Abstract
Eucalyptus rust is caused by the biotrophic fungus, Austropuccinia psidii, which affects commercial plantations of Eucalyptus, a major raw material for the pulp and paper industry in Brazil. In this manuscript we aimed to uncover the molecular mechanisms involved in rust resistance and susceptibility in Eucalyptus grandis. Epifluorescence microscopy was used to follow the fungus development inside the leaves of two contrasting half-sibling genotypes (rust-resistance and rust-susceptible), and also determine the comparative time-course of changes in metabolites and proteins in plants inoculated with rust. Within 24 h of complete fungal invasion, the analysis of 709 metabolomic features showed the suppression of many metabolites 6 h after inoculation (hai) in the rust-resistant genotype, with responses being induced after 12 hai. In contrast, the rust-susceptible genotype displayed more induced metabolites from 0 to 18 hai time-points, but a strong suppression occurred at 24 hai. Multivariate analyses of genotypes and time points were used to select 16 differential metabolites mostly classified as phenylpropanoid-related compounds. Applying the Weighted Gene Co-Expression Network Analysis (WGCNA), rust-resistant and rust-susceptible genotypes had, respectively, 871 and 852 proteins grouped into 5 and 6 modules, of which 5 and 4 of them were significantly correlated to the selected metabolites. Functional analyses revealed roles for photosynthesis and oxidative-dependent responses leading to temporal activity of metabolites and related enzymes after 12 hai in rust-resistance; while the initial over-accumulation of those molecules and suppression of supporting mechanisms at 12 hai caused a lack of progressive metabolite-enzyme responses after 12 hai in rust-susceptible genotype. This study provides some insights on how E. grandis plants are functionally modulated to integrate secondary metabolites and related enzymes from phenylpropanoid pathway and lead to temporal divergences of resistance and susceptibility responses to rust.
Highlights
Eucalyptus ssp. is a genus highly utilized in commercial forestry, with more than 700 species involved in many industrial agribusinesses (EMBRAPA, 2019)
Aiming to briefly understand the molecular mechanisms surrounding the early interaction between E. grandis and A. psidii, we describe a detailed time-course microscopy study to characterize the specific events that occur during the development of the A. psidii infection in both, resistant and susceptible genotypes
Evidence of rust disease was observed in inoculated S4 plants appearing as yellow pustules containing spores on leaf surfaces at 11 dai, while inoculated R3 leaves displayed mild flecking response for resistance mediated by HR
Summary
Eucalyptus ssp. is a genus highly utilized in commercial forestry, with more than 700 species involved in many industrial agribusinesses (EMBRAPA, 2019). Because of its vigor and rapid growth (Moon et al, 2007), Eucalyptus grandis and its hybrids are continuously improved to enhance their capacity to provide raw material for the pulp and paper companies in Brazil, the second largest producer of cellulose in the world (EMBRAPA, 2019). Rust, caused by the biotrophic fungus Austropuccinia psidii (A. psidii), is one of the most harmful diseases affecting Eucalyptus plantations, and considerably reduces their productivity, in the first 2 years of plant development (Takahashi, 2002). Since E. grandis is commonly susceptible to pathogens, geneticists and breeders have used genomic tools applied to conventional breeding to select new rust-resistant genotypes and enhance the development of the generation trees (Zamprogno et al, 2008; Boava et al, 2010; Silva et al, 2013; Laia et al, 2015; Butler et al, 2016). In plant immune regulation, there has been evidence describing that even the induction of transcripts cannot sufficiently predict temporal changes in protein abundance (Xu et al, 2017)
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