681533.
30. Dubos C, Le Provost G, Pot D, Salin F, Lalane C, Madur D, Frigerio JM, Plomion C. Identification and characterization of water-stress-responsive genes in hydroponically grown maritime pine (Pinus pinaster) seedlings. Tree Physiology 2003, 23(3):169-179.
31. Dubos C, Plomion C. Identification of water-deficit responsive genes in maritime pine (Pinus pinaster Ait.) roots. Plant Molecular Biology 2003, 51(2):249-262. 10.1023/A:1021168811590, 12602883.
32. Lorenz WW, Sun F, Liang C, Kolychev D, Wang HM, Zhao X, Cordonnier-Pratt MM, Pratt LH, Dean JFD. Water stress-responsive genes in loblolly pine (Pinus taeda) roots identified by analyses of expressed sequence tag libraries. Tree Physiology 2006, 26(1):1-16. 10.1093/treephys/26.1.1, 16203709.
33. Vásquez-Robinet C, Watkinson JI, Sioson AA, Ramakrishnan N, Heath LS, Grene R. Differential expression of heat shock protein genes in preconditioning for photosynthetic acclimation in water-stressed loblolly pine. Plant Physiology and Biochemistry 2010, 48(4):256-264. 10.1016/j.plaphy.2009.12.005, 20171112.
34. Lorenz WW, Dean JFD. SAGE Profiling and demonstration of differential gene expression along the axial developmental gradient of lignifying xylem in loblolly pine (Pinus taeda). Tree Physiology 2002, 22(5):301-310.
35. http://fungen.org/Pine.htm
36. Lorenz WW, Yu YS, Simões M, Dean JFD. Processing the Loblolly Pine PtGen2 cDNA Microarray. Journal of Visualized Experiments 2009, 25.
37. Zhang B, Horvath S. A general framework for weighted gene co-expression network analysis. Statistical Applications in Genetics and Molecular Biology 2005, 4. (Article 17).
38. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 2008, 9(1):559. 10.1186/1471-2105-9-559, 2631488, 19114008.
39. Kerr MK. Design considerations for efficient and effective microarray studies. Biometrics 2003, 59(4):822-828. 10.1111/j.0006-341X.2003.00096.x, 14969460.
40. Nairn CJ, Lennon DM, Wood-Jones A, Nairn AV, Dean JFD. Carbohydrate-related genes and cell wall biosynthesis in vascular tissues of loblolly pine (Pinus taeda). Tree Physiology 2008, 28(7):1099-1110.
41. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21(18):3674-3676. 10.1093/bioinformatics/bti610, 16081474.
42. Chang S, Puryear J, Cairney J. A simple and efficient method for extracting RNA from pine trees. Plant Molecular Biology Reporter 1993, 11(2):113-116.
43. Lorenz WW, Yu YS, Dean JFD. An improved method of RNA isolation from loblolly pine (P. taeda L.) and other conifer species. Journal of Visualized Experiments 2010, 36.
44. Alba R, Fei ZJ, Payton P, Liu Y, Moore SL, Debbie P, Cohn J, D'Ascenzo M, Gordon JS, Rose JKC, Martin G, Tanksley SD, Bouzayen M, Jahn MM, Giovannoni J. ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant J 2004, 39(5):697-714. 10.1111/j.1365-313X.2004.02178.x, 15315633.
45. Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ. Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 2005, 17(11):2954-2965. 10.1105/tpc.105.036053, 1276022, 16243903.
46. Rocke DM, Durbin B. A model for measurement error for gene expression arrays. Journal of Computational Biology 2001, 8(6):557. 10.1089/106652701753307485, 11747612.
47. Simon R, Lam A, Li MC, Ngan M, Menenzes S, Zhao Y. Analysis of Gene Expression Data Using BRB-Array Tools. Cancer Informatics 2007, 3:11-17. 2675854, 19455231.
48. Wang X, Hessner MJ, Wu Y, Pati N, Ghosh S. Quantitative quality control in microarray experiments and the application in data filtering, normalization and false positive rate prediction. Bioinformatics 2003, 19(11):1341-1347. 10.1093/bioinformatics/btg154, 12874045.
49. Troyanskaya O, Cantor M, Sherlock G, Brown P, Hastie T, Tibshirani R, Botstein D, Altman RB. Missing value estimation methods for DNA microarrays. Bioinformatics 2001, 17(6):520-525. 10.1093/bioinformatics/17.6.520, 11395428.
50. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, Christmas R, Avila-Campilo I, Creech M, Gross B, Hanspers K, Isserlin R, Kelley R, Killcoyne S, Lotia S, Maere S, Morris J, Ono K, Pavlovic V, Pico AR, Vailaya A, Wang PL, Adler A, Conklin BR, Hood L, Kuiper M, Sander C, Schmulevich I, Schwikowski B, Warner GJ, et al. Integration of biological networks and gene expression data using Cytoscape. Nat Protocols 2007, 2(10):2366-2382.
51. Assenov Y, Ramirez F, Schelhorn SE, Lengauer T, Albrecht M. Computing topological parameters of biological networks. Bioinformatics 2008, 24(2):282-284. 10.1093/bioinformatics/btm554, 18006545.
52. Gene Expression Omnibus (GEO). , http://www.ncbi.nlm.nih.gov/geo/
53. Yuen T, Wurmbach E, Pfeffer RL, Ebersole BJ, Sealfon SC. Accuracy and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucl Acids Res 2002, 30(10):e48. 10.1093/nar/30.10.e48, 115302, 12000853.
54. Draghici S, Khatri P, Eklund AC, Szallasi Z. Reliability and reproducibility issues in DNA microarray measurements. Trends in Genetics 2006, 22(2):101-109. 10.1016/j.tig.2005.12.005, 2386979, 16380191.
55. Singh KB, Foley RC, Onate-Sanchez L. Transcription factors in plant defense and stress responses. Current Opinion in Plant Biology 2002, 5(5):430-436. 10.1016/S1369-5266(02)00289-3, 12183182.
56. Yamaguchi-Shinozaki K, Shinozaki K. Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends in Plant Science 2005, 10(2):88-94. 10.1016/j.tplants.2004.12.012, 15708346.
57. Barabasi AL, Albert R. Emergence of scaling in random networks. Science 1999, 286(5439):509-512. 10.1126/science.286.5439.509, 10521342.
58. Barabasi AL, Oltvai ZN. Network biology: Understanding the cell's functional organization. Nat Rev Genet 2004, 5(2):101-U115. 10.1038/nrg1272, 14735121.
59. Watts DJ, Strogatz SH. Collective dynamics of 'small-world' networks. Nature 1998, 393(6684):440-442. 10.1038/30918, 9623998.
60. http://www.cytoscape.org/
61. http://med.bioinf.mpi-inf.mpg.de/netanalyzer/
62. Lorenz WW, Simões M, Miguel C, Dean JFD. Analysis of gene expression changes in Pinus species using a loblolly pine cDNA microarray. IUFRO-CITA 2008 Joint Conference: 2008; Quebec City, Quebec 2008, 174.
63. 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. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 2002, 31(3):279-292. 10.1046/j.1365-313X.2002.01359.x, 12164808.
64. 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. Monitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca. 7000 full-length cDNA microarray. The Plant Journal 2003, 34(6):868-887. 10.1046/j.1365-313X.2003.01774.x, 12795706.
65. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA get-blot analyses. Plant Physiology 2003, 133(4):1755-1767. 10.1104/pp.103.025742, 300730, 14645724.
66. Ozturk ZN, Talame V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ. Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Molecular Biology 2002, 48(5):551-573. 10.1023/A:1014875215580, 11999834.
67. Ueda A, Kathiresan A, Inada M, Narita Y, Nakamura T, Shi WM, Takabe T, Bennett J. Osmotic stress in barley regulates expression of a different set of genes than salt stress does. Journal of Experimental Botany 2004, 55(406):2213-2218. 10.1093/jxb/erh242, 15361537.
68. Cramer G, Ergül A, Grimplet J, Tillett R, Tattersall E, Bohlman M, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D, Schlauch K, Schooley D, Cushman J. Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Functional & Integrative Genomics 2007, 7(2):111-134. 10.1007/s10142-006-0039-y, 21614800.
69. Mena-Petite A, Lacuesta M, Munoz-Rueda A. Ammonium assimilation in Pinus radiata seedlings: effects of storage treatments, transplanting stress and water regimes after planting under simulated field conditions. Environ Exp Bot 2006, 55(1-2):1-14.
70. Rossi S, Simard S, Rathgeber CBK, Deslauriers A, De Zan C. Effects of a 20-day-long dry period on cambial and apical meristem growth in Abies balsamea seedlings. Trees-Struct Funct 2009, 23(1):85-93.
71. Mena-Petite A, Gonzalez-Moro B, Gonzalez-Murua C, Lacuesta M, Rueda AM. Sequential effects of acidic precipitation and drought on photosynthesis and chlorophyll fluorescence parameters of Pinus radiata d. don seedlings. Journal of Plant Physiology 2000, 156(1):84-92.
72. Brodribb TJ, Cochard H. Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers. Plant Physiology 2009, 149(1):575-584. 10.1104/pp.108.129783, 2613726, 19011001.
73. Dure L, Crouch M, Harada J, Ho T-HD, Mundy J, Quatrano R, Thomas T, Sung ZR. Common amino acid sequence domains among the LEA proteins of higher plants. Plant Molecular Biology 1989, 12(5):475-486.
74. Tunnacliffe A, Wise M. The continuing conundrum of the LEA proteins. Naturwissenschaften 2007, 94(10):791-812. 10.1007/s00114-007-0254-y, 17479232.
75. Rorat T. Plant dehydrins - Tissue location, structure and function (vol 11, pg 536, 2006). Cellular & Molecular Biology Letters 2007, 12(1):148. 10.2478/s11658-006-0071-x, 21614753.
76. Crowe JH, Crowe LM, Carpenter JF, Wistrom CA. Stabilization of dry phospholipid-bilayers and protein by sugars. Biochem J 1987, 242(1):1-10. 1147656, 2954537.
77. Hincha DK, Hagemann M. Stabilization of model membranes during drying by compatible solutes involved in the stress tolerance of plants and microorganisms. Biochem J 2004, 383:277-283. 10.1042/BJ20040746, 1134068, 15225123.
78. Toldi O, Tuba Z, Scott P. Vegetative desiccation tolerance: Is it a goldmine for bioengineering crops?. Plant Science 2009, 176(2):187-199.
79. Zhuang Y, Ren G, Yue G, Li Z, Qu X, Hou G, Zhu Y, Zhang J. Effects of water-deficit stress on the transcriptomes of developing immature ear and tassel in maize. Plant Cell Reports 2007, 26(12):2137-2147. 10.1007/s00299-007-0419-3, 17668218.
80. Xu C, Huang B. Root proteomic responses to heat stress in two Agrostis grass species contrasting in heat tolerance. Journal of Experimental Botany 2008, 59(15):4183-4183. 10.1093/jxb/ern258, 2639019, 19008411.
81. Boscariol-Camargo RL, Berger IJ, Souza AA, do Amaral AM, Carlos EF, Freitas-Astua J, Takita MA, Targon M, Medina CL, Reis MS, Machado MA. In silico analysis of ESTs from roots of Rangpur lime (Citrus limonia Osbeck) under water stress. Genet Mol Biol 2007, 30(3):906-916.
82. Bois G, Bigras FJ, Bertrand A, Piche Y, Fung MYP, Khasa DP. Ectomycorrhizal fungi affect the physiological responses of Picea glauca and Pinus banksiana seedlings exposed to an NaCl gradient. Tree Physiology 2006, 26(9):1185-1196.
83. Munoz FJ, Baroja-Fernandez E, Moran-Zorzano MT, Viale AM, Etxeberria E, Alonso-Casajus N, Pozueta-Romero J. Sucrose synthase controls both intracellular ADP glucose levels and transitory starch biosynthesis in source leaves. Plant and Cell Physiology 2005, 46(8):1366-1376. 10.1093/pcp/pci148, 15951568.
84. Hare PD, Cress WA, Van Staden J. Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 1998, 21(6):535-553.
85. Roitsch T. Source-sink regulation by sugar and stress. Current Opinion in Plant Biology 1999, 2(3):198-206. 10.1016/S1369-5266(99)80036-3, 10375568.
86. Roitsch T, Balibrea ME, Hofmann M, Proels R, Sinha AK. Extracellular invertase: key metabolic enzyme and PR protein. Journal of Experimental Botany 2003, 54(382):513-524. 10.1093/jxb/erg050, 12508062.
87. Saravitz DM, Pharr DM, Carter TE. Galactinol synthase activity and soluble sugars in developing seeds of 4 soybean genotypes. Plant Physiology 1987, 83(1):185-189. 10.1104/pp.83.1.185, 1056321, 16665199.
88. Panikulangara TJ, Eggers-Schumacher G, Wunderlich M, Stransky H, Schoffl F. Galactinol synthase1. A novel heat shock factor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiol 2004, 136(2):3148-3158. 10.1104/pp.104.042606, 523375, 15466240.
89. Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K. Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 2002, 29(4):417-426. 10.1046/j.0960-7412.2001.01227.x, 11846875.
90. Nishizawa A, Yabuta Y, Shigeoka S. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 2008, 147(3):1251-1263. 10.1104/pp.108.122465, 2442551, 18502973.
91. Bohnert HJ, Nelson DE, Jensen RG. Adaptations to environmental stresses. Plant Cell 1995, 7(7):1099-1111. 160917, 12242400.
92. Miyazaki S, Rice M, Quigley F, Bohnert HJ. Expression of plant inositol transporters in yeast. Plant Science 2004, 166(1):245-252.
93. Luu DT, Maurel C. Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant, Cell & Environment 2005, 28:85-96. Blackwell Publishing Limited, 10.1111/j.1365-3040.2004.01295.x, 21614643.
94. Galmés J, Pou A, Alsina M, Tomàs M, Medrano H, Flexas J. Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): relationship with ecophysiological status. Planta 2007, 226(3):671-681. 10.1007/s00425-007-0515-1, 17447082.
95. Smart LB, Moskal WA, Cameron KD, Bennett AB. MIP genes are down-regulated under drought stress in Nicotiana glauca. Plant Cell Physiol 2001, 42(7):686-693. 10.1093/pcp/pce085, 11479374.
96. Jang JY, Kim DG, Kim YO, Kim JS, Kang H. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Molecular Biology 2004, 54(5):713-725.
97. Porcel R, Aroca R, Azcón R, Ruiz-Lozano J. PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Molecular Biology 2006, 60(3):389-404. 10.1007/s11103-005-4210-y, 16514562.
98. Aroca R, Ferrante A, Vernieri P, Chrispeels MJ. Drought, abscisic acid and transpiration rate effects on the regulation of PIP aquaporin gene expression and abundance in Phaseolus vulgaris plants. Ann Bot 2006, 98(6):1301-1310. 10.1093/aob/mcl219, 2803586, 17028296.
99. Yu QJ, Hu YL, Li JF, Wu Q, Lin ZP. Sense and antisense expression of plasma membrane aquaporin BnPIP1 from Brassica napus in tobacco and its effects on plant drought resistance. Plant Science 2005, 169(4):647-656.
100. Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G. Overexpression of a Plasma Membrane Aquaporin in Transgenic Tobacco Improves Plant Vigor under Favorable Growth Conditions but Not under Drought or Salt Stress. Plant Cell 2003, 15(2):439-447. 10.1105/tpc.009225, 141212, 12566583.
101. Alexandersson E, Fraysse L, Sjövall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P. Whole Gene Family Expression and Drought Stress Regulation of Aquaporins. Plant Molecular Biology 2005, 59(3):469-484. 10.1007/s11103-005-0352-1, 16235111.
102. Mahdieh M, Mostajeran A, Horie T, Katsuhara M. Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant and Cell Physiology 2008, 49(5):801-813. 10.1093/pcp/pcn054, 18385163.
103. Eulgem T, Rushton P, Robatzek S, Somssich I. The WRKY superfamily of plant transcription factors. Trends Plant Sci 2000, 5(5):199-206. 10.1016/S1360-1385(00)01600-9, 10785665.
104. Ulker B, Somssich I. WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 2004, 7(5):491-498. 10.1016/j.pbi.2004.07.012, 15337090.
105. Berri S, Abbruscato P, Faivre-Rampant O, Brasileiro A, Fumasoni I, Satoh K, Kikuchi S, Mizzi L, Morandini P, Pe M, Piffanelli P. Characterization of WRKY co-regulatory networks in rice and Arabidopsis. BMC Plant Biology 2009, 9(1):120. 10.1186/1471-2229-9-120, 2761919, 19772648.
106. Ramamoorthy R, Jiang SY, Kumar N, Venkatesh PN, Ramachandran S. A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol 2008, 49(6):865-879. 10.1093/pcp/pcn061, 18413358.
107. Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K. Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Reports 2009, 28(1):21-30. 10.1007/s00299-008-0614-x, 18818929.
108. Wei W, Zhang Y, Han L, Guan Z, Chai T. A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco. Plant Cell Reports 2008, 27(4):795-803. 10.1007/s00299-007-0499-0, 18183400.
109. Ren XZ, Chen ZZ, Liu Y, Zhang HR, Zhang M, Liu QA, Hong XH, Zhu JK, Gong ZZ. ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 2010, 63(3):417-429.
110. Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY. Soybean WRKY-type transcription factor genes,GmWRKY13, GmWRKY21, GmWRKY55, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnology Journal 2008, 6(5):486-503. 10.1111/j.1467-7652.2008.00336.x, 18384508.
111. Wang Z, Zhu Y, Wang LL, Liu X, Liu YX, Phillips J, Deng X. A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta 2009, 230(6):1155-1166. 10.1007/s00425-009-1014-3, 19760263.
112. Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frey N, Leung J. An update on abscisic acid signaling in plants and more. Mol Plant 2008, 1(2):198-217. 10.1093/mp/ssm022, 19825533.
113. Christmann A, Hoffmann T, Teplova I, Grill E, Muller A. Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant Physiol 2005, 137(1):209-219. 10.1104/pp.104.053082, 548852, 15618419.
114. Taylor IB, Burbidge A, Thompson AJ. Control of abscisic acid synthesis. Journal of Experimental Botany 2000, 51(350):1563-1574. 10.1093/jexbot/51.350.1563, 11006307.
115. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K. Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 2001, 27(4):325-333. 10.1046/j.1365-313x.2001.01096.x, 11532178.
116. Yang JF, Guo ZF. Cloning of a 9-cis-epoxycarotenoid dioxygenase gene (SgNCED1) from Stylosanthes guianensis and its expression in response to abiotic stresses. Plant Cell Reports 2007, 26(8):1383-1390. 10.1007/s00299-007-0325-8, 17333017.
117. Munne-Bosch S, Falara V, Pateraki I, Lopez-Carbonella M, Cela J, Kanellis AK. Physiological and molecular responses of the isoprenoid biosynthetic pathway in a drought-resistant Mediterranean shrub, Cistus creticus exposed to water deficit. Journal of Plant Physiology 2009, 166(2):136-145. 10.1016/j.jplph.2008.02.011, 18455260.
118. Havlova M, Dobrev PI, Motyka V, Storchova H, Libus J, Dobra J, Malbek J, Gaudinova A, Vankova R. The role of cytokinins in responses to water deficit in tobacco plants over-expressing trans-zeatin O-glucosyltransferase gene under 35S or SAG12 promoters. Plant, Cell & Environment 2008, 31(3):341-353. 10.1111/j.1365-3040.2007.01766.x, 21614643.
119. Martin RC, Mok DWS, Smets R, Van Onckelen HA, Mok MC. Development of transgenic tobacco harboring a zeatin O-glucosyltransferase gene from Phaseolus. In Vitro Cell Dev Biol-Plant 2001, 37(3):354-360.
120. Brzobohaty B, Moore I, Kristoffersen P, Bako L, Campos N, Schell J, Palme K. Release of active cytokinin by a beta-glucosidase localized to the maize root-meristem. Science 1993, 262(5136):1051-1054. 10.1126/science.8235622, 8235622.
121. Mao LY, Van Hemert JL, Dash S, Dickerson JA. Arabidopsis gene co-expression network and its functional modules. BMC Bioinformatics 2009, 10:24. 10.1186/1471-2105-10-24, 2657898, 19152705.
122. Li P, Ma S, Bohnert HJ. Coexpression characteristics of trehalose-6-phosphate phosphatase subfamily genes reveal different functions in a network context. Physiologia Plantarum 2008, 133(3):544-556. 10.1111/j.1399-3054.2008.01101.x, 18435695.
123. Lee TH, Kim YK, Pham TTM, Song SI, Kim JK, Kang KY, An G, Jung KH, Galbraith DW, Kim M, Yoon UH, Nahm BH. RiceArrayNet: A Database for Correlating Gene Expression from Transcriptome Profiling, and Its Application to the Analysis of Coexpressed Genes in Rice. Plant Physiology 2009, 151(1):16-33. 10.1104/pp.109.139030, 2735985, 19605550.