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Auxin production by the plant trypanosomatid Phytomonas serpens and auxin homoeostasis in infected tomato fruits

Published online by Cambridge University Press:  07 May 2014

SUSAN IENNE ,
LUCIANO FRESCHI ,
VANESSA F. VIDOTTO ,
TIAGO A. DE SOUZA Open the ORCID record for TIAGO A. DE SOUZA [Opens in a new window] ,
EDUARDO PURGATTO  and
BIANCA ZINGALES
SUSAN IENNE
Affiliation:
Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, Av. Prof. Lineu Prestes, 748, São Paulo, 05508-000, Brazil
LUCIANO FRESCHI
Affiliation:
Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, travessa 14, 277, São Paulo, 05508-090, Brazil
VANESSA F. VIDOTTO
Affiliation:
Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, Av. Prof. Lineu Prestes, 748, São Paulo, 05508-000, Brazil
TIAGO A. DE SOUZA
Affiliation:
CEFAP-USP (Centro de Facilidades de Apoio à Pesquisa-USP), Instituto de Ciências Biomédicas, Universidade de São Paulo, Av. Prof. Lineu Prestes, 1730, São Paulo, 05508-000, Brazil
EDUARDO PURGATTO
Affiliation:
Departamento de Alimentos e Nutrição Experimental, NAPAN – Núcleo de Apoio à Pesquisa em Alimentos e Nutrição, Faculdade de Ciências Farmacêuticas, Universidade de São Paulo, Av. Prof. Lineu Prestes, 580, São Paulo, 05508-000, Brazil
BIANCA ZINGALES*
Affiliation:
Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, Av. Prof. Lineu Prestes, 748, São Paulo, 05508-000, Brazil
*
*Corresponding author: Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, Av. Prof. Lineu Prestes, 748, São Paulo, 05508-000, Brazil. E-mail: [email protected]
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Summary

Previously we have characterized the complete gene encoding a pyruvate decarboxylase (PDC)/indolepyruvate decarboxylase (IPDC) of Phytomonas serpens, a trypanosomatid highly abundant in tomato fruits. Phylogenetic analyses indicated that the clade that contains the trypanosomatid protein behaves as a sister group of IPDCs of γ-proteobacteria. Since IPDCs are key enzymes in the biosynthesis of the plant hormone indole-3-acetic acid (IAA), the ability for IAA production by P. serpens was investigated. Similar to many microorganisms, the production of IAA and related indolic compounds, quantified by high performance liquid chromatography, increased in P. serpens media in response to amounts of tryptophan. The auxin functionality was confirmed in the hypocotyl elongation assay. In tomato fruits inoculated with P. serpens the concentration of free IAA had no significant variation, whereas increased levels of IAA-amide and IAA-ester conjugates were observed. The data suggest that the auxin produced by the flagellate is converted to IAA conjugates, keeping unaltered the concentration of free IAA. Ethanol also accumulated in P. serpens-conditioned media, as the result of a PDC activity. In the article we discuss the hypothesis of the bifunctionality of P. serpens PDC/IPDC and provide a three-dimensional model of the enzyme.

Keywords

Indole-3-acetic acidconjugated auxinindole-pyruvate decarboxylasePhytomonas-plant interaction
Type
Research Article
Information
Parasitology , Volume 141 , Issue 10 , September 2014 , pp. 1299 - 1310
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Alves, J. M., Voegtly, L., Matveyev, A. V., Lara, A. M., da Silva, F. M., Serrano, M. G., Buck, G. A., Teixeira, M. M. and Camargo, E. P. (2011). Identification and phylogenetic analysis of heme synthesis genes in trypanosomatids and their bacterial endosymbionts. PLoS One 6, e23518.CrossRefGoogle ScholarPubMed
Andrews, F. H. and McLeish, M. J. (2012). Substrate specificity in thiamin diphosphate-dependent decarboxylases. Bioorganic Chemistry 43, 26–36.CrossRefGoogle ScholarPubMed
Arnold, K., Bordoli, L., Kopp, J. and Schwede, T. (2006). The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195–201.CrossRefGoogle ScholarPubMed
Brandl, M. T. and Lindow, S. E. (1996). Cloning and characterization of a locus encoding an indolepyruvate carboxylase involved in indole-3-acetic acid synthesis in Erwinia herbicola . Applied and Environmental Microbiology 62, 4121–4128.CrossRefGoogle Scholar
Bringaud, F., Rivière, L. and Coustou, V. (2006). Energy metabolism of trypanosomatids: adaptation to available carbon sources. Molecular and Biochemical Parasitology 149, 1–9.CrossRefGoogle ScholarPubMed
Brown, H. M. and Purves, W. K. (1980). Indoleacetaldehyde reductase of Cucumis sativus L: kinetic properties and role in auxin biosynthesis. Plant Physiology 65, 107–113.CrossRefGoogle ScholarPubMed
Camargo, E. P. (1999). Phytomonas and other trypanosomatid parasites of plants and fruit. Advances in Parasitology 42, 29–112.CrossRefGoogle ScholarPubMed
Catalá, C., Ostin, A., Chamarro, J., Sandberg, G. and Crozier, A. (1992). Metabolism of indole-3-acetic acid by pericarp discs from immature and mature tomato (Lycopersicon esculentum Mill). Plant Physiology 100, 1457–1463.CrossRefGoogle ScholarPubMed
Cazzulo, J. J., Franke de Cazzulo, B. M., Engel, J. C. and Cannata, J. J. (1985). End products and enzyme levels of aerobic glucose fermentation in trypanosomatids. Molecular and Biochemical Parasitology 16, 329–343.CrossRefGoogle ScholarPubMed
Chaumont, F., Schanck, A. N., Blum, J. J. and Opperdoes, F. R. (1994). Aerobic and anaerobic glucose metabolism of Phytomonas sp. isolated from Euphorbia characias . Molecular and Biochemical Parasitology 67, 321–331.CrossRefGoogle ScholarPubMed
Chen, C. C., Hwang, J. K. and Yang, J. M. (2009). (PS)2-v2: template-based protein structure prediction server. BMC Bioinformatics 10, 366.CrossRefGoogle ScholarPubMed
Chen, K. H., Miller, A. N., Patterson, G. W. and Cohen, J. D. (1988). A rapid and simple procedure for purification of indole-3-acetic acid prior to GC-SIM-MS analysis. Plant Physiology 86, 822–825.CrossRefGoogle ScholarPubMed
Dobbelaere, S., Croonenborghs, A., Thys, A., Vande Broek, A. and Vanderleyden, J. (1999). Analysis and relevance of the phytostimulatory effect of genetically modified Azospirillum brasilense strains upon wheat inoculation. Plant and Soil 212, 155–164.CrossRefGoogle Scholar
Dobritzsch, D., Konig, S., Schneider, G. and Lu, G. (1998). High resolution crystal structure of pyruvate decarboxylase from Zymomonas mobilis. Implications for substrate activation in pyruvate decarboxylases. Journal of Biological Chemistry 273, 20196–20204.CrossRefGoogle ScholarPubMed
Dollet, M. (1984). Plant diseases caused by flagellate Protozoa. Annual Review of Phytopathology 22, 115–132.CrossRefGoogle Scholar
Dollet, M. (2001). Phloem-restricted trypanosomatids form a clearly characterised monophyletic group among trypanosomatids isolated from plants. International Journal for Parasitology 31, 459–467.CrossRefGoogle Scholar
Duggleby, R. G. (2006). Domain relationships in thiamine diphosphate-dependent enzymes. Accounts of Chemical Research 39, 550–557.CrossRefGoogle ScholarPubMed
el Sawalhy, A., Seed, J. R., el Attar, H. and Hall, J. E. (1995). Catabolism of tryptophan by Trypanosoma evansi . Journal of Eukaryotic Microbiology 42, 684–690.CrossRefGoogle ScholarPubMed
Fedorov, D. N., Doronina, N. V. and Trotsenko, Y. A. (2010). Cloning and characterization of indolepyruvate decarboxylase from Methylobacterium extorquens AM1. Biochemistry (Mosc.) 75, 1435–1443.CrossRefGoogle ScholarPubMed
Gibson, R. A., Schneider, E. A. and Wightman, F. (1972). Biosynthesis and metabolism of indol-3yl-acetic acid: II. In vivo experiments with 14C-labelled precursors of IAA in tomato and barley shoots. Journal of Experimental Botany 23, 381–399.CrossRefGoogle Scholar
Hall, T. A. (1999). BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Ienne, S., Pappas, G. Jr., Benabdellah, K., González, A. and Zingales, B. (2012). Horizontal gene transfer confers fermentative metabolism in the respiratory-deficient plant trypanosomatid Phytomonas serpens . Infection, Genetics and Evolution 12, 539–548.CrossRefGoogle ScholarPubMed
Jankevicius, J. V., Jankevicius, S. I., Campaner, M., Conchon, I., Maeda, L. A., Teixeira, M. M. G., Freymuller, E. and Camargo, E. P. (1989). Life cycle and culturing of Phytomonas serpens (Gibbs), a trypanosomatid parasite of tomatoes. Journal of Protozoology 36, 265–271.CrossRefGoogle Scholar
Kelly, M. O. and Bradford, K. J. (1986). Insensitivity of the diageotropica tomato mutant to auxin. Plant Physiology 82, 713–717.CrossRefGoogle ScholarPubMed
Kiefer, F., Arnold, K., Künzli, M., Bordoli, L. and Schwede, T. (2009). The SWISS-MODEL Repository and associated resources. Nucleic Acids Research 37, D387–D392.CrossRefGoogle ScholarPubMed
Koga, J. (1995). Structure and function of indolepyruvate decarboxylase, a key enzyme in indole-3-acetic acid biosynthesis. Biochimica et Biophysica Acta 1249, 1–13.CrossRefGoogle ScholarPubMed
Koga, J., Adachi, T. and Hidaka, H. (1991). IAA biosynthetic pathway from tryptophan via indole-3-pyruvic acid in Enterobacter cloacae . Agricultural and Biological Chemistry 55, 701–706.Google Scholar
Koga, J., Adachi, T. and Hidaka, H. (1992). Purification and characterization of indolepyruvate decarboxylase. A novel enzyme for indole-3-acetic acid biosynthesis in Enterobacter cloacae . Journal of Biological Chemistry 267, 15823–15828.CrossRefGoogle ScholarPubMed
Korený, L., Lukes, J. and Oborník, M. (2010). Evolution of the haem synthetic pathway in kinetoplastid flagellates: an essential pathway that is not essential after all? International Journal for Parasitology 40, 149–156.CrossRefGoogle ScholarPubMed
Lovell, S. C., Davis, I. W., Arendall, W. B. III, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S. and Richardson, D. C. (2003). Structure validation by Cα geometry: ϕ/ψ and Cβ deviation. Proteins 50, 437–450.CrossRefGoogle ScholarPubMed
Ludwig-Müller, J. (2011). Auxin conjugates: their role for plant development and in the evolution of land plants. Journal of Experimental Botany 62, 1757–1773.CrossRefGoogle ScholarPubMed
Ludwig-Müller, J., Georgiev, M. and Bley, T. (2008). Metabolite and hormonal status of hairy root cultures of Devil's claw (Harpagophytum procumbens) in flasks and in a bubble column bioreactor. Process Biochemistry 43, 15–23.CrossRefGoogle Scholar
Maslov, D. A., Nawathean, P. and Scheel, J. (1999). Partial kinetoplast-mitochondrial gene organization and expression in the respiratory deficient plant trypanosomatid Phytomonas serpens . Molecular and Biochemical Parasitology 99, 207–221.CrossRefGoogle ScholarPubMed
Moore, T. C. and Shaner, C. A. (1968). Synthesis of indoleacetic acid from tryptophan via indolepyruvic acid in cell-free extracts of pea seedlings. Archives of Biochemistry and Biophysics 127, 61321.CrossRefGoogle ScholarPubMed
Morris, R. O. (1995). Genes specifying auxin and cytokinin biosynthesis in prokaryotes. In Plant Hormones: Physiology, Biochemistry and Molecular Biology (ed. Davies, P. J.), pp. 318–339. Kluwer Academic, Dordrecht, the Netherlands.CrossRefGoogle Scholar
Murashige, T. and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.CrossRefGoogle Scholar
Nawathean, P. and Maslov, D. A. (2000). The absence of genes for cytochrome c oxidase and reductase subunits in maxicircle kinetoplast DNA of the respiration-deficient plant trypanosomatid Phytomonas serpens . Current Genetics 38, 95–103.CrossRefGoogle ScholarPubMed
Opperdoes, F. R. and Michels, P. A. (2007). Horizontal gene transfer in trypanosomatids. Trends in Parasitology 23, 470–476.CrossRefGoogle ScholarPubMed
Pei, X. Y., Erixon, K. M., Luisi, B. F. and Leeper, F. J. (2010). Structural insights into the prereaction state of pyruvate decarboxylase from Zymomonas mobilis . Biochemistry 49, 1727–1736.CrossRefGoogle ScholarPubMed
Peitsch, M. C. (1995). Protein modeling by e-mail. Nature Biotechnology 13, 658–660.CrossRefGoogle Scholar
Pino-Nunes, L. E., de O. Figueira, A. V., Tulmann Neto, A., Zsögön, A., Piotto, F. A., Silva, J. A., Bernardi, W. F. and Peres, L. E. P. (2009). Induced mutagenesis and natural genetic variation in tomato ‘Micro-Tom’. Acta Horticulturae 821, 63–72.CrossRefGoogle Scholar
Purgatto, E., Nascimento, J. R. O., Lajolo, F. M. and Cordenunsi, B. R. (2002). The onset of starch degradation during banana ripening is concomitant to changes in the content of free and conjugated forms of indole-3-acetic acid. Journal of Plant Physiology 159, 1105–1111.CrossRefGoogle Scholar
Rosquete, M. R., Barbez, E. and Kleine-Vehn, J. (2012). Cellular auxin homeostasis: gatekeeping is housekeeping. Molecular Plant 5, 772–786.CrossRefGoogle ScholarPubMed
Sanchez-Moreno, M., Lasztity, D., Coppens, I. and Opperdoes, F. R. (1992). Characterization of carbohydrate metabolism and demonstration of glycosomes in a Phytomonas sp. isolated from Euphorbia characias . Molecular and Biochemical Parasitology 54, 185–199.CrossRefGoogle Scholar
Sbravate, C., Campaner, M., Camargo, L. E. A., Conchon, I., Teixseira, M. M. G. and Camargo, E. P. (1989). Culture and generic identification of trypanosomatids of phytophagous Hemiptera in Brazil. Journal of Eukaryotic Microbiology 36, 543–547.Google Scholar
Schütz, A., Golbik, R., Tittmann, K., Svergun, D. I., Koch, M. H., Hübner, G. and König, S. (2003 a). Studies on structure-function relationships of indolepyruvate decarboxylase from Enterobacter cloacae, a key enzyme of the indole acetic acid pathway. European Journal of Biochemistry 270, 2322–2331.CrossRefGoogle ScholarPubMed
Schütz, A., Sandalova, T., Ricagno, S., Hübner, G., König, S. and Schneider, G. (2003 b). Crystal structure of thiamindiphosphate-dependent indolepyruvate decarboxylase from Enterobacter cloacae, an enzyme involved in the biosynthesis of the plant hormone indole-3-acetic acid. European Journal of Biochemistry 270, 2312–2321.CrossRefGoogle ScholarPubMed
Seidel, C., Walz, A., Park, S., Cohen, J. D. and Ludwig-Müller, J. (2006). Indole-3-acetic acid protein conjugates: novel players in auxin homeostasis. Plant Biology (Stuttgart, Germany) 8, 340–345.CrossRefGoogle ScholarPubMed
Shin, M., Shinguu, T., Sano, K. and Umezawa, C. (1991). Metabolic fates of L-tryptophan in Saccharomyces uvarum (Saccharomyces carlsbergensis). Chemical and Pharmaceutical Bulletin 39, 1792–1795.CrossRefGoogle ScholarPubMed
Spaepen, S., Vanderleyden, J. and Remans, R. (2007). Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiology Reviews 31, 425–448.CrossRefGoogle ScholarPubMed
Teale, W. D., Paponov, I. A. and Palme, K. (2006). Auxin in action: signalling, transport and the control of plant growth and development. Nature Reviews Molecular Cell Biology 7, 847–859.CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Truelsen, T. A. (1973). Indole-3-pyruvic acid as an intermediate in the conversion of tryptophan to indole-3-acetic acid. II. Distribution of tryptophan transaminase. Physiologia Plantarum 28, 67–70.CrossRefGoogle Scholar
Woodward, A. W. and Bartel, B. (2005). Auxin: regulation, action, and interaction. Annals of Botany 95, 707–735.CrossRefGoogle ScholarPubMed
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