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Dynamic metabolic reprogramming of steroidal glycol-alkaloid and phenylpropanoid biosynthesis may impart early blight resistance in wild tomato (Solanum arcanum Peralta)

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Exploration with high throughput leaf metabolomics along with functional genomics in wild tomato unreveal potential role of steroidal glyco-alkaloids and phenylpropanoids during early blight resistance.

Abstract

Alternaria solani severely affects tomato (Solanum lycopersicum L.) yield causing early blight (EB) disease in tropical environment. Wild relative, Solanum arcanum Peralta could be a potential source of EB resistance; however, its underlying molecular mechanism largely remains unexplored. Hence, non-targeted metabolomics was applied on resistant and susceptible S. arcanum accessions upon A. solani inoculation to unravel metabolic dynamics during different stages of disease progression. Total 2047 potential metabolite peaks (mass signals) were detected of which 681 and 684 metabolites revealed significant modulation and clear differentiation in resistant and susceptible accessions, respectively. Majority of the EB-triggered metabolic changes were active from steroidal glycol-alkaloid (SGA), lignin and flavonoid biosynthetic pathways. Further, biochemical and gene expression analyses of key enzymes from these pathways positively correlated with phenotypic variation in the S. arcanum accessions indicating their potential role in EB. Additionally, transcription factors regulating lignin biosynthesis were also up-regulated in resistant plants and electrophoretic mobility shift assay revealed sequence-specific binding of rSaWRKY1 with MYB20 promoter. Moreover, transcript accumulation of key genes from phenylpropanoid and SGA pathways along with WRKY and MYB in WRKY1 transgenic tomato lines supported above findings. Overall, this study highlights vital roles of SGAs as phytoalexins and phenylpropanoids along with lignin accumulation unrevealing possible mechanistic basis of EB resistance in wild tomato.

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Acknowledgements

BAS and ACK are thankful to University Grant Commission (UGC) and Council of Scientific and Industrial Research (CSIR), New Delhi, India for senior research fellowship and financial support [60(0101)/11/EMR-II] to Savitribai Phule Pune University, respectively, along-with funding under XII 5 year plan project BSC0107 to CSIR-National Chemical Laboratory. Authors thank Dr. Oren Tzfadia (Ghent University, Belgium) for co-expression analysis.

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Authors and Affiliations

  1. Department of Botany, Savitribai Phule Pune University, Pune, Maharashtra, 411007, India

    Balkrishna A. Shinde, Khalid Hussain, Sayantan Panda & Avinash C. Kamble

  2. Division of Biochemical Sciences, Plant Molecular Biology Unit, CSIR-National Chemical Laboratory, Pune, Maharashtra, 411008, India

    Balkrishna A. Shinde, Bhushan B. Dholakia & Ashok P. Giri

  3. Department of Plant and Environmental Sciences, Weizmann Institute of Science, 7610001, Rehovot, Israel

    Balkrishna A. Shinde, Sayantan Panda, Sagit Meir, Ilana Rogachev & Asaph Aharoni

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  1. Balkrishna A. Shinde
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  2. Bhushan B. Dholakia
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  3. Khalid Hussain
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  9. Avinash C. Kamble
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Contributions

BAS, APG and ACK planned and designed the study. BAS performed majority of the experiments. SM, SP and IR acquired and analyzed the metabolic data. KH carried out transgenic and lignin quantification assay. AA provided tomato transcriptomic data and helped in analysis of it. BAS and BBD analyzed the data, prepared the figures, tables and wrote the manuscript. APG, ACK and AA corrected the manuscript.

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Correspondence to Ashok P. Giri or Avinash C. Kamble.

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Shinde, B.A., Dholakia, B.B., Hussain, K. et al. Dynamic metabolic reprogramming of steroidal glycol-alkaloid and phenylpropanoid biosynthesis may impart early blight resistance in wild tomato (Solanum arcanum Peralta). Plant Mol Biol 95, 411–423 (2017). https://doi.org/10.1007/s11103-017-0660-2

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