Flower development under drought stress: Morphological and transcriptomic analyses reveal acute responses and long-term acclimation in Arabidopsis

Plant Cell

Volumn 25, Issue 10, 2013, Pages 3785-3807

  Su, Zhao ^a   Ma, Xuan ^a,b   Guo, Huihong ^a,c   Sukiran, Noor Liyana ^a   Guo, Bin ^a,d   Assmann, Sarah M ^a   Ma, Hong ^a,b,d  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c BEIJING FORESTRY UNIVERSITY   (China)

^d FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; DREB1A PROTEIN, ARABIDOPSIS; MYB21 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ACCLIMATIZATION; ARABIDOPSIS; DROUGHT; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGICAL STRESS; PLANT GENE; REPRODUCTION;

ACCLIMATIZATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DROUGHTS; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; REPRODUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84888416432     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.115428     Document Type: Article

References (142)

1. Adamczyk, B.J., and Fernandez, D.E. (2009). MIKC* MADS domain heterodimers are required for pollen maturation and tube growth in Arabidopsis. Plant Physiol. 149: 1713-1723.
2. Adie, B.A., Pérez-Pérez, J., Pérez-Pérez, M.M., Godoy, M., Sánchez-Serrano, J.J., Schmelz, E.A., and Solano, R. (2007). ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19: 1665-1681.
3. Alexander, M.P. (1969). Differential staining of aborted and nonaborted pollen. Stain Technol. 44: 117-122.
4. Andersen, M.N., Asch, F., Wu, Y., Jensen, C.R., Naested, H., Mogensen, V.O., and Koch, K.E. (2002). Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize. Plant Physiol. 130: 591-604.
5. Avanci, N.C., Luche, D.D., Goldman, G.H., and Goldman, M.H. (2010). Jasmonates are phytohormones with multiple functions, including plant defense and reproduction. Genet. Mol. Res. 9: 484-505.
6. Bailey, T.L., and Elkan, C. (1994). Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2: 28-36.
7. Bari, R., and Jones, J.D. (2009). Role of plant hormones in plant defence responses. Plant Mol. Biol. 69: 473-488.
8. Bernier, G., and Périlleux, C. (2005). A physiological overview of the genetics of flowering time control. Plant Biotechnol. J. 3: 3-16.
9. Bernoux, M., Timmers, T., Jauneau, A., Brière, C., de Wit, P.J., Marco, Y., and Deslandes, L. (2008). RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 effector. Plant Cell 20: 2252-2264.
10. Bhaskara, G.B., Nguyen, T.T., and Verslues, P.E. (2012). Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs. Plant Physiol. 160: 379-395.
11. Bosch, M., Cheung, A.Y., and Hepler, P.K. (2005). Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol. 138: 1334-1346.
12. Boyer, J.S., and Westgate, M.E. (2004). Grain yields with limited water. J. Exp. Bot. 55: 2385-2394.
13. Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N. E., Davis, K.R., and Görlach, J. (2001). Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell 13: 1499-1510.
14. Breshears, D.D., et al. (2005). Regional vegetation die-off in response to global-change-type drought. Proc. Natl. Acad. Sci. USA 102: 15144-15148.
15. Bu, Q., Jiang, H., Li, C.B., Zhai, Q., Zhang, J., Wu, X., Sun, J., Xie, Q., and Li, C. (2008). Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res. 18: 756-767.
16. Busch, W., Wunderlich, M., and Schöffl, F. (2005). Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J. 41: 1-14.
17. Calderón Villalobos, L.I., et al. (2012). A combinatorial TIR1/AFBAux/IAA co-receptor system for differential sensing of auxin. Nat. Chem. Biol. 8: 477-485.
18. Canales, C., Bhatt, A.M., Scott, R., and Dickinson, H. (2002). EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr. Biol. 12: 1718-1727.
19. Chaves, M.M., Flexas, J., and Pinheiro, C. (2009). Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. Ann. Bot. (Lond.) 103: 551-560.
20. Cheng, H., Song, S., Xiao, L., Soo, H.M., Cheng, Z., Xie, D., and Peng, J. (2009). Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet. 5: e1000440.
21. Choi, A.M., Lee, S.B., Cho, S.H., Hwang, I., Hur, C.G., and Suh, M. C. (2008). Isolation and characterization of multiple abundant lipid transfer protein isoforms in developing sesame (Sesamum indicum L.) seeds. Plant Physiol. Biochem. 46: 127-139.
22. Clay, N.K., Adio, A.M., Denoux, C., Jander, G., and Ausubel, F.M. (2009). Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323: 95-101.
23. Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., and Abrams, S.R. (2010). Abscisic acid: Emergence of a core signaling network. Annu. Rev. Plant Biol. 61: 651-679.
24. Dolferus, R., Jacobs, M., Peacock, W.J., and Dennis, E.S. (1994). Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol. 105: 1075-1087.
25. Du, Z., Zhou, X., Ling, Y., Zhang, Z., and Su, Z. (2010). agriGO: A GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38: W64-70.
26. Farooq, M., Wahid, A., and Kobayashi, N., D., F., and Basra, S.M.A. (2009). Plant drought stress: Effects, mechanisms and management. Sustainable Agric. 29: 185-212.
27. Freeling, M., Rapaka, L., Lyons, E., Pedersen, B., and Thomas, B. C. (2007). G-boxes, bigfoot genes, and environmental response: Characterization of intragenomic conserved noncoding sequences in Arabidopsis. Plant Cell 19: 1441-1457.
28. Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.Y., Cutler, S.R., Sheen, J., Rodriguez, P.L., and Zhu, J.K. (2009). In vitro reconstitution of an abscisic acid signalling pathway. Nature 462: 660-664.
29. Fujimoto, S.Y., Ohta, M., Usui, A., Shinshi, H., and Ohme-Takagi, M. (2000). Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12: 393-404.
30. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2006). Crosstalk between abiotic and biotic stress responses: A current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 9: 436-442.
31. Gigon, A., Matos, A.R., Laffray, D., Zuily-Fodil, Y., and Pham-Thi, A.T. (2004). Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). Ann. Bot. (Lond.) 94: 345-351.
32. Griffiths, J., Murase, K., Rieu, I., Zentella, R., Zhang, Z.L., Powers, S.J., Gong, F., Phillips, A.L., Hedden, P., Sun, T.P., and Thomas, S.G. (2006). Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399-3414.
33. Haake, V., Cook, D., Riechmann, J.L., Pineda, O., Thomashow, M. F., and Zhang, J.Z. (2002). Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol. 130: 639-648.
34. Hammes, U.Z., Meier, S., Dietrich, D., Ward, J.M., and Rentsch, D. (2010). Functional properties of the Arabidopsis peptide transporters AtPTR1 and AtPTR5. J. Biol. Chem. 285: 39710-39717.
35. Hirayama, T., and Shinozaki, K. (2007). Perception and transduction of abscisic acid signals: Keys to the function of the versatile plant hormone ABA. Trends Plant Sci. 12: 343-351.
36. Honma, T., and Goto, K. (2001). Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409: 525-529.
37. Hopkins, R.J., van Dam, N.M., and van Loon, J.J. (2009). Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu. Rev. Entomol. 54: 57-83.
38. Hord, C.L., Chen, C., Deyoung, B.J., Clark, S.E., and Ma, H. (2006). The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18: 1667-1680.
39. Hord, C.L., Sun, Y.J., Pillitteri, L.J., Torii, K.U., Wang, H., Zhang, S., and Ma, H. (2008). Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol. Plant 1: 645-658.
40. Hwang, J.U., Gu, Y., Lee, Y.J., and Yang, Z. (2005). Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol. Biol. Cell 16: 5385-5399.
41. Ito, T., Wellmer, F., Yu, H., Das, P., Ito, N., Alves-Ferreira, M., Riechmann, J.L., and Meyerowitz, E.M. (2004). The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430: 356-360.
42. Ito, Y., Katsura, K., Maruyama, K., Taji, T., Kobayashi, M., Seki, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2006). Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol. 47: 141-153.
43. Jakobsen, M.K., Poulsen, L.R., Schulz, A., Fleurat-Lessard, P., Møller, A., Husted, S., Schiøtt, M., Amtmann, A., and Palmgren, M.G. (2005). Pollen development and fertilization in Arabidopsis is dependent on the MALE GAMETOGENESIS IMPAIRED ANTHERS gene encoding a type V P-type ATPase. Genes Dev. 19: 2757-2769.
44. Ji, X., Shiran, B., Wan, J., Lewis, D.C., Jenkins, C.L., Condon, A.G., Richards, R.A., and Dolferus, R. (2010). Importance of preanthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant Cell Environ. 33: 926-942.
45. Jiang, H., Li, H., Bu, Q., and Li, C. (2009). The RHA2a-interacting proteins ANAC019 and ANAC055 may play a dual role in regulating ABA response and jasmonate response. Plant Signal. Behav. 4: 464-466.
46. Jiang, L., Yang, S.L., Xie, L.F., Puah, C.S., Zhang, X.Q., Yang, W.C., Sundaresan, V., and Ye, D. (2005). VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17: 584-596.
47. Johnson-Brousseau, S.A., and McCormick, S. (2004). A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant J. 39: 761-775.
48. Jung, C., and Müller, A.E. (2009). Flowering time control and applications in plant breeding. Trends Plant Sci. 14: 563-573.
49. Kakumanu, A., Ambavaram, M.M., Klumas, C., Krishnan, A., Batlang, U., Myers, E., Grene, R., and Pereira, A. (2012). Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol. 160: 846-867.
50. Kasuga, M., Miura, S., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2004). A combination of the Arabidopsis DREB1A gene and stressinducible rd29A promoter improved drought-and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol. 45: 346-350.
51. Katsir, L., Schilmiller, A.L., Staswick, P.E., He, S.Y., and Howe, G. A. (2008). COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc. Natl. Acad. Sci. USA 105: 7100-7105.
52. Kawasaki, S., Borchert, C., Deyholos, M., Wang, H., Brazille, S., Kawai, K., Galbraith, D., and Bohnert, H.J. (2001). Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13: 889-905.
53. Klingler, J.P., Batelli, G., and Zhu, J.K. (2010). ABA receptors: The START of a new paradigm in phytohormone signalling. J. Exp. Bot. 61: 3199-3210.
54. Kreps, J.A., Wu, Y., Chang, H.S., Zhu, T., Wang, X., and Harper, J.F. (2002). Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130: 2129-2141.
55. Lackman, P., et al. (2011). Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc. Natl. Acad. Sci. USA 108: 5891-5896.
56. Lalonde, S., Beebe, D.U., and Saini, H.S. (1997). Early signs of disruption of wheat anther development associated with the induction of male sterility by meiotic-stage water deficit. Sex. Plant Reprod. 10: 40-48.
57. Lata, C., and Prasad, M. (2011). Role of DREBs in regulation of abiotic stress responses in plants. J. Exp. Bot. 62: 4731-4748.
58. Liljegren, S.J., Ditta, G.S., Eshed, Y., Savidge, B., Bowman, J.L., and Yanofsky, M.F. (2000). SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404: 766-770.
59. Liu, F.L., Andersen, M.N., and Jensen, C.R. (2003). Loss of pod set caused by drought stress is associated with water status and ABA content of reproductive structures in soybean. Funct. Plant Biol. 30: 271-280.
60. Liu, J., et al. (2008). Targeted degradation of the cyclin-dependent kinase inhibitor ICK4/KRP6 by RING-type E3 ligases is essential for mitotic cell cycle progression during Arabidopsis gametogenesis. Plant Cell 20: 1538-1554.
61. Liu, J.X., Liao, D.Q., Oane, R., Estenor, L., Yang, X.E., Li, Z.C., and Bennett, J. (2006). Genetic variation in the sensitivity of anther dehiscence to drought stress in rice. Field Crops Res. 97: 87-100.
62. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., and 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. Plant Cell 10: 1391-1406.
63. Lloyd, D.G. (1980). Sexual strategies in plants. I. An hypothesis of serial adjustment of maternal investment during one reproductive session. New Phytol. 86: 69-79.
64. Lohmann, J.U., Hong, R.L., Hobe, M., Busch, M.A., Parcy, F., Simon, R., and Weigel, D. (2001). A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105: 793-803.
65. Long, J.A., Moan, E.I., Medford, J.I., and Barton, M.K. (1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66-69.
66. Luan, S. (2003). Protein phosphatases in plants. Annu. Rev. Plant Biol. 54: 63-92.
67. Ma, H. (2005). Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. 56: 393-434.
68. Magome, H., Yamaguchi, S., Hanada, A., Kamiya, Y., and Oda, K. (2004). dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant J. 37: 720-729.
69. Mäkelä, P., McLaughlin, J.E., and Boyer, J.S. (2005). Imaging and quantifying carbohydrate transport to the developing ovaries of maize. Ann. Bot. (Lond.) 96: 939-949.
70. Mandaokar, A., and Browse, J. (2009). MYB108 acts together with MYB24 to regulate jasmonate-mediated stamen maturation in Arabidopsis. Plant Physiol. 149: 851-862.
71. Mandaokar, A., Thines, B., Shin, B., Lange, B.M., Choi, G., Koo, Y. J., Yoo, Y.J., Choi, Y.D., Choi, G., and Browse, J. (2006). Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J. 46: 984-1008.
72. Maruyama, K., Sakuma, Y., Kasuga, M., Ito, Y., Seki, M., Goda, H., Shimada, Y., Yoshida, S., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2004). Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J. 38: 982-993.
73. Matsukura, S., Mizoi, J., Yoshida, T., Todaka, D., Ito, Y., Maruyama, K., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2010). Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol. Genet. Genomics 283: 185-196.
74. Mayer, K.F., Schoof, H., Haecker, A., Lenhard, M., Jürgens, G., and Laux, T. (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95: 805-815.
75. McLaughlin, J.E., and Boyer, J.S. (2004). Sugar-responsive gene expression, invertase activity, and senescence in aborting maize ovaries at low water potentials. Ann. Bot. (Lond.) 94: 675-689.
76. Melcher, K., et al. (2009). A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462: 602-608.
77. Moffat, C.S., Ingle, R.A., Wathugala, D.L., Saunders, N.J., Knight, H., and Knight, M.R. (2012). ERF5 and ERF6 play redundant roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis. PLoS ONE 7: e35995.
78. +) channel in Arabidopsis. Genes Dev. 16: 339-350.
79. Nakano, T., Suzuki, K., Fujimura, T., and Shinshi, H. (2006). Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140: 411-432.
80. Niewiadomski, P., Knappe, S., Geimer, S., Fischer, K., Schulz, B., Unte, U.S., Rosso, M.G., Ache, P., Flügge, U.I., and Schneider, A. (2005). The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17: 760-775.
81. Nicolas, M.E., Gleadow, R.M., and Dalling, M.J. (1985). Effect of post-anthesis drought on cell division and starch accumulation in developing wheat grains. Ann. Bot. (Lond.) 55: 433-444.
82. Nilson, S.E., and Assmann, S.M. (2010). Heterotrimeric G proteins regulate reproductive trait plasticity in response to water availability. New Phytol. 185: 734-746.
83. Oñate-Sánchez, L., and Singh, K.B. (2002). Identification of Arabidopsis ethylene-responsive element binding factors with distinct induction kinetics after pathogen infection. Plant Physiol. 128: 1313-1322.
84. Ooka, H., et al. (2003). Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res. 10: 239-247.
85. Oshino, T., Abiko, M., Saito, R., Ichiishi, E., Endo, M., Kawagishi-Kobayashi, M., and Higashitani, A. (2007). Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants. Mol. Genet. Genomics 278: 31-42.
86. Pagnussat, G.C., Yu, H.J., and Sundaresan, V. (2007). Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1. Plant Cell 19: 3578-3592.
87. Palaniswamy, S.K., James, S., Sun, H., Lamb, R.S., Davuluri, R.V., and Grotewold, E. (2006). AGRIS and AtRegNet. a platform to link cis-regulatory elements and transcription factors into regulatory networks. Plant Physiol. 140: 818-829.
88. Parenicová, L., de Folter, S., Kieffer, M., Horner, D.S., Favalli, C., Busscher, J., Cook, H.E., Ingram, R.M., Kater, M.M., Davies, B., Angenent, G.C., and Colombo, L. (2003). Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: New openings to the MADS world. Plant Cell 15: 1538-1551.
89. Park, S.O., Hwang, S., and Hauser, B.A. (2004). The phenotype of Arabidopsis ovule mutants mimics the morphology of primitive seed plants. Proc. Biol. Sci. 271: 311-316.
90. Park, S.Y., et al. (2009). Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071.
91. Pelaz, S., Ditta, G.S., Baumann, E., Wisman, E., and Yanofsky, M.F. (2000). B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405: 200-203.
92. Pinyopich, A., Ditta, G.S., Savidge, B., Liljegren, S.J., Baumann, E., Wisman, E., and Yanofsky, M.F. (2003). Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424: 85-88.
93. Portereiko, M.F., Lloyd, A., Steffen, J.G., Punwani, J.A., Otsuga, D., and Drews, G.N. (2006). AGL80 is required for central cell and endosperm development in Arabidopsis. Plant Cell 18: 1862-1872.
94. Putterill, J., Laurie, R., and Macknight, R. (2004). It's time to flower: The genetic control of flowering time. Bioessays 26: 363-373.
95. Riboni, M., Galbiati, M., Tonelli, C., and Conti, L. (2013). GIGANTEA enables drought escape response via abscisic acid-dependent activation of the florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS. Plant Physiol. 162: 1706-1719.
96. Robert-Seilaniantz, A., Grant, M., and Jones, J.D. (2011). Hormone crosstalk in plant disease and defense: More than just jasmonatesalicylate antagonism. Annu. Rev. Phytopathol. 49: 317-343.
97. Röckel, N., Wolf, S., Kost, B., Rausch, T., and Greiner, S. (2008). Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tip involves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins. Plant J. 53: 133-143.
98. Russinova, E., Borst, J.W., Kwaaitaal, M., Caño-Delgado, A., Yin, Y., Chory, J., and de Vries, S.C. (2004). Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16: 3216-3229.
99. Saini, H.S. (1997). Effects of water stress on male gametophyte development in plants. Sex. Plant Reprod. 10: 67-73.
100. Schiefthaler, U., Balasubramanian, S., Sieber, P., Chevalier, D., Wisman, E., and Schneitz, K. (1999). Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96: 11664-11669.
101. Schneider, K., Kienow, L., Schmelzer, E., Colby, T., Bartsch, M., Miersch, O., Wasternack, C., Kombrink, E., and Stuible, H.P. (2005). A new type of peroxisomal acyl-coenzyme A synthetase from Arabidopsis thaliana has the catalytic capacity to activate biosynthetic precursors of jasmonic acid. J. Biol. Chem. 280: 13962-13972.
102. Schröter, D., et al. (2005). Ecosystem service supply and vulnerability to global change in Europe. Science 310: 1333-1337.
103. Sengupta, S., and Majumder, A.L. (2009). Insight into the salt tolerance factors of a wild halophytic rice, Porteresia coarctata: A physiological and proteomic approach. Planta 229: 911-929.
104. Seo, H.S., Song, J.T., Cheong, J.J., Lee, Y.H., Lee, Y.W., Hwang, I., Lee, J.S., and Choi, Y.D. (2001). Jasmonic acid carboxyl methyltransferase: A key enzyme for jasmonate-regulated plant responses. Proc. Natl. Acad. Sci. USA 98: 4788-4793.
105. Setter, T.L., and Flannigan, B.A. (2001). Water deficit inhibits cell division and expression of transcripts involved in cell proliferation and endoreduplication in maize endosperm. J. Exp. Bot. 52: 1401-1408.
106. Sharp, R.E., Hsiao, T.C., and Silk, W.K. (1990). Growth of the Maize primary root at low water potentials: II. Role of growth and deposition of hexose and potassium in osmotic adjustment. Plant Physiol. 93: 1337-1346.
107. Sheoran, I.S., and Saini, H.S. (1996). Drought-induced male sterility in rice: Changes in carbohydrate levels and enzyme activityies associated with the inhibition of starch accumulation in pollen. Sex. Plant Reprod. 9: 161-169.
108. Shinozaki, K., and Yamaguchi-Shinozaki, K. (2007). Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 58: 221-227.
109. Shinozaki, K., Yamaguchi-Shinozaki, K., and Seki, M. (2003). Regulatory network of gene expression in the drought and cold stress responses. Curr. Opin. Plant Biol. 6: 410-417.
110. Shinwari, Z.K., Nakashima, K., Miura, S., Kasuga, M., Seki, M., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1998). An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem. Biophys. Res. Commun. 250: 161-170.
111. Smart, R.E. (1974). Rapid estimates of relative water content. Plant Physiol. 53: 258-260.
112. Smyth, D.R., Bowman, J.L., and Meyerowitz, E.M. (1990). Early flower development in Arabidopsis. Plant Cell 2: 755-767.
113. Song, S., Qi, T., Huang, H., Ren, Q., Wu, D., Chang, C., Peng, W., Liu, Y., Peng, J., and Xie, D. (2011). The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23: 1000-1013.
114. Sorensen, A.M., Kröber, S., Unte, U.S., Huijser, P., Dekker, K., and Saedler, H. (2003). The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J. 33: 413-423.
115. Sun, K., Hunt, K., and Hauser, B.A. (2004). Ovule abortion in Arabidopsis triggered by stress. Plant Physiol. 135: 2358-2367.
116. Sun, K., Cui, Y., and Hauser, B.A. (2005). Environmental stress alters genes expression and induces ovule abortion: Reactive oxygen species appear as ovules commit to abort. Planta 222: 632-642.
117. Umezawa, T., Sugiyama, N., Mizoguchi, M., Hayashi, S., Myouga, F., Yamaguchi-Shinozaki, K., Ishihama, Y., Hirayama, T., and Shinozaki, K. (2009). Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc. Natl. Acad. Sci. USA 106: 17588-17593.
118. Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K., and 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. Proc. Natl. Acad. Sci. USA 97: 11632-11637.
119. Urano, K., Kurihara, Y., Seki, M., and Shinozaki, K. (2010). 'Omics' analyses of regulatory networks in plant abiotic stress responses. Curr. Opin. Plant Biol. 13: 132-138.
120. Verslues, P.E., and Juenger, T.E. (2011). Drought, metabolites, and Arabidopsis natural variation: A promising combination for understanding adaptation to water-limited environments. Curr. Opin. Plant Biol. 14: 240-245.
121. Wang, R.S., Pandey, S., Li, S., Gookin, T.E., Zhao, Z., Albert, R., and Assmann, S.M. (2011). Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells. BMC Genomics 12: 216.
122. Wang, Y., Zhang, W.Z., Song, L.F., Zou, J.J., Su, Z., and Wu, W.H. (2008). Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol. 148: 1201-1211.
123. Wijeratne, A.J., Zhang, W., Sun, Y., Liu, W., Albert, R., Zheng, Z., Oppenheimer, D.G., Zhao, D., and Ma, H. (2007). Differential gene expression in Arabidopsis wild-type and mutant anthers: Insights into anther cell differentiation and regulatory networks. Plant J. 52: 14-29.
124. Wilson, Z.A., Morroll, S.M., Dawson, J., Swarup, R., and Tighe, P.J. (2001). The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J. 28: 27-39.
125. Wolters, H., and Jürgens, G. (2009). Survival of the flexible: Hormonal growth control and adaptation in plant development. Nat. Rev. Genet. 10: 305-317.
126. Wu, G., Gu, Y., Li, S., and Yang, Z. (2001). A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. Plant Cell 13: 2841-2856.
127. Wu, G., Robertson, A.J., Liu, X., Zheng, P., Wilen, R.W., Nesbitt, N.T., and Gusta, L.V. (2004). A lipid transfer protein gene BG-14 is differentially regulated by abiotic stress, ABA, anisomycin, and sphingosine in bromegrass (Bromus inermis). J. Plant Physiol. 161: 449-458.
128. Xiong, L., Schumaker, K.S., and Zhu, J.K. (2002). Cell signaling during cold, drought, and salt stress. Plant Cell 14 (Suppl): S165-S183.
129. Xu, Z., Zhou, G., and Shimizu, H. (2010). Plant responses to drought and rewatering. Plant Signal. Behav. 5: 649-654.
130. Xue, T., Wang, D., Zhang, S., Ehlting, J., Ni, F., Jakab, S., Zheng, C., and Zhong, Y. (2008). Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genomics 9: 550.
131. Yamaguchi-Shinozaki, K., and Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57: 781-803.
132. Yamasaki, S., and Dillenburg, L.R. (1999). Measurements of leaf relative water content in Araucaria angustifolia. Rev. Bras. Fisiol. Vegetal 11: 69-75.
133. Yancey, P.H. (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208: 2819-2830.
134. Yang, S.L., Xie, L.F., Mao, H.Z., Puah, C.S., Yang, W.C., Jiang, L., Sundaresan, V., and Ye, D. (2003). Tapetum determinant1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15: 2792-2804.
135. Yang, S.L., Jiang, L., Puah, C.S., Xie, L.F., Zhang, X.Q., Chen, L.Q., Yang, W.C., and Ye, D. (2005). Overexpression of TAPETUM DETERMINANT1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with excess microsporocytes1/extra sporogenous cells. Plant Physiol. 139: 186-191.
136. Yang, W.C., Ye, D., Xu, J., and Sundaresan, V. (1999). The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13: 2108-2117.
137. Yoshida, T., Fujita, Y., Sayama, H., Kidokoro, S., Maruyama, K., Mizoi, J., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2010). AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61: 672-685.
138. Zhang, W., Sun, Y., Timofejeva, L., Chen, C., Grossniklaus, U., and Ma, H. (2006). Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133: 3085-3095.
139. Zhao, D.Z., Wang, G.F., Speal, B., and Ma, H. (2002). The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16: 2021-2031.
140. Zhao, Z., Zhang, W., Stanley, B.A., and Assmann, S.M. (2008). Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. Plant Cell 20: 3210-3226.
141. Zhu, J.K. (2001). Plant salt tolerance. Trends Plant Sci. 6: 66-71.
142. Zhu, J.K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53: 247-273.