ABA as a Universal Plant Hormone

Part of the Progress in Botany book series (BOTANY, volume 75)


Abscisic acid (ABA) is a sesquiterpene known to regulate environmental stress responses in angiosperms, such as water-loss-induced stomatal closure, development of seed desiccation tolerance during maturation, and salt-, desiccation-, and freezing-stress tolerance of vegetative tissues. An ABA-induced increase in stress tolerance is also reported in other land plant lineages, including nonvascular bryophytes that diverged from vascular plants more than 420 million years ago. Thus, it is hypothesized that acquisition of sensing and response mechanisms for ABA by land plant ancestors was critical for invasion of and adaptation to land. Because bryophytes are key organisms in plant evolution, clarification of their ABA-dependent processes is important for understanding land plant evolutionary adaptation. Based on past and current studies on ABA in non-seed plants and phylogenetic analysis of genome information from various plant species, we discuss the evolution of ABA function and biosynthesis, transport, and signaling network pathways as well as calcium signaling because of its importance in ABA signaling in angiosperms. Future directions of ABA research in the evo-devo field are also discussed.


  1. Albani D, Hammond-Kosack MC, Smith C, Conlan S, Colot V, Holdsworth M, Bevan MW (1997) The wheat transcriptional activator SPA: a seed-specific bZIP protein that recognizes the GCN4-like motif in the bifactorial endosperm box of prolamin genes. Plant Cell 9:171–184PubMedGoogle Scholar
  2. Albrecht V, Weinl S, Blazevic D, D'Angelo C, Batistic O, Kolukisaoglu U, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470PubMedCrossRefGoogle Scholar
  3. Alonso R, Oñate-Sánchez L, Weltmeier F, Ehlert A, Diaz I, Dietrich K, Vicente-Carbajosa J, Dröge-Laser W (2009) A pivotal role of the basic leucine zipper transcription factor bZIP53 in the regulation of Arabidopsis seed maturation gene expression based on heterodimerization and protein complex formation. Plant Cell 21:1747–1761PubMedCrossRefGoogle Scholar
  4. Anderson LWJ (1978) Abscisic acid induces formation of floating leaves in the heterophyllous aquatic angiosperm Potamogeton nodosus. Science 201:1135–1138PubMedCrossRefGoogle Scholar
  5. Aya K, Hiwatashi Y, Kojima M, Sakakibara H, Ueguchi-Tanaka M, Hasebe M, Matsuoka M (2011) The Gibberellin perception system evolved to regulate a pre-existing GAMYB-mediated system during land plant evolution. Nat Commun 2:544PubMedCrossRefGoogle Scholar
  6. Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713PubMedCrossRefGoogle Scholar
  7. Batistic O, Waadt R, Steinhorst L, Held K, Kudla J (2010) CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J 61:211–222PubMedCrossRefGoogle Scholar
  8. Beckett RP (1999) Partial dehydration and ABA induce tolerance to desiccation-induced ion leakage in the moss Atrichum androgynum. S Afr J Bot 65:212–217Google Scholar
  9. Bensmihen S, Rippa S, Lambert G, Jublot D, Pautot V, Granier F, Giraudat J, Parcy F (2002) The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 14:1391–1403PubMedCrossRefGoogle Scholar
  10. Bensmihen S, Giraudat J, Parcy F (2005) Characterization of three homologous basic leucine zipper transcription factors (bZIP) of the ABI5 family during Arabidopsis thaliana embryo maturation. J Exp Bot 56:597–603PubMedCrossRefGoogle Scholar
  11. Bewley JD (1978) Physiological aspects of desiccation toleance. Annu Rev Plant Physiol 30:195–238CrossRefGoogle Scholar
  12. Bewley JD (1979) Physiological aspects of desiccation tolerance. Annu Rev Plant Physiol 30:195–238CrossRefGoogle Scholar
  13. Bezanilla M, Pan A, Quatrano RS (2003) RNA interference in the moss Physcomitrella patens. Plant Physiol 133:470–474PubMedCrossRefGoogle Scholar
  14. Bhatla SC, Chopra RN (1981) Hormonal regulation of gametangial formation in the moss Bryum argenteum Hedw. J Exp Bot 32:1243–1256CrossRefGoogle Scholar
  15. Bhyan SB, Minami A, Kaneko Y, Suzuki S, Arakawa K, Sakata Y, Takezawa D (2012) Cold acclimation in the moss Physcomitrella patens involves abscisic acid-dependent signaling. J Plant Physiol 169(2):137–145PubMedCrossRefGoogle Scholar
  16. Boyer GL, Zeevaart JA (1982) Isolation and quantitation of beta-d-glucopyranosyl abscisate from leaves of Xanthium and spinach. Plant Physiol 70:227–231PubMedCrossRefGoogle Scholar
  17. Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjärvi J, Ghassemian M, Stephan AB, Hu H, Schroeder JI (2012) Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci USA 109(26):10593–10598PubMedCrossRefGoogle Scholar
  18. Bray EA, Zeevaart JA (1985) The compartmentation of abscisic acid and beta-d-glucopyranosyl abscisate in mesophyll cells. Plant Physiol 79:719–722PubMedCrossRefGoogle Scholar
  19. Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585PubMedCrossRefGoogle Scholar
  20. Burch J, Wilkinson T (2002) Cryopreservation of protonemata of Ditrichum cornubicum (paton) comparing the effectiveness of four cryoprotectant pretreatments. Cryo Letters 23:197–208PubMedGoogle Scholar
  21. Carles C, Bies-Ethève N, Aspart L, Léon-Kloosterziel KM, Koornneef M, Echeverria M, Delseny M (2002) Regulation of Arabidopsis thaliana Em genes: role of ABI5. Plant J 30:373–383PubMedCrossRefGoogle Scholar
  22. Casaretto J, Ho T-HD (2003) The transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells. Plant Cell 15:271–284PubMedCrossRefGoogle Scholar
  23. Charron AJ, Quatrano RS (2009) Between a rock and a dry place: the water-stressed moss. Mol Plant 2:478–486PubMedCrossRefGoogle Scholar
  24. Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ (2011) Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution. Curr Biol 21:1025–1029PubMedCrossRefGoogle Scholar
  25. Chen TH, Gusta LV (1983) Abscisic acid-induced freezing resistance in cultured plant cells. Plant Physiol 73:71–75PubMedCrossRefGoogle Scholar
  26. Cheng JY, Schraudolf V (1974) Nachweis von Abscisinsure in Sporen and jungen Prothallien von Anemia phyllitidis L. Sw. Z Pflanzenphysiol 71:366–369CrossRefGoogle Scholar
  27. Cheong YH, Kim K-N, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845PubMedCrossRefGoogle Scholar
  28. Chia SGE, Raghavan V (1982) Abscisic acid effects on spore germination and protonemal growth in the fern Mohria caffrorum. New Phytol 92:31–37CrossRefGoogle Scholar
  29. Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730PubMedCrossRefGoogle Scholar
  30. Chopra RN, Kapur A (1989) Effect of abscisic acid and kinetin on protonemal differentiation in Timmiella anomala. Plant Sci 61:203–206CrossRefGoogle Scholar
  31. Chopra RN, Mehta P (1987) Effect of some known growth regulators on growth and fertility in male clones of the moss Microdus brasiliensis (Dub.) Ther. J Exp Bot 38:331–339CrossRefGoogle Scholar
  32. Christianson ML (1998) A simple protocol for cryopreservation of mosses. Bryologist 101:32–35Google Scholar
  33. Christianson ML (2000) ABA prevents the second cytokinin-mediated event during the induction of shoot buds in the moss Funaria hygrometrica. Am J Bot 87:1540–1545PubMedCrossRefGoogle Scholar
  34. Correa LGG, Riaño-Pachón DM, Schrago CG, dos Santos RV, Mueller-Roeber B, Vincentz M (2008) The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes. PLoS One 3:e2944PubMedCrossRefGoogle Scholar
  35. Cuming AC, Cho SH, Kamisugi Y, Graham H, Quatrano RS (2007) Microarray analysis of transcriptional responses to abscisic acid and osmotic, salt, and drought stress in the moss, Physcomitrella patens. New Phytol 176:275–287PubMedCrossRefGoogle Scholar
  36. Daie J, Campbell WF (1981) Response of tomato plants to stressful temperatures : increase in abscisic acid concentrations. Plant Physiol 67:26–29PubMedCrossRefGoogle Scholar
  37. D'Angelo C, Weinl S, Batistic O, Pandey GK, Cheong YH, Schültke S, Albrecht V, Ehlert B, Schulz B, Harter K, Luan S, Bock R, Kudla J (2006) Alternative complex formation of the Ca-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J 48:857–872PubMedCrossRefGoogle Scholar
  38. Day IS, Reddy VS, Shad Ali G, Reddy ASN (2002) Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol 3:RESEARCH0056PubMedCrossRefGoogle Scholar
  39. Delk NA, Johnson KA, Chowdhury NI, Braam J (2005) CML24, regulated in expression by diverse stimuli, encodes a potential Ca2+ sensor that functions in responses to abscisic acid, daylength, and ion stress. Plant Physiol 139:240–253PubMedCrossRefGoogle Scholar
  40. Duckett JG, Pressel S, P’ng KMY, Renzaglia KS (2009) Exploding a myth: the capsule dehiscence mechanism and the function of pseudostomata in Sphagnum. New Phytol 183:1053–1063PubMedCrossRefGoogle Scholar
  41. Endo A, Sawada Y, Takahashi H, Okamoto M, Ikegami K, Koiwai H, Seo M, Toyomasu T, Mitsuhashi W, Shinozaki K, Nakazono M, Kamiya Y, Koshiba T, Nambara E (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol 147:1984–1993PubMedCrossRefGoogle Scholar
  42. Farrant J (2010) Editorial: special issue GROW “plant desiccation stress”. Plant Growth Regul 62:189–191CrossRefGoogle Scholar
  43. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609PubMedGoogle Scholar
  44. Finkelstein RR, Rock CD (2002) Abscisic acid biosynthesis and response. Arabidopsis Book, vol 1, pp e0058Google Scholar
  45. Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl):S15–S45PubMedGoogle Scholar
  46. Finkelstein R, Gampala SSL, Lynch TJ, Thomas TL, Rock CD (2005) Redundant and distinct functions of the ABA response loci ABA-INSENSITIVE(ABI)5 and ABRE-BINDING FACTOR (ABF)3. Plant Mol Biol 59:253–267PubMedCrossRefGoogle Scholar
  47. Fujii H, Zhu J-K (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385PubMedCrossRefGoogle Scholar
  48. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488PubMedCrossRefGoogle Scholar
  49. Galon Y, Finkler A, Fromm H (2010) Calcium-regulated transcription in plants. Mol Plant 3:653–669PubMedCrossRefGoogle Scholar
  50. Gilmour SJ, Thomashow MF (1991) Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 17:1233–1240PubMedCrossRefGoogle Scholar
  51. Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261PubMedGoogle Scholar
  52. Gonzalez-Guzman M, Pizzio GA, Antoni R, Vera-Sirera F, Merilo E, Bassel GW, Fernández MA, Holdsworth MJ, Perez-Amador MA, Kollist H, Rodriguez PL (2012) Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell 24:2483–2496PubMedCrossRefGoogle Scholar
  53. Goode JA, Stead AD, Duckett JG (1993) Redifferentiation of moss protonemata: an experimental and immunofluorescence study of brood cell formation. Can J Bot 71:1510–1519CrossRefGoogle Scholar
  54. Gusta L, Trischuk R, Weiser CJ (2005) Plant cold acclimation: the role of abscisic acid. J Plant Growth Regul 24:308–318CrossRefGoogle Scholar
  55. Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 97:3735–3740PubMedCrossRefGoogle Scholar
  56. Hanson PI, Schulman H (1992) Neuronal Ca2+/calmodulin-dependent protein kinases. Annu Rev Biochem 61:559–601PubMedCrossRefGoogle Scholar
  57. Harmon AC, Gribskov M, Harper JF (2000) CDPKs – a kinase for every Ca2+ signal? Trends Plant Sci 5:154–159PubMedCrossRefGoogle Scholar
  58. Hartung W, Gimmler H (1994) VII. A stress physiological role for abscisic acid (ABA) in lower plants. Prog Bot 55:157–173CrossRefGoogle Scholar
  59. Hartung W, Weller EW, Volk OH (1987) Immunochemical evidence that abscisic acid is produced by several species of Anthocerotae and Marchantiales. Bryologist 90:393–400CrossRefGoogle Scholar
  60. Hellwege EM, Volk OH, Hartung W (1992) A physiological role of abscisic acid in the liverwort Riccia fluitans L. J Plant Physiol 140:553–556CrossRefGoogle Scholar
  61. Hickok LG (1983) Abscisic acid blocks antheridiogen-induced antheridium formation in gametophytes of the fern Ceratopteris. Can J Bot 61:888–892CrossRefGoogle Scholar
  62. Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H, Kojima M, Katoh E, Xiang H, Tanahashi T, Hasebe M, Banks JA, Ashikari M, Kitano H, Ueguchi-Tanaka M, Matsuoka M (2007) The GID1-mediated gibberellin perception mechanism is conserved in the Lycophyte Selaginella moellendorffii but not in the Bryophyte Physcomitrella patens. Plant Cell 19:3058–3079PubMedCrossRefGoogle Scholar
  63. Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96:15348–15353PubMedCrossRefGoogle Scholar
  64. Hsu TC, Liu HC, Wang JS, Chen RW, Wang YC, Lin BL (2001) Early genes responsive to abscisic acid during heterophyllous induction in Marsilea quadrifolia. Plant Mol Biol 47:703–715PubMedCrossRefGoogle Scholar
  65. Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F, bZIP Research Group (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111PubMedCrossRefGoogle Scholar
  66. Jouve L, Franck T, Gaspars T, Cattivelli L, Hausman J-F (2000) Poplar acclimation to cold during in vitro conservation at low non-freezing temperature: metabolic and proteic changes. J Plant Physiol 157:117–123CrossRefGoogle Scholar
  67. Kamisugi Y, von Stackelberg M, Lang D, Care M, Reski R, Rensing SA, Cuming AC (2008) A sequence-anchored genetic linkage map for the moss, Physcomitrella patens. Plant J 56:855–866PubMedCrossRefGoogle Scholar
  68. Kang J, Hwang J-U, Lee M, Kim Y-Y, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci USA 107:2355–2360PubMedCrossRefGoogle Scholar
  69. Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M, Koshiba T, Kamiya Y, Seo M (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proc Natl Acad Sci USA 109:9653–9658PubMedCrossRefGoogle Scholar
  70. Khandelwal A, Cho SH, Marella H, Sakata Y, Perroud P-F, Pan A, Quatrano RS (2010) Role of ABA and ABI3 in desiccation tolerance. Science 327:546PubMedCrossRefGoogle Scholar
  71. Khraiwesh B, Ossowski S, Weigel D, Reski R, Frank W (2008) Specific gene silencing by artificial MicroRNAs in Physcomitrella patens: an alternative to targeted gene knockouts. Plant Physiol 148:684–693PubMedCrossRefGoogle Scholar
  72. Kim K-N, Cheong YH, Grant JJ, Pandey GK, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411–423PubMedCrossRefGoogle Scholar
  73. Kim MC, Chung WS, Yun D-J, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21PubMedCrossRefGoogle Scholar
  74. Knight CD, Sehgal A, Atwal K, Wallace JC, Cove DJ, Coates D, Quatrano RS, Bahadur S, Stockley PG, Cuming AC (1995) Molecular responses to abscisic acid and stress are conserved between moss and cereals. Plant Cell 7:499–506PubMedGoogle Scholar
  75. Knight H, Zarka DG, Okamoto H, Thomashow MF, Knight MR (2004) Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol 135:1710–1717PubMedCrossRefGoogle Scholar
  76. Koiwai H, Nakaminami K, Seo M, Mitsuhashi W, Toyomasu T, Koshiba T (2004) Tissue-specific localization of an abscisic acid biosynthetic enzyme, AAO3, in Arabidopsis. Plant Physiol 134:1697–1707PubMedCrossRefGoogle Scholar
  77. Komatsu K, Nishikawa Y, Ohtsuka T, Taji T, Quatrano RS, Tanaka S, Sakata Y (2009) Functional analyses of the ABI1-related protein phosphatase type 2C reveal evolutionarily conserved regulation of abscisic acid signaling between Arabidopsis and the moss Physcomitrella patens. Plant Mol Biol 70:327–340PubMedCrossRefGoogle Scholar
  78. Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidipsis thaliana. Physiol Plant 61:377–383CrossRefGoogle Scholar
  79. Koster K, Balsamo R, Espinoza C, Oliver M (2010) Desiccation sensitivity and tolerance in the moss Physcomitrella patens: assessing limits and damage. Plant Growth Regul 62:293–302CrossRefGoogle Scholar
  80. Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563PubMedCrossRefGoogle Scholar
  81. Kumra S, Chopra RN (1986) Combined effect of some growth regulators on growth and gametangial formation in the liverwort Riccia gangetica Ahmad. J Exp Bot 37:1552–1557CrossRefGoogle Scholar
  82. Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci USA 107:2361–2366PubMedCrossRefGoogle Scholar
  83. Kuromori T, Sugimoto E, Shinozaki K (2011) Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant J 67:885–894PubMedCrossRefGoogle Scholar
  84. Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656PubMedCrossRefGoogle Scholar
  85. Lalk I, Dorffling K (1985) Hardening, abscisic acid, proline and freezing resistance in two winter wheat varieties. Physiol Plant 63:287–292CrossRefGoogle Scholar
  86. Lara P, Oñate-Sánchez L, Abraham Z, Ferrándiz C, Diaz I, Carbonero P, Vicente-Carbajosa J (2003) Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2. J Biol Chem 278:21003–21011PubMedCrossRefGoogle Scholar
  87. Leckie CP, McAinsh MR, Montgomery L, Priestley AJ, Staxen I, Webb AAR, Hetherington AM (1998) Second messengers in guard cells. J Exp Bot 49:339–349Google Scholar
  88. Lee KH, Piao HL, Kim H-Y, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee I-J, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–1120PubMedCrossRefGoogle Scholar
  89. Lehnert B, Bopp M (1983) The hormonal regulation of protonema development in mosses I. Auxin-cytokinin interaction. Z Pflanzenphysiol 110:379–391Google Scholar
  90. Li X, Syrkin Wurtele E, Lamotte CE (1994) Abscisic acid is present in liverworts. Phytochemistry 37:625–627CrossRefGoogle Scholar
  91. Ligrone R, Duckett JG, Renzaglia KS (2012a) Major transitions in the evolution of early land plants: a bryological perspective. Ann Bot 109:851–871PubMedCrossRefGoogle Scholar
  92. Ligrone R, Duckett JG, Renzaglia KS (2012b) The origin of the sporophyte shoot in land plants: a bryological perspective. Ann Bot 110:935–941PubMedCrossRefGoogle Scholar
  93. Lin BL, Wang HJ, Wang JS, Zaharia LI, Abrams SR (2005) Abscisic acid regulation of heterophylly in Marsilea quadrifolia L.: effects of R-(−) and S-(+) isomers. J Exp Bot 56:2935–2948PubMedCrossRefGoogle Scholar
  94. Liu BLL (1984) Abscisic induces land form characteristics in Marsilia quadrifolia L. Am J Bot 71:638–644CrossRefGoogle Scholar
  95. Liu X, Yue Y, Li B, Nie Y, Li W, Wu W-H, Ma L (2007) A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315:1712–1716PubMedCrossRefGoogle Scholar
  96. Liu MS, Chien CT, Lin TP (2008) Constitutive components and induced gene expression are involved in the desiccation tolerance of Selaginella tamariscina. Plant Cell Physiol 49:653–663PubMedCrossRefGoogle Scholar
  97. Luan S (2009) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14:37–42PubMedCrossRefGoogle Scholar
  98. Lucas JR, Renzaglia KS (2002) Structure and function of hornwort stomata. Microsc Microanal 8:1090–1091Google Scholar
  99. Lynch T, Erickson BJ, Finkelstein RR (2012) Direct interactions of ABA-insensitive(ABI)-clade protein phosphatase(PP)2Cs with calcium-dependent protein kinases and ABA response element-binding bZIPs may contribute to turning off ABA response. Plant Mol Biol 80:647–658PubMedCrossRefGoogle Scholar
  100. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068PubMedGoogle Scholar
  101. Magnan F, Ranty B, Charpenteau M, Sotta B, Galaud J-P, Aldon D (2008) Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid. Plant J 56:575–589PubMedCrossRefGoogle Scholar
  102. Marcotte WRJ, Russell SH, Quatrano RS (1989) Abscisic acid-responsive sequences from the em gene of wheat. Plant Cell 1:969–976PubMedGoogle Scholar
  103. Marella HH, Sakata Y, Quatrano RS (2006) Characterization and functional analysis of ABSCISIC ACID INSENSITIVE3-like genes from Physcomitrella patens. Plant J 46:1032–1044PubMedCrossRefGoogle Scholar
  104. Maruyama K, Todaka D, Mizoi J, Yoshida T, Kidokoro S, Matsukura S, Takasaki H, Sakurai T, Yamamoto YY, Yoshiwara K, Kojima M, Sakakibara H, Shinozaki K, Yamaguchi-Shinozaki K (2012) Identification of cis-acting promoter elements in cold- and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res 19:37–49PubMedCrossRefGoogle Scholar
  105. Matakiadis T, Alboresi A, Jikumaru Y, Tatematsu K, Pichon O, Renou J-P, Kamiya Y, Nambara E, Truong H-N (2009) The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiol 149:949–960PubMedCrossRefGoogle Scholar
  106. Mayaba N, Beckett RP, Csintalan Z, Tuba Z (2001) ABA increases the desiccation tolerance of photosynthesis in the afromontane understorey moss Atrichum androgynum. Ann Bot 88:1093–1100CrossRefGoogle Scholar
  107. McAdam SAM, Brodribb TJ (2012) Fern and lycophyte guard cells do not respond to endogenous abscisic acid. Plant Cell 24:1510–1521PubMedCrossRefGoogle Scholar
  108. McAinsh MR, Martin R, Brownlee C, Hetherington AM (1990) Abscisic acid-induced elevation of guard cell cytosolic Ca2+ precedes stomatal closure. Nature 343:186–188CrossRefGoogle Scholar
  109. McAinsh MR, Webb A, Taylor JE, Hetherington AM (1995) Stimulus-induced oscillations in guard cell cytosolic free calcium. Plant Cell 7:1207–1219PubMedGoogle Scholar
  110. McCarty DR, Carson CB, Stinard PS, Robertson DS (1989) Molecular analysis of viviparous-1: an abscisic acid-insensitive mutant of maize. Plant Cell 1:523–532PubMedGoogle Scholar
  111. McCormack E, Tsai Y-C, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389PubMedCrossRefGoogle Scholar
  112. Menon MKC, Lal M (1974) Morphogenetic role of kinetin and abscisic acid in the moss Physcomitrium. Planta 115:319–328CrossRefGoogle Scholar
  113. Milborrow BV (1974) The chemistry and physiology of abscisic acid. Annu Rev Plant Physiol 25:259–307CrossRefGoogle Scholar
  114. Minami A, Nagao M, Arakawa K, Fujikawa S, Takezawa D (2003) Abscisic acid-induced freezing tolerance in the moss Physcomitrella patens is accompanied by increased expression of stress-related genes. J Plant Physiol 160:475–483PubMedCrossRefGoogle Scholar
  115. Minami A, Nagao M, Ikegami K, Koshiba T, Arakawa K, Fujikawa S, Takezawa D (2005) Cold acclimation in bryophytes: low-temperature-induced freezing tolerance in Physcomitrella patens is associated with increases in expression levels of stress-related genes but not with increase in level of endogenous abscisic acid. Planta 220:414–423PubMedCrossRefGoogle Scholar
  116. Mori IC, Murata Y (2011) ABA signaling in stomatal guard cells: lessons from Commelina and Vicia. J Plant Res 124:477–487PubMedCrossRefGoogle Scholar
  117. Mori IC, Murata Y, Yang Y, Munemasa S, Wang Y-F, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca(2+)-permeable channels and stomatal closure. PLoS Biol 4:e327PubMedCrossRefGoogle Scholar
  118. Nagao M, Minami A, Arakawa K, Fujikawa S, Takezawa D (2005) Rapid degradation of starch in chloroplasts and concomitant accumulation of soluble sugars associated with ABA-induced freezing tolerance in the moss Physcomitrella patens. J Plant Physiol 162:169–180PubMedCrossRefGoogle Scholar
  119. Nagao M, Oku K, Minami A, Mizuno K, Sakurai M, Arakawa K, Fujikawa S, Takezawa D (2006) Accumulation of theanderose in association with development of freezing tolerance in the moss Physcomitrella patens. Phytochemistry 67:702–709PubMedCrossRefGoogle Scholar
  120. Nakamura S, Lynch TJ, Finkelstein RR (2001) Physical interactions between ABA response loci of Arabidopsis. Plant J 26:627–635PubMedCrossRefGoogle Scholar
  121. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185PubMedCrossRefGoogle Scholar
  122. Nambara E, Keith K, McCourt P, Naito S (1995) A regulatory role for the ABI3 gene in the establishment of embryo maturation in Arabidopsis thaliana. Development 121:629–636Google Scholar
  123. Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148PubMedCrossRefGoogle Scholar
  124. Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8'-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107PubMedCrossRefGoogle Scholar
  125. Okamoto M, Kushiro T, Jikumaru Y, Abrams SR, Kamiya Y, Seki M, Nambara E (2011) ABA 9′-hydroxylation is catalyzed by CYP707A in Arabidopsis. Phytochemistry 72:717–722PubMedCrossRefGoogle Scholar
  126. Oldenhof H, Wolkers WF, Bowman JL, Tablin F, Crowe JH (2006) Freezing and desiccation tolerance in the moss Physcomitrella patens: an in situ Fourier transform infrared spectroscopic study. Biochim Biophys Acta 1760:1226–1234PubMedCrossRefGoogle Scholar
  127. Oliver MJ (1991) Influence of protoplasmic water loss on the control of protein synthesis in the desiccation-tolerant moss Tortula ruralis: ramifications for a repair-based mechanism of desiccation tolerance. Plant Physiol 97:1501–1511PubMedCrossRefGoogle Scholar
  128. Oliver MJ, Tuba Z, Mishler BD (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151:85–100CrossRefGoogle Scholar
  129. Oliver MJ, Velten J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr Comp Biol 45:788–799PubMedCrossRefGoogle Scholar
  130. Oñate L, Vicente-Carbajosa J, Lara P, Díaz I, Carbonero P (1999) Barley BLZ2, a seed-specific bZIP protein that interacts with BLZ1 in vivo and activates transcription from the GCN4-like motif of B-hordein promoters in barley endosperm. J Biol Chem 274:9175–9182PubMedCrossRefGoogle Scholar
  131. Pandey GK, Cheong YH, Kim K-N, Grant JJ, Li L, Hung W, D'Angelo C, Weinl S, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924PubMedCrossRefGoogle Scholar
  132. Pandey GK, Grant JJ, Cheong YH, Kim B-G, Li LG, Luan S (2008) Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination. Mol Plant 1:238–248PubMedCrossRefGoogle Scholar
  133. Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136:136–148PubMedCrossRefGoogle Scholar
  134. Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-FF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu J-K, Schroeder JI, Volkman BF et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071PubMedGoogle Scholar
  135. Pei ZM, Kuchitsu K, Ward JM, Schwarz M, Schroeder JI (1997) Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell 9:409–423PubMedGoogle Scholar
  136. Pence VC (1998) Cryopreservation of bryophytes: the effects of abscisic acid and encapsulation dehydration. Bryologist 101:278–281Google Scholar
  137. Pence VC (2000) Cryopreservation of in vitro grown fern gametophytes. Am Fern J 90:16–23CrossRefGoogle Scholar
  138. Pence VC, Dunford SS, Redella S (2005) Differential effects of abscisic acid on desiccation tolerance and carbohydrates in three species of liverworts. J Plant Physiol 162:1331–1337PubMedCrossRefGoogle Scholar
  139. Pilate G, Sossountzov L, Miginiac E (1989) Hormone levels and apical dominance in the aquatic fern Marsilea drummondii A. Br. Plant Physiol 90:907–912PubMedCrossRefGoogle Scholar
  140. Ponce DE, León I, Schmelz EA, Gaggero C, Castro A, Alvarez A, Montesano M (2012) Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection. Mol Plant Pathol 13:960–974CrossRefGoogle Scholar
  141. Popescu SC, Popescu GV, Bachan S, Zhang Z, Seay M, Gerstein M, Snyder M, Dinesh-Kumar SP (2007a) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc Natl Acad Sci USA 104:4730–4735PubMedCrossRefGoogle Scholar
  142. Popescu SC, Snyder M, Dinesh-Kumar S (2007b) Arabidopsis protein microarrays for the high-throughput identification of protein-protein interactions. Plant Signal Behav 2:416–420PubMedCrossRefGoogle Scholar
  143. Quatrano RS, McDaniel SF, Khandelwal A, Perroud P-F, Cove DJ (2007) Physcomitrella patens: mosses enter the genomic age. Curr Opin Plant Biol 10:182PubMedCrossRefGoogle Scholar
  144. Qudeimat E, Faltusz AMC, Wheeler G, Lang D, Holtorf H, Brownlee C, Reski R, Frank W (2008) A PIIB-type Ca2+−ATPase is essential for stress adaptation in Physcomitrella patens. Proc Natl Acad Sci USA 105:19555–19560PubMedCrossRefGoogle Scholar
  145. Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032PubMedCrossRefGoogle Scholar
  146. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud P-F, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin-I T, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S-I, Yamaguchi K et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69PubMedCrossRefGoogle Scholar
  147. Reynolds TL, Bewley JD (1993a) Abscisic acid enhances the ability of the desiccation-tolerant fern Polypodium virginianum to withstand drying. J Exp Bot 44:1771–1779CrossRefGoogle Scholar
  148. Reynolds TL, Bewley JD (1993b) Characterization of protein synthetic changes in a desiccation-tolerant fern, Polypodium virginianum. Comparison of the effects of drying, rehydration and abscisic acid. J Exp Bot 44:921–928CrossRefGoogle Scholar
  149. Richardt S, Timmerhaus G, Lang D, Qudeimat E, Corrêa LGG, Reski R, Rensing SA, Frank W (2010) Microarray analysis of the moss Physcomitrella patens reveals evolutionarily conserved transcriptional regulation of salt stress and abscisic acid signalling. Plant Mol Biol 72:27–45PubMedCrossRefGoogle Scholar
  150. Risk JM, Day CL, Macknight RC (2009) Reevaluation of abscisic acid-binding assays shows that G-protein-coupled receptor2 does not bind abscisic Acid. Plant Physiol 150:6–11PubMedCrossRefGoogle Scholar
  151. Rock CD, Sakata Y, Quatrano RS (2010) Stress signaling I: the role of abscisic acid (ABA). In: Pareek A, Sopory SA, Bohner HJ, Govindjee (eds) Abiotic stress adaptation in plants. Springer, Dordrecht, pp 33–73Google Scholar
  152. Russell AJ, Knight MR, Cove DJ, Knight CD, Trewavas AJ, Wang TL (1996) The moss, Physcomitrella patens, transformed with apoaequorin cDNA responds to cold shock, mechanical perturbation and pH with transient increases in cytoplasmic calcium. Transgenic Res 5:167–170PubMedCrossRefGoogle Scholar
  153. Russell AJ, Cove DJ, Trewavas AJ, Wang TL (1998) Blue light but not red light induces a calcium transient in the moss Physcomitrella patens (Hedw.) B., S. & G. Planta 206:278–283CrossRefGoogle Scholar
  154. Ruszala EM, Beerling DJ, Franks PJ, Chater C, Casson SA, Gray JE, Hetherington AM (2011) Land plants acquired active stomatal control early in their evolutionary history. Curr Biol 21:1030–1035PubMedCrossRefGoogle Scholar
  155. Rütten D, Santarius KA (1992) Relationship between frost tolerance and sugar concentration of various bryophytes in summer and winter. Oecologia 91:260–265CrossRefGoogle Scholar
  156. Sakata Y, Nakamura I, Taji T, Tanaka S, Quatrano RS (2010) Regulation of the ABA-responsive Em promoter by ABI3 in the moss Physcomitrella patens: role of the ABA response element and the RY element. Plant Signal Behav 5:1061–1066PubMedCrossRefGoogle Scholar
  157. Schaefer DG, Zryd JP (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206PubMedCrossRefGoogle Scholar
  158. Schmidt RJ, Ketudat M, Aukerman MJ, Hoschek G (1992) Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kD zein genes. Plant Cell 4:689–700PubMedGoogle Scholar
  159. Schnepf E, Reinhard C (1997) Brachycytes in Funaria protonemate: induction by abscisic acid and fine structure. J Plant Physiol 151:166–175CrossRefGoogle Scholar
  160. Schroeder JI, Hagiwara S (1990) Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. Proc Natl Acad Sci USA 87:9305–9309PubMedCrossRefGoogle Scholar
  161. Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658PubMedCrossRefGoogle Scholar
  162. Schwabe WW, Valio IFM (1970) Growth and dormancy in Lunularia cruciata (L.) Dum. J Exp Bot 21:122–137CrossRefGoogle Scholar
  163. Scott HB, Oliver MJ (1994) Accumulation and polysomal recruitment of transcripts in response to desiccation and rehydration of the moss Tortula ruralis. J Exp Bot 45:577–583CrossRefGoogle Scholar
  164. Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2:282–291PubMedCrossRefGoogle Scholar
  165. Seo M, Koshiba T (2011) Transport of ABA from the site of biosynthesis to the site of action. J Plant Res 124:501–507PubMedCrossRefGoogle Scholar
  166. Shen Y-Y, Wang X-F, Wu F-Q, Du S-Y, Cao Z, Shang Y, Wang X-L, Peng C-C, Yu X-C, Zhu S-Y, Fan R-C, Xu Y-H, Zhang D-P (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826PubMedCrossRefGoogle Scholar
  167. Siegel RS, Xue S, Murata Y, Yang Y, Nishimura N, Wang A, Schroeder JI (2009) Calcium elevation-dependent and attenuated resting calcium-dependent abscisic acid induction of stomatal closure and abscisic acid-induced enhancement of calcium sensitivities of S-type anion and inward-rectifying K channels in Arabidopsis guard cells. Plant J 59:207–220PubMedCrossRefGoogle Scholar
  168. Smoleńska-Sym G, Gawrońska H, Kacperska A (1995) Modifications of abscisic acid level in winter oilseed rape leaves during acclimation of plants to freezing temperatures. Plant Growth Regul 17:61–65Google Scholar
  169. Sun M-M, Li L-H, Xie H, Ma R-C, He Y-K (2007) Differentially expressed genes under cold acclimation in Physcomitrella patens. J Biochem Mol Biol 40:986–1001PubMedCrossRefGoogle Scholar
  170. Suzuki M, Kao CY, McCarty DR (1997) The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity. Plant Cell 9:799–807PubMedGoogle Scholar
  171. Swami P, Raghavan V (1980) Control of morphogenesis in the gametophyte of a fern by light and growth hormones. Can J Bot 58:1464–1473CrossRefGoogle Scholar
  172. Takezawa D, Komatsu K, Sakata Y (2011) ABA in bryophytes: how a universal growth regulator in life became a plant hormone? J Plant Res 124:437–453PubMedCrossRefGoogle Scholar
  173. Tougane K, Komatsu K, Bhyan SB, Sakata Y, Ishizaki K, Yamato KT, Kohchi T, Takezawa D (2010) Evolutionarily conserved regulatory mechanisms of abscisic acid signaling in land plants: characterization of ABSCISIC ACID INSENSITIVE1-like type 2C protein phosphatase in the liverwort Marchantia polymorpha. Plant Physiol 152:1529–1543PubMedCrossRefGoogle Scholar
  174. Trewavas AJ, Malhó R (1998) Ca2+ signalling in plant cells: the big network! Curr Opin Plant Biol 1:428–433PubMedCrossRefGoogle Scholar
  175. Tsay Y-F, Chiu C-C, Tsai C-B, Ho C-H, Hsu P-K (2007) Nitrate transporters and peptide transporters. FEBS Lett 581:2290–2300PubMedCrossRefGoogle Scholar
  176. Tsuzuki T, Takahashi K, Inoue S-I, Okigaki Y, Tomiyama M, Hossain MA, Shimazaki K-I, Murata Y, Kinoshita T (2011) Mg-chelatase H subunit affects ABA signaling in stomatal guard cells, but is not an ABA receptor in Arabidopsis thaliana. J Plant Res 124:527–538PubMedCrossRefGoogle Scholar
  177. Tucker EB, Lee M, Alli S, Sookhdeo V, Wada M, Imaizumi T, Kasahara M, Hepler PK (2005) UV-A induces two calcium waves in Physcomitrella patens. Plant Cell Physiol 46:1226–1236PubMedCrossRefGoogle Scholar
  178. Umezawa T, Okamoto M, Kushiro T, Nambara E, Oono Y, Seki M, Kobayashi M, Koshiba T, Kamiya Y, Shinozaki K (2006) CYP707A3, a major ABA 8'-hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana. Plant J 46:171–182PubMedCrossRefGoogle Scholar
  179. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839PubMedCrossRefGoogle Scholar
  180. 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. Proc Natl Acad Sci USA 97:11632–11637PubMedCrossRefGoogle Scholar
  181. Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539PubMedGoogle Scholar
  182. Vahisalu T, Kollist H, Wang Y-F, Nishimura N, Chan W-Y, Valerio G, Lamminmäki A, Brosché M, Moldau H, Desikan R, Schroeder JI, Kangasjärvi J (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452:487–491PubMedCrossRefGoogle Scholar
  183. Valadon LRG, Mummery RS (1971) Quantitative relationship between various growth substances and bud production in Funaria hygrometrica. A bioassay for abscisic acid. Physiol Plant 24:232–234CrossRefGoogle Scholar
  184. Vasil V, Marcotte WRJ, Rosenkrans L, Cocciolone SM, Vasil IK, Quatrano RS, McCarty DR (1995) Overlap of Viviparous1 (VP1) and abscisic acid response elements in the Em promoter: G-box elements are sufficient but not necessary for VP1 transactivation. Plant Cell 7:1511–1518PubMedGoogle Scholar
  185. Vatén A, Bergmann DC (2012) Mechanisms of stomatal development: an evolutionary view. Evodevo 3:11PubMedCrossRefGoogle Scholar
  186. Warne TR, Hickok LG (1991) Control of sexual development in gametophytes of Ceratopteris-richardii antheridiogen and abscisic acid. Bot Gaz 152:148–153CrossRefGoogle Scholar
  187. Weiler EW (1979) Radioimmunoassay for the determination of free and conjugated abscisic acid. Planta 144:255–263CrossRefGoogle Scholar
  188. Werner O, Ros Espín RM, Bopp M, Atzorn R (1991) Abscisic-acid-induced drought tolerance in Funaria hygrometrica Hedw. Planta 186:99CrossRefGoogle Scholar
  189. Xiang Y, Huang Y, Xiong L (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol 144:1416–1428PubMedCrossRefGoogle Scholar
  190. Xiong L, Zhu J-K (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36PubMedCrossRefGoogle Scholar
  191. Xu Z-Y, Lee KH, Dong T, Jeong JC, Jin JB, Kanno Y, Kim DH, Kim SY, Seo M, Bressan RA, Yun D-J, 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. Plant Cell 24:2184–2199PubMedCrossRefGoogle Scholar
  192. 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. Plant Cell 6:251–264PubMedGoogle Scholar
  193. Yamane H, Sato Y, Takahashi N, Takeno K, Furuya M (1980) Endogenous inhibitors for spore germination in Lygodium japonicum and their inhibitory effects on pollen germinations in Camellia japonica and Camellia sinensis. Agric Biol Chem 44:1697–1699CrossRefGoogle Scholar
  194. Yamane H, Fujioka S, Spray CR, Phinney BO, MacMillan J, Gaskin P, Takahashi N (1988) Endogenous gibberellins from sporophytes of two tree ferns, Cibotium glaucum and Dicksonia antarctica. Plant Physiol 86:857–862PubMedCrossRefGoogle Scholar
  195. Yang T, Chaudhuri S, Yang L, Chen Y, Poovaiah BW (2004) Calcium/calmodulin up-regulates a cytoplasmic receptor-like kinase in plants. J Biol Chem 279:42552–42559PubMedCrossRefGoogle Scholar
  196. Yang T, Chaudhuri S, Yang L, Du L, Poovaiah BW (2010a) A calcium/calmodulin-regulated member of the receptor-like kinase family confers cold tolerance in plants. J Biol Chem 285:7119–7126PubMedCrossRefGoogle Scholar
  197. Yang T, Shad Ali G, Yang L, Du L, Reddy ASN, Poovaiah BW (2010b) Calcium/calmodulin-regulated receptor-like kinase CRLK1 interacts with MEKK1 in plants. Plant Signal Behav 5:991–994PubMedCrossRefGoogle Scholar
  198. Yoo JH, Park CY, Kim JC, Heo WD, Cheong MS, Park HC, Kim MC, Moon BC, Choi MS, Kang YH, Lee JH, Kim HS, Lee SM, Yoon HW, Lim CO, Yun D-J, Lee SY, Chung WS, Cho MJ (2005) Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in arabidopsis. J Biol Chem 280:3697–3706PubMedCrossRefGoogle Scholar
  199. Yoshida K (2005) Evolutionary process of stress response systems controlled by abscisic acid in photosynthetic organisms. Yakugaku Zasshi-J Pharma Soc Jpn 125:927–936CrossRefGoogle Scholar
  200. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, 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 61:672–685PubMedCrossRefGoogle Scholar
  201. Zeevaart JAD, Creelman RA (1988) Metabolism and physiology of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol 39:439–473CrossRefGoogle Scholar
  202. Zhang X, Garreton V, Chua N-H (2005) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev 19:1532–1543PubMedCrossRefGoogle Scholar
  203. Zhou R, Cutler AJ, Ambrose SJ, Galka MM, Nelson KM, Squires TM, Loewen MK, Jadhav AS, Ross ARS, Taylor DC, Abrams SR (2004) A new abscisic acid catabolic pathway. Plant Physiol 134:361–369PubMedCrossRefGoogle Scholar
  204. Zhu S-Y, Yu X-C, Wang X-J, Zhao R, Li Y, Fan R-C, Shang Y, Du S-Y, Wang X-F, Wu F-Q, Xu Y-H, Zhang X-Y, Zhang D-P (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Yoichi Sakata
    • 1
  • Kenji Komatsu
    • 2
  • Daisuke Takezawa
    • 3
  1. 1.Department of BioscienceTokyo University of AgricultureTokyoJapan
  2. 2.Department of Bioproduction TechnologyJunior College of Tokyo University of AgricultureTokyoJapan
  3. 3.Graduate School of Science and Engineering and Institute for Environmental Science and TechnologySaitama UniversitySaitamaJapan

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