Integration of Abscisic Acid Signaling with Other Signaling Pathways in Plant Stress Responses and Development
Abstract
:1. Introduction
2. Ubiquitination in ABA Signaling
3. ABA Signaling under Stress
3.1. Calcium Signaling Integration with ABA Signaling Pathway and Stomatal Regulation
3.2. Abiotic Stress Signaling Integration with the ABA Signaling Pathway
3.3. Biotic Stress Signaling Integration with the ABA Signaling Pathway
4. ABA Signaling in Plant Development
4.1. Role of ABA Signaling in Seed Germination and Lateral Root Formation
4.2. ABA and Light Signaling Convergence
4.3. ABA Signaling and Control of Flowering Time
5. Other Aspects of ABA Signaling
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Seo, M.; Koshiba, T. Complex regulation of ABA biosynthesis in plants. Trends Plant Sci. 2002, 7, 41–48. [Google Scholar] [CrossRef]
- Wang, D.L.; Gao, Z.Z.; Du, P.Y.; Xiao, W.; Tan, Q.P.; Chen, X.D.; Li, L.; Gao, D.S. Expression of ABA Metabolism-Related Genes Suggests Similarities and Differences Between Seed Dormancy and Bud Dormancy of Peach (Prunus persica). Front. Plant Sci. 2016, 6. [Google Scholar] [CrossRef] [PubMed]
- Chandler, P.M.; Robertson, M. Gene-Expression Regulated by Abscisic-Acid and Its Relation to Stress Tolerance. Annu. Rev. Plant Biol. 1994, 45, 113–141. [Google Scholar] [CrossRef]
- Hocking, T.J.; Hillman, J.R. Studies on the role of abscisic acid in the initiation of bud dormancy in Alnus glutinosa and Betula pubescens. Planta 1975, 125, 235–242. [Google Scholar] [CrossRef]
- Schopfer, P.; Bajracharya, D.; Plachy, C. Control of Seed-Germination by Abscisic-Acid.1. Time Course of Action in Sinapis-Alba L. Plant Physiol. 1979, 64, 822–827. [Google Scholar] [CrossRef] [Green Version]
- Hiron, R.; Wright, S. The role of endogenous abscisic acid in the response of plants to stress. J. Exp. Bot. 1973, 24, 769–780. [Google Scholar] [CrossRef]
- Ohkuma, K.; Smith, O.E.; Lyon, J.L.; Addicott, F.T. Abscisin 2, an Abscission-Accelerating Substance from Young Cotton Fruit. Science 1963, 142, 1592–1593. [Google Scholar] [CrossRef]
- Addicott, F.T.; Lyon, J.L.; Ohkuma, K.; Thiessen, W.E.; Carns, H.R.; Smith, O.E.; Cornforth, J.W.; Milborrow, B.V.; Ryback, G.; Wareing, P.F. Abscisic Acid—A New Name for Abscisin 2 (Dormin). Science 1968, 159, 1493. [Google Scholar] [CrossRef] [Green Version]
- Aharoni, N.; Benyehoshua, S.; Richmond, A.E. Effects of Water Stress on Ethylene Emanation and Endogenous Content of Abscisic-Acid and Gibberellins in Detached Lettuce Leaves (Lactuca-Sativa-L). Israel J. Bot. 1975, 24, 55. [Google Scholar]
- Davies, W.J.; Kozlowski, T.T. Effects of Applied Abscisic-Acid and Plant Water Stress on Transpiration of Woody Angiosperms. For. Sci. 1975, 21, 191–195. [Google Scholar]
- Hartung, W. Effect of Water Stress on Transport of [2-C-14]Abscisic Acid in Intact Plants of Phaseolus-Coccineus-L. Oecologia 1976, 26, 177–183. [Google Scholar] [CrossRef] [PubMed]
- Hoad, G.V. Effect of Water Stress on Abscisic-Acid Levels in White Lupin (Lupinus-Albus L) Fruit, Leaves and Phloem Exudate. Planta 1978, 142, 287–290. [Google Scholar] [CrossRef] [PubMed]
- Ismail, M.M.; Storey, J.B. Effect of Water Stress on Accumulation of Abscisic-Acid in Pecan Leaves (Carya-Illinoensis-(Wang) K-Koch). Hortscience 1978, 13, 345. [Google Scholar]
- Nordin, A. Effects of Water Stress and Abscisic-Acid on Transpiration Regulation in Wheat. Physiol. Plant. 1976, 38, 233–239. [Google Scholar] [CrossRef]
- Quarrie, S.A.; Jones, H.G. Effects of Abscisic-Acid and Water Stress on Development and Morphology of Wheat. J. Exp. Bot. 1977, 28, 192–203. [Google Scholar] [CrossRef]
- Walton, D.C.; Harrison, M.A.; Cote, P. Effects of Water Stress on Abscisic-Acid Levels and Metabolism in Roots of Phaseolus-Vulgaris-L and Other Plants. Planta 1976, 131, 141–144. [Google Scholar] [CrossRef]
- Willmer, C.M.; Don, R.; Parker, W. Levels of Short-Chain Fatty-Acids and of Abscisic-Acid in Water-Stressed and Non-Stressed Leaves and Their Effects on Stomata in Epidermal Strips and Excised Leaves. Planta 1978, 139, 281–287. [Google Scholar] [CrossRef]
- Addicott, F.T.; Lyon, J.L. Citation Classic—Physiology of Abscisic-Acid and Related Substances. Curr. Contents Agric. Biol. Environ. Sci. 1979, 18, 12. [Google Scholar]
- Pourtau, N.; Mares, M.; Purdy, S.; Quentin, N.; Ruel, A.; Wingler, A. Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence. Planta 2004, 219, 765–772. [Google Scholar] [CrossRef]
- Rivero, R.M.; Kojima, M.; Gepstein, A.; Sakakibara, H.; Mittler, R.; Gepstein, S.; Blumwald, E. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Natl. Acad. Sci. USA 2007, 104, 19631–19636. [Google Scholar] [CrossRef] [Green Version]
- Carrera, E.; Holman, T.; Medhurst, A.; Dietrich, D.; Footitt, S.; Theodoulou, F.L.; Holdsworth, M.J. Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant J. 2008, 53, 214–224. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ko, D.; Helariutta, Y. Shoot-Root Communication in Flowering Plants. Curr. Biol. 2017, 27, R973–R978. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de Torres-Zabala, M.; Truman, W.; Bennett, M.H.; Lafforgue, G.; Mansfield, J.W.; Rodriguez Egea, P.; Bogre, L.; Grant, M. Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J. 2007, 26, 1434–1443. [Google Scholar] [CrossRef] [PubMed]
- Asselbergh, B.; De Vleesschauwer, D.; Hofte, M. Global switches and fine-tuning - ABA modulates plant pathogen defense. Mol. Plant Microbe Interact. 2008, 21, 709–719. [Google Scholar] [CrossRef] [Green Version]
- Stec, N.; Banasiak, J.; Jasinski, M. Abscisic acid—An overlooked player in plant-microbe symbioses formation? Acta Biochim. Pol. 2016, 63, 53–58. [Google Scholar] [CrossRef]
- Sakthivel, P.; Sharma, N.; Klahn, P.; Gereke, M.; Bruder, D. Abscisic Acid: A Phytohormone and Mammalian Cytokine as Novel Pharmacon with Potential for Future Development into Clinical Applications. Curr. Med. Chem. 2016, 23, 1549–1570. [Google Scholar] [CrossRef]
- Spence, C.A.; Lakshmanan, V.; Donofrio, N.; Bais, H.P. Crucial Roles of Abscisic Acid Biogenesis in Virulence of Rice Blast Fungus Magnaporthe oryzae. Front. Plant Sci. 2015, 6, 1082. [Google Scholar] [CrossRef] [Green Version]
- Siewers, V.; Kokkelink, L.; Smedsgaard, J.; Tudzynski, P. Identification of an abscisic acid gene cluster in the grey mold Botrytis cinerea. Appl. Environ. Microb. 2006, 72, 4619–4626. [Google Scholar] [CrossRef] [Green Version]
- Cohen, A.C.; Bottini, R.; Piccoli, P.N. Azospirillum brasilense Sp 245 produces ABA in chemically-defined culture medium and increases ABA content in arabidopsis plants. Plant Growth Regul. 2008, 54, 97–103. [Google Scholar] [CrossRef]
- Goel, A.K.; Lundberg, D.; Torres, M.A.; Matthews, R.; Akimoto-Tomiyama, C.; Farmer, L.; Dangl, J.L.; Grant, S.R. The Pseudomonas syringae type III effector HopAM1 enhances virulence on water-stressed plants. Mol. Plant Microbe Interact. 2008, 21, 361–370. [Google Scholar] [CrossRef] [Green Version]
- Jang, J.Y.; Kim, D.G.; Kim, Y.O.; Kim, J.S.; Kang, H.S. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol. Biol. 2004, 54, 713–725. [Google Scholar] [CrossRef] [PubMed]
- Cui, J.; Li, P.; Li, G.; Xu, F.; Zhao, C.; Li, Y.H.; Yang, Z.N.; Wang, G.; Yu, Q.B.; Li, Y.X.; et al. AtPID: Arabidopsis thaliana protein interactome database—An integrative platform for plant systems biology. Nucleic Acids Res. 2008, 36, D999–D1008. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kaldenhoff, R.; Ribas-Carbo, M.; Flexas, J.; Lovisolo, C.; Heckwolf, M.; Uehlein, N. Aquaporins and plant water balance. Plant Cell Environ. 2008, 31, 658–666. [Google Scholar] [CrossRef] [PubMed]
- Finkelstein, R.R. Studies of abscisic acid perception finally flower. Plant Cell 2006, 18, 786–791. [Google Scholar] [CrossRef] [PubMed]
- Grill, E.; Christmann, A. A plant receptor with a big family. Science 2007, 315, 1676–1677. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Razem, F.A.; El-Kereamy, A.; Abrams, S.R.; Hill, R.D. The RNA-binding protein FCA is an abscisic acid receptor. Nature 2006, 439, 290–294. [Google Scholar] [CrossRef]
- Verslues, P.E.; Zhu, J.K. New developments in abscisic acid perception and metabolism. Curr. Opin. Plant Biol. 2007, 10, 447–452. [Google Scholar] [CrossRef]
- McCourt, P.; Creelman, R. The ABA receptors—We report you decide. Curr. Opin. Plant Biol. 2008, 11, 474–478. [Google Scholar] [CrossRef]
- Wang, X.F.; Zhang, D.P. Abscisic acid receptors: Multiple signal-perception sites. Ann. Bot. 2008, 101, 311–317. [Google Scholar] [CrossRef] [Green Version]
- Guo, J.J.; Yang, X.H.; Weston, D.J.; Chen, J.G. Abscisic Acid Receptors: Past, Present and Future. J. Integr. Plant Biol. 2011, 53, 469–479. [Google Scholar] [CrossRef]
- Ma, Y.; Szostkiewicz, I.; Korte, A.; Moes, D.; Yang, Y.; Christmann, A.; Grill, E. Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors. Science 2009, 324, 1064–1068. [Google Scholar] [CrossRef] [PubMed]
- Park, S.Y.; Fung, P.; Nishimura, N.; Jensen, D.R.; Fujii, H.; Zhao, Y.; Lumba, S.; Santiago, J.; Rodrigues, A.; Chow, T.F.F.; et al. Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins. Science 2009, 324, 1068–1071. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nishimura, N.; Sarkeshik, A.; Nito, K.; Park, S.Y.; Wang, A.; Carvalho, P.C.; Lee, S.; Caddell, D.F.; Cutler, S.R.; Chory, J.; et al. PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J. 2010, 61, 290–299. [Google Scholar] [CrossRef] [PubMed]
- Santiago, J.; Rodrigues, A.; Saez, A.; Rubio, S.; Antoni, R.; Dupeux, F.; Park, S.Y.; Marquez, J.A.; Cutler, S.R.; Rodriguez, P.L. Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J. 2009, 60, 575–588. [Google Scholar] [CrossRef] [PubMed]
- Pennisi, E. Breakthrough of the year: The runners-up. Science 2009, 326, 1600–1607. [Google Scholar] [CrossRef]
- Adler, E.M. 2009: Signaling breakthroughs of the year. Sci. Signal. 2010, 3, eg1. [Google Scholar] [CrossRef]
- Melcher, K.; Ng, L.M.; Zhou, X.E.; Soon, F.F.; Xu, Y.; Suino-Powell, K.M.; Park, S.Y.; Weiner, J.J.; Fujii, H.; Chinnusamy, V.; et al. A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 2009, 462, 602–608. [Google Scholar] [CrossRef] [Green Version]
- Miyazono, K.; Miyakawa, T.; Sawano, Y.; Kubota, K.; Kang, H.J.; Asano, A.; Miyauchi, Y.; Takahashi, M.; Zhi, Y.H.; Fujita, Y.; et al. Structural basis of abscisic acid signalling. Nature 2009, 462, 609–679. [Google Scholar] [CrossRef]
- Ng, L.M.; Soon, F.F.; Zhou, X.E.; West, G.M.; Kovach, A.; Suino-Powell, K.M.; Chalmers, M.J.; Li, J.; Yong, E.L.; Zhu, J.K.; et al. Structural basis for basal activity and autoactivation of abscisic acid (ABA) signaling SnRK2 kinases. Proc. Natl. Acad. Sci. USA 2011, 108, 21259–21264. [Google Scholar] [CrossRef] [Green Version]
- Yin, P.; Fan, H.; Hao, Q.; Yuan, X.Q.; Wu, D.; Pang, Y.X.; Yan, C.Y.; Li, W.Q.; Wang, J.W.; Yan, N. Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nat. Struct. Mol. Biol. 2009, 16, 1230–1242. [Google Scholar] [CrossRef]
- Soon, F.F.; Ng, L.M.; Zhou, X.E.; West, G.M.; Kovach, A.; Tan, M.H.E.; Suino-Powell, K.M.; He, Y.Z.; Xu, Y.; Chalmers, M.J.; et al. Molecular Mimicry Regulates ABA Signaling by SnRK2 Kinases and PP2C Phosphatases. Science 2012, 335, 85–88. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suzuki, M.; McCarty, D.R. Functional symmetry of the B3 network controlling seed development. Curr. Opin. Plant Biol. 2008, 11, 548–553. [Google Scholar] [CrossRef] [PubMed]
- Edel, K.H.; Kudla, J. Integration of calcium and ABA signaling. Curr. Opin. Plant Biol. 2016, 33, 83–91. [Google Scholar] [CrossRef] [PubMed]
- Sreenivasulu, N.; Harshavardhan, V.T.; Govind, G.; Seiler, C.; Kohli, A. Contrapuntal role of ABA: Does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene 2012, 506, 265–273. [Google Scholar] [CrossRef]
- Nakashima, K.; Yamaguchi-Shinozaki, K. ABA signaling in stress-response and seed development. Plant Cell Rep. 2013, 32, 959–970. [Google Scholar] [CrossRef]
- Yoshida, T.; Mogami, J.; Yamaguchi-Shinozaki, K. ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr. Opin. Plant Biol. 2014, 21, 133–139. [Google Scholar] [CrossRef]
- Liu, Y.K. Roles of mitogen-activated protein kinase cascades in ABA signaling. Plant Cell Rep. 2012, 31, 1–12. [Google Scholar] [CrossRef]
- de Zelicourt, A.; Colcombet, J.; Hirt, H. The Role of MAPK Modules and ABA during Abiotic Stress Signaling. Trends Plant Sci. 2016, 21, 677–685. [Google Scholar] [CrossRef]
- Vishwakarma, K.; Upadhyay, N.; Kumar, N.; Yadav, G.; Singh, J.; Mishra, R.K.; Kumar, V.; Verma, R.; Upadhyay, R.G.; Pandey, M.; et al. Abscisic Acid Signaling and Abiotic Stress Tolerance in Plants: A Review on Current Knowledge and Future Prospects. Front. Plant Sci. 2017, 8, 161. [Google Scholar] [CrossRef] [Green Version]
- Yu, F.; Wu, Y.; Xie, Q. Ubiquitin-Proteasome System in ABA Signaling: From Perception to Action. Mol. Plant 2016, 9, 21–33. [Google Scholar] [CrossRef] [Green Version]
- Vierstra, R.D. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. 2003, 8, 135–142. [Google Scholar] [CrossRef]
- Smalle, J.; Vierstra, R.D. The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 2004, 55, 555–590. [Google Scholar] [CrossRef]
- Bueso, E.; Rodriguez, L.; Lorenzo-Orts, L.; Gonzalez-Guzman, M.; Sayas, E.; Munoz-Bertomeu, J.; Ibanez, C.; Serrano, R.; Rodriguez, P.L. The single-subunit RING-type E3 ubiquitin ligase RSL1 targets PYL4 and PYR1 ABA receptors in plasma membrane to modulate abscisic acid signaling. Plant J. 2014, 80, 1057–1071. [Google Scholar] [CrossRef]
- Irigoyen, M.L.; Iniesto, E.; Rodriguez, L.; Puga, M.I.; Yanagawa, Y.; Pick, E.; Strickland, E.; Paz-Ares, J.; Wei, N.; De Jaeger, G.; et al. Targeted Degradation of Abscisic Acid Receptors Is Mediated by the Ubiquitin Ligase Substrate Adaptor DDA1 in Arabidopsis. Plant Cell 2014, 26, 712–728. [Google Scholar] [CrossRef] [Green Version]
- Kong, L.Y.; Cheng, J.K.; Zhu, Y.J.; Ding, Y.L.; Meng, J.J.; Chen, Z.Z.; Xie, Q.; Guo, Y.; Li, J.G.; Yang, S.H.; et al. Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases. Nat. Commun. 2015, 6, 8630. [Google Scholar] [CrossRef] [Green Version]
- Seo, J.S.; Zhao, P.Z.; Jung, C.; Chua, N.H. PLANT U-BOX PROTEIN 10 negatively regulates abscisic acid response in Arabidopsis. Appl. Biol. Chem. 2019, 62, 39. [Google Scholar] [CrossRef] [Green Version]
- Lyzenga, W.J.; Liu, H.X.; Schofield, A.; Muise-Hennessey, A.; Stone, S.L. Arabidopsis CIPK26 interacts with KEG, components of the ABA signalling network and is degraded by the ubiquitin-proteasome system. J. Exp. Bot. 2013, 64, 2779–2791. [Google Scholar] [CrossRef] [Green Version]
- Stone, S.L.; Williams, L.A.; Farmer, L.M.; Vierstra, R.D.; Callis, J. KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 2006, 18, 3415–3428. [Google Scholar] [CrossRef] [Green Version]
- Liu, H.X.; Stone, S.L. Abscisic Acid Increases Arabidopsis ABI5 Transcription Factor Levels by Promoting KEG E3 Ligase Self-Ubiquitination and Proteasomal Degradation. Plant Cell 2010, 22, 2630–2641. [Google Scholar] [CrossRef] [Green Version]
- Cheng, M.C.; Liao, P.M.; Kuo, W.W.; Lin, T.P. The Arabidopsis ETHYLENE RESPONSE FACTOR1 Regulates Abiotic Stress-Responsive Gene Expression by Binding to Different cis-Acting Elements in Response to Different Stress Signals. Plant Physiol. 2013, 162, 1566–1582. [Google Scholar] [CrossRef] [Green Version]
- Pick, E.; Lau, O.S.; Tsuge, T.; Menon, S.; Tong, Y.C.; Dohmae, N.; Plafker, S.M.; Deng, X.W.; Wei, N. Mammalian DET1 regulates Cul4A activity and forms stable complexes with E2 ubiquitin-conjugating enzymes. Mol. Cell. Biol. 2007, 27, 4708–4719. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, J.H.; Yoon, H.J.; Terzaghi, W.; Martinez, C.; Dai, M.Q.; Li, J.G.; Byun, M.O.; Deng, X.W. DWA1 and DWA2, Two Arabidopsis DWD Protein Components of CUL4-Based E3 Ligases, Act Together as Negative Regulators in ABA Signal Transduction. Plant Cell 2010, 22, 1716–1732. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seo, K.I.; Lee, J.H.; Nezames, C.D.; Zhong, S.W.; Song, E.; Byun, M.O.; Deng, X.W. ABD1 Is an Arabidopsis DCAF Substrate Receptor for CUL4-DDB1-Based E3 Ligases That Acts as a Negative Regulator of Abscisic Acid Signaling. Plant Cell 2014, 26, 695–711. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kurup, S.; Jones, H.D.; Holdsworth, M.J. Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds. Plant J. 2000, 21, 143–155. [Google Scholar] [CrossRef] [PubMed]
- Nagamune, K.; Hicks, L.M.; Fux, B.; Brossier, F.; Chini, E.N.; Sibley, L.D. Abscisic acid controls calcium-dependent egress and development in Toxoplasma gondii. Nature 2008, 451, 207–U211. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kumar, M.; Lee, S.C.; Kim, J.Y.; Kim, S.J.; Aye, S.S.; Kim, S.R. Over-expression of dehydrin gene, OsDhn1, improves drought and salt stress tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). J. Plant Biol. 2014, 57, 383–393. [Google Scholar] [CrossRef]
- Kumar, M. Crop plants and abiotic stresses. J. Biomol. Res. Ther. 2013, 3, 1000e125. [Google Scholar] [CrossRef] [Green Version]
- Kumar, M.; Kesawat, M.S. Mechanism of Salt Stress Tolerance and Pathways in Crop Plants. In Metabolic Adaptations in Plants During Abiotic Stress; CRC Press: Boca Raton, FL, USA, 2018; pp. 27–44. [Google Scholar]
- Kumar, M.; Gho, Y.S.; Jung, K.H.; Kim, S.R. Genome-Wide Identification and Analysis of Genes, Conserved between japonica and indica Rice Cultivars, that Respond to Low-Temperature Stress at the Vegetative Growth Stage. Front. Plant Sci. 2017, 8, 1120. [Google Scholar] [CrossRef] [Green Version]
- Kwak, J.M.; Mori, I.C.; Pei, Z.M.; Leonhardt, N.; Torres, M.A.; Dangl, J.L.; Bloom, R.E.; Bodde, S.; Jones, J.D.G.; Schroeder, J.I. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 2003, 22, 2623–2633. [Google Scholar] [CrossRef]
- Munemasa, S.; Muroyama, D.; Nagahashi, H.; Nakamura, Y.; Mori, I.C.; Murata, Y. Regulation of reactive oxygen species-mediated abscisic acid signaling in guard cells and drought tolerance by glutathione. Front. Plant Sci. 2013, 4, 472. [Google Scholar] [CrossRef] [Green Version]
- Mitula, F.; Tajdel, M.; Ciesla, A.; Kasprowicz-Maluski, A.; Kulik, A.; Babula-Skowronska, D.; Michalak, M.; Dobrowolska, G.; Sadowski, J.; Ludwikow, A. Arabidopsis ABA-Activated Kinase MAPKKK18 is Regulated by Protein Phosphatase 2C ABI1 and the Ubiquitin-Proteasome Pathway. Plant Cell Physiol. 2015, 56, 2351–2367. [Google Scholar] [CrossRef] [PubMed]
- Irving, H.R.; Gehring, C.A.; Parish, R.W. Changes in Cytosolic Ph and Calcium of Guard-Cells Precede Stomatal Movements. Proc. Natl. Acad. Sci. USA 1992, 89, 1790–1794. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brandt, B.; Munemasa, S.; Wang, C.; Nguyen, D.; Yong, T.M.; Yang, P.G.; Poretsky, E.; Belknap, T.F.; Waadt, R.; Aleman, F.; et al. Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. Elife 2015, 4, e03599. [Google Scholar] [CrossRef]
- Clapham, D.E. Calcium signaling. Cell 1995, 80, 259–268. [Google Scholar] [CrossRef] [Green Version]
- Clapham, D.E. Calcium signaling. Cell 2007, 131, 1047–1058. [Google Scholar] [CrossRef] [Green Version]
- Kudla, J.; Batistic, O.; Hashimoto, K. Calcium Signals: The Lead Currency of Plant Information Processing. Plant Cell 2010, 22, 541–563. [Google Scholar] [CrossRef]
- Edel, K.H.; Kudla, J. Increasing complexity and versatility: How the calcium signaling toolkit was shaped during plant land colonization. Cell Calcium 2015, 57, 231–246. [Google Scholar] [CrossRef]
- Hashimoto, K.; Kudla, J. Calcium decoding mechanisms in plants. Biochimie 2011, 93, 2054–2059. [Google Scholar] [CrossRef]
- Batistic, O.; Kudla, J. Analysis of calcium signaling pathways in plants. Biochim. Biophys. Acta Gen. Subj. 2012, 1820, 1283–1293. [Google Scholar] [CrossRef]
- Kudla, J.; Xu, Q.; Harter, K.; Gruissem, W.; Luan, S. Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc. Natl. Acad. Sci. USA 1999, 96, 4718–4723. [Google Scholar] [CrossRef] [Green Version]
- Shi, J.R.; Kim, K.N.; Ritz, O.; Albrecht, V.; Gupta, R.; Harter, K.; Luan, S.; Kudla, J. Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 1999, 11, 2393–2405. [Google Scholar] [CrossRef] [PubMed]
- Steinhorst, L.; Kudla, J. Signaling in cells and organisms—Calcium holds the line. Curr. Opin. Plant Biol. 2014, 22, 14–21. [Google Scholar] [CrossRef]
- Liese, A.; Romeis, T. Biochemical regulation of in vivo function of plant calcium-dependent protein kinases (CDPK). Biochim. Biophys. Acta Mol. Cell Res. 2013, 1833, 1582–1589. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maierhofer, T.; Diekmann, M.; Offenborn, J.N.; Lind, C.; Bauer, H.; Hashimoto, K.; Al-Rasheid, K.A.S.; Luan, S.; Kudla, J.; Geiger, D.; et al. Site- and kinase-specific phosphorylation-mediated activation of SLAC1, a guard cell anion channel stimulated by abscisic acid. Sci. Signal. 2014, 7, ra86. [Google Scholar] [CrossRef] [PubMed]
- Dubiella, U.; Seybold, H.; Durian, G.; Komander, E.; Lassig, R.; Witte, C.P.; Schulze, W.X.; Romeis, T. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc. Natl. Acad. Sci. USA 2013, 110, 8744–8749. [Google Scholar] [CrossRef] [Green Version]
- Boudsocq, M.; Sheen, J. CDPKs in immune and stress signaling. Trends Plant Sci. 2013, 18, 30–40. [Google Scholar] [CrossRef] [Green Version]
- Acharya, B.R.; Jeon, B.W.; Zhang, W.; Assmann, S.M. Open Stomata 1 (OST1) is limiting in abscisic acid responses of Arabidopsis guard cells. New Phytol. 2013, 200, 1049–1063. [Google Scholar] [CrossRef]
- Mustilli, A.C.; Merlot, S.; Vavasseur, A.; Fenzi, F.; Giraudat, J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 2002, 14, 3089–3099. [Google Scholar] [CrossRef] [Green Version]
- Yoshida, R.; Umezawa, T.; Mizoguchi, T.; Takahashi, S.; Takahashi, F.; Shinozaki, K. 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. 2006, 281, 5310–5318. [Google Scholar] [CrossRef] [Green Version]
- Fujii, H.; Chinnusamy, V.; Rodrigues, A.; Rubio, S.; Antoni, R.; Park, S.Y.; Cutler, S.R.; Sheen, J.; Rodriguez, P.L.; Zhu, J.K. In vitro reconstitution of an abscisic acid signalling pathway. Nature 2009, 462, 660–664. [Google Scholar] [CrossRef] [Green Version]
- Zhou, X.; Hao, H.; Zhang, Y.; Bai, Y.; Zhu, W.; Qin, Y.; Yuan, F.; Zhao, F.; Wang, M.; Hu, J.; et al. PKS5/CIPK11, a SnRK3-Type Protein Kinase, is Important for ABA Responses in Arabidopsis through Phosphorylation of ABI5. Plant Physiol. 2015, 114.255455. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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.; et al. Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 2007, 19, 3019–3036. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, S.C.; Lan, W.; Buchanan, B.B.; Luan, S. A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc. Natl. Acad. Sci. USA 2009, 106, 21419–21424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lan, W.Z.; Lee, S.C.; Che, Y.F.; Jiang, Y.Q.; Luan, S. Mechanistic analysis of AKT1 regulation by the CBL-CIPK-PP2CA interactions. Mol. Plant 2011, 4, 527–536. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.; Li, H.D.; Chen, L.Q.; Wang, Y.; Liu, L.L.; He, L.; Wu, W.H. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 2006, 125, 1347–1360. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cherel, I.; Michard, E.; Platet, N.; Mouline, K.; Alcon, C.; Sentenac, H.; Thibaud, J.B. Physical and functional interaction of the Arabidopsis K(+) channel AKT2 and phosphatase AtPP2CA. Plant Cell 2002, 14, 1133–1146. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Held, K.; Pascaud, F.; Eckert, C.; Gajdanowicz, P.; Hashimoto, K.; Corratge-Faillie, C.; Offenborn, J.N.; Lacombe, B.; Dreyer, I.; Thibaud, J.B.; et al. Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res 2011, 21, 1116–1130. [Google Scholar] [CrossRef] [Green Version]
- Ronzier, E.; Corratge-Faillie, C.; Sanchez, F.; Prado, K.; Briere, C.; Leonhardt, N.; Thibaud, J.B.; Xiong, T.C. CPK13, a noncanonical Ca2+-dependent protein kinase, specifically inhibits KAT2 and KAT1 shaker K+ channels and reduces stomatal opening. Plant Physiol 2014, 166, 314–326. [Google Scholar] [CrossRef] [Green Version]
- Locascio, A.; Marques, M.C.; Garcia-Martinez, G.; Corratge-Faillie, C.; Andres-Colas, N.; Rubio, L.; Fernandez, J.A.; Very, A.A.; Mulet, J.M.; Yenush, L. BCL2-ASSOCIATED ATHANOGENE4 Regulates the KAT1 Potassium Channel and Controls Stomatal Movement. Plant Physiol 2019, 181, 1277–1294. [Google Scholar] [CrossRef] [Green Version]
- Leran, S.; Edel, K.H.; Pervent, M.; Hashimoto, K.; Corratge-Faillie, C.; Offenborn, J.N.; Tillard, P.; Gojon, A.; Kudla, J.; Lacombe, B. Nitrate sensing and uptake in Arabidopsis are enhanced by ABI2, a phosphatase inactivated by the stress hormone abscisic acid. Sci. Signal 2015, 8, ra43. [Google Scholar] [CrossRef]
- Ho, C.H.; Lin, S.H.; Hu, H.C.; Tsay, Y.F. CHL1 functions as a nitrate sensor in plants. Cell 2009, 138, 1184–1194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, X.; Peng, H.; Liao, W.; Luo, A.; Cai, M.; He, J.; Zhang, X.; Luo, Z.; Jiang, H.; Xu, L. MiR-181a/b induce the growth, invasion, and metastasis of neuroblastoma cells through targeting ABI1. Mol. Carcinog. 2018, 57, 1237–1250. [Google Scholar] [CrossRef] [PubMed]
- Hedrich, R.; Geiger, D. Biology of SLAC1-type anion channels - from nutrient uptake to stomatal closure. New Phytol. 2017, 216, 46–61. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sirichandra, C.; Gu, D.; Hu, H.C.; Davanture, M.; Lee, S.; Djaoui, M.; Valot, B.; Zivy, M.; Leung, J.; Merlot, S.; et al. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. Febs Lett. 2009, 583, 2982–2986. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Drerup, M.M.; Schlucking, K.; Hashimoto, K.; Manishankar, P.; Steinhorst, L.; Kuchitsu, K.; Kudla, J. The Calcineurin B-Like Calcium Sensors CBL1 and CBL9 Together with Their Interacting Protein Kinase CIPK26 Regulate the Arabidopsis NADPH Oxidase RBOHF. Mol. Plant 2013, 6, 559–569. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zheng, X.; Kang, S.; Jing, Y.; Ren, Z.; Li, L.; Zhou, J.M.; Berkowitz, G.; Shi, J.; Fu, A.; Lan, W.; et al. Danger-Associated Peptides Close Stomata by OST1-Independent Activation of Anion Channels in Guard Cells. Plant Cell 2018, 30, 1132–1146. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Demir, F.; Horntrich, C.; Blachutzik, J.O.; Scherzer, S.; Reinders, Y.; Kierszniowska, S.; Schulze, W.X.; Harms, G.S.; Hedrich, R.; Geiger, D.; et al. Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc. Natl. Acad. Sci. USA 2013, 110, 8296–8301. [Google Scholar] [CrossRef] [Green Version]
- Geiger, D.; Maierhofer, T.; Al-Rasheid, K.A.; Scherzer, S.; Mumm, P.; Liese, A.; Ache, P.; Wellmann, C.; Marten, I.; Grill, E.; et al. Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci. Signal 2011, 4, ra32. [Google Scholar] [CrossRef]
- Lee, S.C.; Lim, C.W.; Lan, W.Z.; He, K.; Luan, S. ABA Signaling in Guard Cells Entails a Dynamic Protein-Protein Interaction Relay from the PYL-RCAR Family Receptors to Ion Channels. Mol. Plant 2013, 6, 528–538. [Google Scholar] [CrossRef] [Green Version]
- Sato, A.; Sato, Y.; Fukao, Y.; Fujiwara, M.; Umezawa, T.; Shinozaki, K.; Hibi, T.; Taniguchi, M.; Miyake, H.; Goto, D.B.; et al. Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase. Biochem. J. 2009, 424, 439–448. [Google Scholar] [CrossRef] [Green Version]
- Mori, I.C.; Murata, Y.; Yang, Y.Z.; Munemasa, S.; Wang, Y.F.; Andreoli, S.; Tiriac, H.; Alonso, J.M.; Harper, J.F.; Ecker, J.R.; et al. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol. 2006, 4, 1749–1762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Geiger, D.; Scherzer, S.; Mumm, P.; Stange, A.; Marten, I.; Bauer, H.; Ache, P.; Matschi, S.; Liese, A.; Al-Rasheid, K.A.S.; et al. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc. Natl. Acad. Sci. USA 2009, 106, 21425–21430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Geiger, D.; Scherzer, S.; Mumm, P.; Marten, I.; Ache, P.; Matschi, S.; Liese, A.; Wellmann, C.; Al-Rasheid, K.A.S.; Grill, E.; et al. Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc. Natl. Acad. Sci. USA 2010, 107, 8023–8028. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brandt, B.; Brodsky, D.E.; Xue, S.W.; Negi, J.; Iba, K.; Kangasjarvi, J.; Ghassemian, M.; Stephan, A.B.; Hu, H.H.; Schroeder, J.I. 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 2012, 109, 10593–10598. [Google Scholar] [CrossRef] [Green Version]
- Kulik, A.; Wawer, I.; Krzywinska, E.; Bucholc, M.; Dobrowolska, G. SnRK2 Protein Kinases-Key Regulators of Plant Response to Abiotic Stresses. Omics 2011, 15, 859–872. [Google Scholar] [CrossRef]
- Fujita, Y.; Fujita, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. ABA-mediated transcriptional regulation in response to osmotic stress in plants. J. Plant Res. 2011, 124, 509–525. [Google Scholar] [CrossRef]
- Tuteja, N. Abscisic Acid and abiotic stress signaling. Plant Signal. Behav. 2007, 2, 135–138. [Google Scholar] [CrossRef] [Green Version]
- Yamaguchi-Shinozaki, K.; Shinozaki, K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 2006, 57, 781–803. [Google Scholar] [CrossRef] [Green Version]
- Nakashima, K.; Ito, Y.; Yamaguchi-Shinozaki, K. Transcriptional Regulatory Networks in Response to Abiotic Stresses in Arabidopsis and Grasses. Plant Physiol. 2009, 149, 88–95. [Google Scholar] [CrossRef] [Green Version]
- Maruyama, K.; Todaka, D.; Mizoi, J.; Yoshida, T.; Kidokoro, S.; Matsukura, S.; Takasaki, H.; Sakurai, T.; Yamamoto, Y.Y.; Yoshiwara, K.; et al. Identification of Cis-Acting Promoter Elements in Cold- and Dehydration-Induced Transcriptional Pathways in Arabidopsis, Rice, and Soybean. DNA Res. 2012, 19, 37–49. [Google Scholar] [CrossRef]
- Nakabayashi, K.; Okamoto, M.; Koshiba, T.; Kamiya, Y.; Nambara, E. Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: Epigenetic and genetic regulation of transcription in seed. Plant J. 2005, 41, 697–709. [Google Scholar] [CrossRef] [PubMed]
- Fujita, Y.; Fujita, M.; Satoh, R.; Maruyama, K.; Parvez, M.M.; Seki, M.; Hiratsu, K.; Ohme-Takagi, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 2005, 17, 3470–3488. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kang, J.Y.; Choi, H.I.; Im, M.Y.; Kim, S.Y. Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 2002, 14, 343–357. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.; Kang, J.Y.; Cho, D.I.; Park, J.H.; Kim, S.Y. ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J. 2004, 40, 75–87. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, T.; Fujita, Y.; Sayama, H.; Kidokoro, S.; Maruyama, K.; Mizoi, J.; Shinozaki, K.; Yamaguchi-Shinozaki, K. 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. 2010, 61, 672–685. [Google Scholar] [CrossRef] [PubMed]
- Zhang, D.W.; Ye, H.X.; Guo, H.Q.; Johnson, A.; Zhang, M.S.; Lin, H.H.; Yin, Y.H. Transcription factor HAT1 is phosphorylated by BIN2 kinase and mediates brassinosteroid repressed gene expression in Arabidopsis. Plant J. 2014, 77, 59–70. [Google Scholar] [CrossRef] [PubMed]
- Tan, W.R.; Zhang, D.W.; Zhou, H.P.; Zheng, T.; Yin, Y.H.; Lin, H.H. Transcription factor HAT1 is a substrate of SnRK2.3 kinase and negatively regulates ABA synthesis and signaling in Arabidopsis responding to drought. PLoS Genet. 2018, 14, e1007336. [Google Scholar] [CrossRef] [Green Version]
- Danquah, A.; de Zelicourt, A.; Colcombet, J.; Hirt, H. The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol. Adv. 2014, 32, 40–52. [Google Scholar] [CrossRef]
- Knetsch, M.L.W.; Wang, M.; SnaarJagalska, B.E.; HeimovaaraDijkstra, S. Abscisic acid induces mitogen-activated protein kinase activation in barley aleurone protoplasts. Plant Cell 1996, 8, 1061–1067. [Google Scholar] [CrossRef] [Green Version]
- Brock, A.K.; Willmann, R.; Kolb, D.; Grefen, L.; Lajunen, H.M.; Bethke, G.; Lee, J.; Nurnberger, T.; Gust, A.A. The Arabidopsis Mitogen-Activated Protein Kinase Phosphatase PP2C5 Affects Seed Germination, Stomatal Aperture, and Abscisic Acid-Inducible Gene Expression. Plant Physiol. 2010, 153, 1098–1111. [Google Scholar] [CrossRef] [Green Version]
- Xing, Y.; Jia, W.S.; Zhangl, J.H. AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J. 2008, 54, 440–451. [Google Scholar] [CrossRef] [PubMed]
- Jammes, F.; Song, C.; Shin, D.J.; Munemasa, S.; Takeda, K.; Gu, D.; Cho, D.; Lee, S.; Giordo, R.; Sritubtim, S.; et al. MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc. Natl. Acad. Sci. USA 2009, 106, 20520–20525. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Umezawa, T.; Sugiyama, N.; Takahashi, F.; Anderson, J.C.; Ishihama, Y.; Peck, S.C.; Shinozaki, K. Genetics and Phosphoproteomics Reveal a Protein Phosphorylation Network in the Abscisic Acid Signaling Pathway in Arabidopsis thaliana. Sci. Signal. 2013, 6, rs8. [Google Scholar] [CrossRef] [PubMed]
- Ortiz-Masia, D.; Perez-Amador, M.A.; Carbonell, J.; Marcote, M.J. Diverse stress signals activate the C1 subgroup MAP kinases of Arabidopsis. Febs Lett. 2007, 581, 1834–1840. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Danquah, A.; de Zelicourt, A.; Boudsocq, M.; Neubauer, J.; Frey, N.F.D.; Leonhardt, N.; Pateyron, S.; Gwinner, F.; Tamby, J.P.; Ortiz-Masia, D.; et al. Identification and characterization of an ABA-activated MAP kinase cascade in Arabidopsis thaliana. Plant J. 2015, 82, 232–244. [Google Scholar] [CrossRef]
- Matsuoka, D.; Yasufuku, T.; Furuya, T.; Nanmori, T. An abscisic acid inducible Arabidopsis MAPKKK, MAPKKK18 regulates leaf senescence via its kinase activity. Plant Mol. Biol. 2015, 87, 565–575. [Google Scholar] [CrossRef]
- Boudsocq, M.; Danquah, A.; de Zelicourt, A.; Hirt, H.; Colcombet, J. Plant MAPK cascades: Just rapid signaling modules? Plant Signal. Behav. 2015, 10, e1062197. [Google Scholar] [CrossRef] [Green Version]
- Mauch-Mani, B.; Mauch, F. The role of abscisic acid in plant-pathogen interactions. Curr. Opin. Plant Biol. 2005, 8, 409–414. [Google Scholar] [CrossRef]
- Ku, Y.S.; Sintaha, M.; Cheung, M.Y.; Lam, H.M. Plant Hormone Signaling Crosstalks between Biotic and Abiotic Stress Responses. Int. J. Mol. Sci. 2018, 19, 3206. [Google Scholar] [CrossRef] [Green Version]
- Yang, J.; Duan, G.H.; Li, C.Q.; Liu, L.; Han, G.Y.; Zhang, Y.L.; Wang, C.M. The Crosstalks Between Jasmonic Acid and Other Plant Hormone Signaling Highlight the Involvement of Jasmonic Acid as a Core Component in Plant Response to Biotic and Abiotic Stresses. Front. Plant Sci. 2019, 10, 1349. [Google Scholar] [CrossRef] [Green Version]
- Kusajima, M.; Yasuda, M.; Kawashima, A.; Nojiri, H.; Yamane, H.; Nakajima, M.; Akutsu, K.; Nakashita, H. Suppressive effect of abscisic acid on systemic acquired resistance in tobacco plants. J. Gen. Plant Pathol. 2010, 76, 161–167. [Google Scholar] [CrossRef]
- Xia, X.J.; Wang, Y.J.; Zhou, Y.H.; Tao, Y.; Mao, W.H.; Shi, K.; Asami, T.; Chen, Z.X.; Yu, J.Q. Reactive Oxygen Species Are Involved in Brassinosteroid- Induced Stress Tolerance in Cucumber. Plant Physiol. 2009, 150, 801–814. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Melotto, M.; Underwood, W.; Koczan, J.; Nomura, K.; He, S.Y. Plant stomata function in innate immunity against bacterial invasion. Cell 2006, 126, 969–980. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Conrath, U.; Pieterse, C.M.J.; Mauch-Mani, B. Priming in plant-pathogen interactions. Trends Plant Sci. 2002, 7, 210–216. [Google Scholar] [CrossRef] [Green Version]
- Jakab, G.; Ton, J.; Flors, V.; Zimmerli, L.; Metraux, J.P.; Mauch-Mani, B. Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol. 2005, 139, 267–274. [Google Scholar] [CrossRef] [Green Version]
- Yao, L.M.; Zhong, Y.P.; Wang, B.; Yan, J.H.; Wu, T.L. BABA application improves soybean resistance to aphid through activation of phenylpropanoid metabolism and callose deposition. Pest Manag. Sci. 2019, 76, 384–394. [Google Scholar] [CrossRef]
- Tworkoski, T.; Wisniewski, M.; Artlip, T. Application of BABA and s-ABA for drought resistance in apple. J. Appl. Hortic. 2011, 13, 85–90. [Google Scholar]
- Ton, J.; Jakab, G.; Toquin, V.; Flors, V.; Iavicoli, A.; Maeder, M.N.; Metraux, J.P.; Mauch-Mani, B. Dissecting the beta-aminobutyric acid-induced priming phenomenon in arabidopsis. Plant Cell 2005, 17, 987–999. [Google Scholar] [CrossRef] [Green Version]
- Thevenet, D.; Pastor, V.; Baccelli, I.; Balmer, A.; Vallat, A.; Neier, R.; Glauser, G.; Mauch-Mani, B. The priming molecule beta-aminobutyric acid is naturally present in plants and is induced by stress. New Phytol. 2017, 213, 552–559. [Google Scholar] [CrossRef]
- Chini, A.; Grant, J.J.; Seki, M.; Shinozaki, K.; Loake, G.J. Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J. 2004, 38, 810–822. [Google Scholar] [CrossRef]
- Jagodzik, P.; Tajdel-Zielinska, M.; Ciesla, A.; Marczak, M.; Ludwikow, A. Mitogen-Activated Protein Kinase Cascades in Plant Hormone Signaling. Front. Plant Sci. 2018, 9, 1387. [Google Scholar] [CrossRef] [PubMed]
- Kumar, M.; Choi, J.; An, G.; Kim, S.R. Ectopic Expression of OsSta2 Enhances Salt Stress Tolerance in Rice. Front. Plant Sci. 2017, 8, 316. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dubois, M.; Skirycz, A.; Claeys, H.; Maleux, K.; Dhondt, S.; De Bodt, S.; Vanden Bossche, R.; De Milde, L.; Yoshizumi, T.; Matsui, M.; et al. ETHYLENE RESPONSE FACTOR6 Acts as a Central Regulator of Leaf Growth under Water-Limiting Conditions in Arabidopsis. Plant Physiol. 2013, 162, 319–332. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seo, Y.J.; Park, J.B.; Cho, Y.J.; Jung, C.; Seo, H.S.; Park, S.K.; Nahm, B.H.; Song, J.T. Overexpression of the Ethylene-Responsive Factor Gene BrERF4 from Brassica rapa Increases Tolerance to Salt and Drought in Arabidopsis Plants. Mol. Cells 2010, 30, 271–277. [Google Scholar] [CrossRef] [PubMed]
- Sewelam, N.; Kazan, K.; Thomas-Hall, S.R.; Kidd, B.N.; Manners, J.M.; Schenk, P.M. Ethylene Response Factor 6 Is a Regulator of Reactive Oxygen Species Signaling in Arabidopsis. PLoS ONE 2013, 8, e70289. [Google Scholar] [CrossRef] [Green Version]
- Park, J.M.; Park, C.J.; Lee, S.B.; Ham, B.K.; Shin, R.; Paek, K.H. Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-Type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 2001, 13, 1035–1046. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.; Huang, Z.J.; Chen, Q.; Zhang, Z.J.; Zhang, H.B.; Wu, Y.M.; Huang, D.F.; Huang, R.F. Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance. Plant Mol. Biol. 2004, 55, 183–192. [Google Scholar] [CrossRef]
- Zhang, G.Y.; Chen, M.; Li, L.C.; Xu, Z.S.; Chen, X.P.; Guo, J.M.; Ma, Y.Z. Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J. Exp. Bot. 2009, 60, 3781–3796. [Google Scholar] [CrossRef] [Green Version]
- Zhai, Y.; Wang, Y.; Li, Y.J.; Lei, T.T.; Yan, F.; Su, L.T.; Li, X.W.; Zhao, Y.; Sun, X.; Li, J.W.; et al. Isolation and molecular characterization of GmERF7, a soybean ethylene-response factor that increases salt stress tolerance in tobacco. Gene 2013, 513, 174–183. [Google Scholar] [CrossRef]
- Finkelstein, R.R.; Gampala, S.S.L.; Rock, C.D. Abscisic acid signaling in seeds and seedlings. Plant Cell 2002, 14, S15–S45. [Google Scholar] [CrossRef] [Green Version]
- Luerssen, K.; Kirik, V.; Herrmann, P.; Misera, S. FUSCA3 encodes a protein with a conserved VP1/ABI3-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J. 1998, 15, 755–764. [Google Scholar] [CrossRef]
- Stone, S.L.; Kwong, L.W.; Yee, K.M.; Pelletier, J.; Lepiniec, L.; Fischer, R.L.; Goldberg, R.B.; Harada, J.J. Leafy Cotyledon2 encodes a B3 domain transcription factor that induces embryo development. Proc. Natl. Acad. Sci. USA 2001, 98, 11806–11811. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brocard-Gifford, I.M.; Lynch, T.J.; Finkelstein, R.R. Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signaling. Plant Physiol. 2003, 131, 78–92. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bensmihen, S.; Rippa, S.; Lambert, G.; Jublot, D.; Pautot, V.; Granier, F.; Giraudat, J.; Parcy, F. The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 2002, 14, 1391–1403. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bensmihen, S.; Giraudat, J.; Parcy, F. Characterization of three homologous basic leucine zipper transcription factors (bZIP) of the ABI5 family during Arabidopsis thaliana embryo maturation. J. Exp. Bot. 2005, 56, 597–603. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lopez-Molina, L.; Mongrand, S.; Chua, N.H. A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the AB15 transcription factor in Arabidopsis. Proc. Natl. Acad. Sci. USA 2001, 98, 4782–4787. [Google Scholar] [CrossRef] [Green Version]
- Dekkers, B.J.W.; He, H.Z.; Hanson, J.; Willems, L.A.J.; Jamar, D.C.L.; Cueff, G.; Rajjou, L.; Hilhorst, H.W.M.; Bentsink, L. The Arabidopsis Delay of Germination 1 gene affects ABSCISIC ACID Insensitive 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development. Plant J. 2016, 85, 451–465. [Google Scholar] [CrossRef]
- Kanai, M.; Nishimura, M.; Hayashi, M. A peroxisomal ABC transporter promotes seed germination by inducing pectin degradation under the control of ABI5. Plant J. 2010, 62, 936–947. [Google Scholar] [CrossRef]
- Skubacz, A.; Daszkowska-Golec, A.; Szarejko, L. The Role and Regulation of ABI5 (ABA-Insensitive 5) in Plant Development, Abiotic Stress Responses and Phytohormone Crosstalk. Front. Plant Sci. 2016, 7, 1884. [Google Scholar] [CrossRef] [Green Version]
- Seo, P.J.; Xiang, F.N.; Qiao, M.; Park, J.Y.; Lee, Y.N.; Kim, S.G.; Lee, Y.H.; Park, W.J.; Park, C.M. The MYB96 Transcription Factor Mediates Abscisic Acid Signaling during Drought Stress Response in Arabidopsis. Plant Physiol. 2009, 151, 275–289. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.H.; Hyun, W.Y.; Nguyen, H.N.; Jeong, C.Y.; Xiong, L.; Hong, S.W.; Lee, H. AtMyb7, a subgroup 4 R2R3 Myb, negatively regulates ABA-induced inhibition of seed germination by blocking the expression of the bZIP transcription factor ABI5. Plant Cell Environ. 2015, 38, 559–571. [Google Scholar] [CrossRef] [PubMed]
- Duan, L.N.; Dietrich, D.; Ng, C.H.; Chan, P.M.Y.; Bhalerao, R.; Bennett, M.J.; Dinneny, J.R. Endodermal ABA Signaling Promotes Lateral Root Quiescence during Salt Stress in Arabidopsis Seedlings. Plant Cell 2013, 25, 324–341. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Achard, P.; Cheng, H.; De Grauwe, L.; Decat, J.; Schoutteten, H.; Moritz, T.; Van Der Straeten, D.; Peng, J.R.; Harberd, N.P. Integration of plant responses to environmentally activated phytohormonal signals. Science 2006, 311, 91–94. [Google Scholar] [CrossRef] [PubMed]
- Casal, J.J.; Fankhauser, C.; Coupland, G.; Blazquez, M.A. Signalling for developmental plasticity. Trends Plant Sci. 2004, 9, 309–314. [Google Scholar] [CrossRef]
- Piskurewicz, U.; Jikumaru, Y.; Kinoshita, N.; Nambara, E.; Kamiya, Y.; Lopez-Molina, L. The Gibberellic Acid Signaling Repressor RGL2 Inhibits Arabidopsis Seed Germination by Stimulating Abscisic Acid Synthesis and ABI5 Activity. Plant Cell 2008, 20, 2729–2745. [Google Scholar] [CrossRef] [Green Version]
- Tang, W.J.; Ji, Q.; Huang, Y.P.; Jiang, Z.M.; Bao, M.Z.; Wang, H.Y.; Lin, R.C. Far-Red Elongated hypocotyl3 and far-red impaired response1 Transcription Factors Integrate Light and Abscisic Acid Signaling in Arabidopsis. Plant Physiol. 2013, 163, 857–866. [Google Scholar] [CrossRef] [Green Version]
- Oh, E.; Kang, H.; Yamaguchi, S.; Park, J.; Lee, D.; Kamiya, Y.; Choi, G. Genome-Wide Analysis of Genes Targeted by Phytochrome Interacting Factor 3-LIKE5 during Seed Germination in Arabidopsis. Plant Cell 2009, 21, 403–419. [Google Scholar] [CrossRef] [Green Version]
- Xu, D.Q.; Li, J.G.; Gangappa, S.N.; Hettiarachchi, C.; Lin, F.; Andersson, M.X.; Jiang, Y.; Deng, X.W.; Holm, M. Convergence of Light and ABA Signaling on the ABI5 Promoter. PLoS Genet. 2014, 10, e1004197. [Google Scholar] [CrossRef]
- Rock, C.D. Pathways to abscisic acid-regulated gene expression. New Phytol. 2000, 148, 357–396. [Google Scholar] [CrossRef]
- Martínez-Zapater, J.M.; Coupland, G.; Dean, C.; Koornneef, M. 16 The Transition to Flowering in Arabidopsis. Cold Spring Harb. Monogr. Arch. 1994, 27, 403–433. [Google Scholar]
- Michaels, S.D.; Amasino, R.M. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 1999, 11, 949–956. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chiang, G.C.K.; Barua, D.; Kramer, E.M.; Amasino, R.M.; Donohue, K. Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2009, 106, 11661–11666. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Choi, H.I.; Hong, J.H.; Ha, J.O.; Kang, J.Y.; Kim, S.Y. ABFs, A family of ABA-responsive element binding factors. J. Biol. Chem. 2000, 275, 1723–1730. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jakoby, M.; Weisshaar, B.; Droge-Laser, W.; Vicente-Carbajosa, J.; Tiedemann, J.; Kroj, T.; Parcy, F.; Grp, B.R. BZIP transcription factors in Arabidopsis. Trends Plant Sci. 2002, 7, 106–111. [Google Scholar] [CrossRef]
- Abe, M.; Kobayashi, Y.; Yamamoto, S.; Daimon, Y.; Yamaguchi, A.; Ikeda, Y.; Ichinoki, H.; Notaguchi, M.; Goto, K.; Araki, T. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 2005, 309, 1052–1056. [Google Scholar] [CrossRef]
- Wang, Y.P.; Li, L.; Ye, T.T.; Lu, Y.M.; Chen, X.; Wu, Y. The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. J. Exp. Bot. 2013, 64, 675–684. [Google Scholar] [CrossRef]
- Xiong, F.; Ren, J.J.; Yu, Q.; Wang, Y.Y.; Lu, C.C.; Kong, L.J.; Otegui, M.S.; Wang, X.L. AtU2AF65b functions in abscisic acid mediated flowering via regulating the precursor messenger RNA splicing of ABI5 and FLC in Arabidopsis. New Phytol. 2019, 223, 277–292. [Google Scholar] [CrossRef]
- Kang, J.; Hwang, J.U.; Lee, M.; Kim, Y.Y.; Assmann, S.M.; Martinoia, E.; Lee, Y. PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc. Natl. Acad. Sci. USA 2010, 107, 2355–2360. [Google Scholar] [CrossRef] [Green Version]
- Kang, J.; Yim, S.; Choi, H.; Kim, A.; Lee, K.P.; Lopez-Molina, L.; Martinoia, E.; Lee, Y. Abscisic acid transporters cooperate to control seed germination. Nat. Commun. 2015, 6, 8113. [Google Scholar] [CrossRef] [Green Version]
- Kuromori, T.; Miyaji, T.; Yabuuchi, H.; Shimizu, H.; Sugimoto, E.; Kamiya, A.; Moriyama, Y.; Shinozaki, K. ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc. Natl. Acad. Sci. USA 2010, 107, 2361–2366. [Google Scholar] [CrossRef] [Green Version]
- Kanno, Y.; Hanada, A.; Chiba, Y.; Ichikawa, T.; Nakazawa, M.; Matsui, M.; Koshiba, T.; Kamiya, Y.; Seo, M. Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proc. Natl. Acad. Sci. USA 2012, 109, 9653–9658. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ge, K.; Liu, X.; Li, X.Y.; Hu, B.; Li, L. Isolation of an ABA Transporter-Like 1 Gene from Arachis hypogaea That Affects ABA Import and Reduces ABA Sensitivity in Arabidopsis. Front. Plant Sci. 2017, 8, 1150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pawela, A.; Banasiak, J.; Biala, W.; Martinoia, E.; Jasinski, M. MtABCG20 is an ABA exporter influencing root morphology and seed germination of Medicago truncatula. Plant J. 2019, 98, 511–523. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kumar, M.; Kim, I.; Kim, Y.K.; Heo, J.B.; Suh, M.C.; Kim, H.U. Strigolactone Signaling Genes Showing Differential Expression Patterns in Arabidopsis max Mutants. Plants 2019, 8, 352. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lopez-Raez, J.A.; Kohlen, W.; Charnikhova, T.; Mulder, P.; Undas, A.K.; Sergeant, M.J.; Verstappen, F.; Bugg, T.D.H.; Thompson, A.J.; Ruyter-Spira, C.; et al. Does abscisic acid affect strigolactone biosynthesis? New Phytol. 2010, 187, 343–354. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, X.Z.; Hou, L.Y.; Meng, J.J.; You, H.W.; Li, Z.; Gong, Z.Z.; Yang, S.H.; Shi, Y.T. The Antagonistic Action of Abscisic Acid and Cytokinin Signaling Mediates Drought Stress Response in Arabidopsis. Mol. Plant 2018, 11, 970–982. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Waters, M.T.; Smith, S.M. Karrikin-KAI2 signalling provides Arabidopsis seeds with tolerance to abiotic stress and inhibits germination under conditions unfavourable to seedling establishment. New Phytol. 2018, 219, 605–618. [Google Scholar] [CrossRef] [Green Version]
- Kumar, M.; Le, D.T.; Hwang, S.; Seo, P.J.; Kim, H.U. Role of the Indeterminate Domain Genes in Plants. Int. J. Mol. Sci. 2019, 20, 2286. [Google Scholar] [CrossRef] [Green Version]
- Daviere, J.M.; Achard, P. A Pivotal Role of DELLAs in Regulating Multiple Hormone Signals. Mol. Plant 2016, 9, 10–20. [Google Scholar] [CrossRef] [Green Version]
Gene Name | Accession Number | Main Function | Regulated by Ca2+-Dependent ABA Signaling | Regulated by Ca2+-Independent ABA Signaling | Reference |
---|---|---|---|---|---|
ABI5 | AT2G36270 | bZIP TF | CIPK11/26, activates by phosphorylation | SnRK2s’ phosphorylation activation; PP2Cs’ dephosphorylated inactivation | [67,101,102] |
ABF1/4 | AT1G49720/ AT3G19290 | bZIP TF | CPK4/11, activates by phosphorylation | SnRK2s’ phosphorylation activation; PP2Cs’ dephosphorylated inactivation | [101,103] |
AKT1 | AT2G26650 | Potassium ion channel | CBL1/9/CIPK23, activates by phosphorylation | HAI2 and PP2CA, regulate AKT1 | [104,105,106] |
AKT2 | AT4G22200 | Potassium ion channel | CBL4/CIPK6, localized in the plasma membrane | PP2CA, regulates AKT2 | [107,108] |
KAT1 | AT5G46240 | Potassium channel | Inhibited by the SnRK2s and involved in the stomatal closure | Inhibition by SnRK2s is inhibited by ABI1, involved in the stomatal opening | [109,110] |
NPF6.3 | AT1G12110 | Nitrate transporter | CBL1/9CIPK23, deactivates under high nitrate conditions and increases the nitrate sensitivity | ABI2 involved in the dephosphorylation or deactivation of CBL1/CIPK23 | [111,112] |
SLAC1 | AT1G12480 | Plasma membrane anion channel | Induced by the SnRK2s and involved in stomatal closure | Induction by SnRK2s is inhibited byABI1, involved in the stomatal opening | [113,114] |
RBOHF | AT1G64060 | Plasma membrane superoxide generation | CBL1/9/IPK26, activates by phosphorylation | OST1 involved in phosphorylation | [115,116] |
RBOHD | AT5G47910 | Plasma membrane superoxide generation | CPK5, activates by phosphorylation | - | [96] |
SnRK2.6/OST1 | AT4G33950 | Calcium-independent ABA-activated protein kinase | CBL/CIPL/CDPK, activates by phosphorylation | SnRK2.6 involved in phosphorylation | [112,117] |
SLAH3 | AT5G24030 | Anion channel | CBL1/9/CIPK23 | ABI1 involved in deactivation | [95,118,119] |
CPK21 involved in phosphorylated activation; CPK21 also recruits SLAH3 onto the membrane |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kumar, M.; Kesawat, M.S.; Ali, A.; Lee, S.-C.; Gill, S.S.; Kim, H.U. Integration of Abscisic Acid Signaling with Other Signaling Pathways in Plant Stress Responses and Development. Plants 2019, 8, 592. https://doi.org/10.3390/plants8120592
Kumar M, Kesawat MS, Ali A, Lee S-C, Gill SS, Kim HU. Integration of Abscisic Acid Signaling with Other Signaling Pathways in Plant Stress Responses and Development. Plants. 2019; 8(12):592. https://doi.org/10.3390/plants8120592
Chicago/Turabian StyleKumar, Manu, Mahipal Singh Kesawat, Asjad Ali, Sang-Choon Lee, Sarvajeet Singh Gill, and Hyun Uk Kim. 2019. "Integration of Abscisic Acid Signaling with Other Signaling Pathways in Plant Stress Responses and Development" Plants 8, no. 12: 592. https://doi.org/10.3390/plants8120592