Under salt stress guard cells rewire ion transport and abscisic acid signaling.
abscisic acid (ABA)
glycophyte Arabidopsis
guard cell
halophyte Thellungiella/Eutrema
ion transport
salt stress
soil
stomata
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
19
01
2021
accepted:
22
03
2021
pubmed:
29
3
2021
medline:
13
7
2021
entrez:
28
3
2021
Statut:
ppublish
Résumé
Soil salinity is an increasingly global problem which hampers plant growth and crop yield. Plant productivity depends on optimal water-use efficiency and photosynthetic capacity balanced by stomatal conductance. Whether and how stomatal behavior contributes to salt sensitivity or tolerance is currently unknown. This work identifies guard cell-specific signaling networks exerted by a salt-sensitive and salt-tolerant plant under ionic and osmotic stress conditions accompanied by increasing NaCl loads. We challenged soil-grown Arabidopsis thaliana and Thellungiella salsuginea plants with short- and long-term salinity stress and monitored genome-wide gene expression and signals of guard cells that determine their function. Arabidopsis plants suffered from both salt regimes and showed reduced stomatal conductance while Thellungiella displayed no obvious stress symptoms. The salt-dependent gene expression changes of guard cells supported the ability of the halophyte to maintain high potassium to sodium ratios and to attenuate the abscisic acid (ABA) signaling pathway which the glycophyte kept activated despite fading ABA concentrations. Our study shows that salinity stress and even the different tolerances are manifested on a single cell level. Halophytic guard cells are less sensitive than glycophytic guard cells, providing opportunities to manipulate stomatal behavior and improve plant productivity.
Substances chimiques
Arabidopsis Proteins
0
Abscisic Acid
72S9A8J5GW
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1040-1055Informations de copyright
© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.
Références
Ache P, Becker D, Ivashikina N, Dietrich P, Roelfsema MRG, Hedrich R. 2000. GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K+-selective, K+-sensing ion channel. FEBS Letters 486: 93-98.
Ball JT. 1987. Calculations related to gas exchange. In: Zeiger E, Farquhar G, Cowan I, eds. Stomatal Function. Stanford, CA, USA: Stanford University Press 20: 445-476.
Bauer H, Ache P, Lautner S, Fromm J, Hartung W, Al-Rasheid K, Sonnewald S, Sonnewald U, Kneitz S, Lachmann N et al. 2013. The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Current Biology 23: 53-57.
Bauer S, Grossmann S, Vingron M, Robinson PN. 2008. Ontologizer 2.0 - a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics 24: 1650-1651.
Beilby MJ, Shepherd VA. 2001. Modeling the current-voltage characteristics of charophyte membranes. II. The effect of salinity on membranes of Lamprothamnium papulosum. Journal of Membrane Biology 181: 77-89.
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological) 57: 289-300.
Böhm J, Messerer M, Müller HM, Scholz-Starke J, Gradogna A, Scherzer S, Maierhofer T, Bazihizina N, Zhang H, Stigloher C et al. 2018. Understanding the molecular basis of salt sequestration in epidermal bladder cells of Chenopodium quinoa. Current Biology 28: 3075-3085.
Bose J, Munns R, Shabala S, Gilliham M, Pogson B, Tyerman SD. 2017. Chloroplast function and ion regulation in plants growing on saline soils: lessons from halophytes. Journal of Experimental Botany 68: 3129-3143.
Bryant DM, Johnson K, DiTommaso T, Tickle T, Couger MB, Payzin-Dogru D, Lee TJ, Leigh ND, Kuo T-H, Davis FG et al. 2017. A tissue-mapped axolotl de novo transcriptome enables identification of limb regeneration factors. Cell Reports 18: 762-776.
Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P. 2011. Salinity stress and salt tolerance. In: Shunker A, Venkateswarlu B, eds. Abiotic stress in plants. [WWW document] URL https://www.intechopen.com/books/ [accessed 1 September 2011].
Chaves MM, Flexas J, Pinheiro C. 2009. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103: 551-560.
Cotelle V, Leonhardt N. 2019. Chapter four - ABA signaling in guard cells. In: Seo M, Marion-Poll A, eds. Advances in Botanical Research. Academic Press 92: 115-170.
Dietrich P, Moeder W, Yoshioka K. 2020. Plant cyclic nucleotide-gated channels: new insights on their functions and regulation. Plant Physiology 184: 27-38.
Dittrich M, Mueller HM, Bauer H, Peirats-Llobet M, Rodriguez PL, Geilfus C-M, Carpentier SC, Al Rasheid KAS, Kollist H, Merilo E et al. 2019. The role of Arabidopsis ABA receptors from the PYR/PYL/RCAR family in stomatal acclimation and closure signal integration. Nature Plants 5: 1002-1011.
Edel KH, Kudla J. 2016. Integration of calcium and ABA signaling. Current Opinion in Plant Biology 33: 83-91.
Fernando VCD, Schroeder DF. 2016. Role of ABA in Arabidopsis salt, drought, and desiccation tolerance. In: Shanker AK, Shanker C, eds. Abiotic and biotic stress in plants - recent advances and future perspectives. [WWW document] URL https://www.intechopen.com/books/ [accessed February 2016].
Flowers TJ, Colmer TD. 2015. Plant salt tolerance: adaptations in halophytes. Annals of Botany 115: 327-331.
Franco-Navarro JD, Rosales MA, Cubero-Font P, Calvo P, Álvarez R, Diaz-Espejo A, Colmenero-Flores JM. 2019. Chloride as a macronutrient increases water-use efficiency by anatomically driven reduced stomatal conductance and increased mesophyll diffusion to CO2. The Plant Journal 99: 815-831.
Franzisky BL, Geilfus CM, Romo-Pérez ML, Fehrle I, Erban A, Kopka J, Zoerb C. 2020. Acclimatization of guard cell metabolism to long-term salinity. Plant, Cell & Environment 44: 870-884.
Fromm J, Essiamah S, Eschrich W. 1987. Displacement of frequently occurring heavy metals in autumn leaves of beech (Fagus sylvatica). Trees 1: 164-171.
Geiger D, Maierhofer T, AL-Rasheid Kas, Scherzer S, Mumm P, Liese A, Ache P, Wellmann C, Marten I, Grill E et al. 2011. Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Science Signaling 4: ra32.
Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KAS et al. 2009. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proceedings of National Academy of Sciences, USA 106: 21425-21430.
Geilfus C-M. 2018. Chloride: from nutrient to toxicant. Plant, Cell and Physiology 59: 877-886.
Geilfus CM, Mithöfer A, Ludwig-Müller J, Zoerb C, Muehling KH. 2015. Chloride-inducible transient apoplastic alkalinizations induce stomata closure by controlling abscisic acid distribution between leaf apoplast and guard cells in salt-stressed Vicia faba. New Phytologist 208: 803-816.
Golldack D, Li C, Mohan H, Probst N. 2014. Tolerance to drought and salt stress in plants: unraveling the signaling networks. Frontiers in Plant Science 5: 151.
Gong Q, Li P, Ma S, Rupassara S, Bohnert HJ. 2005. Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. The Plant Journal 44: 826-839.
Grossmann S, Bauer S, Robinson PN, Vingron M. 2007. Improved detection of overrepresentation of Gene-Ontology annotations with parent child analysis. Bioinformatics 23: 3024-3031.
Hedrich R. 2012. Ion channels in plants. Physiological Reviews 92: 1777-1811.
Hedrich R, Geiger D. 2017. Biology of SLAC1-type anion channels - from nutrient uptake to stomatal closure. New Phytologist 216: 46-61.
Hedrich R, Shabala S. 2018. Stomata in a saline world. Current Opinion in Plant Biology 46: 87-95.
Heijde M, Binkert M, Yin R, Ares-Orpel F, Rizzini L, Van De Slijke E, Persiau G, Nolf J, Gevaert K, De Jaeger G et al. 2013. Constitutively active UVR8 photoreceptor variant in Arabidopsis. Proceedings of National Academy of Sciences, USA 110: 20326-20331.
Hetherington A, Woodward F. 2003. The role of stomata in sensing and driving environmental change. Nature 424: 901-908.
Hoffmann RD, Olsen LI, Ezike CV, Pedersen JT, Manstretta R, López-Marqués RL, Palmgren M. 2019. Roles of plasma membrane proton ATPases AHA2 and AHA7 in normal growth of roots and root hairs in Arabidopsis thaliana. Physiologia Plantarum 166: 848-861.
Hoth S, Morgante M, Sanchez JP, Hanafey MK, Tingey SV, Chua NH. 2002. Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. Journal of Cell Science 115: 4891-4900.
Huang S, Waadt R, Nuhkat M, Kollist H, Hedrich R, Roelfsema MRG. 2019. Calcium signals in guard cells enhance the efficiency by which abscisic acid triggers stomatal closure. New Phytologist 224: 177-187.
Huber W, Carey VJ, Gentleman R, Anders S, Carlson M, Carvalho BS, Bravo HC, Davis S, Gatto L, Girke T et al. 2015. Orchestrating high-throughput genomic analysis with Bioconductor. Nature Methods 12: 115-121.
Imes D, Mumm P, Boehm J, Al-Rasheid KAS, Marten I, Geiger D, Hedrich R. 2013. Open stomata 1 (OST1) kinase controls R-type anion channel QUAC1 in Arabidopsis guard cells. The Plant Journal 74: 372-382.
Isayenkov SV, Maathuis FJ. 2019. Plant salinity stress: Many unanswered questions remain. Frontiers in Plant Science 10: 80.
Ivashikina N, Deeken R, Fischer S, Ache P, Hedrich R. 2005. AKT2/3 subunits render guard cell K+ channels Ca2+ sensitive. Journal of General Physiology 125: 483-492.
Jalakas P, Yarmolinsky D, Kollist H, Brosche M. 2017. Isolation of guard-cell enriched tissue for RNA extraction. Bio-protocol 7: e2447.
James RA, Von Caemmerer S, Condon AGT, Zwart AB, Munns R. 2008. Genetic variation in tolerance to the osmotic stress component of salinity stress in durum wheat. Functional Plant Biology 35: 111-123.
Ji H, Pardob JM, Batellic G, Van Oostend MJ, Bressane R, Lia X. 2013. The salt overly sensitive (SOS) pathway: established and emerging roles. Molecular Plant 6: 275-286.
Jia W, Wang Y, Zhang S, Zhang J. 2002. Salt-stress-induced ABA accumulation is more sensitively triggered in roots than in shoots. Journal of Experimental Botany 53: 2201-2206.
Julkowska MM, Testerink C. 2015. Tuning plant signaling and growth to survive salt. Trends in Plant Science 20: 586-594.
Kerstiens G, Tych W, Robinson MF, Mansfield TA. 2002. Sodium-related partial stomatal closure and salt tolerance of Aster tripolium. New Phytologist 153: 509-515.
Ko D, Helariutta Y. 2017. Shoot-root communication in flowering plants. Current Biology 27: R973-R978.
Lahr W, Raschke K. 1988. Abscisic-acid contents and concentrations in protoplasts from guard cells and mesophyll cells of Vicia faba L. Planta 173: 528-531.
Lawson T, Vialet-Chabrand S. 2019. Speedy stomata, photosynthesis and plant water use efficiency. New Phytologist 221: 93-98.
Lee SC, Lan W, Buchanan BB, Luan S. 2009. A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proceedings of National Academy of Sciences, USA 106: 21419-21424.
Lee YP, Giorgi FM, Lohse M, Kvederaviciute K, Klages S, Usadel B, Meskiene I, Reinhardt R, Hincha DK. 2013. Transcriptome sequencing and microarray design for functional genomics in the extremophile Arabidopsis relative Thellungiella salsuginea (Eutrema salsugineum). BMC Genomics 14: 793.
Levchenko V, Konrad KR, Dietrich P, Roelfsema MR, Hedrich R. 2005. Cytosolic abscisic acid activates guard cell anion channels without preceding Ca2+ signals. Proceedings of National Academy of Sciences, USA 102: 4203-4208.
Li B, Tester M, Gilliham M. 2017. Chloride on the Move. Trends in Plant Science 23: 237-248.
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064-1068.
Maathuis FJ. 2014. Sodium in plants: perception, signaling, and regulation of sodium fluxes. Journal of Experimental Botany 65: 849-858.
MacLeod MJ, Dedrick J, Ashton C, Sung WW, Champigny MJ, Weretilnyk EA. 2015. Exposure of two Eutrema salsugineum (Thellungiella salsuginea) accessions to water deficits reveals different coping strategies in response to drought. Physiologia Plantarum 155: 267-280.
Maierhofer T, Diekmann M, Offenborn JN, Lind C, Bauer H, Hashimoto K, Al-Rasheid KAS, Luan S, Kudla J, Geiger D et al. 2014. Site- and kinase-specific phosphorylation-mediated activation of SLAC1, a guard cell anion channel stimulated by abscisic acid. Science Signaling 7: ra86.
Misyura M, Colasanti J, Rothstein SJ. 2013. Physiological and genetic analysis of Arabidopsis thaliana anthocyanin biosynthesis mutants under chronic adverse environmental conditions. Journal of Experimental Botany 64: 229-240.
Muchate NS, Nikalje GC, Rajurkar NS, Suprasanna P, Nikam TD. 2016. Plant salt stress: Adaptive responses, tolerance mechanism and bioengineering for salt tolerance. Botanical Review 82: 371-406.
Mueller HM, Schaefer N, Bauer H, Geiger D, Lautner S, Fromm J, Riederer M, Bueno A, Nussbaumer T, Mayer K et al. 2017. The desert plant Phoenix dactylifera closes stomata via nitrate regulated SLAC1 anion channel. New Phytologist 16: 150-162.
Munns R. 2002. Comparative physiology of salt and water stress. Plant, Cell & Environment 25: 239-250.
Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology 59: 651-681.
Munns R, Wallace PA, Teakle NL, Colmer TD. 2010. Measuring soluble ion concentrations (Na+, K+, Cl−) in salt-treated plants. Plant Stress Tolerance 639: 371-382.
Nishimura N, Sarkeshik A, Nito K, Park S-Y, Wang A, Carvalho PC, Lee S, Caddell DF, Cutler SR, Chory J et al. 2010. PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. The Plant Journal 61: 290-299.
Oksanen J, Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin P, O’Hara R, Simpson G, Solymos P, et al. 2020. Vegan: community ecology package. R package v.2.5-7. [WWW document] URL https://CRAN.R-project.org/package=vegan.
Park S-y, Fung P, Nishimura N, Jensen Dr, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-f F et al. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071.
Polley HW. 2002. Implications of atmospheric and climatic change for crop yield and water use efficiency. Crop Sciences. 42: 131-140.
R Core Team. 2011. R: A language and environment for statistical computing, v.2.14.1. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL https://www.r-project.org.
R Core Team. 2019. A language and environment for statistical computing, v.3.6.2. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL https://www.R-project.org.
Raschke K, Hedrich R. 1989. Patch clamp measurements on isolated guard-cell protoplasts and vacuoles. In: Fleischer S, Fleischer B, Abelson J, Simon M, eds. Methods in enzymology. Cambridge, MA, USA: Academic Press, 174: 312-330.
Reintanz B, Szyroki A, Ivashikina N, Ache P, Godde M, Becker D, Palme K, Hedrich R. 2002. AtKC1, a silent Arabidopsis potassium channel alpha -subunit modulates root hair K+ influx. Proceedings of National Academy of Sciences, USA 99: 4079-4084.
Rienmüller F, Beyhl B, Lautner S, Fromm F, Al-Rasheid KAS, Ache P, Farmer EE, Marten I, Hedrich R. 2010. Guard cell-specific calcium sensitivity of high density and activity sv/tpc1 channels. Plant, Cell & Physiology 51: 1548-1554.
Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. 2015. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Research 43: e47.
Robinson MF, Véry AA, Sanders D, Mansfield TA. 1997. How can stomata contribute to salt tolerance? Annals of Botany 80: 387-393.
Roelfsema MRG, Hedrich R, Geiger D. 2012. Anion channels: master switches of stress responses. Trends in Plant Science 17: 221-229.
Rondeau RE. 1966. Slush baths. Journal of Chemical & Engineering Data 11: 124.
Sheen HT, Kahler HL. 1938. Effect of ions on Mohr method for chloride determination. Industrial and Engineering Chemistry 10: 628-629.
Shepherd VA, Beilby MJ, Al Khazaaly SA, Shimmen T. 2008. Mechano-perception in Chara cells: the influence of salinity and calcium on touch-activated receptor potentials, action potentials and ion transport. Plant, Cell & Environment 31: 1575-1591.
Shi W, Oshlack A, Smyth GK. 2010. Optimizing the noise versus bias trade-off for Illumina whole genome expression Bead Chips. Nucleic Acids Research 38: e204.
Stepien P, Johnson GN. 2009. Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiology 149: 1154-1165.
Stingl N, Krischke M, Fekete A, Mueller MJ. 2013. Analysis of defense signals in Arabidopsis thaliana leaves by ultra-performance liquid chromatography/tandem mass spectrometry: Jasmonates, salicylic acid, abscisic acid. Methods in Molecular Biology 1009: 103-113.
Sun Y, Kong X, Li C, Liu Y, Ding Z. 2015. Potassium retention under salt stress is associated with natural variation in salinity tolerance among Arabidopsis accessions. PLoS ONE 10: e0124032.
Szyroki A, Ivashikina N, Dietrich P, Roelfsema MRG, Ache P, Reintanz B, Deeken R, Godde M, Felle H, Steinmeyer R et al. 2001. KAT1 is not essential for stomatal opening. Proceedings of National Academy of Sciences, USA 98: 2917-2921.
Tambussi E, Bort J, Araus J. 2007. Water use efficiency in C3 cereals under Mediterranean conditions: a review of physiological aspects. Annals of Applied Biology 150: 307-321.
Thor K, Jiang S, Michard E, George J, Scherzer S, Huang S, Dindas J, Derbyshire P, Leitão N, DeFalco TA et al. 2020. The calcium-permeable channel OSCA1.3 regulates plant stomatal immunity. Nature 585: 569-573.
Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G, Lamminmäki A, Brosché M, Moldau H, Desikan R et al. 2008. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signaling. Nature 452: 487-491.
Very A-A, Robinson MF, Mansfield TA, Sanders D. 1998. Guard cell cation channels are involved in Na+-induced stomatal closure in a halophyte. The Plant Journal 14: 509-521.
Wang Y, Wu W-H. 2013. Potassium transport and signaling in higher plants. Annual Review of Plant Biology 64: 451-476.
Wege S, Gilliham M, Henderson SW. 2017. Chloride: not simply a ‘cheap osmoticum’, but a beneficial plant macronutrient. Journal of Experimental Botany 68: 3057-3069.
Weiler EW, Schnabl H, Hornberg C. 1982. Stress-related levels of abscisic acid in guard cell protoplasts of Vicia faba L. Planta 154: 24-28.
Wu H, Zhang X, Giraldo JP, Shabala S. 2018. It is not all about sodium: revealing tissue specificity and signalling roles of potassium in plant responses to salt stress. Plant and Soil 431: 1-17.
Yu Y, Assmann SM. 2016. The effect of NaCl on stomatal opening in Arabidopsis wild type and agb1 heterotrimeric G-protein mutant plants. Plant Signaling and Behavior 11: e1085275.
Yuan F, Yang H, Xue Y, Kong D, Ye R, Li C, Zhang J, Theprungsirikul L, Shrift T, Krichilsky B et al. 2014. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514: 367-371.
Van Zelm E, Zhang Y, Testerink C. 2020. Salt tolerance mechanisms of plants. Annual Review of Plant Biology 71: 24.1-24.31.