Plasticity of Phymatotrichopsis omnivora infection strategies is dependent on host and nonhost plant responses

Prasanna Kankanala, Piet Jones, Raja Sekhar Nandety, Daniel A. Jacobson, Kirankumar S. Mysore

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

Abstract

Necrotrophic fungi constitute the largest group of plant fungal pathogens that cause heavy crop losses worldwide. Phymatotrichopsis omnivora is a broad host, soil-borne necrotrophic fungal pathogen that infects over 2,000 dicotyledonous plants. The molecular basis of such broad host range is unknown. We conducted cell biology and transcriptomic studies in Medicago truncatula (susceptible), Brachypodium distachyon (resistant/nonhost), and Arabidopsis thaliana (partially resistant) to understand P. omnivora virulence mechanisms. We performed defence gene analysis, gene enrichments, and correlational network studies during key infection stages. We identified that P. omnivora infects the susceptible plant as a traditional necrotroph. However, it infects the partially resistant plant as a hemi-biotroph triggering salicylic acid-mediated defence pathways in the plant. Further, the infection strategy in partially resistant plants is determined by the host responses during early infection stages. Mutant analyses in A. thaliana established the role of small peptides PEP1 and PEP2 in defence against P. omnivora. The resistant/nonhost B. distachyon triggered stress responses involving sugars and aromatic acids. Bdwat1 mutant analysis identified the role of cell walls in defence. This is the first report that describes the plasticity in infection strategies of P. omnivora providing insights into broad host range.

Original languageEnglish
Pages (from-to)1084-1101
Number of pages18
JournalPlant Cell and Environment
Volume43
Issue number4
DOIs
StatePublished - Apr 1 2020

Funding

We thank Dr Maria Harrison for transgenic Medicago truncatula lines expressing marker genes, Drs Yusuke Saijo, Wolf Schieble, and Yube Yamaguchi for Arabidopsis thaliana mutant lines, and Dr John Vogel for Brachypodium distachyon mutant line. We greatly appreciate the help received from Dr Hee-Kyung Lee and Ms Sunhee Oh in conducting the experiments. This work was supported by Noble Research Institute, LLC. This research used resources of the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory (ORNL), which is supported by the Office of Science (OoS) of the U.S. Department of Energy (DOE) under Contract No. DE-AC05-00OR22725. This research was also supported by the Plant-Microbe Interfaces SFA in the Office of Biological and Environmental Research in the DOE OoS, and by DOE LDRD funding (ProjectID 8321) at ORNL.

Keywords

  • Phymatotrichopsis root rot
  • RNA sequencing
  • fungal plasticity
  • hemi-biotrophy
  • necrotrophy
  • nonhost resistance
  • plant–fungal interactions
  • systems biology

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