Dynamic metabolic reprogramming of steroidal glycol-alkaloid and phenylpropanoid biosynthesis may impart early blight resistance in wild tomato (Solanum arcanum Peralta)
- 495 Downloads
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.
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.
KeywordsEarly blight Metabolomics MYB SGA Solanum arcanum Tomato WRKY
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.
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.
Compliance with ethical standards
Conflict of interest
Authors declare no conflict of interest.
- Agrios GN (2005) Plant pathology, 5th edn. Academic Press, New YorkGoogle Scholar
- Barvkar VT, Pardeshi VC, Kale SM, Qiu S, Rollins M, Datla R, Gupta VS, Kadoo NY (2013) Genome-wide identification and characterization of microRNA genes and their targets in flax (Linum usitatissimum): characterization of flax miRNA genes. Planta 237:1149–1161. doi: 10.1007/s00425-012-1833-5 CrossRefPubMedGoogle Scholar
- Bonello P, Storer AJ, Gordon TR, Wood DL, Heller W (2003) Systemic effects of Heterobasidion annosum on ferulic acid glucoside and lignin of presymptomatic ponderosa pine phloem, and potential effects on bark-beetle-associated fungi. J Chem Ecol 29:1167–1182. doi: 10.1023/A:1023833707382 CrossRefPubMedGoogle Scholar
- Eynck C, Koopmann B, Grunewaldt-Stoecker G, Karlovsky P, Tiedemann A (2007) Differential interactions of Verticillium longisporum and V. dahliae with Brassica napus detected with molecular and histological techniques. Eur J Plant Pathol 118:259–274. doi: 10.1007/s10658-007-9144-6 CrossRefGoogle Scholar
- Grunewald W, De Smet I, Lewis DR, Löfke C, Jansen L, Goeminne G, Vanden Bosschea R, Karimi M, De Rybela B, Vanholmea B, Teichmannf T, Boerjana W, Van Montagub MCE, Gheysenc G, Mudaye GK, Frimla J, Beeckman T (2011) Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on fl avonol biosynthesis. Proc Natl Acad Sci USA 109:1554–1559. doi: 10.1073/pnas.1121134109 CrossRefGoogle Scholar
- Heinig U, Aharoni A (2014) Analysis of steroidal alkaloids and saponins in Solanaceae plant extracts using UPLC-qTOF mass spectrometry. In: Rodríguez-Concepción M (ed) Plant isoprenoids. Methods in molecular biology (methods and protocols), vol 1153. Humana Press, New York, pp 171–185Google Scholar
- Itkin M, Rogachev I, Alkan N, Rosenberg T, Malitsky S, Masini L, Meir S, Iijima Y, Aoki K, de Vos R, Prusky D, Burdman S, Beekwilder J, Aharoni A (2011) GLYCOALKALOID METABOLISM1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato. Plant Cell 23:4507–4525. doi: 10.1105/tpc.111.088732 CrossRefPubMedPubMedCentralGoogle Scholar
- Itkin M, Heinig U, Tzfadia O, Bhide AJ, Shinde B, Cardenas PD, Bocobza SE, Unger T, Malitsky S, Finkers R, Tikunov Y, Bovy A, Chikate Y, Singh P, Rogachev I, Beekwilder J, Giri AP, Aharoni A (2013) Biosynthesis of antinutritional alkaloids in solanaceous crops Is mediated by clustered genes. Science 341:175–179. doi: 10.1021/jf061471t CrossRefPubMedGoogle Scholar
- Lattanzio V, Lattanzio VMT, Cardinali A, Amendola V (2006) Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. In: Imperato F (ed) Phytochemistry: advances in research. Research Signpost, Trivandrum, pp 23–67Google Scholar
- Saha P, Das S (2012) Assessment of yield loss due to early blight (Alternaria solani) in tomato. Indian J Plant Prot 40:195–198Google Scholar
- Schenk ST, Hernández-Reyes C, Samans B, Stein E, Neumann C, Schikora M, Reichelt M, Mithöfer A, Becker A, Kogel K-H, Schikora A (2014) N-Acyl-homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. Plant Cell 26:2708–2723. doi: 10.1105/tpc.114.126763 CrossRefPubMedPubMedCentralGoogle Scholar
- Taylor-Teeples M, Lin L, De Lucas M, Turco G, Toal TW, Gaudinier A, Young NF, Trabucco GM, Veling MT, Lamothe R, Handakumbura PP, Xiong G, Wang C, Corwin J, Tsoukalas A, Zhang L, Ware D, Pauly M, Kliebenstein DJ, Dehesh K, Tagkopoulos I, Breton G, Pruneda-Paz JL, Ahnert SE, Kay SA, Hazen SP, Brady SM (2015) An Arabidopsis gene regulatory network for secondary cell wall synthesis. Nature 517:571–575. doi: 10.1038/nature14099 CrossRefPubMedGoogle Scholar