Dynamic thermal imaging confirms local but not fast systemic ABA responses.
abscisic acid
guard cells
infrared imaging
stomata
systemic stomatal responses
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
29
08
2020
revised:
30
11
2020
accepted:
04
12
2020
pubmed:
10
12
2020
medline:
14
7
2021
entrez:
9
12
2020
Statut:
ppublish
Résumé
Abscisic acid (ABA) signals regulating stomatal aperture and water loss are usually studied in detached leaves or isolated epidermal peels and at infrequent timepoints. Measuring stomatal ABA responses in attached leaves across a time course enables the study of stomatal behaviour in the physiological context of the plant. Infrared thermal imaging is often used to characterize steady-state stomatal conductance via comparisons of leaf surface temperature but is rarely used to capture stomatal responses over time or across different leaf surfaces. We used dynamic thermal imaging as a robust, but sensitive, tool to observe stomatal ABA responses in a whole plant context. We detected stomatal responses to low levels of ABA in both monocots and dicots and identified differences between the responses of different leaves. Using whole plant thermal imaging, stomata did not always behave as described previously for detached samples: in Arabidopsis, we found no evidence for fast systemic ABA-induced stomatal closure, and in barley, we observed no requirement for exogenous nitrate during ABA-induced stomatal closure. Thus, we recommend dynamic thermal imaging as a useful approach to complement detached sample assays for the study of local and systemic stomatal responses and molecular mechanisms underlying stomatal responses to ABA in the whole plant context.
Substances chimiques
Plant Growth Regulators
0
Abscisic Acid
72S9A8J5GW
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
885-899Subventions
Organisme : Biotechnology and Biological Sciences Research Council
Pays : United Kingdom
Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Bailey, S., Walters, R. G., Jansson, S., & Horton, P. (2001). Acclimation of Arabidopsis thaliana to the light environment: The existence of separate low light and high light responses. Planta, 213, 794-801.
Bertolino, L. T., Caine, R. S., Gray, J. E. (2019). Impact of stomatal density and morphology on water-use efficiency in a changing world. Frontiers in Plant Science, 10. http://dx.doi.org/10.3389/fpls.2019.00225.
Brodribb, T. J., & McAdam, S. A. M. (2011). Passive origins of stomatal control in vascular plants. Science, 331, 582-585.
Cao, H., Bowling, S. A., Gordon, A. S., & Dong, X. (1994). Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. The Plant Cell, 6, 1583-1592.
Cao, H., Glazebrook, J., Clarke, J. D., Volko, S., & Dong, X. (1997). The Arabidopsis NPR1 Gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell, 88, 57-63.
Ceciliato, P. H. O., Zhang, J., Liu, Q., Shen, X., Hu, H., Liu, C., … Schroeder, J. I. (2019). Intact leaf gas exchange provides a robust method for measuring the kinetics of stomatal conductance responses to abscisic acid and other small molecules in Arabidopsis and grasses. Plant Methods, 15, 38.
Costa, J. M., Monnet, F., Jannaud, D., Leonhardt, N., Ksas, B., Reiter, I. M., … Genty, B. (2015). Open all night long: The dark side of stomatal control. Plant Physiology, 167, 289-294.
Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R., & Abrams, S. R. (2010). Abscisic acid: Emergence of a core signaling network. Annual Review of Plant Biology, 61, 651-679.
Dengler, N. G. (2006). The shoot apical meristem and development of vascular architecture. Canadian Journal of Botany, 84, 1660-1671.
Devireddy, A. R., Arbogast, J., & Mittler, R. (2020). Coordinated and rapid whole-plant systemic stomatal responses. New Phytologist, 225, 21-25.
Devireddy, A. R., Zandalinas, S. I., Gómez-Cadenas, A., Blumwald, E., & Mittler, R. (2018). Coordinating the overall stomatal response of plants: Rapid leaf-to-leaf communication during light stress. Science Signaling, 11, eaam9514.
Ehonen, S., Holtta, T., & Kangasjärvi, J. (2020). Systemic signaling in the regulation of stomatal conductance. Plant Physiology, 182, 1829-1832.
Farmer, E., Mousavi, S., & Lenglet, A. (2013). Leaf numbering for experiments on long distance signalling in Arabidopsis. Protocol Exchange. http://dx.doi.org/10.1038/protex.2013.071.
Frey, A., Effroy, D., Lefebvre, V., Seo, M., Perreau, F., Berger, A., … Marion-Poll, A. (2012). Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. The Plant Journal, 70, 501-512.
Fu, Z. Q., & Dong, X. (2013). Systemic acquired resistance: Turning local infection into global defense. Annual Review of Plant Biology, 64, 839-863.
Hashimoto, M., Negi, J., Young, J., Israelsson, M., Schroeder, J. I., & Iba, K. (2006). Arabidopsis HT1 kinase controls stomatal movements in response to CO2. Nature Cell Biology, 8, 391-397.
Jones, H. G. (1999). Use of thermography for quantitative studies of spatial and temporal variation of stomatal conductance over leaf surfaces. Plant, Cell & Environment, 22, 1043-1055.
Kane, C. N., Jordan, G. J., Jansen, S., & McAdam, S. A. M. (2020). A permeable cuticle, not open stomata, Is the primary source of water loss from expanding leaves. Frontiers in Plant Science, 11. http://dx.doi.org/10.3389/fpls.2020.00774.
Kang, J., Hwang, J.-U., Lee, M., Kim, Y.-Y., Assmann, S. M., Martinoia, E., & Lee, Y. (2010). PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proceedings of the National Academy of Sciences of the United States of America, 107, 2355-2360.
Kanno, Y., Hanada, A., Chiba, Y., Ichikawa, T., Nakazawa, M., Matsui, M., … Seo, M. (2012). Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proceedings of the National Academy of Sciences of the United States of America, 109, 9653-9658.
Kuhn, J. M., Boisson-Dernier, A., Dizon, M. B., Maktabi, M. H., & Schroeder, J. I. (2006). The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiology, 140, 127-139.
Kuromori, T., Miyaji, T., Yabuuchi, H., Shimizu, H., Sugimoto, E., Kamiya, A., … Shinozaki, K. (2010). ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proceedings of the National Academy of Sciences of the United States of America, 107, 2361-2366.
Kuromori, T., Sugimoto, E., & Shinozaki, K. (2011). Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. The Plant Journal, 67, 885-894.
Leymarie, J., Lascève, G., & Vavasseur, A. (1998). Interaction of stomatal responses to ABA and CO2 in Arabidopsis thaliana. Functional Plant Biology, 25, 785-791.
Leymarie, J., Vavasseur, A., & Lascève, G. (1998). CO2 sensing in stomata of abi1-1 and abi2-1 mutants of Arabidopsis thaliana. Plant Physiology and Biochemistry, 36, 539-543.
Martynenko, A., Shotton, K., Astatkie, T., Petrash, G., Fowler, C., Neily, W., & Critchley, A. T. (2016). Thermal imaging of soybean response to drought stress: the effect of Ascophyllum nodosum seaweed extract. SpringerPlus, 5(1). http://dx.doi.org/10.1186/s40064-016-3019-2.
McAinsh, M. R., Brownlee, C., Hetherington, A. M., & Mansfield, T. A. (1991). Partial inhibition of ABA-induced stomatal closure by calcium-channel blockers. Proceedings of the Royal Society of London. Series B: Biological Sciences, 243, 195-201.
McAusland, L., Davey, P. A., Kanwal, N., Baker, N. R., & Lawson, T. (2013). A novel system for spatial and temporal imaging of intrinsic plant water use efficiency. Journal of Experimental Botany, 64, 4993-5007.
Medeiros, D. B., Souza, L. P., Antunes, W. C., Araújo, W. L., Daloso, D. M., & Fernie, A. R. (2018). Sucrose breakdown within guard cells provides substrates for glycolysis and glutamine biosynthesis during light-induced stomatal opening. The Plant Journal, 94, 583-594.
Merilo, E., Jalakas, P., Kollist, H., & Brosché, M. (2015). The role of ABA recycling and transporter proteins in rapid stomatal responses to reduced air humidity, elevated CO2, and exogenous ABA. Molecular Plant, 8, 657-659.
Merlot, S., Mustilli, A.-C., Genty, B., North, H., Lefebvre, V., Sotta, B., … Giraudat, J. (2002). Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation. The Plant Journal, 30, 601-609.
Meyer, S., & Genty, B. (1998). Mapping intercellular CO2 mole fraction (Ci) in Rosa rubiginosa leaves fed with abscisic acid by using chlorophyll fluorescence imaging: Significance of Ci estimated from leaf gas exchange. Plant Physiology, 116, 947-957.
Mousavi, S. A. R., Chauvin, A., Pascaud, F., Kellenberger, S., & Farmer, E. E. (2013). Glutamate receptor-like genes mediate leaf-to-leaf wound signalling. Nature, 500, 422-426.
Müller, H. M., Schäfer, N., Bauer, H., Geiger, D., Lautner, S., Fromm, J., … Hedrich, R. (2017). The desert plant Phoenix dactylifera closes stomata via nitrate-regulated SLAC1 anion channel. New Phytologist, 216, 150-162.
Mustilli, A.-C., Merlot, S., Vavasseur, A., Fenzi, F., & Giraudat, J. (2002). Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. The Plant Cell, 14, 3089-3099.
Nawrath, C., & Métraux, J.-P. (1999). Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of Camalexin after pathogen inoculation. The Plant Cell, 11, 1393-1404.
Omasa, K., & Takayama, K. (2003). Simultaneous measurement of stomatal conductance, non-photochemical quenching, and photochemical yield of photosystem II in intact leaves by thermal and chlorophyll fluorescence imaging. Plant and Cell Physiology, 44, 1290-1300.
Page, G. F. M., Liénard, J. F., Pruett, M. J., & Moffett, K. B. (2018). Spatiotemporal dynamics of leaf transpiration quantified with time-series thermal imaging. Agricultural and Forest Meteorology, 256-257, 304-314.
Pantin, F., Monnet, F., Jannaud, D., Costa, J. M., Renaud, J., Muller, B., … Genty, B. (2013). The dual effect of abscisic acid on stomata. New Phytologist, 197, 65-72.
Pantin, F., Renaud, J., Barbier, F., Vavasseur, A., Le Thiec, D., Rose, C., … Simonneau, T. (2013). Developmental priming of stomatal sensitivity to abscisic acid by leaf microclimate. Current Biology, 23, 1805-1811.
Raschke, K. (1975). Simultaneous requirement of carbon dioxide and abscisic acid for stomatal closing in Xanthium strumarium L. Planta, 125, 243-259.
Raskin, I., & Ladyman, J. A. R. (1988). Isolation and characterization of a barley mutant with abscisic-acid-insensitive stomata. Planta, 173, 73-78.
Schäfer, N., Maierhofer, T., Herrmann, J., Jørgensen, M. E., Lind, C., von Meyer, K., … Hedrich, R. (2018). A tandem amino acid residue motif in guard cell SLAC1 Anion Channel of grasses allows for the control of stomatal aperture by nitrate. Current Biology, 28, 1370-1379.
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 Years of image analysis. Nature Methods, 9, 671-675.
Shatil-Cohen, A., Attia, Z., & Moshelion, M. (2011). Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: A target of xylem-borne ABA? The Plant Journal, 67, 72-80.
Sweet, K. J., Peak, D., & Mott, K. A. (2017). Stomatal heterogeneity in responses to humidity and temperature: Testing a mechanistic model. Plant, Cell & Environment, 40, 2771-2779.
Takemiya, A., Yamauchi, S., Yano, T., Ariyoshi, C., & Shimazaki, K. (2013). Identification of a regulatory subunit of protein phosphatase 1 which mediates blue light signaling for stomatal opening. Plant and Cell Physiology, 54, 24-35.
Tõldsepp, K., Zhang, J., Takahashi, Y., Sindarovska, Y., Hõrak, H., Ceciliato, P. H. O., … Schroeder, J. I. (2018). Mitogen-activated protein kinases MPK4 and MPK12 are key components mediating CO2-induced stomatal movements. The Plant Journal, 96, 1018-1035.
Uraji, M., Katagiri, T., Okuma, E., Ye, W., Hossain, M. A., Masuda, C., … Murata, Y. (2012). Cooperative function of PLDδ and PLDα1 in abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiology, 159, 450-460.
Vialet-Chabrand, S., & Lawson, T. (2019). Dynamic leaf energy balance: Deriving stomatal conductance from thermal imaging in a dynamic environment. Journal of Experimental Botany, 70, 2839-2855.
Viger, M., Rodriguez-Acosta, M., Rae, A. M., Morison, J. I. L., & Taylor, G. (2013). Toward improved drought tolerance in bioenergy crops: QTL for carbon isotope composition and stomatal conductance in Populus. Food and Energy Security, 2, 220-236.
Vollsnes, A. V., Eriksen, A. B., Otterholt, E., Kvaal, K., Oxaal, U., & Futsaether, C. M. (2009). Visible foliar injury and infrared imaging show that daylength affects short-term recovery after ozone stress in Trifolium subterraneum. Journal of Experimental Botany, 60, 3677-3686.
West, J. D., Peak, D., Peterson, J. Q., & Mott, K. A. (2005). Dynamics of stomatal patches for a single surface of Xanthium strumarium L. leaves observed with fluorescence and thermal images. Plant, Cell & Environment, 28, 633-641.
Wildermuth, M. C., Dewdney, J., Wu, G., & Ausubel, F. M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414, 562-565.
Xie, X., Wang, Y., Williamson, L., Holroyd, G. H., Tagliavia, C., Murchie, E., … Hetherington, A. M. (2006). The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Current Biology, 16, 882-887.
Xu, Y.-H., Liu, R., Yan, L., Liu, Z.-Q., Jiang, S.-C., Shen, Y.-Y., … Zhang, D.-P. (2012). Light-harvesting chlorophyll a/b-binding proteins are required for stomatal response to abscisic acid in Arabidopsis. Journal of Experimental Botany, 63, 1095-1106.
Yamamoto, Y., Negi, J., Wang, C., Isogai, Y., Schroeder, J. I., & Iba, K. (2016). The transmembrane region of guard cell SLAC1 channels perceives CO2 signals via an ABA-independent pathway in Arabidopsis. The Plant Cell, 28, 557-567.
Yoshida, R., Hobo, T., Ichimura, K., Mizoguchi, T., Takahashi, F., Aronso, J., … Shinozaki, K. (2002). ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant and Cell Physiology, 43, 1473-1483.