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Identification, conservation, and relative expression of V-ATPase cDNAs in tomato plants

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Abstract

Vacuolar H+-ATPases (V-ATPases) are multi-subunit enzymes that pump protons into intracellular compartments, thereby regulating pH levels. Because V-ATPase genes are highly conserved, using known sequences inArabidopsis to identify orthologous genes in other plants is possible. Using expressed sequence tags (ESTs) in the TIGR Tomato Gene Index, we have identified 23 distinct cDNAs representing all 13 known V-ATPase subunits. The subunits composing the 2-hexamer ring structures are the most highly conserved, whereas those forming peripheral stalks are the least conserved. Relative expression analyses using the same data set suggested several broad patterns of gene expression in tomato plants. V-ATPase ESTs were found in 26 of 27 libraries, normally within a 3-fold level of relative expression. EST frequencies were highest in roots, then in fruits, and essentially identical in all other tissues. In the libraries sampled, relative expression values for individual subunits varied widely and suggest that mRNAs encoding subunits a, e, and F are in low abundance in most tomato plant tissues. Finally, V-ATPase relative expression levels increased over the course of fruit ripening. The identification of cDNAs, description of conservation patterns, and preliminary expression analyses in this work should open the door for future V-ATPase studies in tomato plants.

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Abbreviations

BLAST:

basic local alignment search tool

EST:

expressed sequence tag

TC:

tentative consensus sequence

TIGR TGI:

the Institute for Genomic Research Tomato Gene Index

V-ATPase:

vacuolar ATPase

References

  • Adams MD, Kerlavage AR, Fleischmann RD, Fuldner RA, Bult CJ, Lee NH, Kirkness EF, Weinstock KG, Gocayne JD, White O, et al. (1995) Initial assessment of human gene diversity and expression patterns based upon 83 million nucleotides of cDNA sequence. Nature 377: 3–17.

    PubMed  CAS  Google Scholar 

  • Almeida DPF and Huber DJ (1999) Apoplastic pH and inorganic ion levels in tomato fruit: A potential means for regulation of cell wall metabolism during ripening. Physiologia Plantarum 105: 506–512.

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schiffer AA, Zhang J, Zhang Z, Miller W, and Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25: 3389–3402.

    Article  PubMed  CAS  Google Scholar 

  • Aviezer-Hagai K, Nelson H, and Nelson N (2000) Cloning and expression of cDNAs encoding plant V-ATPase subunits in the corresponding yeast null mutants. Biochimica et Biophysica Acta-Bioenergetics 1459: 489–498.

    Article  CAS  Google Scholar 

  • Barakat A, Szick-Miranda K, Chang I-F, Guyot R, Blanc G, Cooke R, Delseny M, and Bailey-Serres J (2001) The organization of cytoplasmic ribosomal protein genes in theArabidopsis genome. Plant Physiol 127: 398–415.

    Article  PubMed  CAS  Google Scholar 

  • Barkla BJ and Pantoja O (1996) Physiology of ion transport across the tonoplast of higher plants. Annu Rev Plant Physiol Plant Mol Biol 47: 159–184.

    Article  PubMed  CAS  Google Scholar 

  • Bartley GE and Ishida BK (2002) Digital fruit ripening: Data mining in the TIGR Tomato Gene Index. Plant Mol Biol Rep 20: 115–130.

    Article  CAS  Google Scholar 

  • Brune A, Muller M, Taiz L, Gonzalez P, and Etxeberria E (2002) Vacuolar acidification in citrus fruit: Comparison between acid lime (Citrus aurantifolia) and sweet lime (Citrus limmetioides) juice cells. J Amer Soc Hort Sc 127: 171–177.

    CAS  Google Scholar 

  • Cerana R, Giromini L, and Colombo R (1995) Malate-regulated channels permeable to an-ions in vacuoles ofArabidopsis thaliana. Aust J Plant Physiol 22: 115–121.

    Article  CAS  Google Scholar 

  • Charsky CM, Schumann NJ, and Kane PM (2000) Mutational analysis of subunit G (Vma10p) of the yeast vacuolar H+-ATPase. J Biol Chem 275: 37232–37239.

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Kanokporn T, Zeng Q, Wilkins TA, and Wood AJ (2002) Characterization of the V-type H+-ATPase in the resurrection plantTortula ruralis: accumulation and polysomal recruitment of the proteolipid c subunit in response to salt stress. J Exper Bot 53: 225–232.

    Article  CAS  Google Scholar 

  • Coker JS and Davies E (2002) Correspondence re: A.H. Ree et al., Expression of a Novel Factor in Human Breast Cancer Cells with Metastatic Potential (Cancer Res., 59: 4675–4680, 1999). Cancer Res 62: 4164–4165.

    PubMed  CAS  Google Scholar 

  • Coker JS, Jones D and Davies E (2003) Supplementary materials — Amino acid alignments for putative V-ATPase proteins inLycopersicon andArabidopsis. 1 June 2003 <www. cals.ncsu.edu/botany/faculty/edavies/edlab/atpasesegs.htm>

  • Cooke R, Raynal M, Laudie M, and Delseny M (1997) Identification of members of gene families inArabidopsis thaliana by contig construction from partial cDNA sequences: 106 genes encoding 50 cytoplasmic ribosomal proteins. Plant J 11: 1127–1140.

    Article  PubMed  CAS  Google Scholar 

  • Cooley MB, Yang H, Dahal P, Mella RA, Downie AB, Haigh AM, and Bradford KJ (1999) Vacuolar H+-ATPase is expressed in response to gibberellin during tomato seed germination. Plant Physiol 121: 1339–1348.

    Article  PubMed  CAS  Google Scholar 

  • Davies E, Vian A, Vian C, and Stanković B (1997) Rapid systemic up-regulation of genes after heat-wounding and electrical stimulation. Physiologiae Plantarum 19(4): 571–576.

    Article  CAS  Google Scholar 

  • Davies JN and Hobson GE (1981) The constituents of tomato fruit — the influence of environment, nutrition, and genotype. CRC Crit Rev Food Sci Nutri 15: 205–280.

    Article  CAS  Google Scholar 

  • Domgall I, Venzke D, Liittge U, Ratajczak R, and Bottcher B (2002) Three-dimensional map of a plant V-ATPase based on electron microscopy. J Biol Chem 277: 13115–13121.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Milner ID, Ho LC, and Hall JL (1995) Properties of proton and sugar transport at the tonoplast of tomato (Lycopersicon esculentum) fruit. Physiologia Plantarum 94: 399–410.

    Article  CAS  Google Scholar 

  • Muller ML, Irkens-Kiesecker U, Rubinstein B, and Taiz L (1996) On the mechanism of hyperacidification in lemon — Comparison of the vacuolar H+-ATPase activities of fruits and epicotyls. J Biol Chem 271: 1916–1924.

    Article  PubMed  CAS  Google Scholar 

  • Muller ML, Jensen M, and Taiz L (1999) The vacuolar H+-ATPase of lemon fruits is regulated by variable H+/ATP coupling and slip. J Biol Chem 274: 10706–10716.

    Article  PubMed  CAS  Google Scholar 

  • Muller ML and Taiz L (2002) Regulation of the lemon-fruit V-ATPase by variable stoichiometry and organic acids. J Membrane Biol 185: 209–220.

    Article  CAS  Google Scholar 

  • Nishi T and Forgac M (2002) The vacuolar (H+)-ATPases: Nature's most versatile proton pumps. Nature Reviews Mol Cell Biol 3: 94–103.

    Article  CAS  Google Scholar 

  • Oleski N, Mahdavi P, and Bennett AB (1987) Transport properties of the tomato fruit tonoplast. II. Citrate transport. Plant Physiol 84: 997–1000.

    Article  PubMed  CAS  Google Scholar 

  • Pantoja O and Smith JAC (2002) Sensitivity of the plant vacuolar malate channel to pH, Ca2+ and anion-channel blockers. J Membrane Biol 186: 31–42.

    Article  CAS  Google Scholar 

  • Perera IY, Li X, and Sze H (1995) Several distinct genes encode nearly identical 16 kDa proteolipids of the vacuolar H+-ATPase fromArabidopsis thaliana. Plant Mol Biol 29: 227–244.

    Article  PubMed  CAS  Google Scholar 

  • Sagermann M, Stevens TH, and Matthews BW (2001) Crystal structure of the regulatory subunit H of the V-type ATPase ofSaccharomyces cerevisiae. Proc Natl Acad Sci USA 98: 7134–7139.

    Article  PubMed  CAS  Google Scholar 

  • Schumacher K, Vafeados D, McCarthy M, Sze H, Wilkins T, and Chory J (1999) TheArabidopsis det3 mutant reveals a central role for the vacuolar-H+-ATPase in plant growth and development. Genes Dev 13: 3259–3270.

    Article  PubMed  CAS  Google Scholar 

  • Stanković B, Vian A, Henry-Vian C, and Davies E (2000) Molecular cloning and characterization of a tomato cDNA encoding a systemically wound-inducible bZIP DNA-binding protein. Planta 212: 60–66.

    Article  PubMed  Google Scholar 

  • Stekel DJ, Git Y, and Falciani F (2000) The comparison of gene expression from multiple cDNA libraries. Genome Res 10: 2055–2061.

    Article  PubMed  CAS  Google Scholar 

  • Sze H, Schumacher K, Miiller ML, Padmanaban S, and Taiz L (2002) A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H+-ATPase. Trends in Plant Sci 7: 157–161.

    Article  CAS  Google Scholar 

  • Terrier N, Francois-Xavier S, Ageorges A, and Romieu C (2001) Changes in acidity and in proton transport at the tonoplast of grape berries during development. Planta 213: 20–28.

    Article  PubMed  CAS  Google Scholar 

  • Tomato Gene Index (TGI). The Institute for Genomic Research. 25 Apr. 2002 <www. tigr.org/tdb/tgi/lgi/>

  • Van der Hoeven R, Ronning C, Giovannoni J, Martin G, and Tanksley S (2002) Deductions about number, organization, and evolution of genes in the tomato genome based on analysis of a large expressed sequence tag collection and selective genomic sequencing. Plant Cell 14: 1441–1456.

    Article  PubMed  Google Scholar 

  • VecScreen. National Center for Biotechnology Information. 4 May 2001 <http://www. ncbi.nlm.nih.gov/VecScreen/VecScreen.html>.

  • Vian A, Henry-Vian C, and Davies E (1999) Rapid and systemic accumulation of chloroplast mRNA-binding protein transcripts after flame stimulus in tomato. Plant Physiol 121: 517–524.

    Article  PubMed  CAS  Google Scholar 

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  1. Jeffrey S. Coker

    Present address: Department of Botany, North Carolina State University, Campus Box 7612, 27695, Raleigh, North Carolina

Authors and Affiliations

  1. Department of Botany, North Carolina State University, Campus Box 7612, 27695, Raleigh, North Carolina

    Derek Jones & Eric Davies

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  1. Jeffrey S. Coker
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  2. Derek Jones
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Correspondence to Jeffrey S. Coker.

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Coker, J.S., Jones, D. & Davies, E. Identification, conservation, and relative expression of V-ATPase cDNAs in tomato plants. Plant Mol Biol Rep 21, 145–158 (2003). https://doi.org/10.1007/BF02774241

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