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Abscisic Acid Signaling and Biosynthesis: Protein Structures and Molecular Probes

  • Jonathan D. M. Helander
  • Sean R. Cutler
Chapter

Abstract

Abscisic acid (ABA) is an apocarotenoid plant hormone that mediates responses to abiotic stress and modulates multiple growth and developmental processes. ABA acts through a negative regulatory signaling module that is present in all land plant genomes sequenced. Here we review ABA’s biosynthesis, perception, and its core signaling network, focusing on the wealth of X-ray crystallographic data for the receptors, phosphatases, and kinases that form the core ABA response module. We unite these structural insights with progress in the development of ABA biosynthesis and signaling modulators and cover both inhibitors of 9-cis-expoycarotenoid dioxygenases (NCEDs) and ABA receptor modulators including the agonist quinabactin and antagonist AS6. Quinabactin preferentially activates dimeric subfamily III ABA receptors and its biological activity has defined pyrabactin resistance 1 (PYR1) and its close relatives as key targets for controlling transpiration. Structural analyses of receptor-ligand complexes have facilitated the design of ABA analogs such as AS6 that antagonize signaling by disrupting receptor-PP2C interactions. Thus, the extensive structural data now available is facilitating the development of chemical and genetic tools to manipulate ABA biosynthesis and signaling and has refined our understanding of these new druggable target sites.

References

  1. Abrams SR, Rose PA, Cutler AJ, Balsevich JJ, Lei B, Walker-Simmons MK (1997) 8[prime]-methylene Abscisic acid (an effective and persistent analog of Abscisic acid). Plant Physiol 114:89–97PubMedPubMedCentralCrossRefGoogle Scholar
  2. Anderberg RJ, Walker-Simmons MK (1992) Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases. Proc Natl Acad Sci U S A 89:10183–10187PubMedPubMedCentralCrossRefGoogle Scholar
  3. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479PubMedPubMedCentralCrossRefGoogle Scholar
  4. Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321PubMedCrossRefGoogle Scholar
  5. Belin C, de Franco P-O, Bourbousse C, Chaignepain S, Schmitter J-M, Vavasseur A, Giraudat J, Barbier-Brygoo H, Thomine S (2006) Identification of features regulating OST1 kinase activity and OST1 function in guard cells. Plant Physiol 141:1316–1327PubMedPubMedCentralCrossRefGoogle Scholar
  6. Benson CL, Kepka M, Wunschel C, Rajagopalan N, Nelson KM, Christmann A, Abrams SR, Grill E, Loewen MC (2015) Abscisic acid analogs as chemical probes for dissection of abscisic acid responses in Arabidopsis thaliana. Phytochemistry 113:96–107PubMedCrossRefGoogle Scholar
  7. Bhaskara GB, Nguyen TT, Verslues PE (2012) Unique drought resistance functions of the highly ABA-induced clade a protein phosphatase 2Cs. Plant Physiol 160:379–395PubMedPubMedCentralCrossRefGoogle Scholar
  8. Cao M, Liu X, Zhang Y, Xue X, Zhou XE, Melcher K, Gao P, Wang F, Zeng L, Zhao Y, Zhao Y, Deng P, Zhong D, Zhu J-K, Xu HE, Xu Y (2013) An ABA-mimicking ligand that reduces water loss and promotes drought resistance in plants. Cell Res 23:1043–1054PubMedPubMedCentralCrossRefGoogle Scholar
  9. Chiwocha SDS, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross ARS, Kermode AR (2005) The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J 42:35–48PubMedCrossRefGoogle Scholar
  10. Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root-to-shoot signalling of water shortage. Plant J 52:167–174PubMedCrossRefGoogle Scholar
  11. Cohen P (1989) The structure and regulation of protein phosphatases. Annu Rev Biochem 58:453–508PubMedCrossRefGoogle Scholar
  12. Creelman RA, Mason HS, Bensen RJ, Boyer JS (1990) Water deficit and abscisic acid cause differential inhibition of shoot versus root growth in soybean seedlings analysis of growth, sugar accumulation, and gene expression. Plant Physiology 92(1):205–214PubMedPubMedCentralCrossRefGoogle Scholar
  13. Creelman RA, Bell E, Mullet JE (1992) Involvement of a lipoxygenase-like enzyme in abscisic acid biosynthesis. Plant Physiol 99:1258–1260PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P (1996) A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science 273:1239–1241PubMedCrossRefGoogle Scholar
  15. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679PubMedCrossRefGoogle Scholar
  16. De Smet I, Signora L, Beeckman T, Inzé D (2003) An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. The PlantGoogle Scholar
  17. De Smet I, Zhang H, Inzé D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439PubMedCrossRefGoogle Scholar
  18. Deak KI, Malamy J (2005) Osmotic regulation of root system architecture. Plant J 43:17–28PubMedCrossRefGoogle Scholar
  19. Duan L, Dietrich D, Ng CH, Chan PMY, Bhalerao R, Bennett MJ, Dinneny JR (2013) Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell 25:324–341PubMedPubMedCentralCrossRefGoogle Scholar
  20. Dupeux F, Santiago J, Betz K, Twycross J, Park S-Y, Rodriguez L, Gonzalez-Guzman M, Jensen MR, Krasnogor N, Blackledge M, Holdsworth M, Cutler SR, Rodriguez PL, Márquez JA (2011a) A thermodynamic switch modulates abscisic acid receptor sensitivity. EMBO J 30:4171–4184PubMedPubMedCentralCrossRefGoogle Scholar
  21. Dupeux F, Antoni R, Betz K, Santiago J, Gonzalez-Guzman M, Rodriguez L, Rubio S, Park S-Y, Cutler SR, Rodriguez PL, Márquez JA (2011b) Modulation of abscisic acid signaling in vivo by an engineered receptor-insensitive protein phosphatase type 2C allele. Plant Physiol 156:106–116PubMedPubMedCentralCrossRefGoogle Scholar
  22. Endo A, Okamoto M, Koshiba T (2014) ABA biosynthetic and catabolic pathways. In: Zhang D-P (ed) Abscisic acid: metabolism, transport and signaling. Springer, Dordrecht, pp 21–45Google Scholar
  23. Fedoroff NV (2002) Cross-talk in abscisic acid signaling. Sci STKE 2002:re10PubMedGoogle Scholar
  24. Fuchs S, Tischer SV, Wunschel C, Christmann A, Grill E (2014) Abscisic acid sensor RCAR7/PYL13, specific regulator of protein phosphatase coreceptors. Proc Natl Acad Sci U S A 111:5741–5746PubMedPubMedCentralCrossRefGoogle Scholar
  25. 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 U S A 106:8380–8385PubMedPubMedCentralCrossRefGoogle Scholar
  26. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462:660–664PubMedPubMedCentralCrossRefGoogle Scholar
  27. Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50:2123–2132PubMedCrossRefGoogle Scholar
  28. Gao S, Gao J, Zhu X, Song Y, Li Z, Ren G, Zhou X, Kuai B (2016) ABF2, ABF3, and ABF4 promote ABA-mediated chlorophyll degradation and leaf senescence by transcriptional activation of chlorophyll catabolic genes and senescence-associated genes in Arabidopsis. Mol Plant 9:1272–1285PubMedCrossRefGoogle Scholar
  29. Geng Y, Wu R, Wee CW, Xie F, Wei X, Chan PMY, Tham C, Duan L, Dinneny JR (2013) A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell 25:2132–2154PubMedPubMedCentralCrossRefGoogle Scholar
  30. 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.  https://doi.org/10.1105/tpc.112.098574
  31. Gonzalez-Guzman M, Rodriguez L, Lorenzo-Orts L, Pons C, Sarrion-Perdigones A, Fernandez MA, Peirats-Llobet M, Forment J, Moreno-Alvero M, Cutler SR, Albert A, Granell A, Rodriguez PL (2014) Tomato PYR/PYL/RCAR abscisic acid receptors show high expression in root, differential sensitivity to the abscisic acid agonist quinabactin, and the capability to enhance plant drought resistance. J Exp Bot 65(15):4451–4464PubMedPubMedCentralCrossRefGoogle Scholar
  32. Gosti F, Beaudoin N, Serizet C, Webb AA, Vartanian N, Giraudat J (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11:1897–1910PubMedPubMedCentralCrossRefGoogle Scholar
  33. Gusta LV, Trischuk R, Weiser CJ (2005) Plant cold acclimation: the role of Abscisic acid. J Plant Growth Regul 24:308–318CrossRefGoogle Scholar
  34. Han S-Y, Inoue H, Terada T, Kamoda S, Saburi Y, Sekimata K, Saito T, Kobayashi M, Shinozaki K, Yoshida S, Asami T (2002) Design and synthesis of lignostilbene-α,β-dioxygenase inhibitors. Bioorg Med Chem Lett 12:1139–1142PubMedCrossRefGoogle Scholar
  35. Han S-Y, Inoue H, Terada T, Kamoda S, Saburi Y, Sekimata K, Saito T, Kobayashi M, Shinozaki K, Yoshida S, Asami T (2003) N -Benzylideneaniline and N -Benzylaniline are Potent Inhibitors of Lignostilbene-α,β-dioxygenase, a Key Enzyme in Oxidative Cleavage of the Central Double Bond of Lignostilbene. J Enzyme Inhib Med Chem 18:279–283PubMedCrossRefGoogle Scholar
  36. Han S-Y, Kitahata N, Sekimata K, Saito T, Kobayashi M, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K, Yoshida S, Asami T (2004) A novel inhibitor of 9-cis-epoxycarotenoid dioxygenase in abscisic acid biosynthesis in higher plants. Plant Physiol 135:1574–1582PubMedPubMedCentralCrossRefGoogle Scholar
  37. Hao Q, Yin P, Yan C, Yuan X, Li W, Zhang Z, Liu L, Wang J, Yan N (2010) Functional mechanism of the abscisic acid agonist pyrabactin. J Biol Chem 285:28946–28952PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hao Q, Yin P, Li W, Wang L, Yan C, Lin Z, Wu JZ, Wang J, Yan SF, Yan N (2011) The molecular basis of ABA-independent inhibition of PP2Cs by a subclass of PYL proteins. Mol Cell 42:662–672PubMedCrossRefGoogle Scholar
  39. Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8:774–785PubMedCrossRefGoogle Scholar
  40. Harrison PJ, Bugg TDH (2014) Enzymology of the carotenoid cleavage dioxygenases: reaction mechanisms, inhibition and biochemical roles. Arch Biochem Biophys 544:105–111PubMedCrossRefGoogle Scholar
  41. Hartung W (2010) The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Funct Plant Biol 37:806–812CrossRefGoogle Scholar
  42. Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21:R346–R355PubMedPubMedCentralCrossRefGoogle Scholar
  43. He Y, Hao Q, Li W, Yan C, Yan N, Yin P (2014) Identification and characterization of ABA receptors in Oryza sativa. PLoS One 9:e95246PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hedbacker K, Carlson M (2008) SNF1/AMPK pathways in yeast. Front Biosci 13:2408–2420PubMedPubMedCentralCrossRefGoogle Scholar
  45. Helander JDM, Vaidya AS, Cutler SR (2016) Chemical manipulation of plant water use. Bioorg Med Chem 24:493–500PubMedCrossRefGoogle Scholar
  46. Hilhorst HWM, Karssen CM (1992) Seed dormancy and germination: the role of abscisic acid and gibberellins and the importance of hormone mutants. Plant Growth Regul 11:225–238CrossRefGoogle Scholar
  47. Hrabak EM, Chan CWM, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu J-K, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680PubMedPubMedCentralCrossRefGoogle Scholar
  48. Ito T, Kondoh Y, Yoshida K, Umezawa T, Shimizu T, Shinozaki K, Osada H (2015) Novel Abscisic acid antagonists identified with chemical Array screening. Chembiochem 16:2471–2478PubMedCrossRefGoogle Scholar
  49. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333PubMedCrossRefGoogle Scholar
  50. Iyer LM, Koonin EV, Aravind L (2001) Adaptations of the helix-grip fold for ligand binding and catalysis in the START domain superfamily. Proteins 43:134–144PubMedCrossRefGoogle Scholar
  51. Jones AM, Danielson JA, Manojkumar SN, Lanquar V, Grossmann G, Frommer WB (2014) Abscisic acid dynamics in roots detected with genetically encoded FRET sensors. elife 3:e01741PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kerk D, Bulgrien J, Smith DW, Barsam B, Veretnik S, Gribskov M (2002) The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiol 129:908–925PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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
  54. Kitahata N, Han S-Y, Noji N, Saito T, Kobayashi M, Nakano T, Kuchitsu K, Shinozaki K, Yoshida S, Matsumoto S, Tsujimoto M, Asami T (2006) A 9-cis-epoxycarotenoid dioxygenase inhibitor for use in the elucidation of abscisic acid action mechanisms. Bioorg Med Chem 14:5555–5561PubMedCrossRefGoogle Scholar
  55. Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant 61:377–383CrossRefGoogle Scholar
  56. Kulik A, Wawer I, Krzywińska E, Bucholc M, Dobrowolska G (2011) SnRK2 protein kinases—key regulators of plant response to abiotic stresses. OMICS 15:859–872PubMedPubMedCentralCrossRefGoogle Scholar
  57. 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 23:1647–1656PubMedPubMedCentralCrossRefGoogle Scholar
  58. Leube MP, Grill E, Amrhein N (1998) ABI1 of Arabidopsis is a protein serine/threonine phosphatase highly regulated by the proton and magnesium ion concentration. FEBS Lett 424:100–104PubMedCrossRefGoogle Scholar
  59. Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264:1448–1452PubMedCrossRefGoogle Scholar
  60. Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9:759–771PubMedPubMedCentralCrossRefGoogle Scholar
  61. Li J, Assmann SM (1996) An Abscisic acid-activated and calcium-independent protein kinase from guard cells of fava bean. Plant Cell 8:2359–2368PubMedPubMedCentralCrossRefGoogle Scholar
  62. Li J, Wang XQ, Watson MB, Assmann SM (2000) Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287:300–303PubMedCrossRefGoogle Scholar
  63. Li W, Wang L, Sheng X, Yan C, Zhou R, Hang J, Yin P, Yan N (2013) Molecular basis for the selective and ABA-independent inhibition of PP2CA by PYL13. Cell Res 23:1369–1379PubMedPubMedCentralCrossRefGoogle Scholar
  64. Li J, Shi C, Sun D, He Y, Lai C, Lv P, Xiong Y, Zhang L, Wu F, Tian C (2015) The HAB1 PP2C is inhibited by ABA-dependent PYL10 interaction. Sci Rep 5:10890PubMedPubMedCentralCrossRefGoogle Scholar
  65. Liang C, Wang Y, Zhu Y, Tang J, Hu B, Liu L, Ou S, Wu H, Sun X, Chu J, Chu C (2014) OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proc Natl Acad Sci U S A 111:10013–10018PubMedPubMedCentralCrossRefGoogle Scholar
  66. Lind C, Dreyer I, López-Sanjurjo EJ, von Meyer K, Ishizaki K, Kohchi T, Lang D, Zhao Y, Kreuzer I, Al-Rasheid KAS, Ronne H, Reski R, Zhu J-K, Geiger D, Hedrich R (2015) Stomatal guard cells co-opted an ancient ABA-dependent desiccation survival system to regulate stomatal closure. Curr Biol.  https://doi.org/10.1016/j.cub.2015.01.067
  67. Littler DR, Walker JR, Davis T, Wybenga-Groot LE, Finerty PJ Jr, Newman E, Mackenzie F, Dhe-Paganon S (2010) A conserved mechanism of autoinhibition for the AMPK kinase domain: ATP-binding site and catalytic loop refolding as a means of regulation. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:143–151PubMedPubMedCentralCrossRefGoogle Scholar
  68. Louis-Flamberg P, Krupinski-Olsen R, Shorter AL, Kemal C (1988) Reductive inhibition of soybean Lipoxygenase-1 by NDGA a possible mechanism for regulation of Lipoxygenase Activitya. Ann N Y Acad Sci 524:382–384CrossRefGoogle Scholar
  69. Lozano-Juste J, Cutler SR (2014) Plant genome engineering in full bloom. Trends Plant Sci 19:284–287PubMedCrossRefGoogle Scholar
  70. Luan S (2003) Protein phosphatases in plants. Annu Rev Plant Biol 54:63–92PubMedCrossRefGoogle Scholar
  71. Lumba S, Toh S, Handfield L-F, Swan M, Liu R, Youn J-Y, Cutler SR, Subramaniam R, Provart N, Moses A, Desveaux D, McCourt P (2014) A mesoscale abscisic acid hormone interactome reveals a dynamic signaling landscape in Arabidopsis. Dev Cell 29:360–372PubMedCrossRefGoogle Scholar
  72. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009a) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064PubMedGoogle Scholar
  73. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009b) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064PubMedGoogle Scholar
  74. Mayak S, Halevy AH (1972) Interrelationships of ethylene and abscisic acid in the control of rose petal senescence. Plant Physiol 50:341–346PubMedPubMedCentralCrossRefGoogle Scholar
  75. McAdam SAM, Brodribb TJ, Banks JA, Hedrich R, Atallah NM, Cai C, Geringer MA, Lind C, Nichols DS, Stachowski K, Geiger D, Sussmilch FC (2016) Abscisic acid controlled sex before transpiration in vascular plants. Proc Natl Acad Sci U S A.  https://doi.org/10.1073/pnas.1606614113
  76. McAinsh MR, Brownlee C, Hetherington AM et al (1990) Abscisic acid-induced elevation of guard cell cytosolic Ca2+ precedes stomatal closure. Nature 343:186–188CrossRefGoogle Scholar
  77. Melcher K, Ng L-M, Zhou XE, Soon F-F, Xu Y, Suino-Powell KM, Park S-Y, Weiner JJ, Fujii H, Chinnusamy V, Kovach A, Li J, Wang Y, Li J, Peterson FC, Jensen DR, Yong E-L, Volkman BF, Cutler SR, Zhu J-K, Xu HE (2009) A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462:602–608PubMedPubMedCentralCrossRefGoogle Scholar
  78. Melcher K, Xu Y, Ng L-M, Zhou XE, Soon F-F, Chinnusamy V, Suino-Powell KM, Kovach A, Tham FS, Cutler SR, Li J, Yong E-L, Zhu J-K, Xu HE (2010) Identification and mechanism of ABA receptor antagonism. Nat Struct Mol Biol 17:1102–1108PubMedPubMedCentralCrossRefGoogle Scholar
  79. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedCrossRefGoogle Scholar
  80. Menges M, Hennig L, Gruissem W, Murray JAH (2002) Cell cycle-regulated gene expression in Arabidopsis. J Biol Chem 277:41987–42002PubMedCrossRefGoogle Scholar
  81. Messing SAJ, Gabelli SB, Echeverria I, Vogel JT, Guan JC, Tan BC, Klee HJ, McCarty DR, Mario Amzel L (2010) Structural insights into maize viviparous14, a key enzyme in the biosynthesis of the phytohormone abscisic acid.  https://doi.org/10.1105/tpc.110.074815
  82. Meyer K, Leube MP, Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264:1452–1455PubMedCrossRefGoogle Scholar
  83. Milborrow BV (1974) The chemistry and physiology of Abscisic acid. Annu Rev Plant Physiol 25:259–307CrossRefGoogle Scholar
  84. Miyazono K-I, Miyakawa T, Sawano Y, Kubota K, Kang H-J, Asano A, Miyauchi Y, Takahashi M, Zhi Y, Fujita Y, Yoshida T, Kodaira K-S, Yamaguchi-Shinozaki K, Tanokura M (2009) Structural basis of abscisic acid signalling. Nature 462:609–614PubMedCrossRefGoogle Scholar
  85. Mosquna A, Peterson FC, Park S-Y, Lozano-Juste J, Volkman BF, Cutler SR (2011) Potent and selective activation of abscisic acid receptors in vivo by mutational stabilization of their agonist-bound conformation. Proc Natl Acad Sci U S A 108:20838–20843PubMedPubMedCentralCrossRefGoogle Scholar
  86. Mustilli A-C, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099PubMedPubMedCentralCrossRefGoogle Scholar
  87. Nakagawa M, Kagiyama M, Shibata N, Hirano Y, Hakoshima T (2014) Mechanism of high-affinity abscisic acid binding to PYL9/RCAR1. Genes Cells 19:386–404PubMedCrossRefGoogle Scholar
  88. Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363PubMedCrossRefGoogle Scholar
  89. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185PubMedCrossRefGoogle Scholar
  90. Ng L-M, Soon F-F, Zhou XE, West GM, Kovach A, Suino-Powell KM, Chalmers MJ, Li J, Yong E-L, Zhu J-K, Griffin PR, Melcher K, Xu HE (2011) Structural basis for basal activity and autoactivation of abscisic acid (ABA) signaling SnRK2 kinases. Proc Natl Acad Sci U S A 108:21259–21264PubMedPubMedCentralCrossRefGoogle Scholar
  91. Nishimura N, Yoshida T, Kitahata N, Asami T, Shinozaki K, Hirayama T (2007) ABA-hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed. Plant J 50:935–949PubMedCrossRefGoogle Scholar
  92. Nishimura N, Hitomi K, Arvai AS, Rambo RP, Hitomi C, Cutler SR, Schroeder JI, Getzoff ED (2009) Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science 326:1373–1379PubMedPubMedCentralCrossRefGoogle Scholar
  93. Nyangulu JM, Nelson KM, Rose PA, Gai Y, Loewen M, Lougheed B, Wilson Quail J, Cutler AJ, Abrams SR (2006) Synthesis and biological activity of tetralone abscisic acid analogues. Org Biomol Chem 4:1400–1412PubMedCrossRefGoogle Scholar
  94. Ofek P, Ben-Meir D, Kariv-Inbal Z, Oren M, Lavi S (2003) Cell cycle regulation and p53 activation by protein phosphatase 2Cα. J Biol Chem 278:14299–14305PubMedCrossRefGoogle Scholar
  95. Okamoto M, Peterson FC, Defries A, Park S-Y, Endo A, Nambara E, Volkman BF, Cutler SR (2013) Activation of dimeric ABA receptors elicits guard cell closure, ABA-regulated gene expression, and drought tolerance. Proc Natl Acad Sci U S A 110:12132–12137PubMedPubMedCentralCrossRefGoogle Scholar
  96. 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, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071PubMedPubMedCentralGoogle Scholar
  97. Park S-Y, Peterson FC, Mosquna A, Yao J, Volkman BF, Cutler SR (2015) Agrochemical control of plant water use using engineered abscisic acid receptors. Nature 520:545–548PubMedCrossRefGoogle Scholar
  98. Pearce LR, Komander D, Alessi DR (2010) The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 11:9–22PubMedCrossRefGoogle Scholar
  99. Penfield S, Gilday AD, Halliday KJ, Graham IA (2006) DELLA-mediated cotyledon expansion breaks coat-imposed seed dormancy. Curr Biol 16:2366–2370PubMedCrossRefGoogle Scholar
  100. Peterson FC, Burgie ES, Park S-Y, Jensen DR, Weiner JJ, Bingman CA, Chang C-EA, Cutler SR, Phillips GN Jr, Volkman BF (2010) Structural basis for selective activation of ABA receptors. Nat Struct Mol Biol 17:1109–1113PubMedPubMedCentralCrossRefGoogle Scholar
  101. Provart NJ, Alonso J, Assmann SM, Bergmann D, Brady SM, Brkljacic J, Browse J, Chapple C, Colot V, Cutler S, Dangl J, Ehrhardt D, Friesner JD, Frommer WB, Grotewold E, Meyerowitz E, Nemhauser J, Nordborg M, Pikaard C, Shanklin J, Somerville C, Stitt M, Torii KU, Waese J, Wagner D, McCourt P (2015) 50 years of Arabidopsis research: highlights and future directions. New Phytol.  https://doi.org/10.1111/nph.13687
  102. Qin X, Zeevaart JA (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci U S A 96:15354–15361PubMedPubMedCentralCrossRefGoogle Scholar
  103. Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401PubMedCrossRefGoogle Scholar
  104. Rajagopalan N, Nelson KM, Douglas AF, Jheengut V, Alarcon IQ, McKenna SA, Surpin M, Loewen MC, Abrams SR (2016) Abscisic acid analogues that act as universal or selective antagonists of Phytohormone receptors. Biochemistry 55:5155–5164PubMedCrossRefGoogle Scholar
  105. Reinoso H, Travaglia C, Bottini R (2011) ABA Increased Soybean Yield by Enhancing Production of Carbohydrates and Their Allocation in Seed. Soybean–Biochemistry, Chemistry and Physiology InTech, Rijeka, pp 577–598Google Scholar
  106. Robaglia C, Thomas M, Meyer C (2012) Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr Opin Plant Biol 15:301–307PubMedCrossRefGoogle Scholar
  107. Robert N, Merlot S, N’Guyen V, Boisson-Dernier A, Schroeder JI (2006) A hypermorphic mutation in the protein phosphatase 2C HAB1 strongly affects ABA signaling in Arabidopsis. FEBS Lett 580:4691–4696PubMedCrossRefGoogle Scholar
  108. Rodriguez PL, Leube MP, Grill E (1998a) Molecular cloning in Arabidopsis thaliana of a new protein phosphatase 2C (PP2C) with homology to ABI1 and ABI2. Plant Mol Biol 38:879–883PubMedCrossRefGoogle Scholar
  109. Rodriguez PL, Benning G, Grill E (1998b) ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett 421:185–190PubMedCrossRefGoogle Scholar
  110. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709PubMedCrossRefGoogle Scholar
  111. Rubio S, Rodrigues A, Saez A, Dizon MB, Galle A, Kim T-H, Santiago J, Flexas J, Schroeder JI, Rodriguez PL (2009) Triple loss of function of protein phosphatases type 2C leads to partial constitutive response to endogenous abscisic acid. Plant Physiol 150:1345–1355PubMedPubMedCentralCrossRefGoogle Scholar
  112. Saab IN, Sharp RE, Pritchard J, Voetberg GS (1990) Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiol 93:1329–1336PubMedPubMedCentralCrossRefGoogle Scholar
  113. Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O, Rodriguez PL (2004) Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J 37:354–369PubMedCrossRefGoogle Scholar
  114. Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park S-Y, Márquez JA, Cutler SR, Rodriguez PL (2009a) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade a PP2Cs. Plant J 60:575–588PubMedCrossRefGoogle Scholar
  115. Santiago J, Dupeux F, Round A, Antoni R, Park S-Y, Jamin M, Cutler SR, Rodriguez PL, Márquez JA (2009b) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462:665–668PubMedCrossRefGoogle Scholar
  116. Schmidt H, Kurtzer R, Eisenreich W, Schwab W (2006) The Carotenase AtCCD1 from Arabidopsis thaliana is a Dioxygenase. J Biol Chem 281:9845–9851PubMedCrossRefGoogle Scholar
  117. Schwartz SH, Zeevaart JAD (2010) Abscisic acid biosynthesis and metabolism. In: Davies PJ (ed) Plant hormones. Springer, Dordrecht, pp 137–155CrossRefGoogle Scholar
  118. Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874PubMedCrossRefGoogle Scholar
  119. Schweighofer A, Hirt H, Meskiene I (2004) Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci 9:236–243PubMedCrossRefGoogle Scholar
  120. Seo M (2014) ABA transmembrane transport and transporters. In: Zhang D-P (ed) Abscisic acid: metabolism, transport and signaling. Springer, Dordrecht, pp 47–59Google Scholar
  121. Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55:2343–2351PubMedCrossRefGoogle Scholar
  122. Shimizu T, Rådmark O, Samuelsson B (1984) Enzyme with dual lipoxygenase activities catalyzes leukotriene A4 synthesis from arachidonic acid. Proc Natl Acad Sci U S A 81:689–693PubMedPubMedCentralCrossRefGoogle Scholar
  123. Soon F-F, Ng L-M, Zhou XE, West GM, Kovach A, Tan MHE, Suino-Powell KM, He Y, Xu Y, Chalmers MJ, Brunzelle JS, Zhang H, Yang H, Jiang H, Li J, Yong E-L, Cutler S, Zhu J-K, Griffin PR, Melcher K, Xu HE (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335:85–88PubMedCrossRefGoogle Scholar
  124. Sussmilch FC, Brodribb TJ, McAdam SAM (2017) What are the evolutionary origins of stomatal responses to abscisic acid in land plants? J Integr Plant Biol 59:240–260PubMedCrossRefGoogle Scholar
  125. Takahashi S, Oritani T, Yamashita K (1986) Synthesis and biological activities of (±)-Deoxy-abscisic acid isomers. Agric Biol Chem 50:3205–3206Google Scholar
  126. Takeuchi J, Okamoto M, Akiyama T, Muto T, Yajima S, Sue M, Seo M, Kanno Y, Kamo T, Endo A, Nambara E, Hirai N, Ohnishi T, Cutler SR, Todoroki Y (2014) Designed abscisic acid analogs as antagonists of PYL-PP2C receptor interactions. Nat Chem Biol 10:477–482PubMedCrossRefGoogle Scholar
  127. Takeuchi J, Ohnishi T, Okamoto M, Todoroki Y (2015a) The selectivity of 6-nor-ABA and 7′-nor-ABA for abscisic acid receptor subtypes. Bioorg Med Chem Lett 25:3507–3510PubMedCrossRefGoogle Scholar
  128. Takeuchi J, Ohnishi T, Okamoto M, Todoroki Y (2015b) Conformationally restricted 3′-modified ABA analogs for controlling ABA receptors. Org Biomol Chem 13:4278–4288PubMedCrossRefGoogle Scholar
  129. Tan B-C, Joseph LM, Deng W-T, Liu L, Li Q-B, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56PubMedCrossRefGoogle Scholar
  130. Todoroki Y, Hirai N, Koshimizu K (1995) 8′,8′-Difluoro- and 8′,8′,8′-trifluoroabscisic acids as highly potent, long-lasting analogues of abscisic acid. Phytochemistry 38:561–568CrossRefGoogle Scholar
  131. Todoroki Y, Tanaka T, Kisamori M, Hirai N (2001) 3′-Azidoabscisic acid as a photoaffinity reagent for abscisic acid binding proteins. Bioorg Med Chem Lett 11:2381–2384PubMedCrossRefGoogle Scholar
  132. Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14:310–317PubMedCrossRefGoogle Scholar
  133. Travaglia C, Reinoso H, Cohen A, Luna C, Tommasino E, Castillo C, Bottini R (2010) Exogenous ABA increases yield in field-grown wheat with moderate water restriction. J Plant Growth Regul 29:366–374CrossRefGoogle Scholar
  134. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010a) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839PubMedPubMedCentralCrossRefGoogle Scholar
  135. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010b) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839PubMedPubMedCentralCrossRefGoogle Scholar
  136. Van Overtveldt M, TSA H, Verstraeten I, Geelen D, Stevens CV (2015) Phosphonamide pyrabactin analogues as abscisic acid agonists. Org Biomol Chem 13:5260–5264PubMedCrossRefGoogle Scholar
  137. Waadt R, Hitomi K, Nishimura N, Hitomi C, Adams SR, Getzoff ED, Schroeder JI (2014) FRET-based reporters for the direct visualization of abscisic acid concentration changes and distribution in Arabidopsis. elife 3:e01739PubMedPubMedCentralCrossRefGoogle Scholar
  138. Wang Y, Ying J, Kuzma M, Chalifoux M, Sample A, McArthur C, Uchacz T, Sarvas C, Wan J, Dennis DT, McCourt P, Huang Y (2005) Molecular tailoring of farnesylation for plant drought tolerance and yield protection. Plant J 43:413–424PubMedCrossRefGoogle Scholar
  139. Wang P, Xue L, Batelli G, Lee S, Hou Y-J, Van Oosten MJ, Zhang H, Tao WA, Zhu J-K (2013) Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc Natl Acad Sci U S A 110:11205–11210PubMedPubMedCentralCrossRefGoogle Scholar
  140. Watts S, Rodriguez JL, Evans SE, Davies WJ (1981) Root and shoot growth of plants treated with Abscisic acid. Ann Bot 47:595–602CrossRefGoogle Scholar
  141. Weiner JJ, Peterson FC, Volkman BF, Cutler SR (2010) Structural and functional insights into core ABA signaling. Curr Opin Plant Biol 13:495–502PubMedPubMedCentralCrossRefGoogle Scholar
  142. Weng J-K, Ye M, Li B, Noel JP (2016) Co-evolution of hormone metabolism and signaling networks expands plant adaptive plasticity. Cell 166:881–893PubMedCrossRefGoogle Scholar
  143. Wenjian L, Xiaoqiang H, Yumei X, Jinlong F, Yuanzhi Z, Huizhe L, Mingan W, Zhaohai Q (2013) Synthesis, photostability and bioactivity of 2,3-cyclopropanated abscisic acid. Phytochemistry 96:72–80PubMedCrossRefGoogle Scholar
  144. Whitman S, Gezginci M, Timmermann BN, Holman TR (2002) Structure−activity relationship studies of Nordihydroguaiaretic acid inhibitors toward soybean, 12-human, and 15-human Lipoxygenase. J Med Chem 45:2659–2661PubMedCrossRefGoogle Scholar
  145. Xu Z-J, Nakajima M, Suzuki Y, Yamaguchi I (2002) Cloning and characterization of the abscisic acid-specific glucosyltransferase gene from adzuki bean seedlings. Plant Physiol 129:1285–1295PubMedPubMedCentralCrossRefGoogle Scholar
  146. Yang Y, Costa A, Leonhardt N, Siegel RS, Schroeder JI (2008) Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods 4:6PubMedPubMedCentralCrossRefGoogle Scholar
  147. Yang J, Worley E, Udvardi M (2014) A NAP-AAO3 regulatory module promotes chlorophyll degradation via ABA biosynthesis in Arabidopsis leaves. Plant Cell.  https://doi.org/10.1105/tpc.114.133769
  148. Yin P, Fan H, Hao Q, Yuan X, Wu D, Pang Y, Yan C, Li W, Wang J, Yan N (2009) Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nat Struct Mol Biol 16:1230–1236PubMedCrossRefGoogle Scholar
  149. Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T, Shinozaki K, Hirayama T (2006a) ABA-hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol 140:115–126PubMedPubMedCentralCrossRefGoogle Scholar
  150. Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K (2006b) The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J Biol Chem 281:5310–5318PubMedCrossRefGoogle Scholar
  151. Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K (2006c) The regulatory domain of SRK2E/OST1/SnRK2. 6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J Biol Chem 281:5310–5318PubMedCrossRefGoogle Scholar
  152. Yuan X, Yin P, Hao Q, Yan C, Wang J, Yan N (2010) Single amino acid alteration between valine and isoleucine determines the distinct pyrabactin selectivity by PYL1 and PYL2. J Biol Chem 285:28953–28958PubMedPubMedCentralCrossRefGoogle Scholar
  153. Yuan F, Yang H, Xue Y, Kong D, Ye R, Li C, Zhang J, Theprungsirikul L, Shrift T, Krichilsky B, Johnson DM, Swift GB, He Y, Siedow JN, Pei Z-M (2014) OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514:367–371PubMedCrossRefGoogle Scholar
  154. Zhang X, Zhang Q, Xin Q, Yu L, Wang Z, Wu W, Jiang L, Wang G, Tian W, Deng Z, Wang Y, Liu Z, Long J, Gong Z, Chen Z (2012) Complex structures of the abscisic acid receptor PYL3/RCAR13 reveal a unique regulatory mechanism. Structure 20:780–790PubMedCrossRefGoogle Scholar
  155. Zhang X, Jiang L, Wang G, Yu L, Zhang Q, Xin Q, Wu W, Gong Z, Chen Z (2013) Structural insights into the abscisic acid stereospecificity by the ABA receptors PYR/PYL/RCAR. PLoS One 8:e67477PubMedPubMedCentralCrossRefGoogle Scholar
  156. Zhang X, Zhang X, Liu X, Shao L, Sun H, Chen S (2016) Improving winter wheat performance by foliar spray of ABA and FA under water deficit conditions. J Plant Growth Regul 35:83–96CrossRefGoogle Scholar
  157. Zhao Y, Xing L, Wang X, Hou Y-J, Gao J, Wang P, Duan C-G, Zhu X, Zhu J-K (2014) The ABA receptor PYL8 promotes lateral root growth by enhancing MYB77-dependent transcription of auxin-responsive genes. Sci Signal 7:ra53PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute for Integrative Genome Biology, Center for Plant Cell Biology, and Department of Botany and Plant SciencesUniversity of CaliforniaRiversideUSA

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