Resistance against Sclerotinia sclerotiorum in soybean involves a reprogramming of the phenylpropanoid pathway and up-regulation of antifungal activity targeting ergosterol biosynthesis

Ashish Ranjan, Nathaniel M. Westrick, Sachin Jain, Jeff S. Piotrowski, Manish Ranjan, Ryan Kessens, Logan Stiegman, Craig R. Grau, Shawn P. Conley, Damon L. Smith, Mehdi Kabbage

Research output: Contribution to journalArticlepeer-review

Abstract

Sclerotinia sclerotiorum, a predominately necrotrophic fungal pathogen with a broad host range, causes a significant yield-limiting disease of soybean called Sclerotinia stem rot. Resistance mechanisms against this pathogen in soybean are poorly understood, thus hindering the commercial deployment of resistant varieties. We used a multiomic approach utilizing RNA-sequencing, gas chromatography–mass spectrometry-based metabolomics and chemical genomics in yeast to decipher the molecular mechanisms governing resistance to S. sclerotiorum in soybean. Transcripts and metabolites of two soybean recombinant inbred lines, one resistant and one susceptible to S. sclerotiorum were analysed in a time course experiment. The combined results show that resistance to S. sclerotiorum in soybean is associated in part with an early accumulation of JA-Ile ((+)-7-iso-jasmonoyl-L-isoleucine), a bioactive jasmonate, increased ability to scavenge reactive oxygen species, and importantly, a reprogramming of the phenylpropanoid pathway leading to increased antifungal activities. Indeed, we noted that phenylpropanoid pathway intermediates, such as 4-hydroxybenzoate, cinnamic acid, ferulic acid and caffeic acid, were highly accumulated in the resistant line. In vitro assays show that these metabolites and total stem extracts from the resistant line clearly affect S. sclerotiorum growth and development. Using chemical genomics in yeast, we further show that this antifungal activity targets ergosterol biosynthesis in the fungus, by disrupting enzymes involved in lipid and sterol biosynthesis. Overall, our results are consistent with a model where resistance to S. sclerotiorum in soybean coincides with an early recognition of the pathogen, leading to the modulation of the redox capacity of the host and the production of antifungal metabolites.

Original languageEnglish (US)
Pages (from-to)1567-1581
Number of pages15
JournalPlant Biotechnology Journal
Volume17
Issue number8
DOIs
StatePublished - Aug 2019
Externally publishedYes

Bibliographical note

Funding Information:
We thank Grace Brunette and Haley Mesick for their technical assistance. We thank Professor Caitilyn Allen and her group for stimulating discussions. Next-generation sequencing was performed by the Biotechnology Center at the University of Wisconsin-Madison. Funding was provided by the Wisconsin Soybean Marketing Board and the North Central Soybean Research Program.

Publisher Copyright:
© 2019 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.

Keywords

  • Sclerotinia sclerotiorum
  • antifungal metabolites
  • ergosterol
  • jasmonate signalling
  • necrotrophic fungi
  • phenylpropanoid pathway
  • reactive oxygen species
  • resistance

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