Energy costs of salt tolerance in crop plants.
barley and wheat
energy costs
membrane transport
photosynthesis
respiration
root anatomy
salt tolerance
sodium and chloride transport
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
21
12
2018
accepted:
25
03
2019
pubmed:
21
4
2019
medline:
17
12
2020
entrez:
21
4
2019
Statut:
ppublish
Résumé
Agriculture is expanding into regions that are affected by salinity. This review considers the energetic costs of salinity tolerance in crop plants and provides a framework for a quantitative assessment of costs. Different sources of energy, and modifications of root system architecture that would maximize water vs ion uptake are addressed. Energy requirements for transport of salt (NaCl) to leaf vacuoles for osmotic adjustment could be small if there are no substantial leaks back across plasma membrane and tonoplast in root and leaf. The coupling ratio of the H
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1072-1090Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.
Références
Adams P, Nelson DE, Yamada S, Chmara W, Jensen RG, Bohnert HJ, Griffiths H. 1998. Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytologist 138: 171-190.
Alexova R, Nelson CJ, Jacoby RP, Millar AH. 2015. Exposure of barley plants to low Pi leads to rapid changes in root respiration that correlate with specific alterations in amino acid substrates. New Phytologist 206: 696-708.
Amthor JS. 2000. The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Annals of Botany 86: 1-20.
Amthor JS, Bar-Even A, Hanson AD, Millar AH, Stitt M, Sweetlove LJ, Tyerman SD. 2019. Engineering strategies to boost crop productivity by cutting respiratory carbon loss. Plant Cell 31: 297-314.
Asif MA, Schilling RK, Tilbrook J, Brien C, Dowling K, Rabie H, Short L, Trittermann C, Garcia A, Barrett-Lennard EG et al. 2018. Mapping of novel salt tolerance QTL in an Excalibur × Kukri doubled haploid wheat population. Theoretical and Applied Genetics 131: 2179-2196.
Assmann SM, Zeiger E. 1987. Guard cell bioenergetics. In: Zeiger E, Farquhar GD, Cowan IR, eds. Stomatal function. Stanford, CA, USA: Stanford University Press, 163-193.
Barkla BJ, Vera-Estrella R, Camacho-Emiterio J, Pantoja O. 2002. Na+/H+ exchange in the halophyte Mesembryanthemum crystallinum is associated with cellular sites of Na+ storage. Functional Plant Biology 29: 1017-1024.
Bassil E, Tajima H, Liang YC, Ohto M, Ushijima K, Nakano R, Esumi T, Coku A, Belmonte M, Blumwald E. 2011. The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23: 3482-3497.
Bassil E, Zhang S, Gong H, Tajima H, Blumwald E. 2019. Cation specificity of vacuolar NHX-type cation/H+ antiporters. Plant Physiology 179: 616-629.
Beauzamy L, Nakayama N, Boudaoud A. 2014. Flowers under pressure: ins and outs of turgor regulation in development. Annals of Botany 114: 1517-1533.
Bertram R, Gram Pedersen M, Luciani DS, Sherman A. 2006. A simplified model for mitochondrial ATP production. Journal of Theoretical Biology 243: 575-586.
Bijlsma RJ, Lambers H, Kooijman S. 2000. A dynamic whole-plant model of integrated metabolism of nitrogen and carbon. 1. Comparative ecological implications of ammonium-nitrate interactions. Plant and Soil 220: 49-69.
Bloom AJ, Sukrapanna SS, Warner RL. 1992. Root respiration associated with ammonium and nitrate absorption and assimilation by barley. Plant Physiology 99: 1294-1301.
Bonales-Alatorre E, Shabala S, Chen ZH, Pottosin I. 2013. Reduced tonoplast fast-activating and slow-activating channel activity is essential for conferring salinity tolerance in a facultative halophyte, Quinoa. Plant Physiology 162: 940-952.
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.
Bose J, Rodrigo-Moreno A, Shabala S. 2014. ROS homeostasis in halophytes in the context of salinity stress tolerance. Journal of Experimental Botany 65: 1241-1257.
Boursiac Y, Boudet J, Postaire O, Luu DT, Tournaire-Roux C, Maurel C. 2008. Stimulus-induced downregulation of root water transport involves reactive oxygen species-activated cell signalling and plasma membrane intrinsic protein internalization. The Plant Journal 56: 207-218.
Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N, Maurel C. 2005. Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiology 139: 790-805.
Boyer JS, Silk WK, Watt M. 2010. Path of water for root growth. Functional Plant Biology 37: 1105-1116.
Britto DT, Kronzucker HJ. 2006. Futile cycling at the plasma membrane: a hallmark of low-affinity nutrient transport. Trends in Plant Science 11: 529-534.
Britto DT, Kronzucker HJ. 2009. Ussing's conundrum and the search for transport mechanisms in plants. New Phytologist 183: 243-246.
Britto DT, Kronzucker HJ. 2015. Sodium efflux in plant roots: what do we really know? Journal of Plant Physiology 186-187: 1-12.
Buch-Pedersen MJ, Rudashevskaya EL, Berner TS, Venema K, Palmgren MG. 2006. Potassium as an intrinsic uncoupler of the plasma membrane H+-ATPase. Journal of Biological Chemistry 281: 38285-38292.
Byrt CS, Zhao MC, Kourghi M, Bose J, Henderson SW, Qiu JE, Gilliham M, Schultz C, Schwarz M, Ramesh SA et al. 2017. Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant, Cell & Environment 40: 802-815.
Carden DE, Diamond D, Miller AJ. 2001. An improved Na+-selective microelectrode for intracellular measurements in plant cells. Journal of Experimental Botany 52: 1353-1359.
Carden DE, Walker DJ, Flowers TJ, Miller AJ. 2003. Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiology 131: 676-683.
Carillo P. 2018. GABA shunt in durum wheat. Frontiers in Plant Science 9: 100.
Carminati A, Passioura JB, Zarebanadkouki M, Ahmed MA, Ryan PR, Watt M, Delhaize E. 2017. Root hairs enable high transpiration rates in drying soils. New Phytologist 216: 771-781.
Chaumont F, Tyerman SD. 2014. Aquaporins: highly regulated channels controlling plant water relations. Plant Physiology 164: 1600-1618.
Cheeseman JM. 1982. Pump-leak sodium fluxes in low salt corn roots. The Journal of Membrane Biology 70: 157-164.
Cheeseman JM, Bloebaum PD, Wickens LK. 1985. Short term 22Na+ and 42K+ uptake in intact, mid-vegetative plants. Physiologia Plantarum 65: 460-466.
Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S. 2005. Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant, Cell & Environment 28: 1230-1246.
Chen Z-H, Hills A, Bätz U, Amtmann A, Lew VL, Blatt MR. 2012. Systems dynamic modeling of the stomatal guard cell predicts emergent behaviors in transport, signaling, and volume control. Plant Physiology 159: 1235-1251.
Che-Othman MH, Jacoby RP, Millar AH, Taylor NL. 2020. Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress. New Phytologist 225: 1166-1180.
Che-Othman MH, Millar AH, Taylor NL. 2017. Connecting salt stress signalling pathways with salinity-induced changes in mitochondrial metabolic processes in C3 plants. Plant, Cell & Environment 40: 2875-2905.
Choi WG, Toyota M, Kim SH, 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.
Colmenero-Flores JM, Martínez G, Gamba G, Vázquez N, Iglesias DJ, Brumós J, Talón M. 2007. Identification and functional characterization of cation-chloride cotransporters in plants. The Plant Journal 50: 278-292.
Colmer TD, Epstein E, Dvorak J. 1995. Differential solute regulation in leaf blades of various ages in salt-sensitive wheat and a salt-tolerant wheat × Lophopyrum-elongatum (Host) A. Love amphiploid. Plant Physiology 108: 1715-1724.
Cubero-Font P, Maierhofer T, Jaslan J, Rosales Miguel A, Espartero J, Díaz-Rueda P, Müller Heike M, Hürter A-L, Al-Rasheid Khaled AS, Marten I et al. 2016. Silent S-type anion channel subunit SLAH1 gates SLAH3 open for chloride root-to-shoot translocation. Current Biology 26: 2213-2220.
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, Bose J, Stefano G, Deepa JHA, Tester M, Mancuso S, Shabala S. 2011. Assessing the role of root plasma membrane and tonoplast Na/H exchangers in salinity tolerance in wheat: in planta quantification results. Plant, Cell & Environment 34: 947-961.
Cuin TA, Miller AJ, Laurie SA, Leigh RA. 2003. Potassium activities in cell compartments of salt-grown barley leaves. Journal of Experimental Botany 54: 657-661.
Davenport R, James RA, Zakrisson-Plogander A, Tester M, Munns R. 2005. Control of sodium transport in durum wheat. Plant Physiology 137: 807-818.
Davenport RJ, Muñoz-Mayor A, Jha D, Essah PA, Rus A, Tester M. 2007. The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant, Cell & Environment 30: 497-507.
Davenport RJ, Tester M. 2000. A weakly voltage-dependent, nonselective cation channel mediates toxic sodium influx in wheat. Plant Physiology 122: 823-834.
Delfine S, Alvino A, Villani MC, Loreto F. 1999. Restrictions to carbon dioxide conductance and photosynthesis in spinach leaves recovering from salt stress. Plant Physiology 119: 1101-1106.
Del-Saz NF, Florez-Sarasa I, Clemente-Moreno MJ, Mhadhbi H, Flexas J, Fernie AR, Ribas-Carbó M. 2016. Salinity tolerance is related to cyanide-resistant alternative respiration in Medicago truncatula under sudden severe stress. Plant, Cell & Environment 39: 2361-2369.
Del-Saz NF, Ribas-Carbo M, McDonald AE, Lambers H, Fernie AR, Florez-Sarasa I. 2017. An in vivo perspective of the role(s) of the alternative oxidase pathway. Trends in Plant Science 23: 206-219.
Demidchik V, Maathuis FJM. 2007. Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytologist 175: 387-404.
Demidchik V, Shabala S, Isayenkov S, Cuin TA, Pottosin I. 2018. Calcium transport across plant membranes: mechanisms and functions. New Phytologist 220: 49-69.
Demidchik V, Tester M. 2002. Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiology 128: 379-387.
Dietz KJ, Schramm M, Lang B, Lanzl-Schramm A, Durr C, Martinoia E. 1992. Characterization of the epidermis from barley primary leaves: II. The role of the epidermis in ion compartmentation. Planta 187: 431-437.
Faiyue B, Al-Azzawi MJ, Flowers TJ. 2012. A new screening technique for salinity resistance in rice (Oryza sativa L.) seedlings using bypass flow. Plant, Cell & Environment 35: 1099-1108.
Felle HH. 1994. The H+/Cl− symporter in root-hair cells of Sinapsis alba. Plant Physiology 106: 1131-1136.
Ferjani A, Segami S, Horiguchi G, Sakata A, Maeshima M, Tsukaya H. 2012. Regulation of pyrophosphate levels by H+-PPase is central for proper resumption of early plant development. Plant Signaling & Behavior 7: 38-42.
Flam-Shepherd R, Huynh WQ, Coskun D, Hamam AM, Britto DT, Kronzucker HJ. 2018. Membrane fluxes, bypass flows, and sodium stress in rice: the influence of silicon. Journal of Experimental Botany 69: 1679-1692.
Flowers TJ, Glenn EP, Volkov V. 2018. Could vesicular transport of Na+ and Cl− be a feature of salt tolerance in halophytes? Annals of Botany 123: 1-18.
Foster KJ, Miklavcic SJ. 2015. Toward a biophysical understanding of the salt stress response of individual plant cells. Journal of Theoretical Biology 385: 130-142.
Foster KJ, Miklavcic SJ. 2016. Modeling root zone effects on preferred pathways for the passive transport of ions and water in plant roots. Frontiers in Plant Science 7: 914.
Foster KJ, Miklavcic SJ. 2017. A comprehensive biophysical model of ion and water transport in plant roots. I. Clarifying the roles of endodermal barriers in the salt stress response. Frontiers in Plant Science 8: 1326.
Fricke W. 2015. The significance of water co-transport for sustaining transpirational water flow in plants: a quantitative approach. Journal of Experimental Botany 66: 731-739.
Fricke W. 2017. Water transport and energy. Plant, Cell & Environment 40: 977-994.
Fricke W. 2020. Energy costs of salinity tolerance in crop plants: night-time transpiration and growth. New Phytologist 225: 1152-1165.
Fricke W, Leigh RA, Tomos AD. 1994. Concentrations of inorganic and organic solutes in extracts from individual epidermal, mesophyll and bundle-sheath cells of barley leaves. Planta 192:310-316.
Fricke W, Leigh RA, Tomos AD. 1996. The intercellular distribution of vacuolar solutes in the epidermis and mesophyll of barley leaves changes in response to NaCl. Journal of Experimental Botany 47: 1413-1426.
Gaxiola RA, Regmi K, Paez-Valencia J, Pizzio G, Zhang S. 2016. Plant H+-PPases: reversible enzymes with contrasting functions dependent on membrane environment. Molecular Plant 9: 317-319.
Gilliham M, Dayod M, Hocking BJ, Xu B, Conn SJ, Kaiser BN, Leigh RA, Tyerman SD. 2011. Calcium delivery and storage in plant leaves: exploring the link with water flow. Journal of Experimental Botany 62: 2233-2250.
Han Y, Yin SY, Huang L, Wu XL, Zeng JB, Liu XH, Qiu L, Munns R, Chen ZH, Zhang GP. 2018. A sodium transporter HvHKT1;1 confers salt tolerance in barley via regulating tissue and cell ion homeostasis. Plant and Cell Physiology 59: 1976-1989.
He Y, Fu J, Yu C, Wang X, Jiang Q, Hong J, Lu K, Xue G, Yan C, James A. 2015. Increasing cyclic electron flow is related to Na+ sequestration into vacuoles for salt tolerance in soybean. Journal of Experimental Botany 66: 6877-6889.
Hedrich R, Mueller TD, Becker D, Marten I. 2018. Structure and function of TPC1 vacuole SV channel gains shape. Molecular Plant 11: 764-775.
Henderson SW, Dunlevy JD, Wu Y, Blackmore DH, Walker RR, Edwards EJ, Gilliham M, Walker AR. 2018. Functional differences in transport properties of natural HKT1;1 variants influence shoot Na+ exclusion in grapevine rootstocks. New Phytologist 217: 1113-1127.
Hills A, Chen Z-H, Amtmann A, Blatt MR, Lew VL. 2012. OnGuard, a computational platform for quantitative kinetic modeling of guard cell physiology. Plant Physiology 159: 1026-1042.
Honscher C, Mari M, Auffarth K, Bohnert M, Griffith J, Geerts W, van der Laan M, Cabrera M, Reggiori F, Ungermann C. 2014. Cellular metabolism regulates contact sites between vacuoles and mitochondria. Developmental Cell 30: 86-94.
Husain S, von Caemmerer S, Munns R. 2004. Control of salt transport from roots to shoots of wheat in saline soil. Functional Plant Biology 31: 1115-1126.
Isayenkov S, Isner JC, Maathuis FJM. 2010. Vacuolar ion channels: roles in plant nutrition and signalling. FEBS Letters 584: 1982-1988.
Jacoby RP, Che-Othman MH, Millar AH, Taylor NL. 2016. Analysis of the sodium chloride-dependent respiratory kinetics of wheat mitochondria reveals differential effects on phosphorylating and non-phosphorylating electron transport pathways. Plant, Cell & Environment 39: 823-833.
Jacoby RP, Millar AH, Taylor NL. 2013. Investigating the role of respiration in plant salinity tolerance by analyzing mitochondrial proteomes from wheat and a salinity-tolerant Amphiploid (wheat x Lophopyrum elongatum). Journal of Proteome Research 12: 4807-4829.
Jacoby RP, Taylor NL, Millar AH. 2011. The role of mitochondrial respiration in salinity tolerance. Trends in Plant Science 16: 614-623.
James RA, Rivelli AR, Munns R, von Caemmerer S. 2002. Factors affecting CO2 assimilation, leaf injury and growth in salt-stressed durum wheat. Functional Plant Biology 29: 1393-1403.
Janicka-Russak M, Kabala K, Wdowikowska A, Klobus G. 2013. Modification of plasma membrane proton pumps in cucumber roots as an adaptation mechanism to salt stress. Journal of Plant Physiology 170: 915-922.
Julkowska MM, Testerink C. 2015. Tuning plant signaling and growth to survive salt. Trends in Plant Science 20: 586-59.
Kerkeb L, Venema K, Donaire JP, Rodríguez-Rosales MP. 2002. Enhanced H+/ATP coupling ratio of H+-ATPase and increased 14-3-3 protein content in plasma membrane of tomato cells upon osmotic shock. Physiologia Plantarum 116: 37-41.
Khadilkar AS, Yadav UP, Salazar C, Shulaev V, Paez-Valencia J, Pizzio GA, Gaxiola RA, Ayre BG. 2016. Constitutive and companion cell-specific overexpression of AVP1, encoding a proton-pumping pyrophosphatase, enhances biomass accumulation, phloem loading, and long-distance transport. Plant Physiology 170: 401-414.
Kooijman S, Troost TA. 2007. Quantitative steps in the evolution of metabolic organisation as specified by the Dynamic Energy Budget theory. Biological Reviews 82: 113-142.
Kourghi M, Nourmohammadi S, Pei JXV, Qiu JE, McGaughey S, Tyerman SD, Byrt CS, Yool AJ. 2017. Divalent cations regulate the ion conductance properties of diverse classes of aquaporins. International Journal of Molecular Sciences 18: 19.
Kramer DM, Evans JR. 2011. The importance of energy balance in improving photosynthetic productivity. Plant Physiology 155: 70-78.
Krasensky J, Jonak C. 2012. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. Journal of Experimental Botany 63: 1593-1608.
Kriegel A, Andrés Z, Medzihradszky A, Krüger F, Scholl S, Delang S, Patir-Nebioglu MG, Gute G, Yang H, Murphy AS et al. 2015. Job sharing in the endomembrane system: vacuolar acidification requires the combined activity of V-ATPase and V-PPase. Plant Cell 27: 3383-3396.
Krishnamurthy P, Ranathunge K, Nayak S, Schreiber L, Mathew MK. 2011. Root apoplastic barriers block Na+ transport to shoots in rice (Oryza sativa L.). Journal of Experimental Botany 62: 4215-4228.
Kronzucker HJ, Britto DT. 2011. Sodium transport in plants: a critical review. New Phytologist 189: 54-81.
Kurimoto K, Day DA, Lambers H, Noguchi K. 2004. Effect of respiratory homeostasis on plant growth in cultivars of wheat and rice. Plant, Cell & Environment 27: 853-862.
Leigh R, Tomos A. 1993. Ion distribution in cereal leaves: pathways and mechanisms. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 341: 75-86.
Li B, Tester M, Gilliham M. 2017. Chloride on the move. Trends in Plant Science 22: 236-248.
Li L, Nelson CJ, Trösch J, Castleden I, Huang S, Millar AH. 2017. Protein degradation rate in Arabidopsis thaliana leaf growth and development. Plant Cell 29: 207-228.
Li WYF, Wong FL, Tsai SN, Phang TH, Shao GH, Lam HM. 2006. Tonoplast-located GmCLC1 and GmNHX1 from soybean enhance NaCl tolerance in transgenic bright yellow (BY)-2 cells. Plant, Cell & Environment 29: 1122-1137.
Löfke C, Dünser K, Scheuring D, Kleine-Vehn J. 2015. Auxin regulates SNARE-dependent vacuolar morphology restricting cell size. eLife 4: e05868.
Lorenzen I, Aberle T, Plieth C. 2004. Salt stress-induced chloride flux: a study using transgenic Arabidopsis expressing a fluorescent anion probe. The Plant Journal 38: 539-544.
Malagoli P, Britto DT, Schulze LM, Kronzucker HJ. 2008. Futile Na+ cycling at the root plasma membrane in rice (Oryza sativa L.): kinetics, energetics, and relationship to salinity tolerance. Journal of Experimental Botany 59: 4109-4117.
Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L. 2015. Aquaporins in plants. Physiological Reviews 95: 1321-1358.
McGaughey SA, Qiu J, Tyerman SD, Byrt CS. 2018. Regulating root aquaporin function in response to changes in salinity. Annual Plant Reviews online. doi: 10.1002/9781119312994.apr0626.
Millar AH, Atkin OK, Menz RI, Henry B, Farquhar G, Day DA. 1998. Analysis of respiratory chain regulation in roots of soybean seedlings. Plant Physiology 117: 1083-1093.
Millar AH, Whelan J, Soole KL, Day DA. 2011. Organization and regulation of mitochondrial respiration in plants. Annual Reviews of Plant Biology 62: 79-104.
Miller GAD, Suzuki N, Ciftci-Yilmaz S, Mittler RON. 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33: 453-467.
Munns R. 2002. Comparative physiology of salt and water stress. Plant, Cell & Environment 25: 239-250.
Munns R, Gilliham M. 2015. Salinity tolerance of crops - what is the cost? New Phytologist 208: 668-673.
Munns R, James RA, Xu B, Athman A, Conn SJ, Jordans C, Byrt CS, Hare RA, Tyerman SD, Tester M et al. 2012. Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nature Biotechnology 30: 360-364.
Munns R, Passioura JB, Colmer TD, Byrt CS. 2020. Osmotic adjustment and energy limitations to plant growth in saline soil. New Phytologist 225: 1091-1096.
Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology 59: 651-681.
Nestler J, Keyes SD, Wissuwa M. 2016. Root hair formation in rice (Oryza sativa L.) differs between root types and is altered in artificial growth conditions. Journal of Experimental Botany 67: 3699-3708.
Nguyen CT, Agorio A, Jossier M, Depre S, Thomine S, Filleur S. 2016. Characterization of the chloride channel-like, AtCLCg, involved in chloride tolerance in Arabidopsis thaliana. Plant and Cell Physiology 57: 764-775.
Nunes-Nesi A, Araújo WL, Obata T, Fernie AR. 2013. Regulation of the mitochondrial tricarboxylic acid cycle. Current Opinion in Plant Biology 16: 335-343.
Palmgren MG. 2001. Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annual Review of Plant Physiology and Plant Molecular Biology 52: 817-845.
Pedersen JT, Kanashova T, Dittmar G, Palmgren M. 2018. Isolation of native plasma membrane H+-ATPase (Pma1p) in both the active and basal activation states. FEBS Open Bio 8: 774-783.
Peng C, Uygun S, Shiu SH, Last RL. 2015. The impact of the branched-chain ketoacid dehydrogenase complex on amino acid homeostasis in Arabidopsis. Plant Physiology 169: 1807-1820.
Percey WJ, McMinn A, Bose J, Breadmore MC, Guijt RM, Shabala S. 2016. Salinity effects on chloroplast photosystem II performance in glycophytes and halophytes. Functional Plant Biology 43: 1003-1015.
Perez V, Wherrett T, Shabala S, Muniz J, Dobrovinskaya O, Pottosin I. 2008. Homeostatic control of slow vacuolar channels by luminal cations and evaluation of the channel-mediated tonoplast Ca2+ fluxes in situ. Journal of Experimental Botany 59: 3845-3855.
Picco A, Mund M, Ries J, Nédélec F, Kaksonen M. 2015. Visualizing the functional architecture of the endocytic machinery. eLife 4: e04535.
Pitman MG, Courtice AC, Lee B. 1968. Comparison of potassium and sodium uptake by barley roots at high and low salt status. Australian Journal of Biological Sciences 21: 871-881.
Pizzio GA, Paez-Valencia J, Khadilkar AS, Regmi K, Patron-Soberano A, Zhang S, Sanchez-Lares J, Furstenau T, Li J, Sanchez-Gomez C et al. 2015. Arabidopsis type I proton-pumping pyrophosphatase expresses strongly in phloem, where it is required for pyrophosphate metabolism and photosynthate partitioning. Plant Physiology 167: 1541-1553.
Pottosin I, Dobrovinskaya O. 2018. Two-pore cation (TPC) channel: not a shorthanded one. Functional Plant Biology 45: 83-92.
Pottosin I, Schnknecht G. 2007. Vacuolar calcium channels. Journal of Experimental Botany 58: 1559-1569.
Prinz WA. 2014. Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. Journal of Cell Biology 205: 759-769.
Rahnama A, Munns R, Poustini K, Watt M. 2011. A screening method to identify genetic variation in root growth response to a salinity gradient. Journal of Experimental Botany 62: 69-77.
Qiu J, Henderson SW, Tester M, Roy SJ, Gilliham M. 2017. SLAH1, a homologue of the slow type anion channel SLAC1, modulates shoot Cl− accumulation and salt tolerance in Arabidopsis thaliana. Journal of Experimental Botany 68: 4495-4505.
Raven JA. 1985. Regulation of pH and generation of osmolarity in vascular plants - a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytologist 101: 25-77.
Rawson H. 1986. Gas exchange and growth in wheat and barley grown in salt. Functional Plant Biology 13: 475-489.
Rawson HM, Gardner PA, Long MJ. 1987. Sources of variation in specific leaf-area in wheat grown at high-temperature. Australian Journal of Plant Physiology 14: 287-298.
Reinhardt DH, Rost TL. 1995. On the correlation of primary root growth and tracheary element size and distance from the tip in cotton seedlings grown under salinity. Environmental and Experimental Botany 35: 575-588.
Ribas-Carbo M, Taylor NL, Giles L, Busquets S, Finnegan PM, Day DA, Lambers H, Medrano H, Berry JA, Flexas J. 2005. Effects of water stress on respiration in soybean leaves. Plant Physiology 139: 466-473.
Rich SM, Watt M. 2013. Soil conditions and cereal root system architecture: review and considerations for linking Darwin and Weaver. Journal of Experimental Botany 64: 1193-1208.
Rivelli AR, James RA, Munns R, Condon AG. 2002. Effect of salinity on water relations and growth of wheat genotypes with contrasting sodium uptake. Functional Plant Biology 29: 1065-1074.
Sade N, Galle A, Flexas J, Lerner S, Peleg G, Yaaran A, Moshelion M. 2014. Differential tissue-specific expression of NtAQP1 in Arabidopsis thaliana reveals a role for this protein in stomatal and mesophyll conductance of CO2 under standard and salt-stress conditions. Planta 239: 357-366.
Saleh L, Plieth C. 2013. A9C sensitive Cl−-accumulation in A. thaliana root cells during salt stress is controlled by internal and external calcium. Plant Signaling & Behavior 8: e24259.
Scafaro AP, Negrini ACA, O'Leary B, Rashid FAA, Hayes L, Fan YZ, Zhang Y, Chochois V, Badger MR, Millar AH et al. 2017. The combination of gas-phase fluorophore technology and automation to enable high-throughput analysis of plant respiration. Plant Methods 13: 13.
Scheurwater I, Dunnebacke M, Eising R, Lambers H. 2000. Respiratory costs and rate of protein turnover in the roots of a fast-growing (Dactylis glomerata L.) and a slow-growing (Festuca ovina L.) grass species. Journal of Experimental Botany 51: 1089-1097.
Schilling RK, Tester M, Marschner P, Plett DC, Roy SJ. 2017. AVP1: one protein, many roles. Trends in Plant Science 22: 154-162.
Schneider HM, Postma JA, Wojciechowski T, Kuppe C, Lynch JP. 2017. Root cortical senescence improves growth under suboptimal availability of N, P, and K. Plant Physiology 174: 2333-2347.
Selinski J, Scheibe R, Day DA, Whelan JB. 2018. Alternative oxidase is positive for plant performance. Trends in Plant Science 23: 588-597.
Shabala S, Shabala L, Barcelo J, Poschenrieder C. 2014. Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding. Plant, Cell & Environment 37: 2216-2233.
Shabala S, Chen G, Chen Z-H, Pottosin I. 2020. The energy cost of the tonoplast futile sodium leak. New Phytologist 225: 1105-1110.
Shabala S, Shabala L, Van Volkenburgh E. 2003. Effect of calcium on root development and root ion fluxes in salinised barley seedlings. Functional Plant Biology 30: 507-514.
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.
Shelden MC, Roessner U, Sharp RE, Tester M, Bacic A. 2013. Genetic variation in the root growth response of barley genotypes to salinity stress. Functional Plant Biology 40: 516-530.
Shi H, Lee B-H, Wu S-J, Zhu J-K. 2003. Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotechnology 21: 81-85.
Shi HZ, Quintero FJ, Pardo JM, Zhu JK. 2002. The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14: 465-477.
Shi L-X, Theg SM. 2013. Energetic cost of protein import across the envelope membranes of chloroplasts. Proceedings of the National Academy of Sciences, USA 110: 930-935.
Siedow JN, Day DA. 2000. Respiration and photorespiration. In: Buchanan BB, Gruissem W, Jones RL, eds. Biochemistry and molecular biology of plants. Rockville, MD, USA: American Society of Plant Physiologists, 676-728.
Skerrett M, Tyerman SD. 1994. A channel that allows inwardly directed fluxes of anions in protoplasts derived from wheat roots. Planta 192: 295-305.
Smith CA, Melino VJ, Sweetman C, Soole KL. 2009. Manipulation of alternative oxidase can influence salt tolerance in Arabidopsis thaliana. Physiologia Plantarum 137: 459-472.
Snapp SS, Shennan C. 1992. Effects of salinity on root growth and death dynamics of tomato, Lycopersicon esculentum Mill. New Phytologist 121: 71-79.
Sotta N, Fujiwara T. 2017. Preparing thin cross sections of Arabidopsis roots without embedding. BioTechniques 63: 281-283.
Teakle NL, Tyerman SD. 2010. Mechanisms of Cl− transport contributing to salt tolerance. Plant, Cell & Environment 33: 566-589.
Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ. 2008. Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biology 6: e7.
Tyerman SD, Oats P, Gibbs J, Dracup M, Greenway H. 1989. Turgor-volume regulation and cellular water relations of Nicotiana tabacum roots grown in high salinities. Australian Journal of Plant Physiology 16: 517-531.
Tyerman SD, Skerrett M, Garrill A, Findlay GP, Leigh RA. 1997. Pathways for the permeation of Na+ and Cl− into protoplasts derived from the cortex of wheat roots. Journal of Experimental Botany 48: 459-480.
Ussing HH. 1947. Interpretation of the exchange of radio-sodium in isolated muscle. Nature 160: 262.
Ussing HH. 1994. Does active transport exist? The Journal of Membrane Biology 137: 91-98.
Van Den Boogaard R, Goubitz S, Veneklaas EJ, Lambers H. 1996. Carbon and nitrogen economy of four Triticum aestivum cultivars differing in relative growth rate and water use efficiency. Plant, Cell & Environment 19: 998-1004.
Vanlerberghe GC. 2013. Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. International Journal of Molecular Sciences 14: 6805-6847.
Varney GT, Canny MJ, Wang XL, McCully ME. 1991. The branch roots of Zea. I. First order branches, their number, sizes and division into classes. Annals of Botany 67: 357-364.
Venema K, Palmgren MG. 1995. Metabolic modulation of transport coupling ratio in yeast plasma-membrane H+-ATPase. Journal of Biological Chemistry 270: 19659-19667.
Volkov V. 2015. Salinity tolerance in plants. Quantitative approach to ion transport starting from halophytes and stepping to genetic and protein engineering for manipulating ion fluxes. Frontiers in Plant Science 6: 25.
Walker BJ, VanLoocke A, Bernacchi CJ, Ort DR. 2016. The costs of photorespiration to food production now and in the future. Annual Review of Plant Biology 67: 107-129.
Wang S-M, Zhang J-L, Flowers TJ. 2007. Low-affinity Na+ uptake in the halophyte Suaeda maritima. Plant Physiology 145: 559-571.
Wang Y, Hills A, Vialet-Chabrand S, Papanatsiou M, Griffiths H, Rogers S, Lawson T, Lew VL, Blatt MR. 2017. Unexpected connections between humidity and ion transport discovered using a model to bridge guard cell-to-leaf scales. Plant Cell 29: 2921-2939.
Watt M, Magee LJ, McCully ME. 2008. Types, structure and potential for axial water flow in the deepest roots of field-grown cereals. New Phytologist 178: 135-146.
Watt M, Schneebeli K, Dong P, Wilson IW. 2009. The shoot and root growth of Brachypodium and its potential as a model for wheat and other cereal crops. Functional Plant Biology 36: 960-969.
Wegner LH. 2015. A thermodynamic analysis of the feasibility of water secretion into xylem vessels against a water potential gradient. Functional Plant Biology 42: 828-835.
Wegner LH. 2017. Cotransport of water and solutes in plant membranes: the molecular basis, and physiological functions. Aims Biophysics 4: 192-209.
Wen Z, Tyerman S, Dechorgnat J, Ovchinnikova E, Dhugga K, Kaiser BN. 2017. Maize NPF6 proteins are homologs of Arabidopsis CHL1 that are selective for both nitrate and chloride. Plant Cell 29: 2581-2596.
Weston LA, Ryan PR, Watt M. 2012. Mechanisms for cellular transport and release of allelochemicals from plant roots into the rhizosphere. Journal of Experimental Botany 63: 3445-3454.
Wingler A, Lea PJ, Quick WP, Leegood RC. 2000. Photorespiration: metabolic pathways and their role in stress protection. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 355: 1517-1529.
Wu H, Carvalho P, Voeltz GK. 2018a. Here, there, and everywhere: the importance of ER membrane contact sites. Science 361: 640.
Wu HH, Shabala L, Azzarello E, Huang YQ, Pandolfi C, Su NN, Wu Q, Cai SG, Bazihizina N, Wang L et al. 2018b. Na+ extrusion from the cytosol and tissue-specific Na+ sequestration in roots confer differential salt stress tolerance between durum and bread wheat. Journal of Experimental Botany 69: 3987-4001.
Wu HH, Shabala L, Liu XH, Azzarello E, Zhou M, Pandolfi C, Chen ZH, Bose J, Mancuso S, Shabala S. 2015. Linking salinity stress tolerance tissue-specific Na+ sequestration in wheat roots. Frontiers in Plant Science 6: 13.
Xu B, Hrmova M, Gilliham M. 2019. High affinity Na+ transport by wheat HKT1;5 is blocked by K+. BioRxiv. doi: 10.1101/280453.
Yeo AR, Yeo ME, Flowers TJ. 1987. The Contribution of an apoplastic pathway to sodium uptake by rice roots in saline conditions. Journal of Experimental Botany 38: 1141-1153.
Zhu M, Zhou M, Shabala L, Shabala S. 2017. Physiological and molecular mechanisms mediating xylem Na+ loading in barley in the context of salinity stress tolerance. Plant, Cell & Environment 40: 1009-1020.
Zolla G, Heimer YM, Barak S. 2010. Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots. Journal of Experimental Botany 61: 211-224.