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Aluminum regulates oxalate secretion and plasma membrane H+-ATPase activity independently in tomato roots

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Abstract

We demonstrated that aluminum (Al)-induced oxalate secretion and plasma membrane (PM) H+-ATPase activity in tomato (Lycopersicon esculentum ‘Hezuo903’) roots were poorly correlated. In addition, vanadate, an inhibitor of PM H+-ATPase, had no effect on Al-induced oxalate secretion, but significantly inhibited enzyme activity. An anion channel inhibitor phenylglyoxal inhibited oxalate secretion, but not PM H+-ATPase activity. Exposure of tomato roots to 10 μM LaCl3 also stimulated PM H+-ATPase activity; however, La failed to induce oxalate secretion. Furthermore, Al-induced changes of PM H+-ATPase activity were not associated with oxalate secretion in two tomato cultivars differing in the ability to secrete oxalate under Al stress. These results indicate that Al independently regulates oxalate secretion and PM H+-ATPase activity in tomato roots. Analysis of expression levels of PM H+-ATPase genes by real-time reverse transcription-PCR and protein by Western blot and immunodetection revealed that the regulation of PM H+-ATPase in response to Al was subjected to transcriptional and posttranscriptional control. However, since neither transcriptional level of genes nor translational level of proteins directly relate to the enzyme activity, posttranslational modification of PM H+-ATPase under Al stress likely contributes to changes in activity of this protein.

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Abbreviations

Al:

Aluminum

La:

LaCl3

PG:

Phenylglyoxal

PM:

Plasma membrane

VA:

Vanadate

References

  • Ahn SJ, Sivaguru M, Osawa H, Chung GC, Matsumoto H (2001) Aluminum inhibits the H+-ATPase activity by permanently altering the PM surface potentials in squash roots. Plant Physiol 126:1381–1390

    Article  PubMed  CAS  Google Scholar 

  • Ahn SJ, Rengel Z, Matsumoto H (2004) Aluminum-induced plasma membrane surface potential and H+-ATPase activity in near-isogenic wheat lines differing in tolerance to aluminum. New Phytol 162:71–79

    Article  CAS  Google Scholar 

  • Ewing NN, Bennett AB (1994) Assessment of the number and expression of P-type H+-ATPase genes in tomato. Plant Physiol 106:547–557

    Article  PubMed  CAS  Google Scholar 

  • Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091

    Article  PubMed  CAS  Google Scholar 

  • Hoekenga OA, Vision TJ, Shaff JE, Monforte AJ, Lee GP, Howell SH, Kochian LV (2003) Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta × Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiol 132:936–948

    Article  PubMed  CAS  Google Scholar 

  • Hoekenga OA, Maron LG, Piñeros MA, Cançado GMA, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto H (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:9738–9743

    Article  PubMed  CAS  Google Scholar 

  • Kim Y-S, Park W, Nian H, Sasaki T, Ezaki B, Jang Y-S, Chung G-C, Bae H-J, Ahn SJ (2010) Aluminum tolerance associated with enhancement of plasma membrane H+-ATPase in the root apex of soybean. Soil Sci Plant Nutr 56:140–149

    Article  CAS  Google Scholar 

  • Kinraide TB (2003) Toxicity factors in acidic forest soils: attempts to evaluate separately the toxic effects of excessive Al3+ and H+ and insufficient Ca2+ and Mg2+ upon root elongation. Eur J Soil Sci 54:323–333

    Article  CAS  Google Scholar 

  • Kochian LV, Hoekenga AO, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Ligaba A, Yamaguch M, Shen H, Sasaki T, Yamamoto Y, Matsumoto H (2004) Phosphorus deficiency enhances plasma membrane H+-ATPase activity and citrate exudation in greater purple lupin (Lupinus pilosus). Funct Plant Biol 31:1075–1083

    Article  CAS  Google Scholar 

  • Ma JF (2000) Role of organic acids in detoxification of Al in higher plants. Plant Cell Physiol 44:383–390

    Google Scholar 

  • Ma JF, Zheng SJ, Matsumoto H, Hiradate S (1997) Detoxifying aluminum with buckwheat. Nature 390:569–570

    Article  Google Scholar 

  • Ma JF, Ryan PR, Delhaize E (2001) Aluminum tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    Article  PubMed  CAS  Google Scholar 

  • Magalhaes JV, Liu J, Guimaraes CT, Lana UGP, Alves VM, Wang YH, Schaffert RE, Hoekenga OA, Pineros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in Sorghum. Nature Genet 39:1156–1161

    Article  PubMed  CAS  Google Scholar 

  • Niu X, Narasimhan ML, Salzman RA, Bressan RA, Hasegawa PM (1993) NaCl regulation of plasma membrane H+-ATPase gene expression in a glycophyte and a halophyte. Plant Physiol 103:713–718

    Article  PubMed  CAS  Google Scholar 

  • Niu X, Damsz B, Kononowicz AK, Bressan RA, Hasegawa PM (1996) NaCl-induced alterations in both cell structure and tissue-specific plasma membrane H+-ATPase gene expression. Plant Physiol 111:679–686

    PubMed  CAS  Google Scholar 

  • Ohno T, Koyama H, Hara T (2003) Characterization of citrate transport through the plasma membrane in a carrot mutant cell line with enhanced citrate excretion. Plant Cell Physiol 44:156–162

    Article  PubMed  CAS  Google Scholar 

  • Osawa H, Matsumoto H (2001) Possible involvement of protein phosphorylation in aluminum-responsive malate efflux in wheat root apex. Plant Physiol 126:411–420

    Article  PubMed  CAS  Google Scholar 

  • Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845

    Article  PubMed  CAS  Google Scholar 

  • Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an Al-tolerance mechanism in maize (Zea mays L.). Planta 196:788–795

    Article  CAS  Google Scholar 

  • Ryan PR, Delhaize E, Randall PJ (1995) Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:103–110

    Article  CAS  Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Plant Physiol Plant Mol Biol 52:527–560

    Article  CAS  Google Scholar 

  • Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653

    Article  PubMed  CAS  Google Scholar 

  • Shaff JE, Schultz BA, Craft EJ, Clark RT, Kochian LV (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330:207–214

    Article  CAS  Google Scholar 

  • Shen H, Ligaba A, Yamaguchi M, Osawa H, Shibata K, Yan XL, Matsumoto H (2004) Effect of K-252a and abscisic acid on the efflux of citrate from soybean roots. J Exp Bot 55:663–671

    Article  PubMed  CAS  Google Scholar 

  • Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287–296

    Article  PubMed  CAS  Google Scholar 

  • Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482

    Article  PubMed  CAS  Google Scholar 

  • von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. In: Date RA, Grundon NJ, Rayment GE, Probert ME (eds) Plant–soil interactions at low pH: principles and management. Kluwer Academic Publishers, Dordrecht, pp 5–19

    Google Scholar 

  • Widell S, Lundborg T, Larsson C (1982) Plasma membrane from oats prepared by partition in an aqueous polymer two-phase system. On the use of light-induced cytochrome b reduction as a marker for the plasma membrane. Plant Physiol 70:1429–1435

    Article  PubMed  CAS  Google Scholar 

  • Yamashita K, Kasai M, Ezaki B, Shibasaka M, Yamamoto Y, Matsumoto H, Sasakawa H (1995) Stimulation of H+ extrusion and plasma-membrane H+-ATPase activity of barley roots by ammonium treatment. Soil Sci Plant Nutr 41:133–140

    CAS  Google Scholar 

  • Yan F, Zhu Y, Müller C, Zörb C, Schubert S (2002) Adaptation of H+-pumping and plasma membrane H+-ATPase activity in proteoid roots white lupin under phosphate deficiency. Plant Physiol 129:50–63

    Article  PubMed  CAS  Google Scholar 

  • Yang ZM, Nian H, Sivaguru M, Tanakamaru S, Matsumoto H (2001) Characterization of aluminum-induced citrate secretion in aluminum-tolerant soybean (Glycine max) plants. Physiol Plant 113:64–71

    Article  CAS  Google Scholar 

  • Yang JL, Zheng SJ, He YF, Matsumoto H (2005) Aluminium resistance requires resistance to acid stress: a case study with spinach that exudes oxalate rapidly when exposed to Al stress. J Exp Bot 56:1197–1203

    Article  PubMed  CAS  Google Scholar 

  • Yang JL, Zheng SJ, He YF, You JF, Zhang L, Yu XH (2006) Comparative studies on the effect of a protein-synthesis inhibitor on aluminium-induced secretion of organic acids from Fagopyrum esculentum Moench and Cassia tora L. roots. Plant Cell Environ 29:240–246

    Article  PubMed  CAS  Google Scholar 

  • Yang JL, You JF, Li YY, Wu P, Zheng SJ (2007) Magnesium enhances aluminum-induced citrate secretion in rice bean roots (Vigna umbellata) by restoring plasma membrane H+-ATPase activity. Plant Cell Physiol 48:66–73

    Article  PubMed  CAS  Google Scholar 

  • You JF, He YF, Yang JL, Zheng SJ (2005) A comparison of aluminum resistance among Polygonum species originating on strongly acidic and neutral soils. Plant Soil 276:143–151

    Article  CAS  Google Scholar 

  • Zhang WH, Ryan PR, Sasaki T, Yamamoto Y, Sullivan W, Tyerman SD (2008) Characterization of the TaALMT1 protein as an Al3+-activated anion channel in transformed tobacco (Nicotiana tabacum L.) cells. Plant Cell Physiol 49:1316–1330

    Article  PubMed  CAS  Google Scholar 

  • Zheng SJ, Ma JF, Matsumoto H (1998) High aluminum resistance in buckwheat: I Al-induced special secretion of oxalic acid from root tips. Plant Physiol 117:745–751

    Article  Google Scholar 

  • Zhu Y, Yan F, Zörb C, Schubert S (2005) A link between citrate and proton release by proteoid roots of white lupin (Lupinus albus L.) grown under phosphorus-deficient conditions? Plant Cell Physiol 46:892–901

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Di T, Xu G, Chen X, Zeng H, Yan F, Shen Q (2009) Adaptation of plasma membrane H+-ATPase of rice to low pH as related to ammonium nutrition. Plant Cell Environ 32:1428–1440

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Fund from Zhejiang Science and Technology Bureau (2008C12005-2), Natural Science Foundation of China (No. 30625026), Changjiang Scholarship and China Postdoctoral Science Foundation Funded Project (20070420234).

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Authors and Affiliations

  1. State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, 310058, People’s Republic of China

    Jian Li Yang, Xiao Fang Zhu, You Xiang Peng, Cheng Zheng & Shao Jian Zheng

  2. Institute of Plant Biology, School of Life Science, Fudan University, 220 Handan Road, Shanghai, 200433, People’s Republic of China

    Feng Ming

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  1. Jian Li Yang
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  2. Xiao Fang Zhu
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  3. You Xiang Peng
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Correspondence to Jian Li Yang.

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Yang, J.L., Zhu, X.F., Peng, Y.X. et al. Aluminum regulates oxalate secretion and plasma membrane H+-ATPase activity independently in tomato roots. Planta 234, 281–291 (2011). https://doi.org/10.1007/s00425-011-1402-3

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