Tobacco leaf tissue rapidly detoxifies direct salt loads without activation of calcium and SOS signaling.
NHX1
NaCl transport
Salt Overly Sensitive pathway
calcium signaling
cytosolic pH
leaf response
osmotic effects
salt stress
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
01 2023
01 2023
Historique:
received:
11
02
2022
accepted:
11
09
2022
pubmed:
22
9
2022
medline:
15
12
2022
entrez:
21
9
2022
Statut:
ppublish
Résumé
Salt stress is a major abiotic stress, responsible for declining agricultural productivity. Roots are regarded as hubs for salt detoxification, however, leaf salt concentrations may exceed those of roots. How mature leaves manage acute sodium chloride (NaCl) stress is mostly unknown. To analyze the mechanisms for NaCl redistribution in leaves, salt was infiltrated into intact tobacco leaves. It initiated pronounced osmotically-driven leaf movements. Leaf downward movement caused by hydro-passive turgor loss reached a maximum within 2 h. Salt-driven cellular water release was accompanied by a transient change in membrane depolarization but not an increase in cytosolic calcium ion (Ca
Substances chimiques
Calcium
SY7Q814VUP
Sodium Chloride
451W47IQ8X
Sodium
9NEZ333N27
Ions
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
217-231Informations de copyright
© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.
Références
Ache P, Becker D, Ivashikina N, Dietrich P, Roelfsema MR, 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.
Apse MP, Aharon GS, Snedden WA, Blumwald E. 1999. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285: 1256-1258.
Arif I, Newman IA, Keenlyside N. 1995. Proton flux measurements from tissues in buffered solution. Plant Cell and Environment 18: 1319-1324.
Assaha DVM, Ueda A, Saneoka H, Al-Yahyai R, Yaish MW. 2017. The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Frontiers in Physiology 8: 509.
Baetz U, Eisenach C, Tohge T, Martinoia E, De Angeli A. 2016. Vacuolar chloride fluxes impact ion content and distribution during early salinity stress. Plant Physiology 172: 1167-1181.
Behera S, Wang N, Zhang C, Schmitz-Thom I, Strohkamp S, Schültke S, Hashimoto K, Xiong L, Kudla J. 2015. Analyses of Ca2+ dynamics using a ubiquitin-10 promoter-driven Yellow Cameleon 3.6 indicator reveal reliable transgene expression and differences in cytoplasmic Ca2+ responses in Arabidopsis and rice (Oryza sativa) roots. New Phytologist 206: 751-760.
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.
Böhm J, Scherzer S, Krol E, Kreuzer I, von Meyer K, Lorey C, Mueller Thomas D, Shabala L, Monte I, Solano R et al. 2016. The venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Current Biology 26: 286-295.
Britto D, Kronzucker H. 2015. Sodium efflux in plant roots: what do we really know? Journal of Plant Physiology 186-187: 1-12.
Cao X-Q, Jiang Z-H, Yi Y-Y, Yang Y, Ke L-P, Pei Z-M, Zhu S. 2017. Biotic and abiotic stresses activate different Ca2+ permeable channels in Arabidopsis. Frontiers in Plant Science 8: 83.
Carillo P, Gibon Y. 2011. PROTOCOL: Determination of glycine betaine. Prometheus Wiki. [WWW document] URL https://prometheusprotocols.net/function/tissue-chemistry/secondary-compounds/extraction-and-determination-of-glycine-betaine/ [accessed 11 October 2022].
Chen L-Q, Cheung LS, Feng L, Tanner W, Frommer WB. 2015. Transport of sugars. Annual Review of Biochemistry 84: 865-894.
Choi W-G, Toyota M, Kim S-H, Hilleary R, Gilroy S. 2014. Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proceedings of the National Academy of Sciences, USA 111: 6497-6502.
Conn S, Gilliham M. 2010. Comparative physiology of elemental distributions in plants. Annals of Botany 105: 1081-1102.
Corso M, Doccula FG, de Melo JRF, Costa A, Verbruggen N. 2018. Endoplasmic reticulum-localized CCX2 is required for osmotolerance by regulating ER and cytosolic Ca2+ dynamics in Arabidopsis. Proceedings of the National Academy of Sciences, USA 115: 3966-3971.
Cuin TA, Betts SA, Chalmandrier R, Shabala S. 2008. A root's ability to retain K+ correlates with salt tolerance in wheat. Journal of Experimental Botany 59: 2697-2706.
Cuin TA, Shabala S. 2005. Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant and Cell Physiology 46: 1924-1933.
Darko E, Gierczik K, Hudák O, Forgó P, Pál M, Türkösi E, Kovács V, Dulai S, Majláth I, Molnár I et al. 2017. Differing metabolic responses to salt stress in wheat-barley addition lines containing different 7H chromosomal fragments. PLoS ONE 12: e0174170.
DeFalco TA, Toyota M, Phan V, Karia P, Moeder W, Gilroy S, Yoshioka K. 2017. Using GCaMP3 to study Ca2+ signaling in Nicotiana species. Plant and Cell Physiology 58: 1173-1184.
Dinneny JR, Long TA, Wang JY, Jung JW, Mace D, Pointer S, Barron C, Brady SM, Schiefelbein J, Benfey PN. 2008. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320: 942-945.
Dong L, Wang Q, Manik SMN, Song Y, Shi S, Su Y, Liu G, Liu H. 2015. Nicotiana sylvestris calcineurin B-like protein NsylCBL10 enhances salt tolerance in transgenic Arabidopsis. Plant Cell Reports 34: 2053-2063.
Dreyer I, Li K, Riedelsberger J, Hedrich R, Konrad KR, Michard E. 2022. Transporter networks can serve plant cells as nutrient sensors and mimic transceptor-like behavior. iScience 25: 104078.
Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, Liu M-C, Maman J, Steinhorst L, Schmitz-Thom I et al. 2018. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Current Biology 28: 666-675.
Gaxiola RA, Sanchez CA, Paez-Valencia J, Ayre BG, Elser JJ. 2012. Genetic manipulation of a “vacuolar” H+-PPase: from salt tolerance to yield enhancement under phosphorus-deficient soils. Plant Physiology 159: 3-11.
Geilfus C-M. 2018. Chloride: from nutrient to toxicant. Plant and Cell Physiology 59: 877-886.
Geng Y, Wu R, Wee CW, Xie F, Wei X, Chan PMY, Tham C, Duan L, Dinneny JR. 2013. A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell 25: 2132-2154.
Ghorbani A, Omran VOG, Razavi SM, Pirdashti H, Ranjbar M. 2019. Piriformospora indica confers salinity tolerance on tomato (Lycopersicon esculentum Mill.) through amelioration of nutrient accumulation, K+/Na+ homeostasis and water status. Plant Cell Reports 38: 1151-1163.
Goodin MM, Zaitlin D, Naidu RA, Lommel SA. 2008. Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Molecular Plant-Microbe Interactions 21: 1015-1026.
Gradogna A, Scholz-Starke J, Pardo JM, Carpaneto A. 2021. Beyond the patch-clamp resolution: functional activity of nonelectrogenic vacuolar NHX proton/potassium antiporters and inhibition by phosphoinositides. New Phytologist 229: 3026-3036.
Graus D, Konrad KR, Bemm F, Patir Nebioglu MG, Lorey C, Duscha K, Güthoff T, Herrmann J, Ferjani A, Cuin TA et al. 2018. High V-PPase activity is beneficial under high salt loads, but detrimental without salinity. New Phytologist 219: 1421-1432.
Guo Q, Tian XX, Mao PC, Meng L. 2020. Overexpression of Iris lactea tonoplast Na+/H+ antiporter gene IlNHX confers improved salt tolerance in tobacco. Biologia Plantarum 64: 50-57.
Gutermuth T, Herbell S, Lassig R, Brosche M, Romeis T, Feijo JA, Hedrich R, Konrad KR. 2018. Tip-localized Ca2+-permeable channels control pollen tube growth via kinase-dependent R- and S-type anion channel regulation. New Phytologist 218: 1089-1105.
Gutermuth T, Lassig R, Portes M-T, Maierhofer T, Romeis T, Borst J-W, Hedrich R, Feijó JA, Konrad KR. 2013. Pollen tube growth regulation by free anions depends on the interaction between the anion channel SLAH3 and calcium-dependent protein kinases CPK2 and CPK20. Plant Cell 25: 4525-4543.
Halfter U, Ishitani M, Zhu J-K. 2000. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proceedings of the National Academy of Sciences, USA 97: 3735-3740.
Hedrich R. 2012. Ion channels in plants. Physiological Reviews 92: 1777-1811.
Hedrich R, Sauer N, Neuhaus HE. 2015. Sugar transport across the plant vacuolar membrane: nature and regulation of carrier proteins. Current Opinion in Plant Biology 25: 63-70.
Huang S, Ding M, Roelfsema MRob G, Dreyer I, Scherzer S, Al-Rasheid KAS, Gao S, Nagel G, Hedrich R, Konrad KR. 2021. Optogenetic control of the guard cell membrane potential and stomatal movement by the light-gated anion channel GtACR1. Science Advances 7: eabg4619.
Isayenkov SV, Maathuis FJM. 2019. Plant salinity stress: many unanswered questions remain. Frontiers in Plant Science 10: 80.
James RA, Munns R, von Caemmerer S, Trejo C, Miller C, Condon TA. 2006. Photosynthetic capacity is related to the cellular and subcellular partitioning of Na+, K+ and Cl− in salt-affected barley and durum wheat. Plant, Cell & Environment 29: 2185-2197.
Jegadeeson V, Kumari K, Pulipati S, Parida A, Venkataraman G. 2019. Expression of wild rice Porteresia coarctata PcNHX1 antiporter gene (PcNHX1) in tobacco controlled by PcNHX1 promoter (PcNHX1p) confers Na+-specific hypocotyl elongation and stem-specific Na+ accumulation in transgenic tobacco. Plant Physiology and Biochemistry 139: 161-170.
Jeon BW, Acharya BR, Assmann SM. 2019. The Arabidopsis heterotrimeric G-protein β subunit, AGB1, is required for guard cell calcium sensing and calcium-induced calcium release. The Plant Journal 99: 231-244.
Ji H, Pardo JM, Batelli G, Van Oosten MJ, Bressan RA, Li X. 2013. The salt overly sensitive (SOS) pathway: established and emerging roles. Molecular Plant 6: 275-286.
Jiang Z, Zhou X, Tao M, Yuan F, Liu L, Wu F, Wu X, Xiang Y, Niu Y, Liu F et al. 2019. Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572: 341-346.
Julkowska MM, Testerink C. 2015. Tuning plant signaling and growth to survive salt. Trends in Plant Science 20: 586-594.
Jung B, Ludewig F, Schulz A, Meißner G, Wöstefeld N, Flügge U-I, Pommerrenig B, Wirsching P, Sauer N, Koch W et al. 2015. Identification of the transporter responsible for sucrose accumulation in sugar beet taproots. Nature Plants 1: 14001.
Karimi SM, Freund M, Wager BM, Knoblauch M, Fromm J, Mueller HM, Ache P, Krischke M, Mueller MJ, Müller T et al. 2021. Under salt stress guard cells rewire ion transport and abscisic acid signaling. New Phytologist 231: 1040-1055.
Khan MS, Ahmad D, Khan MA. 2015. Trends in genetic engineering of plants with Na+/H+ antiporters for salt stress tolerance. Biotechnology & Biotechnological Equipment 29: 815-825.
Köster P, Wallrad L, Edel KH, Faisal M, Alatar AA, Kudla J. 2019. The battle of two ions: Ca2+ signalling against Na+ stress. Plant Biology 21: 39-48.
Kramer DM, Johnson G, Kiirats O, Edwards GE. 2004. New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research 79: 209-218.
Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF. 2002. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology 130: 2129-2141.
Kronzucker HJ, Coskun D, Schulze LM, Wong JR, Britto DT. 2013. Sodium as nutrient and toxicant. Plant and Soil 369: 1-23.
Läuchli A, Grattan SR. 2007. Plant growth and development under salinity stress. In: Jenks MA, Hasegawa PM, Jain SM, eds. Advances in molecular breeding toward drought and salt tolerant crops. Dordrecht, the Netherlands: Springer, 1-32.
Lekshmy S, Sairam RK, Chinnusamy V, Jha SK. 2015. Differential transcript abundance of salt overly sensitive (SOS) pathway genes is a determinant of salinity stress tolerance of wheat. Acta Physiologiae Plantarum 37: 169.
Li B, Tester M, Gilliham M. 2017. Chloride on the move. Trends in Plant Science 22: 236-248.
Li K, Prada J, Damineli DSC, Liese A, Romeis T, Dandekar T, Feijo JA, Hedrich R, Konrad KR. 2021. An optimized genetically encoded dual reporter for simultaneous ratio imaging of Ca2+ and H+ reveals new insights into ion signaling in plants. New Phytologist 230: 2292-2310.
Liu J, Zhu J-K. 1998. A calcium sensor homolog required for plant salt tolerance. Science 280: 1943-1945.
Małgorzata J, Kabała K. 2015. The role of plasma membrane H+-ATPase in salinity stress of plants. Progress in Botany 76: 77-92.
Newman IA. 2001. Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. Plant, Cell & Environment 24: 1-14.
O'Leary BM, Rico A, McCraw S, Fones HN, Preston GM. 2014. The infiltration-centrifugation technique for extraction of apoplastic fluid from plant leaves using Phaseolus vulgaris as an example. Journal of Visualized Experiments 19: 52113.
Palmgren MG. 2001. Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annual Review of Plant Physiology and Plant Molecular Biology 52: 817-845.
Patel MK, Kumar M, Li W, Luo Y, Burritt DJ, Alkan N, Tran L-SP. 2020. Enhancing salt tolerance of plants: from metabolic reprogramming to exogenous chemical treatments and molecular approaches. Cell 9: 2492.
Qiu Q-S, Guo Y, Dietrich MA, Schumaker KS, Zhu J-K. 2002. Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proceedings of the National Academy of Sciences, USA 99: 8436-8441.
Quintero FJ, Blatt MR, Pardo JM. 2000. Functional conservation between yeast and plant endosomal Na+/H+ antiporters 1. FEBS Letters 471: 224-228.
Raddatz N, Morales de los Ríos L, Lindahl M, Quintero FJ, Pardo JM. 2020. Coordinated transport of nitrate, potassium, and sodium. Frontiers in Plant Science 11: 247.
Raschke K, Monteith JL, Weatherley PE. 1976. How stomata resolve the dilemma of opposing priorities. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 273: 551-560.
Razavizadeh R, Ehsanpour AA, Ahsan N, Komatsu S. 2009. Proteome analysis of tobacco leaves under salt stress. Peptides 30: 1651-1659.
Reyer A, Häßler M, Scherzer S, Huang S, Pedersen JT, Al-Rasheid KAS, Bamberg E, Palmgren M, Dreyer I, Nagel G et al. 2020. Channelrhodopsin-mediated optogenetics highlights a central role of depolarization-dependent plant proton pumps. Proceedings of the National Academy of Sciences, USA 117: 20920-20925.
Riedelsberger J, Miller JK, Valdebenito-Maturana B, Pineros MA, Gonzalez W, Dreyer I. 2021. Plant HKT channels: an updated view on structure, function and gene regulation. International Journal of Molecular Sciences 22: 1892.
Scherzer S, Böhm J, Krol E, Shabala L, Kreuzer I, Larisch C, Bemm F, Al-Rasheid KA, Shabala S, Rennenberg H et al. 2015. Calcium sensor kinase activates potassium uptake systems in gland cells of venus flytraps. Proceedings of the National Academy of Sciences, USA 112: 7309-7314.
Seifikalhor M, Aliniaeifard S, Shomali A, Azad N, Hassani B, Lastochkina O, Li T. 2019. Calcium signaling and salt tolerance are diversely entwined in plants. Plant Signaling & Behavior 14: 1665455.
Shabala S. 2000. Ionic and osmotic components of salt stress specifically modulate net ion fluxes from bean leaf mesophyll. Plant, Cell & Environment 23: 825-837.
Shahzad M, Zörb C, Geilfus C-M, Mühling KH. 2013. Apoplastic Na+ in Vicia faba leaves rises after short-term salt stress and is remedied by silicon. Journal of Agronomy and Crop Science 199: 161-170.
Silva P, Gerós H. 2009. Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange. Plant Signaling & Behavior 4: 718-726.
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.
Subba A, Tomar S, Pareek A, Singla-Pareek SL. 2021. The chloride channels: silently serving the plants. Physiologia Plantarum 171: 688-702.
Sun T-J, Fan L, Yang J, Cao R-Z, Yang C-Y, Zhang J, Wang D-M. 2019. A Glycine max sodium/hydrogen exchanger enhances salt tolerance through maintaining higher Na+ efflux rate and K+/Na+ ratio in Arabidopsis. BMC Plant Biology 19: 469.
Sze H, Chanroj S. 2018. Plant endomembrane dynamics: studies of K+/H+ antiporters provide insights on the effects of pH and ion homeostasis. Plant Physiology 177: 875-895.
Véry A-A, Nieves-Cordones M, Daly M, Khan I, Fizames C, Sentenac H. 2014. Molecular biology of K+ transport across the plant cell membrane: what do we learn from comparison between plant species? Journal of Plant Physiology 171: 748-769.
Voss LJ, Hedrich R, Roelfsema MRG. 2016. Current injection provokes rapid expansion of the guard cell cytosolic volume and triggers Ca2+ signals. Molecular Plant 9: 471-480.
Wang H, Ding Q, Wang H. 2018. A new Na+/H+ antiporter gene KvNHX1 isolated from the halophyte Kosteletzkya virginica improves salt tolerance in transgenic tobacco. Biotechnology & Biotechnological Equipment 32: 1378-1386.
Wang H, Wang H, Shao H, Tang X. 2016. Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Frontiers in Plant Science 7: 67.
Wille AC, Lucas WJ. 1984. Ultrastructural and histochemical studies on guard cells. Planta 160: 129-142.
Wu H. 2018. Plant salt tolerance and Na+ sensing and transport. The Crop Journal 6: 215-225.
Wu H, Li Z. 2019. The importance of Cl− exclusion and vacuolar Cl− sequestration: revisiting the role of Cl− transport in plant salt tolerance. Frontiers in Plant Science 10: 1418.
Wu H, Shabala L, Zhou M, Su N, Wu Q, Ul-Haq T, Zhu J, Mancuso S, Azzarello E, Shabala S. 2019. Root vacuolar Na+ sequestration but not exclusion from uptake correlates with barley salt tolerance. The Plant Journal 100: 55-67.
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.
Xiong TC, Ronzier E, Sanchez F, Corratgé-faillie C, Mazars C, Thibaud J-B. 2014. Imaging long distance propagating calcium signals in intact plant leaves with the BRET-based GFP-aequorin reporter. Frontiers in Plant Science 5: 43.
Yamaguchi T, Aharon GS, Sottosanto JB, Blumwald E. 2005. Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+- and pH-dependent manner. Proceedings of the National Academy of Sciences, USA 102: 16107-16112.
Yang Y, Guo Y. 2018. Unraveling salt stress signaling in plants. Journal of Integrative Plant Biology 60: 796-804.
Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM, Pardo JM. 2002. Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. The Plant Journal 30: 529-539.
Yue Y, Zhang M, Zhang J, Duan L, Li Z. 2012. SOS1 gene overexpression increased salt tolerance in transgenic tobacco by maintaining a higher K+/Na+ ratio. Journal of Plant Physiology 169: 255-261.
Zhou Y, Ding M, Gao S, Yu-Strzelczyk J, Krischke M, Duan X, Leide J, Riederer M, Mueller MJ, Hedrich R et al. 2021a. Optogenetic control of plant growth by a microbial rhodopsin. Nature Plants 7: 144-151.
Zhu J-K. 2002. Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53: 247-273.