Roots drive oligogalacturonide-induced systemic immunity in tomato

Abstract

Oligogalacturonides (OGs) are fragments of pectin released from the plant cell wall during insect or pathogen attack. They can be perceived by the plant as damage signals, triggering local and systemic defence responses. Here, we analyse the dynamics of local and systemic responses to OG perception in tomato roots or shoots, exploring their impact across the plant and their relevance in pathogen resistance. Targeted and untargeted metabolomics and gene expression analysis in plants treated with purified OGs revealed that local responses were transient, while distal responses were stronger and more sustained. Remarkably, changes were more conspicuous in roots, even upon foliar application of the OGs. The treatments differentially activated the synthesis of defence-related hormones and secondary metabolites including flavonoids, alkaloids and lignans, some of them exclusively synthetized in roots. Finally, the biological relevance of the systemic defence responses activated upon OG perception was confirmed, as the treatment induced systemic resistance to Botrytis cinerea. Overall, this study shows the differential regulation of tomato defences upon OGs perception in roots and shoots and reveal the key role of roots in the coordination of the plant responses to damage sensing.

The phenylpropanoid pathway inhibitor piperonylic acid induces broad‐spectrum pest and disease resistance in plants

“…This suggests that PA-IR involves systemic transcriptional changes, while direct accumulation of (defence-related) metabolites is mostly confined to local tissues. By contrast, metabolome analysis of tomato plants foliarly treated with oligogalacturonides found greater metabolic changes in distal root tissues than in directly treated leaves (Gamir et al, 2020).…”

“…The accumulation of (often glycosylated) PPP derivatives is a hallmark of IR that has been observed after treatment with diverse IR stimuli in several plant species (Ameye et al, 2020;Gamir et al, 2020;Huang et al, 2021;Mhlongo, Steenkamp, Piater, Madala, & Dubery, 2016 (Mandal, Chakraborty, & Dey, 2010;Saijo & Loo, 2020). Second, PPP derivatives contribute to the PA-IR phenotype through their roles as phytoanticipins/phytoalexins (Desmedt et al, 2020;Yadav et al, 2020) and building blocks for cell wall reinforcement (Vogt, 2010).…”

The plasma membrane–associated Ca2+‐binding protein,PCaP1,is required for oligogalacturonide and flagellin‐induced priming and immunity

“…In the cell wall, the interaction between PGs and polygalacturonase‐inhibiting proteins (PGIPs) enhances the formation of OGs (Benedetti et al, 2015 ; D'Ovidio et al, 2004 ; Mattei et al, 2005 ) capable of inducing a variety of plant defences (Ferrari et al, 2013 ; Galletti et al, 2011 ). Treatment with OGs protects Arabidopsis thaliana , grapevine ( Vitis vinifera ) and tomato ( Solanum lycopersicum ) against infections by the necrotrophic fungus Botrytis cinerea ( Aziz et al, 2007 ; Ferrari et al, 2007 ; Gamir et al, 2020 ) . OGs not only act as DAMPs but also as negative regulators of plant growth and development mainly through their antagonism with auxin (Bellincampi et al, 1993 ; Ferrari et al, 2013 ; Pontiggia et al, 2020 ; Savatin et al, 2011 ).…”