Disclosing proteins in the leaves of cork oak plants associated with the immune response to Phytophthora cinnamomi inoculation in the roots: A long-term proteomics approach

PLoS One. 2021 Jan 22;16(1):e0245148. doi: 10.1371/journal.pone.0245148. eCollection 2021.

Abstract

The pathological interaction between oak trees and Phytophthora cinnamomi has implications in the cork oak decline observed over the last decades in the Iberian Peninsula. During host colonization, the phytopathogen secretes effector molecules like elicitins to increase disease effectiveness. The objective of this study was to unravel the proteome changes associated with the cork oak immune response triggered by P. cinnamomi inoculation in a long-term assay, through SWATH-MS quantitative proteomics performed in the oak leaves. Using the Arabidopis proteome database as a reference, 424 proteins were confidently quantified in cork oak leaves, of which 80 proteins showed a p-value below 0.05 or a fold-change greater than 2 or less than 0.5 in their levels between inoculated and control samples being considered as altered. The inoculation of cork oak roots with P. cinnamomi increased the levels of proteins associated with protein-DNA complex assembly, lipid oxidation, response to endoplasmic reticulum stress, and pyridine-containing compound metabolic process in the leaves. In opposition, several proteins associated with cellular metabolic compound salvage and monosaccharide catabolic process had significantly decreased abundances. The most significant abundance variations were observed for the Ribulose 1,5-Bisphosphate Carboxylase small subunit (RBCS1A), Heat Shock protein 90-1 (Hsp90-1), Lipoxygenase 2 (LOX2) and Histone superfamily protein H3.3 (A8MRLO/At4G40030) revealing a pertinent role for these proteins in the host-pathogen interaction mechanism. This work represents the first SWATH-MS analysis performed in cork oak plants inoculated with P. cinnamomi and highlights host proteins that have a relevant action in the homeostatic states that emerge from the interaction between the oomycete and the host in the long term and in a distal organ.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Phytophthora / immunology*
  • Plant Diseases* / immunology
  • Plant Diseases* / microbiology
  • Plant Leaves / immunology
  • Plant Leaves / microbiology
  • Plant Proteins / immunology*
  • Plant Roots* / immunology
  • Plant Roots* / microbiology
  • Proteomics
  • Quercus* / immunology
  • Quercus* / microbiology
  • Spain

Substances

  • Plant Proteins

Grant support

This work was financially supported by FCT, integrated in projects UID/Multi/00631/2013, UID/Multi/00631/2019 and UIDB/00631/2020 CEOT BASE to CEOT and ACC, GS and RP; UIDB/04326/2020 to CCMAR; fellowship SFRH/BPD/84033/2012 and researcher contract with the University of Algarve under Norma Transitória-DL57/2016/CP1361/CT0015 to PP; contract NIBAP (ALG-01-0247-FEDER-037303) to RP; projects POCI-01-0145-FEDER-007440 (Ref. UIDB/04539/2020), POCI-01-0145-FEDER-016428 (Ref. SAICTPAC/0010/2015), POCI-01-0145-FEDER-029311 (Ref. PTDC/BTM-TEC/29311/2017), POCI-01-0145-FEDER-30943 (Ref. PTDC/MECPSQ/30943/2017) and PTDC/MED-NEU/27946/2017 to CNC, BM and CS. The work at CNC was also funded by the National Mass Spectrometry Network (RNEM) under contract POCI-01-0145-FEDER-402-022125 (Ref. ROTEIRO/0028/2013). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.