Skip to main content
SpringerLink
Log in

Role of Cation/Proton Exchangers in Abiotic Stress Signaling and Stress Tolerance in Plants

  • Chapter
Elucidation of Abiotic Stress Signaling in Plants

Abstract

The generation of cytosolic Ca2+ signals is an early response in plants to many environmental stresses. Ca2+ transporters play a critical role in the generation of these signals and the maintenance of cellular Ca2+ homeostasis. A major class of Ca2+ transporter is the Ca2+/H+ exchanger (CAX), which is almost ubiquitous throughout every domain of life but has been best characterised in higher plants. CAX transporters of Arabidopsis thaliana have been particularly well studied and have been shown to have diverse roles in vacuolar sequestration of Ca2+ and other cations, which provide an important mechanism for ion tolerance. Recent genetic studies of CAX transporters from various plant species indicate that these proteins may also play a role in the response to specific abiotic stresses. Altered sensitivity of CAX mutant plants to abiotic stresses such as salt stress and cold stress has been observed. The potential role of CAX-type cation transporters in environmental stress response is reviewed here. In particular, we discuss whether these high-capacity, low-affinity Ca2+ transporters play a central role in modulating Ca2+ signals in response to abiotic stresses.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agarwal M, Hao YJ, Kapoor A, Dong CH, Fujii H, Zheng XW, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645

    Article  CAS  PubMed  Google Scholar 

  • Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, Chory J, Schroeder JI (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338–2342

    Article  CAS  PubMed  Google Scholar 

  • Athanasiou K, Dyson BC, Webster RE, Johnson GN (2010) Dynamic acclimation of photosynthesis increases plant fitness in changing environments. Plant Physiol 152:366–373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baisakh N, RamanaRao MV, Rajasekaran K, Subudhi P, Janda J, Galbraith D, Vanier C, Pereira A (2012) Enhanced salt stress tolerance of rice plants expressing a vacuolar H+-ATPase subunit c1 (SaVHAc1) gene from the halophyte grass Spartina alterniflora Loisel. Plant Biotechnol J 10:453–464

    Article  CAS  PubMed  Google Scholar 

  • Barkla BJ, Hirschi KD, Pittman JK (2008) Exchangers man the pumps: Functional interplay between proton pumps and proton-coupled Ca2+ exchangers. Plant Signal Behav 3:354–356

    Article  PubMed Central  PubMed  Google Scholar 

  • Baxter I, Tchieu J, Sussman MR, Boutry M, Palmgren MG, Gribskov M, Harper JF, Axelsen KB (2003) Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol 132:618–628

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bickerton PD, Pittman JK (2012) Calcium signaling in plants. In: eLS. Wiley, New York

    Google Scholar 

  • Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD, Twell D, Sze H (2006) Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiol 140:1151–1168

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bonza MC, De Michelis MI (2011) The plant Ca2+-ATPase repertoire: biochemical features and physiological functions. Plant Biol (Stuttg) 13:421–430

    Article  CAS  Google Scholar 

  • Bradshaw HD (2005) Mutations in CAX1 produce phenotypes characteristic of plants tolerant to serpentine soils. New Phytol 167:81–88

    Article  CAS  PubMed  Google Scholar 

  • Case RM, Eisner D, Gurney A, Jones O, Muallem S, Verkhratsky A (2007) Evolution of calcium homeostasis: From birth of the first cell to an omnipresent signaling system. Cell Calcium 42:345–350

    Article  CAS  PubMed  Google Scholar 

  • Catalá R, Santos E, Alonso JM, Ecker JR, Martínez-Zapater JM, Salinas J (2003) Mutations in the Ca2+/H+ transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940–2951

    Article  PubMed Central  PubMed  Google Scholar 

  • Cheng NH, Hirschi KD (2003) Cloning and characterization of CXIP1, a novel PICOT domain-containing Arabidopsis protein that associates with CAX1. J Biol Chem 278:6503–6509

    Article  CAS  PubMed  Google Scholar 

  • Cheng NH, Pittman JK, Shigaki T, Hirschi KD (2002) Characterization of CAX4, an Arabidopsis H+/cation antiporter. Plant Physiol 128:1245–1254

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheng NH, Pittman JK, Barkla BJ, Shigaki T, Hirschi KD (2003) The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15:347–364

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheng NH, Liu JZ, Nelson RS, Hirschi KD (2004a) Characterization of CXIP4, a novel Arabidopsis protein that activates the H+/Ca2+ antiporter, CAX1. FEBS Lett 559:99–106

    Article  CAS  PubMed  Google Scholar 

  • Cheng NH, Pittman JK, Zhu JK, Hirschi KD (2004b) The protein kinase SOS2 activates the Arabidopsis H+/Ca2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279:2922–2926

    Article  CAS  PubMed  Google Scholar 

  • Cheng NH, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, Lahner B, Salt DE, Hirschi KD (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol 138:2048–2060

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cho D, Villiers F, Kroniewicz L, Lee S, Seo YJ, Hirschi KD, Leonhardt N, Kwak JM (2012) Vacuolar CAX1 and CAX3 influence auxin transport in guard cells via regulation of apoplastic pH. Plant Physiol 160:1293–1302

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Conn SJ, Gilliham M, Athman A, Schreiber AW, Baumann U, Moller I, Cheng NH, Stancombe MA, Hirschi KD, Webb AAR, Burton R, Kaiser BN, Tyerman SD, Leigh RA (2011) Cell-specific vacuolar calcium storage mediated by CAX1 regulates apoplastic calcium concentration, gas exchange, and plant productivity in Arabidopsis. Plant Cell 23:240–257

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Connorton JM, Webster RE, Cheng NH, Pittman JK (2012) Knockout of multiple Arabidopsis Cation/H+ exchangers suggests isoform-specific roles in metal stress response, germination and seed mineral nutrition. PLoS One 7:e47455

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Denis V, Cyert MS (2002) Internal Ca2+ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol 156:29–34

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620

    Article  CAS  PubMed  Google Scholar 

  • Edmond C, Shigaki T, Ewert S, Nelson M, Connorton J, Chalova V, Noordally Z, Pittman JK (2009) Comparative analysis of CAX2-like cation transporters indicates functional and regulatory diversity. Biochem J 418:145–154

    Article  CAS  PubMed  Google Scholar 

  • Emery L, Whelan S, Hirschi KD, Pittman JK (2012) Protein phylogenetic analysis of Ca2+/cation antiporters and insights into their evolution in plants. Front Plant Sci 3:1

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Felle HH (2001) pH: Signal and messenger in plant cells. Plant Biol 3:577–591

    Article  CAS  Google Scholar 

  • Gao DJ, Knight MR, Trewavas AJ, Sattelmacher B, Plieth C (2004) Self-reporting Arabidopsis expressing pH and Ca2+ indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol 134:898–908

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Geisler-Lee J, O’Toole N, Ammar R, Provart NJ, Millar AH, Geisler M (2007) A predicted interactome for Arabidopsis. Plant Physiol 145:317–329

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guttery DS, Pittman JK, Frenal K, Poulin B, McFarlane LR, Slavic K, Wheatley SP, Soldati-Favre D, Krishna S, Tewari R, Staines HM (2013) The Plasmodium berghei Ca2+/H+ exchanger, PbCAX, is essential for tolerance to environmental Ca2+ during sexual development. PLoS Pathog 9:e1003191

    Article  PubMed Central  PubMed  Google Scholar 

  • Han N, Lan WJ, He X, Shao Q, Wang BS, Zhao XJ (2012) Expression of a Suaeda salsa vacuolar H+/Ca2+ transporter gene in Arabidopsis contributes to physiological changes in salinity. Plant Mol Biol Rep 30:470–477

    Article  CAS  Google Scholar 

  • Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: Altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hirschi K (2001) Vacuolar H+/Ca2+ transport: who’s directing the traffic? Trends Plant Sci 6:100–104

    Article  CAS  PubMed  Google Scholar 

  • Hirschi KD, Zhen RG, Cunningham KW, Rea PA, Fink GR (1996) CAX1, an H+/Ca2+ antiporter from Arabidopsis. Proc Natl Acad Sci U S A 93:8782–8786

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ho C-L, Wu Y, H-B S, Provart N, Geisler M (2012) A predicted protein interactome for rice. Rice (N Y) 5:15

    Google Scholar 

  • Huda KMK, Banu MSA, Tuteja R, Tuteja N (2013) Global calcium transducer P-type Ca2+-ATPases open new avenues for agriculture by regulating stress signaling. J Exp Bot 64:3099–3109

    Article  CAS  PubMed  Google Scholar 

  • Jammes F, Hu H-C, Villiers F, Bouten R, Kwak JM (2011) Calcium-permeable channels in plant cells. FEBS J 278:4262–4276

    Article  CAS  PubMed  Google Scholar 

  • Ji HT, Pardo JM, Batelli G, Van Oosten MJ, Bressan RA, Li X (2013) The salt overly sensitive (SOS) pathway: established and emerging roles. Mol Plant 6:275–286

    Article  CAS  PubMed  Google Scholar 

  • Kamiya T, Akahori T, Maeshima M (2005) Expression profile of the genes for rice cation/H+ exchanger family and functional analysis in yeast. Plant Cell Physiol 46:1735–1740

    Article  CAS  PubMed  Google Scholar 

  • Kamiya T, Akahori T, Ashikari M, Maeshima M (2006) Expression of the vacuolar Ca2+/H+ exchanger, OsCAX1a, in rice: Cell and age specificity of expression, and enhancement by Ca2+. Plant Cell Physiol 47:96–106

    Article  CAS  PubMed  Google Scholar 

  • Kamiya T, Yamagami M, Hirai MY, Fujiwara T (2012) Establishment of an in planta magnesium monitoring system using CAX3 promoter-luciferase in Arabidopsis. J Exp Bot 63:355–363

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim TH, Bohmer M, Hu HH, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: Advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koren’kov V, Park S, Cheng NH, Sreevidya C, Lachmansingh J, Morris J, Hirschi K, Wagner GJ (2007) Enhanced Cd2+-selective root-tonoplast-transport in tobaccos expressing Arabidopsis cation exchangers. Planta 225:403–411

    Article  PubMed  Google Scholar 

  • Krebs M, Beyhl D, Gorlich E, Al-Rasheid KAS, Marten I, Stierhof Y-D, Hedrich R, Schumacher K (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc Natl Acad Sci U S A 107:3251–3256

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Laanemets K, Brandt B, Li J, Merilo E, Wang Y-F, Keshwani MM, Taylor SS, Kollist H, Schroeder JI (2013) Calcium-dependent and -independent stomatal signaling network and compensatory feedback control of stomatal opening via Ca2+ sensitivity priming. Plant Physiol 163:504–513

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lager I, Andreasson O, Dunbar TL, Andreasson E, Escobar MA, Rasmusson AG (2010) Changes in external pH rapidly alter plant gene expression and modulate auxin and elicitor responses. Plant Cell Environ 33:1513–1528

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lalonde S, Sero A, Pratelli R, Pilot G, Chen J, Sardi MI, Parsa SA, Kim D-Y, Acharya BR, Stein EV, Hu H-C, Villiers F, Takeda K, Yang Y, Han YS, Schwacke R, Chiang W, Kato N, Loque D, Assmann SM, Kwak JM, Schroeder JI, Rhee SY, Frommer WB (2010) A membrane protein/signaling protein interaction network for Arabidopsis version AMPv2. Front Physiol 1:24–24

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16:596–615

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li S, Ehrhardt DW, Rhee SY (2006) Systematic analysis of Arabidopsis organelles and a protein localization database for facilitating fluorescent tagging of full-length Arabidopsis proteins. Plant Physiol 141:527–539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lindberg S, Kader MA, Yemelyanov V (2012) Calcium signaling in plant cells under environmental stress. In: Prasad MNV, Ahmad P (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 325–360

    Chapter  Google Scholar 

  • Liu T-Y, Aung K, Tseng C-Y, Chang T-Y, Chen Y-S, Chiou T-J (2011) Vacuolar Ca2+/H+ transport activity is required for systemic phosphate homeostasis involving shoot-to-root signaling in Arabidopsis. Plant Physiol 156:1176–1189

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Luo GZ, Wang HW, Huang J, Tian AG, Wang YJ, Zhang JS, Chen SY (2005) A putative plasma membrane cation/proton antiporter from soybean confers salt tolerance in Arabidopsis. Plant Mol Biol 59:809–820

    Article  CAS  PubMed  Google Scholar 

  • Maathuis FJM, Filatov V, Herzyk P, Krijger GC, Axelsen KB, Chen SX, Green BJ, Li Y, Madagan KL, Sanchez-Fernandez R, Forde BG, Palmgren MG, Rea PA, Williams LE, Sanders D, Amtmann A (2003) Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. Plant J 35:675–692

    Article  CAS  PubMed  Google Scholar 

  • Manohar M, Shigaki T, Hirschi KD (2011) Plant cation/H+ exchangers (CAXs): biological functions and genetic manipulations. Plant Biol 13:561–569

    Article  CAS  PubMed  Google Scholar 

  • Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJM, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667

    Article  PubMed Central  PubMed  Google Scholar 

  • McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294

    Article  CAS  PubMed  Google Scholar 

  • McAinsh MR, Brownlee C, Hetherington AM (1992) Visualising changes in cytosolic-free Ca2+ during the response of stomatal guard cells to abscisic acid. Plant Cell 4:1113–1122

    PubMed Central  CAS  PubMed  Google Scholar 

  • McAinsh MR, Webb AAR, Taylor JE, Hetherington AM (1995) Stimulus-induced oscillations in guard cell cytosolic-free calcium. Plant Cell 7:1207–1219

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mei H, Zhao J, Pittman JK, Lachmansingh J, Park S, Hirschi KD (2007) In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1. J Exp Bot 58:3419–3427

    Article  CAS  PubMed  Google Scholar 

  • Mei H, Cheng NH, Zhao J, Park P, Escareno RA, Pittman JK, Hirschi KD (2009) Root development under metal stress in Arabidopsis thaliana requires the H+/cation antiporter CAX4. New Phytol 183:95–105

    Article  CAS  PubMed  Google Scholar 

  • Morris J, Hawthorne KM, Hotze T, Abrams SA, Hirschi KD (2008) Nutritional impact of elevated calcium transport activity in carrots. Proc Natl Acad Sci U S A 105:1431–1435

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Narsai R, Castleden I, Whelan J (2010) Common and distinct organ and stress responsive transcriptomic patterns in Oryza sativa and Arabidopsis thaliana. BMC Plant Biol 10

    Google Scholar 

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

    Article  CAS  PubMed  Google Scholar 

  • O’Malley RC, Ecker JR (2010) Linking genotype to phenotype using the Arabidopsis unimutant collection. Plant J 61:928–940

    Article  PubMed  Google Scholar 

  • Park S, Cheng NH, Pittman JK, Yoo KS, Park J, Smith RH, Hirschi KD (2005) Increased calcium levels and prolonged shelf life in tomatoes expressing Arabidopsis H+/Ca2+ transporters. Plant Physiol 139:1194–1206

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Patel RV, Nahal HK, Breit R, Provart NJ (2012) BAR expressolog identification: expression profile similarity ranking of homologous genes in plant species. Plant J 71:1038–1050

    Article  CAS  PubMed  Google Scholar 

  • Peiter E (2011) The plant vacuole: Emitter and receiver of calcium signals. Cell Calcium 50:120–128

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK (2011) Vacuolar Ca2+ uptake. Cell Calcium 50:139–146

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK (2012) Multiple transport pathways for mediating intracellular pH homeostasis: the contribution of H+/ion exchangers. Front Plant Sci 3:11

    Article  PubMed Central  PubMed  Google Scholar 

  • Pittman JK, Hirschi KD (2001) Regulation of CAX1, an Arabidopsis Ca2+/H+ antiporter. Identification of an N-terminal autoinhibitory domain. Plant Physiol 127:1020–1029

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pittman JK, Shigaki T, Cheng NH, Hirschi KD (2002a) Mechanism of N-terminal autoinhibition in the Arabidopsis Ca2+/H+ antiporter CAX1. J Biol Chem 277:26452–26459

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Sreevidya CS, Shigaki T, Ueoka-Nakanishi H, Hirschi KD (2002b) Distinct N-terminal regulatory domains of Ca2+/H+ antiporters. Plant Physiol 130:1054–1062

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pittman JK, Shigaki T, Marshall JL, Morris JL, Cheng NH, Hirschi KD (2004) Functional and regulatory analysis of the Arabidopsis thaliana CAX2 cation transporter. Plant Mol Biol 56:959–971

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Shigaki T, Hirschi KD (2005) Evidence of differential pH regulation of the Arabidopsis vacuolar Ca2+/H+ antiporters CAX1 and CAX2. FEBS Lett 579:2648–2656

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Edmond C, Sunderland PA, Bray CM (2009) A cation-regulated and proton gradient-dependent cation transporter from Chlamydomonas reinhardtii has a role in calcium and sodium homeostasis. J Biol Chem 284:525–533

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Bonza MC, De Michelis MI (2011) Ca2+ pumps and Ca2+ antiporters in plant development. In: Geisler M, Venema K (eds) Transporters and pumps in plant signaling, signaling and communication in plants, vol 7. Springer, Heidelberg, pp 133–161

    Chapter  Google Scholar 

  • Punshon T, Hirschi K, Yang J, Lanzirotti A, Lai B, Guerinot ML (2012) The role of CAX1 and CAX3 in elemental distribution and abundance in Arabidopsis seed. Plant Physiol 158:352–362

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Salt DE, Baxter I, Lahner B (2008) Ionomics and the study of the plant ionome. Annu Rev Plant Biol 59:709–733

    Article  CAS  PubMed  Google Scholar 

  • Senadheera P, Singh RK, Maathuis FJM (2009) Differentially expressed membrane transporters in rice roots may contribute to cultivar dependent salt tolerance. J Exp Bot 60:2553–2563

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shigaki T, Pittman JK, Hirschi KD (2003) Manganese specificity determinants in the Arabidopsis metal/H+ antiporter CAX2. J Biol Chem 278:6610–6617

    Article  CAS  PubMed  Google Scholar 

  • Shigaki T, Rees I, Nakhleh L, Hirschi KD (2006) Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J Mol Evol 63:815–825

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Kanwar P, Yadav AK, Mishra M, Jha SK, Baranwal V, Pandey A, Kapoor S, Tyagi AK, Pandey GK (2014) Genome-wide expressional and functional analysis of calcium transport elements during abiotic stress and development in rice. FEBS J 281:894–915

    Article  CAS  PubMed  Google Scholar 

  • Spalding EP, Harper JF (2011) The ins and outs of cellular Ca2+ transport. Curr Opin Plant Biol 14:715–720

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Swarbreck SM, Colaço R, Davies JM (2013) Plant calcium-permeable channels. Plant Physiol 163:514–522

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: e-Northerns, expression angling, and promoter analyses. Plant J 43:153–163

    Article  CAS  PubMed  Google Scholar 

  • Ueoka-Nakanishi H, Tsuchiya T, Sasaki M, Nakanishi Y, Cunningham KW, Maeshima M (2000) Functional expression of mung bean Ca2+/H+ antiporter in yeast and its intracellular localization in the hypocotyl and tobacco cells. Eur J Biochem 267:3090–3098

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Li Z, Wei J, Zhao Z, Sun D, Cui S (2012) A Na+/Ca2+ exchanger-like protein (AtNCL) involved in salt stress in Arabidopsis. J Biol Chem 287:44062–44070

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang N, Long T, Yao W, Xiong L, Zhang Q, Wu C (2013) Mutant resources for the functional analysis of the rice genome. Mol Plant 6:596–604

    Article  CAS  PubMed  Google Scholar 

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2

    Google Scholar 

  • Wu Q, Shigaki T, Williams KA, Han JS, Kim CK, Hirschi KD, Park S (2011) Expression of an Arabidopsis Ca2+/H+ antiporter CAX1 variant in petunia enhances cadmium tolerance and accumulation. J Plant Physiol 168:167–173

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Zahid KR, He LR, Zhang WW, He X, Zhang XL, Yang XY, Zhu LF (2013) GhCAX3 gene, a novel Ca2+/H+ exchanger from cotton, confers regulation of cold response and ABA induced signal transduction. PLoS One 8:e66303

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao J, Barkla BJ, Marshall J, Pittman JK, Hirschi KD (2008) The Arabidopsis cax3 mutants display altered salt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity. Planta 227:659–669

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Connorton JM, Guo YQ, Li XK, Shigaki T, Hirschi KD, Pittman JK (2009a) Functional studies of split Arabidopsis Ca2+/H+ exchangers. J Biol Chem 284:34075–34083

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao J, Shigaki T, Mei H, Guo YQ, Cheng NH, Hirschi KD (2009b) Interaction between Arabidopsis Ca2+/H+ exchangers CAX1 and CAX3. J Biol Chem 284:4605–4615

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Life Sciences, University of Manchester, Michael Smith Building, Oxford Road, Manchester, M13 9PT, UK

    Peter D. Bickerton & Jon K. Pittman

Authors
  1. Peter D. Bickerton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jon K. Pittman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter D. Bickerton .

Editor information

Editors and Affiliations

  1. Department of Plant Molecular Biology, University of Delhi South Campus, Dhaula Kuan, India

    Girdhar K. Pandey

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Bickerton, P.D., Pittman, J.K. (2015). Role of Cation/Proton Exchangers in Abiotic Stress Signaling and Stress Tolerance in Plants. In: Pandey, G. (eds) Elucidation of Abiotic Stress Signaling in Plants. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2211-6_4

Download citation

Publish with us

Policies and ethics

Search

Navigation