Relay and control of abscisic acid signaling

Current Opinion in Plant Biology

Volumn 6, Issue 5, 2003, Pages 470-479

  Himmelbach, Axel ^a   Yang, Yi ^a   Grill, Erwin ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0141502032     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5266(03)00090-6     Document Type: Review

References (74)

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15. 2+ channel in isolated membrane patches is regulated by ABA. ABA-induced shifts in the voltage-sensitivity of the channels are dependent on phosphorylation. The results support the involvement of a membrane-associated protein kinase and an ocadaic-acid-sensitive PP in ABA signaling at the plasma membrane of stomatal guard cells.
16. Kwak JM, Moon JH, Murata Y, Kuchitsu K, Leonhardt N, DeLong A, Schroeder JI: Disruption of a guard cell-expressed protein phosphatase 2A regulatory subunit, RCN1, confers abscisic acid insensitivity in Arabidopsis. Plant Cell 2002, 14:2849-2861.
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18. 2+ oscillations.
19. Sanchez JP, Chua NH: Arabidopsis PLC1 is required for secondary responses to abscisic acid signals. Plant Cell 2001, 13:1143-1154.
20. Ritchie SM, Swanson SJ, Gilroy S: From common signalling components to cell specific responses: insights from the cereal aleurone. Physiol Plant 2002, 115:342-351.
21. Hunt L, Mills LN, Pical C, Leckie CP, Aitken FL, Kopka J, Mueller-Roeber B, McAinsh MR, Hetherington AM, Gray JE: Phospholipase C is required for the control of stomatal aperture by ABA. Plant J 2003, 34:47-55. The paper supplements an elegant previous study [19] that showed that PLC activity enhances ABA responses. A reduction of guard-cell-localized PLC activity partially impaired stomatal closure that is initiated by ABA. This finding emphasizes the role of PLC in optimizing the closing response and the requirement of additional pathways for stomatal closing.
22. Burnette RN, Gunesekera BM, Gillaspy GE: An Arabidopsis inositol 5-phosphatase gain-of-function alters abscisic acid signaling. Plant Physiol 2003, 132:1011-1019. The authors established an interesting feedback loop in which ABA-mediated upregulation of inositol 5-phosphatase is able to de-phosphorylate InsPS. Transgenic plants in which the specific phosphatase is ectopically expressed had ABA-insensitive stomata, corroborating the ABA-agonistic action of InsP3.
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24. Jung JY, Kim YW, Kwak JM, Hwang JU, Young J, Schroeder JI, Hwang I, Lee Y: Phosphatidylinositol 3- and 4-phosphate are required for normal stomatal movements. Plant Cell 2002, 14:2399-2412. The authors used an original approach to examine the role of phosphatidylinositol metabolism in stomatal responses by expressing green-fluorescent fusion proteins that complex phosphatidylinositol 3- and 4-phosphate. In agreement with pharmacological data, these experiments imply that phosphatidyl-monophosphate is required for optimal ABA-induced Ca -elevations and stomatal closure.
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26. Coursol S, Fan LM, Le Stunff H, Spiegel S, Gilroy S, Assmann SM: Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 2003, 423:651-654.
27. Garcia-Mata C, Lamattina L: Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol 2002, 128:790-792. The authors of this paper and of [28•] highlight the importance of cytosolic redox shifts for ABA-signaling in guard cells. NO-release and ABA synergistically affect the stomatal response. In addition, the external administration of ABA altered the degree of fluorescence of an NO-sensitive dye that could be visualized in guard cells, indicating that ABA is involved in regulating the generation of NO.
28. Neill SJ, Desikan R, Clarke A, Hancock JT: Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 2002, 128:13-16. These authors, together with those of [27•], disclose a fascinating aspect of ABA signaling: they discover that NO is a regulator of ABA-induced stomatal closure, thereby revealing a link between ABA-mediated stress responses and pathogen defense.
29. Jiang M, Zhang J: Involvement of plasma-membrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings. Planta 2002, 215:1022-1030.
30. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI: NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 2003, 22:2623-2633.
31. Desikan R, Griffiths R, Hancock J, Neill S: A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA 2002, 99:16314-16318. These authors make a major breakthrough by clarifying the contribution and source of NO in ABA-induced stomatal closing. The guard cells of Arabidopsis double mutants that were deficient in the nitrate reductases apoproteins NIA1 and NIA2 were unresponsive to ABA and did not generate a NO signal. The abi1 and abi2 mutants generated NO but did not close their stomata, arguing that the ABI1 and ABI2 loci act downstream of NO generation in the signal pathway.
32. Chandok MR, Ytterberg AJ, van Wijk KJ, Klessig DF: The pathogen-inducible nitric oxide synthase (iNOS) in plants is a variant of the P protein of the glycine decarboxylase complex. Cell 2003, 113:469-482.
33. 2-mediated cystine formation and supports a role for the PP2Cs as redox sensors.
34. Lemichez E, Wu Y, Sanchez JP, Mettouchi A, Mathur J, Chua NH: Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev 2001, 15:1808-1816.
35. Zheng ZL, Nafisi M, Tam A, Li H, Crowell DN, Chary SN, Schroeder JI, Shen J, Yang Z: Plasma membrane-associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in Arabidopsis. Plant Cell 2002, 14:2787-2797. This milestone contribution to the field provides a crystal-clear analysis of the RHO-like small G protein ROP10 as a major regulator of ABA responses. The analysis elucidates the negative control exerted by farnesylation on ABA signaling by demonstrating the dependence of ROP10 action on a functional farnesylation site that is required for plasmalemma localization.
36. Allen GJ, Murata Y, Chu SP, Nafisi M, Schroeder JI: Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2. Plant Cell 2002, 14:1649-1662.
37. Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J: RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 2002, 296:2026-2028.
38. Yang Z: Small GTPases: versatile signaling switches in plants. Plant Cell 2002, 14(Suppl):S375-S388.
39. Zhu J, Gong Z, Zhang C, Song CP, Damsz B, Inan G, Koiwa H, Zhu JK, Hasegawa PM, Bressan RA: OSM1/SYP61: a syntaxin protein in Arabidopsis controls abscisic acid-mediated and non-abscisic acid-mediated responses to abiotic stress. Plant Cell 2002, 14:3009-3028. This contribution provides genetic evidence of the requirement of a syntaxin in ABA-induced stomatal responses and heralds the importance of vesicle transport or fusion for the closing and opening of guard cells.
40. Tahtiharju S, Palva T: Antisense inhibition of protein phosphatase 2C accelerates cold acclimation in Arabidopsis thaliana. Plant J 2001, 26:461-470.
41. Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J: The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 2001, 25:295-303.
42. 2+, and that ABI1 rescues the dominant-negative action of abi1. These findings highlight the shortcomings of mutant analyses and the pitfalls that are associated with ectopic expression studies.
43. 2+ elevation and ABI regulation by revealing the physical interaction of the protein kinase PKS3/CIPK15 and its associated CBL with ABI2, and to a lesser extent with ABI1. Genetic analysis supports a negative regulatory function of the resulting protein complex on ABA signal relay. ABA transiently downregulates the kinase activity of CIPK15, which is required to suppress ABA action.
44. Himmelbach A, Hoffmann T, Leube M, Höhener B, Grill E: Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J 2002, 21:3029-3038. This contribution represents a major breakthrough by establishing a connection between ABI1 and a nuclear-localized TF. Expression of the AtHB6 gene is upregulated in an ABA- and ABI1-dependent manner, and results in the ABA desensitization of stomates and ABA desensitization during germination. Thus, the ABI1-AtHB6 interaction defines a node between the regulation of general ABA-signaling steps by ABI1 and an AtHB6-specific response.
45. Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S: CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 2003, 15:411-423. The authors extend our understanding of the role of CIPK-CBL [43••] as negative ABA-response regulators. Genetic disruption of CIPK3 resulted in ABA-hypersensitive seed germination and gene expression in Arabidopsis.
46. Cheng SH, Willmann MR, Chen HC, Sheen J: Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 2002, 129:469-485.
47. Johnson RR, Wagner RL, Verhey SD, Walker-Simmons MK: The abscisic acid-responsive kinase PKABA1 interacts with a seed-specific abscisic acid response element-binding factor, TaABF, and phosphorylates TaABF peptide sequences. Plant Physiol 2002, 130:837-846. The authors identified TaABF, a wheat bZIP TF that is homologous to ABI5, as a binding protein and probable substrate of the ABA-regulated protein kinase PKABA1. TABF gene expression is restricted to early plant development whereas PKABA1 expression implies that this protein kinase also functions in vegetative tissues.
48. Farras R, Ferrando A, Jasik J, Kleinow T, Okresz L, Tiburcio A, Salchert K, del Pozo C, Schell J, Koncz C: SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J 2001, 20:2742-2756.
49. Li J, Kinoshita T, Pandey S, Ng CK, Gygi SP, Shimazaki K, Assmann SM: Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase. Nature 2002, 418:793-797. The discovery of the interaction of the ABA-activated protein kinase AAPK of Vicia with the heterogenous nuclear-like RNA-binding protein AKIP1 is a milestone finding in unraveling ABA-induced posttranscriptional regulation in guard-cell nuclei. Phosphorylation of AKIP1 by AAPK results in the formation of AKIP1-dehydrin mRNA complexes. Dehydrin accumulation is stimulated by ABA, hence the results indicate a role for the AKIP1-mRNA interaction in aiding the expression of dehydrin transcripts.
50. Freiman RN, Tjian R: Regulating the regulators: lysine modifications make their mark. Cell 2003, 112:11-17.
51. 2+.
52. Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K: ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 2002, 43:1473-1483. A protein kinase that is rapidly activated by ABA and low humidity was identified as SRK2E, which is identical to OST1 [51••]. The srk2e knockout line had a wilty phenotype and reduced ABA-induced gene expression, emphasizing the important dual role of OST1/SRK2E as a regulator of stomatal aperture and of ABA-controlled gene expression.
53. Hattori T, Totsuka M, Hobo T, Kagaya Y, Yamamoto-Toyoda A: Experimentally determined sequence requirement of ACGT-containing abscisic acid response element. Plant Cell Physiol 2002, 43:136-140.
54. Kizis D, Pages M: Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. Plant J 2002, 30:679-689. The authors make the important discovery of interference between DRE-binding TFs and ABA-induced gene regulation in maize. Transactivation assays defined DBF1 as an activator of ABA-induced rab17 expression, whereas DBF2 antagonized ABA action. The results highlight the existence of ABA-dependent gene regulation that involves the C-repeat/DRE element.
55. Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K: 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 2003, 34:137-148. The authors describe their in-depth analysis of a drought- and ABA-regulated promoter region. This work revealed the binding of DRE-binding TFs to DRE-similar CEs that are required for optimal ABA response. DRE-binding and ABRE-binding TFs synergistically transactivate ABA-responsive gene expression.
56. Niu X, Helentjaris T, Bate NJ: Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 2002, 14:2565-2575. PCR-based In vitro selection is used to identify the seed-specific protein ZmABI4 as a CE-specific binding protein, thereby closing a major gap in our understanding of ABA-regulated gene expression. Complementation of the Arabidopsis abi4 mutant by ZmABI4 suggests that the ABI homolog is a major player in ABA signaling during germination and in sugar sensing in maize.
57. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K: 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 2000, 97:11632-11637.
58. Kang JY, Choi HI, Im MY, Kim SY: Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 2002, 14:343-357. The authors unraveled the contribution of the ABRE-binding factors ABF3 and ABF4 as positive components of ABA signaling. The constitutive expression of ABF3 or ABF4 in Arabidopsis resulted in symptoms of ABA hypersensitivity, including reduced transpiration and enhanced drought tolerance. At the molecular level, the constitutive expression of these proteins resulted in the altered expression of ABA- and stress-regulated genes.
59. Kagaya Y, Hobo T, Murata M, Ban A, Hattori T: Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 2002, 14:3177-3189. By exploiting an elegant transient activation assay, the authors identified the specific phosphorylation site of the bZIP factor TRAB1 in rice protoplasts. Phosphorylation at this site is crucial for the ABA-mediated activation of pre-formed and nuclear TRAB1.
60. Lopez-Molina L, Mongrand S, Kinoshita N, Chua NH: AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 2003, 17:410-418. This paper is another highlight of recent work on ABA signaling. In it, the authors describe their elucidation of the role of a TF-binding protein, AFP, in controlling turnover of the ABA signal component ABI5. ABI5-binding by AFP reduced ABI5 concentrations probably through ubiquitin-dependent degradation. Hence, AFP-deficient mutants were hypersensitive to ABA's function in inhibiting post-embryonic development. AFP and ABI5 co-localized in subnuclear foci together with CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1), which is associated with the regulated degradation of transcripts by the 26S proteosome.
61. Smalle J, Kurepa J, Yang P, Emborg TJ, Babiychuk E, Kushnir S, Vierstra RD: The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specific function in abscisic acid signaling. Plant Cell 2003, 15:965-980. Genetic knockout of a 19S proteosomal component resulted in the stabilization of ABI5 and increased ABA sensitivity during germination. The pleiotropic phenotype of this knockout mutant indicates that RPN10 affects several regulatory processes, including the selective turnover of ABA-signal mediators by the 26S proteasome.
62. Lu C, Han MH, Guevara-Garcia A, Fedoroff NV: Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid. Proc Natl Acad Sci USA 2002, 99:15812-15817. Mitogen-activated protein kinase (MAPK) and MAPK kinase kinase are found to be activated by ABA, strongly reinforcing the neglected role of MAPK signaling in ABA responses. ABA-mediated ABI5 phosphorylation and AtMPK3 activation are strictly correlated. Both were increased in the pleiotropic hyl1 mutant, which is deficient in a dsRNA-binding protein that is associated with a role in RNA turnover. Ectopic expression of AtMPK3 supports a positive regulatory role for this protein kinase in the ABA-mediated inhibition of germination and seedling development.
63. Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH: ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 2002, 32:317-328.
64. Johannesson H, Wang Y, Hanson J, Engstrom P: The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Mol Biol 2003, 51:719-729.
65. Deng X, Phillips J, Meijer AH, Salamini F, Bartels D: Characterization of five novel dehydration-responsive homeodomain leucine zipper genes from the resurrection plant Craterostigma plantagineum. Plant Mol Biol 2002, 49:601-610.
66. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K: Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 2003, 15:63-78. The authors present an analysis of AtMYC2 and AtMYB2 that impressively demonstrates the complex network of ABA-regulated TFs. AtMYC2 and AtMYB2 are secondary-acting TFs that are induced by ABA and that require protein biosynthesis in order to act as transactivators of ABA- and drought-responsive target genes. Nevertheless, both of these TFs represent important positive mediators of ABA responses, as reflected by the findings that their overexpression causes increased ABA-sensitivity whereas inactivation of AtMYC2 reduced ABA responsiveness. Microarray analysis corroborated the roles of AtMYC2 and AtMYB2 in ABA-regulated gene expression.
67. Hilbricht T, Salamini F, Bartels D: CpR18, a novel SAP-domain plant transcription factor, binds to a promoter region necessary for ABA-mediated expression of the CDeT27-45 gene from the resurrection plant Craterostigma plantagineum Hochst. Plant J 2002, 31:293-303. The authors employed a yeast one-hybrid approach to identify the transcriptional regulator CDeT27-45 of Craterostigma. This TF mediates ABA-responsive gene expression via a novel cis-element and contains a scaffold attachment region contacting protein (SAP) domain that is known to interfere with scaffold-attachment regions. Hence, this analysis points to a novel facet of ABA responses that could include chromatin restructuring.
68. Kim JC, Lee SH, Cheong YH, Yoo CM, Lee SI, Chun HJ, Yun DJ, Hong JC, Lee SY, Lim CO et al.: A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. Plant J 2001, 25:247-259.
69. Koiwa H, Barb AW, Xiong L, Li F, McCully MG, Lee BH, Sokolchik I, Zhu J, Gong Z, Reddy M et al. : C-terminal domain phosphatase-like family members (AtCPLs) differentially regulate Arabidopsis thaliana abiotic stress signaling, growth, and development. Proc Natl Acad Sci USA 2002, 99:10893-10898. An eye-opening contribution that shows the signal-specific regulation of RNA polymerase II activity by AtCPL1 and AtCPL3. AtCPL3 specifically downregulates ABA-responsive gene expression, possibly by contacting the phosphorylated carboxyl terminus of the RNA polymerase.
70. Hugouvieux V, Kwak JM, Schroeder JI: An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 2001, 106:477-487.
71. Hugouvieux V, Murata Y, Young JJ, Kwak JM, Mackesy DZ, Schroeder JI: Localization, ion channel regulation, and genetic interactions during abscisic acid signaling of the nuclear mRNA cap-binding protein, ABH1. Plant Physiol 2002, 130:1276-1287. An interesting contribution that follows up on the breathtaking finding described in [70], The specific interference of the mRNA cap-binding protein with ABA-induced gene transcription is further characterized by detailed physiological, genetic and electrophysiological analyses.
72. Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK: Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 2001, 1:771-781.
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74. Freire MA, Pages M: Functional characteristics of the maize RNA-binding protein MA16. Plant Mol Biol 1995, 29:797-807.