Neutral transcriptome rewiring promotes quantitative disease resistance evolvability at the species level

Area of Science:

• Plant immunity
• Genomics
• Evolutionary biology

Background:

• Quantitative disease resistance (QDR) is a plant immune mechanism that limits pathogen damage through transcriptomic reprogramming.
• The evolution of QDR's underlying gene expression patterns is not well understood.
• QDR involves numerous genes, each contributing minimally to overall plant immunity.

Purpose of the Study:

• To investigate the evolution of transcriptome reprogramming in Quantitative Disease Resistance (QDR).
• To analyze gene expression patterns in response to Sclerotinia sclerotiorum across diverse Arabidopsis accessions.
• To understand how gene expression variation contributes to QDR phenotypes and evolvability.

Main Methods:

• Global gene expression analysis in 23 Arabidopsis accessions challenged with Sclerotinia sclerotiorum.
• Pan-transcriptome analysis to identify responsive genes.
• Coexpression, correlation, and promoter sequence analyses.
• Transcriptome-phenotype mapping.

Main Results:

• Over half of the Arabidopsis pan-transcriptome responded to S. sclerotiorum, with patterns independent of accession phylogeny.
• A core transcriptome of ~11% of responsive genes was common across accessions, characterized by high responsiveness.
• QDR phenotypes arise from integrated expression of numerous genes, with cis-regulatory variations driving rewiring.
• Neutral networks connected diverse QDR transcriptomes without compromising resistance, indicating evolvability.

Conclusions:

• Plant QDR is an evolvable trait shaped by regulatory variation in core genes.
• Transcriptome reprogramming provides a robust and adaptable immune response.
• Understanding QDR evolution informs plant disease dynamics and breeding strategies.