Skip to main content
Log in

Increased tolerance to salt stress in the phosphate-accumulating Arabidopsis mutants siz1 and pho2

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

High salinity is an environmental factor that inhibits plant growth and development, leading to large losses in crop yields. We report here that mutations in SIZ1 or PHO2, which cause more accumulation of phosphate compared with the wild type, enhance tolerance to salt stress. The siz1 and pho2 mutations reduce the uptake and accumulation of Na+. These mutations are also able to suppress the Na+ hypersensitivity of the sos3-1 mutant, and genetic analyses suggest that SIZ1 and SOS3 or PHO2 and SOS3 have an additive effect on the response to salt stress. Furthermore, the siz1 mutation cannot suppress the Li+ hypersensitivity of the sos3-1 mutant. These results indicate that the phosphate-accumulating mutants siz1 and pho2 reduce the uptake and accumulation of Na+, leading to enhanced salt tolerance, and that, genetically, SIZ1 and PHO2 are likely independent of SOS3-dependent salt signaling.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ICP-AES:

Inductively coupled plasma-atomic emission spectrometry

MS:

Murashige and Skoog

NaPi:

Na+-coupled phosphate transporter

Pi:

Phosphate

ROS:

Reactive oxygen species

SA:

Salicylic acid

SUMO:

Small ubiquitin-related modifier

References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42

    Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumward E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiporter in Arabidopsis. Science 285:1256–1258

    Article  PubMed  CAS  Google Scholar 

  • Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011

    Article  PubMed  CAS  Google Scholar 

  • Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  PubMed  CAS  Google Scholar 

  • Binzel ML, Reuveni M (1994) Cellular mechanisms of salt tolerance in plant cells. Hort Rev 16:33–69

    CAS  Google Scholar 

  • Catala R, Ouyang J, Abreu IA, Hu Y, Seo H, Zhang X, Chua NH (2007) The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses. Plant Cell 19:2952–2966

    Article  PubMed  CAS  Google Scholar 

  • Dalhaize E, Randall PJ (1995) Characterization of phosphate-accumulator mutant of Arabidopsis thaliana. Plant Phsyiol 107:207–213

    Google Scholar 

  • 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 Environ 30:497–507

    Article  PubMed  CAS  Google Scholar 

  • Fan TWM, Higashi RM, Norlyn J, Epstein E (1989) In vivo 23Na and 31P NMR measurement of a tonoplast Na+/H+ exchange process and its characteristics in two barley cultivars. Proc Natl Acad Sci USA 86:9856–9860

    Article  PubMed  CAS  Google Scholar 

  • Gassman W, Rubio F, Schroeder JI (1996) Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J 10:869–882

    Article  PubMed  CAS  Google Scholar 

  • Gaxiola RA, Fink GR, Hirschi KD (2002) Genetic manipulation of vacuolar proton pumps and transporters. Plant Physiol 129:967–973

    Article  PubMed  CAS  Google Scholar 

  • Geiss-Friedlander R, Melchior F (2007) Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8:947–956

    Article  PubMed  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  PubMed  CAS  Google Scholar 

  • Gruwel MLH, Rauw VL, Loewen M, Abrams SR (2001) Effects of sodium chloride on plant cells; a 31P and 23Na NMR system to study salt tolerance. Plant Sci 160:785–794

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Halfer U, Ishitani M, Zhu JK (2001) Molecular characterization of functional domains in the protein kinase SOS2 that is required for salt tolerance. Plant Cell 13:1383–1400

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  PubMed  CAS  Google Scholar 

  • He C, Yan J, Shen G, Fu L, Holaday AS, Auld D, Blumwald E, Zhang H (2005) Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field. Plant Cell Physiol 46:1848–1854

    Article  PubMed  CAS  Google Scholar 

  • Helleburst JA (1978) Uptake of organic substrates by Cyclotella cryptica (Bacillariophyceae): effects of ions, ionophores and metabolic and transport inhibitors. J Phycol 14:79–83

    Article  Google Scholar 

  • Inan G, Goto F, Jin JB, Rosado A, Koiwa H, Shi H, Hasegawa PM, Bressan RA, Maggio A, Li X (2007) Isolation and characterization of shs1, a sugar-hypersensitive and ABA-insensitive mutant with multiple stress responses. Plant Mol Biol 65:295–309

    Article  PubMed  CAS  Google Scholar 

  • Ishitani M, Liu J, Halfer U, Kim C-S, Shi W, Zhu J-K (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium-binding. Plant Cell 12:1667–1677

    Article  PubMed  CAS  Google Scholar 

  • Jin JB, Jin YH, Lee J, Miura K, Yoo CY, Kim WY, Oosten MV, Hyun Y, Somers DE, Lee I, Yun DJ, Bressan RA, Hasegawa PM (2008) The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. Plant J 53:530–540

    Article  PubMed  CAS  Google Scholar 

  • Katsuhara M, Kuchitsu K, Takeshige K, Tazawa M (1989) Salt stress-induced cytoplasmic acidification and vacuolar alkalization in Nitellopsis obtusa cells: in vivo 31P-nuclear magnetic resonance study. Plant Physiol 90:1102–1107

    Article  PubMed  CAS  Google Scholar 

  • Kaya C, Kirnak H, Higgs D (2001) Effects of supplementary potassium and phosphorus on physiological development and mineral nutrition of cucumber and pepper cultivars grown at high salinity (NaCl). J Plant Nutr 24:1457–1471

    Article  CAS  Google Scholar 

  • Khan NA, Syeed S, Masood A, Nazar R, Iqbal N (2010) Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity stress. Int J Plant Biol 1:e1

    Google Scholar 

  • Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong Q, Ma S, Bohnert HJ, Kwak SS, Bressan RA, Hasegawa PM, Yun DJ (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90

    Article  PubMed  CAS  Google Scholar 

  • Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Shuai K (2008) Regulation of the sumoylation system in gene expression. Curr Opin Cell Biol 20:288–293

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Zhu JK (1997) An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc Natl Acad Sci USA 94:4960–4964

    Article  Google Scholar 

  • Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945

    Article  PubMed  CAS  Google Scholar 

  • Mahajan S, Pandey GK, Tuteja N (2008) Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Arch Biochem Biophys 471:146–158

    Article  PubMed  CAS  Google Scholar 

  • Marks J, Debnam ES, Unwin RJ (2010) Phosphate homeostasis and the renal-gastrointestinal axis. Am J Physiol Renal Physiol 299:F285–F296

    Article  PubMed  CAS  Google Scholar 

  • Martínez P, Persson B (1998) Identification, cloning and characterization of a derepressible Na+-coupled phosphate transporter in Saccharomyces cerevisiae. Mol Gen Genet 258:628–638

    Article  PubMed  Google Scholar 

  • Mäser P, Hosoo Y, Goshima S, Horie T, Eckelman B, Yamada K, Yoshida K, Bakker EP, Shinmyo A, Oiki S, Schroeder JI, Uozumi N (2002) Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants. Proc Natl Acad Sci USA 99:6428–6433

    Article  PubMed  Google Scholar 

  • Mimura T, Reid RJ, Ohsumi Y, Smith FA (2002) Induction of the Na+/Pi cotransport system in the plasma membrane of Chara corallina requires external Na+ and low levels of Pi. Plant Cell Environ 25:1475–1481

    Article  CAS  Google Scholar 

  • Miura K, Hasegawa PM (2010) Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol 20:223–232

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Ohta M (2010) SIZ1, a small ubiquitin-related modifier ligase, controls cold signaling through regulation of salicylic acid accumulation. J Plant Phsyiol 167:555–560

    Article  CAS  Google Scholar 

  • Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102:7760–7765

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun D-J, Hasegawa PM (2007a) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19:1403–1414

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Jin JB, Hasegawa PM (2007b) Sumoylation, a post-translational regulatory process in plants. Curr Opin Plant Biol 10:495–502

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci USA 106:5418–5423

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Lee J, Miura T, Hasegawa PM (2010) SIZ1 controls cell growth and plant development in Arabidopsis through salicylic acid. Plant Cell Physiol 51:103–113

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011a) SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 155:1000–1012

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Ohta M, Nakazawa M, Ono M, Hasegawa PM (2011b) ICE1 Ser403 is necessary for protein stabilization and regulation of cold signaling and tolerance. Plant J (in press)

  • Nazar R, Iqbal N, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168:807–815

    Article  PubMed  CAS  Google Scholar 

  • Oh DH, Dassanayake M, Haas JS, Kropornika A, Wright C, d’Urzo MP, Hong H, Ali S, Hernandez A, Lambert GM, Inan G, Galbraith DW, Bressan RA, Yun DJ, Zhu JK, Cheeseman JM, Bohnert HJ (2010) Genome structures and halophyte-specific gene expression of the extremophile Thellungiella parvula in comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis. Plant Physiol 154:1040–1052

    Article  PubMed  CAS  Google Scholar 

  • Pavón LR, Lundh F, Lundin B, Mishra A, Persson BL, Spetea C (2008) Arabidopsis ANTR1 is a thylakoid Na+-dependent phosphate transporter: functional characterization in Escherichia coli. J Biol Chem 283:13520–13527

    Article  PubMed  Google Scholar 

  • Qiu Q, 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. Proc Natl Acad Sci USA 99:8436–8441

    Article  PubMed  CAS  Google Scholar 

  • Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci USA 99:9061–9066

    Article  PubMed  CAS  Google Scholar 

  • Rai AK, Sharma NK (2006) Phosphate metabolism in the cyanobacterium Anabaena doliolum under salt stress. Curr Microbiol 52:6–12

    Article  PubMed  CAS  Google Scholar 

  • Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37

    Article  PubMed  CAS  Google Scholar 

  • Rees TA, Cressewell RC, Syrett PJ (1980) Sodium-dependent uptake of nitrate and urea by a marine diatom. Biochim Biophys Acta 596:141–144

    Article  PubMed  CAS  Google Scholar 

  • Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663

    Article  PubMed  CAS  Google Scholar 

  • Rubio F, Schwarz M, Gassmann W, Schroeder JI (1999) Genetic selection of mutations in the high affinity K+ transporter HKT1 that define functions of a loop site for reduced Na+ permeability and increased Na+ tolerance. J Biol Chem 274:6839–6847

    Article  PubMed  CAS  Google Scholar 

  • Rubio L, Linares-Rueda A, García-Sánchez MJ, Fernández JA (2005) Physiological evidence for a sodium-dependent high-affinity phosphate and nitrate transport at the plasma membrane of leaf and root cells of Zostera marina L. J Exp Bot 56:613–622

    Article  PubMed  CAS  Google Scholar 

  • Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee B-h, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc Natl Acad Sci USA 98:14150–14155

    Article  PubMed  CAS  Google Scholar 

  • Rus A, Lee BH, Muñoz-Mayor A, Sharkhuu A, Miura K, Zhu JK, Bressan RA, Hasegawa PM (2004) AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol 136:2500–2511

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Barrena MJ, Fujii H, Angulo I, Martínez-Ripoll M, Zhu J-K, Albert A (2007) The structure of the C-terminal domain of the protein kinase AtSOS2 bound to the calcium sensor AtSOS3. Mol Cell 26:427–435

    Article  PubMed  Google Scholar 

  • Sawada H, Shim IS, Usui K (2006) Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis—modulation by salt stress in rice seedlings. Plant Sci 171:263–270

    Article  CAS  Google Scholar 

  • Schachtman DP, Schroeder JI (1994) Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370:655–658

    Article  PubMed  CAS  Google Scholar 

  • Segawa H, Aranami F, Kaneko I, Tomoe Y, Miyamoto K (2009) The roles of Na/Pi-II transporters in phosphate metabolism. Bone 45:S2–S7

    Article  PubMed  CAS  Google Scholar 

  • Shakirova FM, Sakhabutdinova AR, Bezrukova MV, Fatkhutdinova RA, Fatkhutdinova DR (2003) Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci 164:317–322

    Article  CAS  Google Scholar 

  • Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901

    Article  PubMed  CAS  Google Scholar 

  • Shi H, 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

    Article  PubMed  CAS  Google Scholar 

  • Silva P, Gerós H (2009) Regulation by salt of vacuolar H+-ATPase and H+-pyrophosphatase activities and Na+/H+ exchange. Plant Signal Behav 4:718–726

    Article  PubMed  CAS  Google Scholar 

  • Stevens J, Senaratna T, Sivasithamparam K (2006) Salicylic acid induces salinity tolerance in tomato (Lycopersicon esculentum cv. Roma): associated changes in gas exchange, water relations and membrane stabilization. Plant Growth Regul 49:77–83

    CAS  Google Scholar 

  • Sunarpi HT, Horie T, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938

    Article  PubMed  CAS  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  PubMed  CAS  Google Scholar 

  • Ullrich WR, Glaser E (1982) Sodium-phosphate cotransport in the green alga Ankistrodesmus braunii. Plant Sci Lett 27:155–162

    Article  CAS  Google Scholar 

  • Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S, Tsuboi A, Bakker EP, Nakamura T, Schroeder JI (2000) The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol 122:1249–1259

    Article  PubMed  CAS  Google Scholar 

  • Versaw W, Metzenberg R (1995) Repressible cation-phosphate symporters in Neurospora crassa. Proc Natl Acad Sci USA 92:3884–3887

    Article  PubMed  CAS  Google Scholar 

  • 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. Plant J 30:529–539

    Article  PubMed  CAS  Google Scholar 

  • Yoo CY, Miura K, Jin JB, Lee J, Park HC, Salt DE, Yun D-J, Bressan RA, Hasegawa PM (2006) SIZ1 small ubiquitin-like modifier E3 facilitates basal thermotolerance in Arabidopsis independent of salicylic acid. Plant Physiol 142:1548–1558

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signaling transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed  CAS  Google Scholar 

  • Zhu J, Fu X, Koo YD, Zhu JK, Jenney FE Jr, Adams MW, Zhu Y, Shi H, Yun DJ, Hasegawa PM, Bressan RA (2007) An enhancer mutant of Arabidopsis salt overly sensitive 3 mediates both ion homeostasis and the oxidative stress response. Mol Cell Biol 27:5214–5224

    Article  PubMed  CAS  Google Scholar 

  • Zvyagilskaya R, Parchomenko O, Abramova N, Allard P, Panaretakis T, Pattison-Granberg J, Persson BL (2001) Proton- and sodium-coupled phosphate transport system and energy status of Yarrowia lipolytica cells in acidic and alkaline conditions. J Mem Biol 183:39–50

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Ms. Miyuki Hara, Ms. Risa Osada, Ms. Ami Komata, and Ms. Ayaka Sato for technical support. We are grateful to the Chemical Analysis Center, University of Tsukuba, for use of the ICP-AES spectrometer. This work was supported, in part, by a Special Coordination Funds for Promoting Science and Technology grant from the Ministry of Education, Culture, Sports, Science, and Technology, the Japanese Government, and by The Salt Science Research Foundation, No. 1023.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kenji Miura.

Additional information

The contributions of K. Miura and A. Sato are considered to be equal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miura, K., Sato, A., Ohta, M. et al. Increased tolerance to salt stress in the phosphate-accumulating Arabidopsis mutants siz1 and pho2 . Planta 234, 1191–1199 (2011). https://doi.org/10.1007/s00425-011-1476-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1476-y

Keywords

Navigation