Photosynthesis-dependent/independent control of stomatal responses to CO<inf>2</inf> in mutant barley with surplus electron transport capacity and reduced SLAH3 anion channel transcript

Córdoba Jacoste, Francisco Javier; Molina-Cano, J.-L.; Pérez, P.; Morcuende, R.; Moralejo, M.; Savé, R.; Martínez-Carrasco, R.

doi:10.1016/j.plantsci.2015.07.011

Article (Scientific journals)

Photosynthesis-dependent/independent control of stomatal responses to CO2 in mutant barley with surplus electron transport capacity and reduced SLAH3 anion channel transcript

Córdoba Jacoste, Francisco Javier; Molina-Cano, J.-L.; Pérez, P. et al.

2015 • In Plant Science, 239, p. 15-25

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/219539

DOI
10.1016/j.plantsci.2015.07.011

PubMed
26398787

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Keywords :

CO2; Photosynthetic electron transport; Signalling; SLAH3; Stomatal conductance; Hordeum; Hordeum vulgare; Carbon Dioxide; Electron Transport; Gene Expression Regulation, Plant; Light; Mutation; Photosynthesis; Plant Leaves; Plant Proteins; Plant Stomata; Ribulose-Bisphosphate Carboxylase; Voltage-Dependent Anion Channels

Abstract :

[en] The mechanisms of stomatal sensitivity to CO2 are yet to be fully understood. The role of photosynthetic and non-photosynthetic factors in stomatal responses to CO2 was investigated in wild-type barley (Hordeum vulgare var. Graphic) and in a mutant (G132) with decreased photochemical and Rubisco capacities. The CO2 and DCMU responses of stomatal conductance (gs), gas exchange, chlorophyll fluorescence and levels of ATP, with a putative transcript for stomatal opening were analysed. G132 had greater gs than the wild-type, despite lower photosynthesis rates and higher intercellular CO2 concentrations (Ci). The mutant had Rubisco-limited photosynthesis at very high CO2 levels, and higher ATP contents than the wild-type. Stomatal sensitivity to CO2 under red light was lower in G132 than in the wild-type, both in photosynthesizing and DCMU-inhibited leaves. Under constant Ci and red light, stomatal sensitivity to DCMU inhibition was higher in G132. The levels of a SLAH3-like slow anion channel transcript, involved in stomatal closure, decreased sharply in G132. The results suggest that stomatal responses to CO2 depend partly on the balance of photosynthetic electron transport to carbon assimilation capacities, but are partially regulated by the CO2 signalling network. High gs can improve the adaptation to climate change in well-watered conditions. © 2015 Elsevier Ireland Ltd.

Disciplines :

Biochemistry, biophysics & molecular biology
Genetics & genetic processes
Phytobiology (plant sciences, forestry, mycology...)

Author, co-author :

Córdoba Jacoste, Francisco Javier ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues

Molina-Cano, J.-L.; IRTA (Institute for Food and Agricultural Research and Technology), Field Crops, Av. Alcalde Rovira i Roure, 191, Lérida, Spain

Pérez, P.; Institute of Natural Resources and Agrobiology of Salamanca, IRNASA-CSIC, Cordel de Merinas, 40, Salamanca, Spain

Morcuende, R.; Institute of Natural Resources and Agrobiology of Salamanca, IRNASA-CSIC, Cordel de Merinas, 40, Salamanca, Spain

Moralejo, M.; Universidad de Lleida, Av. Alcalde Rovira i Roure, 191, Lérida, Spain

Savé, R.; IRTA, Environmental Horticulture, Torre Marimon, Caldes de Montbui, Barcelona, Spain

Martínez-Carrasco, R.; Institute of Natural Resources and Agrobiology of Salamanca, IRNASA-CSIC, Cordel de Merinas, 40, Salamanca, Spain

Title :

Photosynthesis-dependent/independent control of stomatal responses to CO2 in mutant barley with surplus electron transport capacity and reduced SLAH3 anion channel transcript

Publication date :

2015

Journal title :

Plant Science

ISSN :

0168-9452

eISSN :

1873-2259

Publisher :

Elsevier Ireland Ltd

Volume :

239

Pages :

15-25

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 30 January 2018

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Bibliography

Del Pozo, A., Pérez, P., Morcuende, R., Alonso, A., Martínez-Carrasco, R., Acclimatory responses of stomatal conductance and photosynthesis to elevated CO2 and temperature in wheat crops grown at varying levels of N supply in a Mediterranean environment (2005) Plant Sci., 169, pp. 908-916
Franks, P.J., Adams, M.A., Amthor, J.S., Barbour, M.M., Berry, J.A., Ellsworth, D.S., Farquhar, G.D., von Caemmerer, S., Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century (2013) New Phytol., 197, pp. 1077-1094
Outlaw, J.W.H., Integration of cellular and physiological functions of guard cells (2003) Critic. Rev. Plant Sci., 22, pp. 503-529
Sánchez-Rodríguez, J., Pérez, P., Martínez-Carrasco, R., Photosynthesis, carbohydrate levels and chlorophyll fluorescence-estimated intercellular CO2 in water-stressed Casuarina equisetifolia Forst. &
Forst (1999) Plant Cell Environ., 22, pp. 867-873
Vahisalu, T., Kollist, H., Wang, Y.F., Nishimura, N., Chan, W.Y., Valerio, G., Lamminmaki, A., Kangasjarvi, J., SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling (2008) Nature, 452, pp. 487-491
Ainsworth, E.A., Yendrek, C.R., Sitch, S., Collins, W.J., Emberson, L.D., The effects of tropospheric ozone on net primary productivity and implications for climate change (2012) Annu. Rev. Plant Biol., 63, pp. 637-661
Merilo, E., Joesaar, I., Brosche, M., Kollist, H., To open or to close: species-specific stomatal responses to simultaneously applied opposing environmental factors (2014) New Phytol., 202, pp. 499-508
Farquhar, G., Wong, S., An empirical model of stomatal conductance (1984) Funct. Plant Biol., 11, pp. 191-210
Sharkey, T.D., Raschke, K., Separation and measurement of direct and indirect effects of light on stomata (1981) Plant Physiol., 68, pp. 33-40
Mott, K.A., Do stomata respond to CO2 concentrations other than intercellular? (1988) Plant Physiol., 86, pp. 200-203
Wong, S.C., Cowan, I.R., Farquhar, G.D., Stomatal conductance correlates with photosynthetic capacity (1979) Nature, 282, pp. 424-426
Busch, F.A., Opinion: the red-light response of stomatal movement is sensed by the redox state of the photosynthetic electron transport chain (2014) Photosynth. Res., 119, pp. 131-140
Ainsworth, E.A., Rogers, A., The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions (2007) Plant Cell Environ., 30, pp. 258-270
Messinger, S.M., Buckley, T.N., Mott, K.A., Evidence for involvement of photosynthetic processes in the stomatal response to CO2 (2006) Plant Physiol., 140, pp. 771-778
Tominaga, M., Kinoshita, T., Shimazaki, K., Guard-cell chloroplasts provide ATP required for H+ pumping in the plasma membrane and stomatal opening (2001) Plant Cell Physiol., 42, pp. 795-802
Haake, V., Zrenner, R., Sonnewald, U., Stitt, M., A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants (1998) Plant J., 14, pp. 147-157
Muschak, M., Willmitzer, L., Fisahn, J., Gas-exchange analysis of chloroplastic fructose-1,6-bisphosphatase antisense potatoes at different air humidities and at elevated CO2 (1999) Planta, 209, pp. 104-111
Price, G.D., Evans, J.R., von Caemmerer, S., Yu, J.W., Badger, M.R., Specific reduction of chloroplast glyceraldehyde-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants (1995) Planta, 195, pp. 369-378
Baroli, I., Price, G.D., Badger, M.R., von Caemmerer, S., The contribution of photosynthesis to the red light response of stomatal conductance (2008) Plant Physiol., 146, pp. 737-747
Hudson, G.S., Evans, J.R., von Caemmerer, S., Arvidsson, Y.B., Andrews, T.J., Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants (1992) Plant Physiol., 98, pp. 294-302
Quick, W.P., Schurr, U., Scheibe, R., Schulze, E.D., Rodermel, S.R., Bogorad, L., Stitt, M., Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with antisense rbcS: I. Impact on photosynthesis in ambient growth conditions (1991) Planta, 183, pp. 542-554
von Caemmerer, S., Lawson, T., Oxborough, K., Baker, N.R., Andrews, T.J., Raines, C.A., Stomatal conductance does not correlate with photosynthetic capacity in transgenic tobacco with reduced amounts of Rubisco (2004) J. Exp. Bot., 55, pp. 1157-1166
Lawson, T., Lefebvre, S., Baker, N.R., Morison, J.I., Raines, C.A., Reductions in mesophyll and guard cell photosynthesis impact on the control of stomatal responses to light and CO2 (2008) J. Exp. Bot., 59, pp. 3609-3619
Frechilla, S., Talbott, L.D., Zeiger, E., The CO2 response of Vicia guard cells acclimates to growth environment (2002) J. Exp. Bot., 53, pp. 545-550
Lodge, R.J., Dijkstra, P., Drake, B.G., Morison, J.I.L., Stomatal acclimation to increased CO2 concentration in a Florida scrub oak species Quercus myrtifolia willd (2001) Plant Cell Environ., 24, pp. 77-88
Talbott, L.D., Srivastava, A., Zeiger, E., Stomata from growth-chamber-grown Vicia faba have an enhanced sensitivity to CO2 (1996) Plant Cell Environ., 19, pp. 1188-1194
Price, G.D., vCaemmerer, S., Evans, J.R., Siebke, K., Anderson, J.M., Badger, M.R., Photosynthesis is strongly reduced by antisense suppression of chloroplastic cytochrome bf complex in transgenic tobacco (1998) Funct. Plant Biol., 25, pp. 445-452
Hu, H., Boisson-Dernier, A., Israelsson-Nordstrom, M., Bohmer, M., Xue, S., Ries, A., Godoski, J., Schroeder, J.I., Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells (2010) Nat. Cell Biol., 12, pp. 87-93
Roelfsema, M.R., Konrad, K.R., Marten, H., Psaras, G.K., Hartung, W., Hedrich, R., Guard cells in albino leaf patches do not respond to photosynthetically active radiation, but are sensitive to blue light, CO2 and abscisic acid (2006) Plant Cell Environ., 29, pp. 1595-1605
Hashimoto, M., Negi, J., Young, J., Israelsson, M., Schroeder, J.I., Iba, K., Arabidopsis HT1 kinase controls stomatal movements in response to CO2 (2006) Nat. Cell Biol., 8, pp. 391-397
Xue, S., Hu, H., Ries, A., Merilo, E., Kollist, H., Schroeder, J.I., Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO2 signal transduction in guard cell (2011) EMBO J., 30, pp. 1645-1658
Negi, J., Matsuda, O., Nagasawa, T., Oba, Y., Takahashi, H., Kawai-Yamada, M., Uchimiya, H., Iba, K., CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells (2008) Nature, 452, pp. 483-486
Merilo, E., Laanemets, K., Hu, H., Xue, S., Jakobson, L., Tulva, I., Gonzalez-Guzman, M., Kollist, H., PYR/RCAR receptors contribute to ozone-, reduced air humidity-, darkness-, and CO2-induced stomatal regulation (2013) Plant Physiol., 162, pp. 1652-1668
Geiger, D., Maierhofer, T., Al-Rasheid, K.A., Scherzer, S., Mumm, P., Liese, A., Ache, P., Hedrich, R., Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1 (2011) Sci. Signal., p. ra32
Kim, T.H., Bohmer, M., Hu, H., Nishimura, N., Schroeder, J.I., Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling (2010) Annu. Rev. Plant Biol., 61, pp. 561-591
Córdoba, J., Pérez, P., Morcuende, R., Martínez-Carrasco, R., Molina-Cano, J.L., Physiological features of a barley mutant with improved response to high CO2 (2013) XIII Congresso Luso-Espanhol de Fisiologia Vegetal. Abstract Book, p. 87. , Sociedade Portuguesa de Fisiologia Vegetal, Oeiras (Portugal), N. Vieira, N. Saibo, M.M. Oliveira (Eds.)
Zadoks, J.C., Chang, T.T., Konzak, C.F., A decimal code for the growth stages of cereals (1974) Weed Res., 14, pp. 415-421
Perez, P., Rabnecz, G., Laufer, Z., Gutierrez, D., Tuba, Z., Martinez-Carrasco, R., Restoration of photosystem II photochemistry and carbon assimilation and related changes in chlorophyll and protein contents during the rehydration of desiccated Xerophyta scabrida leaves (2011) J. Exp. Bot., 62, pp. 895-905
Long, S.P., Bernacchi, C.J., Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error (2003) J. Exp. Bot., 54, pp. 2393-2401
Farquhar, G.D., von Caemmerer, S., Berry, J.A., A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species (1980) Planta, 149, pp. 78-90
Gu, L., Pallardy, S.G., Tu, K., Law, B.E., Wullschleger, S.D., Reliable estimation of biochemical parameters from C3 leaf photosynthesis-intercellular carbon dioxide response curves (2010) Plant Cell Environ., 33, pp. 1852-1874
Mott, K.A., Opinion: stomatal responses to light and CO2 depend on the mesophyll (2009) Plant Cell Environ., 32, pp. 1479-1486
Lowry, O.H., Passonneau, J.V., Chapter 9-a collection of metabolite assays (1972) A Flexible System of Enzymatic Analysis, pp. 146-218. , Academic Press, O.H.L.V. Passonneau (Ed.)
Benson, D.A., Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., Sayers, E.W., GenBank (2015) Nucleic Acids Res., 43, pp. D30-35
Close, T.J., Bhat, P.R., Lonardi, S., Wu, Y., Rostoks, N., Ramsay, L., Druka, A., Waugh, R., Development and implementation of high-throughput SNP genotyping in barley (2009) BMC Genomics, 10, p. 582
Lohse, M., Nagel, A., Herter, T., May, P., Schroda, M., Zrenner, R., Tohge, T., Usadel, B., Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data (2014) Plant Cell Environ., 37, pp. 1250-1258
Morcuende, R., Krapp, A., Hurry, V., Stitt, M., Sucrose-feeding leads to increased rates of nitrate assimilation, increased rates of α-oxoglutarate synthesis, and increased synthesis of a wide spectrum of amino acids in tobacco leaves (1998) Planta, 206, pp. 394-409
Schmittgen, T.D., Livak, K.J., Analyzing real-time PCR data by the comparative C(T) method (2008) Nat. Protoc., 3, pp. 1101-1108
Benjamini, Y., Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple testing (1995)
Morison, J.I.L., Stomatal response to increased CO2 concentration (1998) J. Exp. Bot., 49, pp. 443-452
Lawson, T., Blatt, M.R., Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency (2014) Plant Physiol., 164, pp. 1556-1570
Drake, P.L., Froend, R.H., Franks, P.J., Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance (2013) J. Exp. Bot., 64, pp. 495-505
Stitt, M., Lilley, R.M., Heldt, H.W., Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts (1982) Plant Physiol., 70, pp. 971-977
Buckley, T.N., Mott, K.A., Farquhar, G.D., A hydromechanical and biochemical model of stomatal conductance (2003) Plant Cell Environ., 26, pp. 1767-1785
Jarvis, A.J., Davies, W.J., The coupled response of stomatal conductance to photosynthesis and transpiration (1998) J. Exp. Bot., 49, pp. 399-406
Mott, K.A., Berg, D.G., Hunt, S.M., Peak, D., Is the signal from the mesophyll to the guard cells a vapour-phase ion? (2014) Plant Cell Environ., 37, pp. 1184-1191
Fujita, T., Noguchi, K., Terashima, I., Apoplastic mesophyll signals induce rapid stomatal responses to CO2 in Commelina communis (2013) New Phytol., 199, pp. 395-406
Mott, K.A., Sibbernsen, E.D., Shope, J.C., The role of the mesophyll in stomatal responses to light and CO2 (2008) Plant Cell Environ., 31, pp. 1299-1306
Wong, S.C., Cowan, I.R., Farquhar, G.D., Leaf conductance in relation to rate of CO2 assimilation: I. Influence of nitrogen nutrition, phosphorus nutrition, photon flux density, and ambient partial pressure of CO2 during ontogeny (1985) Plant Physiol., 78, pp. 821-825
Laanemets, K., Brandt, B., Li, J., Merilo, E., Wang, Y.F., Keshwani, M.M., Taylor, S.S., Schroeder, J.I., Calcium-dependent and -independent stomatal signaling network and compensatory feedback control of stomatal opening via Ca2+ sensitivity priming (2013) Plant Physiol., 163, pp. 504-513
Kollist, H., Nuhkat, M., Roelfsema, M.R., Closing gaps: linking elements that control stomatal movement (2014) New Phytol., 203, pp. 44-62
Laanemets, K., Wang, Y.F., Lindgren, O., Wu, J., Nishimura, N., Lee, S., Caddell, D., Kollist, H., Mutations in the SLAC1 anion channel slow stomatal opening and severely reduce K+ uptake channel activity via enhanced cytosolic [Ca2+] and increased Ca2+ sensitivity of K+ uptake channels (2013) New Phytol., 197, pp. 88-98
Wang, Y., Papanatsiou, M., Eisenach, C., Karnik, R., Williams, M., Hills, A., Lew, V.L., Blatt, M.R., Systems dynamic modeling of a guard cell Cl- channel mutant uncovers an emergent homeostatic network regulating stomatal transpiration (2012) Plant Physiol., 160, pp. 1956-1967
Wang, Y., Hills, A., Blatt, M.R., Systems analysis of guard cell membrane transport for enhanced stomatal dynamics and water use efficiency (2014) Plant Physiol., 164, pp. 1593-1599