Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate

Authors

  • Denise Tieman,

    1. Plant Molecular and Cellular Biology Program, Horticultural Sciences, University of Florida, Gainesville, FL 32611-0690, USA
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  • Michelle Zeigler,

    1. Plant Molecular and Cellular Biology Program, Horticultural Sciences, University of Florida, Gainesville, FL 32611-0690, USA
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  • Eric Schmelz,

    1. United States Department of Agriculture – Agricultural Research Service, Center for Medical Agricultural and Veterinary Entomology, 1700 SW 23rd Drive, Gainesville, FL 32608, USA
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  • Mark G. Taylor,

    1. Plant Molecular and Cellular Biology Program, Horticultural Sciences, University of Florida, Gainesville, FL 32611-0690, USA
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  • Sarah Rushing,

    1. Plant Molecular and Cellular Biology Program, Horticultural Sciences, University of Florida, Gainesville, FL 32611-0690, USA
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  • Jeffrey B. Jones,

    1. Plant Molecular and Cellular Biology Program, Horticultural Sciences, University of Florida, Gainesville, FL 32611-0690, USA
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  • Harry J. Klee

    Corresponding author
    1. Plant Molecular and Cellular Biology Program, Horticultural Sciences, University of Florida, Gainesville, FL 32611-0690, USA
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Summary

Methyl salicylate (MeSA) is a volatile plant secondary metabolite that is an important contributor to taste and scent of many fruits and flowers. It is synthesized from salicylic acid (SA), a phytohormone that contributes to plant pathogen defense. MeSA is synthesized by members of a family of O-methyltransferases. In order to elaborate the mechanism of MeSA synthesis in tomato, we screened a set of O-methyltransferases for activity against multiple substrates. An enzyme that specifically catalyzes methylation of SA, SlSAMT, as well as enzymes that act upon jasmonic acid and indole-3-acetic acid were identified. Analyses of transgenic over- and under-producing lines validated the function of SlSAMT in vivo. The SlSAMT gene was mapped to a position near the bottom of chromosome 9. Analysis of MeSA emissions from an introgression population derived from a cross with Solanum pennellii revealed a quantitative trait locus (QTL) linked to higher fruit methyl salicylate emissions. The higher MeSA emissions associate with significantly higher SpSAMT expression, consistent with SAMT gene expression being rate limiting for ripening-associated MeSA emissions. Transgenic plants that constitutively over-produce MeSA exhibited only slightly delayed symptom development following infection with the disease-causing bacterial pathogen, Xanthomonas campestris pv. vesicatoria (Xcv). Unexpectedly, pathogen-challenged leaves accumulated significantly higher levels of SA as well as glycosylated forms of SA and MeSA, indicating a disruption in control of the SA-related metabolite pool. Taken together, the results indicate that SlSAMT is critical for methyl salicylate synthesis and methyl salicylate, in turn, likely has an important role in controlling SA synthesis.

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