Papel del calcio en la apertura y el cierre estomático y sus interacciones con solutos compatibles. Una revisión
Abstract
Los canales transportan el Ca, pero es este el que está involucrado en la transducción de señales. Su apertura resulta en una disminución de la concentración de calcio citoplasmático lo cual genera variaciones espaciales y temporales de este elemento dentro de la célula, y puede llegar a causar diversas respuestas fisiológicas a diferentes estímulos bióticos y abióticos. Los canales de calcio permeables se han reportado en la membrana plasmática, tonoplasto, retículo endoplasmático, cloroplastos y las membranas nucleares de las células vegetales. El cierre de los estomas en presencia del ácido abscísico (ABA) y las actividades de los canales de calcio durante la respuesta al estrés, generan importancia a las variaciones del calcio, pues en las células guarda, las oscilaciones de Ca²+ regulan la apertura de los estomas. La sequía es uno de los mayores problemas de estrés en la agricultura. Las plantas sintetizan principalmente la hormona del estrés ABA en respuesta a la sequía, lo que provoca una cascada de señalización en las células guarda que se traduce en el cierre de los estomas, y reduce la pérdida de agua que puede influir en el uso eficiente del agua (EUA) en las plantas. Este cierre estomático involucra una relación entre el Ca²+ y el óxido nítrico ya que son intermediarios en la transducción de señales de ABA por efecto de la luz en la apertura estomática, pues es conocido que el ABA puede provocar una elevación de la concentración de Ca²+ citosólico de las células guarda, lo que ocasiona el cierre de estomas y la disminución en el proceso fotosintético.
Palabras clave adicionales: células guarda, ácido abscísico, canales de calcio, vacuola, estrés
Author Biography
Andrea Johana Reyes
Administrativo Profesional
Oficina Educación Virtual
References
- Allen, G.J., S.P. Chu, C.L. Harrington, K. Schumacher, T. Hoffman, Y. Tang, E. Grill y J. Schroeder, J.I. 2001. A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411, 1053-1057.
- Assmann, S.M. 1993. Signal transduction in guard cells. Annu. Rev. Cell Biol. 9, 345-375.
- Assmann, S.M. y K. Shimazaki. 1999. The multisensory guard cell. Stomatal responses to blue light and abscisic acid. Plant Physiol. 119, 809-816.
- Assmann, S.M. y X.Q. Wang. 2001. From milliseconds to millions of years: guard cells and environmental responses. Curr. Opin. Plant Biol. 4(5), 421-428.
- Cvetkovska, M., C. Rampitsch, N. Bykova y T. Xing. 2005. Genomic analysis of MAP kinase cascades in Arabidopsis defense responses. Plant Mol. Biol. Rep. 23(4), 331-343.
- Cosgrove, D.J. y R. Hedrich. 1991. Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L. Planta 186(1), 143-153.
- Covington, M.F. y S.L. Harmer. 2007. The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS Biol. 5(8), 1773-1784.
- Desikan, R., R. Graffiths, J. Hancock y S. Neill. 2002. A new role for an old enzyme: nitrate reductasemediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 99(25), 16314- 16318.
- Desikan, R., M.K. Cheung, J. Bright, D. Henson, J.T Hancock y S. Neill. 2004. ABA, hydrogen peroxide and nitric oxide signaling in stomatal guard cells. J. Exp. Bot. 55(395), 205-212.
- Evans, N.H., M.R. McAinsh y A.M. Hetherington. 2001. Calcium oscillations in higher plants. Curr. Opin. Plant Biol. 4(5), 415-420.
- García-Mata, C. y L. Lamattina. 2001. Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol. 126(3), 1196-1204.
- García-Mata, C. y L. Lamattina. 2002. Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol. 128(3), 790-792.
- García-Mata, C. y L. Lamattina. 2007. Abscisic acid (ABA) inhibits light-induced stomatal opening through calcium- and nitric oxide-mediated signaling pathways. Nitric Oxide 17(3-4), 143-151.
- García-Mata, C., R. Gay, S. Sokolovski, A. Hills, L. Lamattina y M. Blatt. 2003. Nitric oxide regulates K+and Cl- channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc. Natl. Acad. Sci. USA. 100(19), 11116-11121.
- Gelli, A. y E. Blumwald. 1997. Hyperpolarization-activated Ca2+-permeable channels in the plasma membrane of tomato cells. J. Membr. Biol. 155(1), 35-45.
- Grabov, A. y M.R. Blatt. 1998. Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proc. Natl. Acad. Sci. USA 95, 4778-4783.
- Guo, X.L., Y.Y. Ma, Z.H. Liu y B.H. Liu. 2008. Effects of exterior abscisic acid on calcium distribution of mesophyll cells and calcium concentration of guard cells in maize seedlings. Agr. Sci. China 7(4), 438-446.
- Hancock, J.T., S.J. Neill e I.D. Wilson. 2011. Nitric oxide and ABA in the control of plant function. Plant Sci. 181, 555-559.
- Hetherington, A.M. 2001. Guard cell signaling. Cell 107(6), 711-714.
- Hetherington, A.M. e I. Woodward. 2003. The role of stomata in sensing and driving environmental change. Nature 424, 901-908.
- Jammes, F.J., H. Heng-Cheng, F. Villiers, R. Bouten y J. Kwak. 2011. Calcium-permeable channels in plant cells. MiniReview. FEBS Journal, 4262-4276.
- Köhler, B., A. Hills y M.R. Blatt. 2003. Control of guard cell ion channels by hydrogen peroxide and abscisic acid indicates their action through alternate signaling pathways. Plant Physiol. 131, 385-388.
- Lee, D., D.H. Polisensky y J. Braam. 2005. Genome-wide identification of touch-and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. New Phytol. 165(2), 429-444.
- Lee, J.S. 2010. Stomatal opening mechanism of CAM plants. J. Plant Biol. 53, 19-23.
- Li, Y., G.X. Wang, M. Xin, H.M. Yang, X.J. Wu y T. Li. 2004. The parameters of guard cell calcium oscillation encodes stomatal oscillation and closure in Vicia faba. Plant Sci. 166(2), 415- 421.
- Lisjak, M., N. Srivastava, T. Teklic, L. Civale, K. Lewandowski, I. Wilson, M.E. Wood, M. Whiteman y J.T. Hancock. 2010. A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol. Biochem. 48, 931-935.
- Liu, Z., Z. Ma, X. Guo, H. Shao, Q. Cui y W. Song. 2010. Changes of cytosolic Ca2+ fluorescence intensity and plasma membrane calcium channels of maize root tip cells under osmotic stress. Plant Physiol. Biochem. 48, 860-865.
- Luo, X., N. Cui, Y. Zhu, L. Cao, H. Zhai, H. Cai, W. Ji, X. Wang, D. Zhu, Y. Li y X. Bai.2012. Over-expression of GsZFP1, an ABA-reponsive C2H2-type zinc finger protein lacking a QALGGH motf, reduces ABA sensitivity and drecreases stomata size. J. Plant Physiol. 169, 1192-1202.
- Maathuis, F.J., S.T. May, N.S. Graham, H.C. Bowen, T.C. Jelitto, P. Trimmer, M.J. Bennett, D. Sanders y P.J.White. 1998. Cell marking in Arabidopsis thaliana and its application to patch-clamp studies. Plant J. 15(6), 843-851.
- MacRobbie, E. 1999. Vesicle trafficking: a role in transtonoplast ion movements?. J. Exp. Bot. 50, 925- 934.
- McAinsh, M.R., C. Brownlee y A.M. Hetherington. 1997. Calcium ions as second messengers in guard cell signal transduction. Physiol. Plant. 100(1), 16- 29.
- Marhl, M., M. Perc y S. Schuster. 2006. A minimal model for decoding of time-limited Ca2+ oscillations. Biophys. Chem. 120(3), 161-167.
- Marten, H., K. Konrad, P. Dietrich, M.R. Roelfsema y R. Hedrich. 2007. Ca2+-dependent and -independent abscisic acid activation of plasma membrane anion channels in guard cells of Nicotiana tabacum. Plant Physiol. 143, 28-37.
- Miles, G.P., M.A. Samuel, A.M. Jones y B.E. Ellis. 2004. Mastoparan rapidly activates plant MAP kinase signaling independent of heterotrimeric G proteins. Plant Physiol. 134(4), 1332-1336.
- Millar, A.H., V. Mittova, G. Kiddle, J.L. Heazlewood, C.G. Bartli, F.L. Theodoulou y C.H. Foyer. 2003. Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol. 133, 443-447.
- Mori, I.C., Y. Murata, Y. Yang, S. Munemasa, Y.F. Wang, S. Andeoli, H. Tiriac, J.M. Alonso, J.F. Harper, J.R. Ecker, J.M Kwak y J. Schroeder. 2006. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+- permeable channels and stomatal closure. PLoS Biol. 4(10), 1749-1762.
- Nakashima, K. y K. Yamaguchi-Shinozaki. 2006. Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol. Plant. 126(1), 62-71
- Neill, S.J., R. Desikan, A. Clarke, R.D Hurst y J. Hancock. 2002. Hydrogen peroxide and nitric oxide as signaling molecules in plants. J. Exp. Bot. 53(372), 1237-1247.
- Neill, S.J., R. Desikan, A. Clarke y J. Hancock. 2002. Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 128(1), 13-16.
- Neill, S.J., R. Desikan y J. Hancock. 2003. Nitric oxide as a mediator of ABA signalling in stomatal guard cells. Bulg. J. Plant Physiol. Esp. 124-132.
- Neill, S.J., R. Barros, J. Bright, R. Desikan, J. Hancock, J. Harrison, P. Morris, D. Ribeiro e I. Wilson. 2008. Nitric oxide, stomatal closure, and abiotic stress. J. Exp. Bot. 59(2), 165-176.
- Niinemets, U., A. Cescatti, M. Rodeghiero y T. Tosens. 2005. Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species. Plant Cell Environ. 28(129), 1552-1566.
- Pandey, S., W. Zhang y S.M. Assmann. 2007. Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett. 581(12), 2325-2336.
- Pérez, V. 2007. Estudio de canales permeables a calcio de membranas intracelulares de células vegetales. Tesis de doctorado. Universidad de Colima, Colima, México.
- Ritte, G., J. Rosenfeld, K. Rohrig y K. Raschke. 1999. Rates of sugar uptake by guard cell protoplasts of Pisum sativum L. related to the solute requirement for stomatal opening. Plant Physiol. 121(2), 647-655.
- Roelfsema, M.R. y R. Hedrich. 2005. In the light of stomatal opening: new insights into 'the Watergate'. New Phytol. 167(3), 665-691.
- Sánchez, C., G. Fischer y D.W. Sanjuanelo. 2013. Stomatal behavior in fruits and leaves of the purple passion fruit (Passiflora edulis Sims) and fruits and cladodes of the yellow pitaya [Hylocereus megalanthus (K. Schum. ex Vaupel) Ralf Bauer]. Agron. Colomb. 31(1), 38-47.
- Schwartz, A., N. Ilan, y D.A. Grantz. 1988. Calcium efects on stomatal movement in Commelina communis L.: use of EGTA to modulate stomatal response to light, KCl and CO2. Plant Physiol. 87(3), 583-587.
- Shao, H. B., W.Y. Song y L.Y. Chu. 2008. Advances of calcium signals involved in plant anti-drought. C.R. Biol. 331(8), 587-596.
- She, X.P., X.G. Song y J.M. He. 2004. Role and relationship of nitric oxide and hydrogen peroxide in light/ dark-regulated stomatal movement in Vicia faba. Acta Bot. Sinica 46(11), 1292-1300.
- Schroeder, J., G. Allen, V. Hugouvieux, J.M. Kwak, D. Waner. 2001. Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 627-646.
- Soni, D., S. Ranjan, R. Singh, P. Khare, U. Pathre y P. Shirke. 2012. Photosynthetic characteristics and the response of stomata to enviromental determinants and ABA in Selaginella bryopteris, a resurrection spike moss species. Plant Sci. 191-192, 43-52.
- Taiz, L. y E. Zeiger. 2006. Plant physiology. 3rd ed. Sinauer Associates, Sunderland, MA.
- Taiz, L. y E. Zeiger. 1998. Plant physiology. 2nd ed. Sinauer Associates, Sunderland, MA.
- Wang, J.Y., J.N. Yu, T. Chen, Z.G. Zhang, Y.J. Hao, J.S. Zhang y S.Y. Chen. 2005. Functional analysis of a putative Ca2+ channel gene TaTPC1 from wheat. J. Exp. Bot. 56(422), 3051-3060.
- White, P.J. 2000. Calcium channels in higher plants. Biochimica et Biophysica Acta (BBA) - Biomembranes 1465(1-2), 171-189.
- White, P.J. y M.R. Broadley. 2003. Calcium in plants. Ann. Bot. 92, 487-511.
- Wu, Y. X. Liu, W. Wang, S. Zhang y B. Xu. 2012. Calcium regalates the cell to cell water flow pathway in maize roots during variable water conditions. Plant Physiol. Biochem. 58, 212-219.
- Yang, H.M., X.Y. Zhang y G.X. Wang. 2004. Cytosolic calcium oscillation signaling in guard cell. Plant Sci. 166(3), 549-556.
- Yang, T. y B. Poovaiah 2003. Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci. 8 (10), 505-512.
- Yang, H.M., X.Y. Zhang, Q.L. Tang y G.X. Wang. 2006. Extacellular calcium is involved in stomatal movement through the regulation of water channels in broda bean. Plant Growth Regul. 50(1), 79-83.
- Yang, J., I. Ordiz, J. Jaworski y R. Beachy. 2011. Induced accumulation of cuticular waxes enhances drought tolerance in Arabidopsis by changes in development of stomata. Plant Physiol. Biochem. 49, 1448-1455.
- Zhang, X., A. Takemiya, T. Kinoshita y K. Shimazaki. 2007. Nitric oxide inhibits blue light-specific stomatal opening via abscisic acid signaling pathways in Vicia guard cells. Plant Cell Physiol. 48(5), 715- 723.
- Zhao, X., X. Qiao, J. Yuan, X. Ma y X. Zhang. 2012. Nitric oxide inhibits blue light-induced stomatal opening by regulating the K+ influx in guard cells. Plant Sci. 184, 29-35.