Gene networks underlying the early regulation of Paraburkholderia phytofirmans PsJN induced systemic resistance in Arabidopsis

PLoS One. 2019 Aug 22;14(8):e0221358. doi: 10.1371/journal.pone.0221358. eCollection 2019.

Abstract

Plant defense responses to biotic stresses are complex biological processes, all governed by sophisticated molecular regulations. Induced systemic resistance (ISR) is one of these defense mechanisms where beneficial bacteria or fungi prime plants to resist pathogens or pest attacks. In ISR, the defense arsenal in plants remains dormant and it is only triggered by an infection, allowing a better allocation of plant resources. Our group recently described that the well-known beneficial bacterium Paraburkholderia phytofirmans PsJN is able to induce Arabidopsis thaliana resistance to Pseudomonas syringae pv. tomato (Pst) DC3000 through ISR, and that ethylene, jasmonate and salicylic acid are involved in this protection. Nevertheless, the molecular networks governing this beneficial interaction remain unknown. To tackle this issue, we analyzed the temporal changes in the transcriptome of PsJN-inoculated plants before and after being infected with Pst DC3000. These data were used to perform a gene network analysis to identify highly connected transcription factors. Before the pathogen challenge, the strain PsJN regulated 405 genes (corresponding to 1.8% of the analyzed genome). PsJN-inoculated plants presented a faster and stronger transcriptional response at 1-hour post infection (hpi) compared with the non-inoculated plants, which presented the highest transcriptional changes at 24 hpi. A principal component analysis showed that PsJN-induced plant responses to the pathogen could be differentiated from those induced by the pathogen itself. Forty-eight transcription factors were regulated by PsJN at 1 hpi, and a system biology analysis revealed a network with four clusters. Within these clusters LHY, WRKY28, MYB31 and RRTF1 are highly connected transcription factors, which could act as hub regulators in this interaction. Concordantly with our previous results, these clusters are related to jasmonate, ethylene, salicylic, acid and ROS pathways. These results indicate that a rapid and specific response of PsJN-inoculated plants to the virulent DC3000 strain could be the pivotal element in the protection mechanism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics*
  • Arabidopsis / immunology
  • Arabidopsis / microbiology
  • Burkholderiaceae / physiology*
  • Cyclopentanes / immunology
  • Cyclopentanes / metabolism
  • Disease Resistance / genetics
  • Ethylenes / immunology
  • Ethylenes / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant / immunology*
  • Gene Regulatory Networks / immunology
  • Oxylipins / immunology
  • Oxylipins / metabolism
  • Plant Diseases / genetics*
  • Plant Diseases / immunology
  • Plant Diseases / microbiology
  • Plant Growth Regulators / immunology
  • Plant Growth Regulators / metabolism
  • Plant Immunity / genetics
  • Principal Component Analysis
  • Pseudomonas syringae / growth & development
  • Pseudomonas syringae / pathogenicity*
  • Salicylic Acid / immunology
  • Salicylic Acid / metabolism
  • Transcription Factors / genetics*
  • Transcription Factors / immunology
  • Transcriptome / immunology

Substances

  • Cyclopentanes
  • Ethylenes
  • Oxylipins
  • Plant Growth Regulators
  • Transcription Factors
  • jasmonic acid
  • ethylene
  • Salicylic Acid

Supplementary concepts

  • Paraburkholderia phytofirmans

Grants and funding

FONDECYT grants 1151130 (B.G) and 1190634 (M.J.P.) and CONICYT PIA/BASAL FB0002 (B.G. and M.J.P.) funded this research. T. Timmermann was supported by a Ph.D. fellowship from the National Commission for Science and Technology, CONICYT, Chile. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.