Comparative meta-analysis of barely transcriptome: Pathogen type determines host preference

Abstract

Fungi and aphids show mutual interactions on barley pathogenesis. Fungi promote pathogenesis, while aphids either weaken or strengthen the infection. Otherwise, fungi alter aphid behavior and performance, further highlighting their complex interactions. Characterizing these synergistic and antagonistic interactions is crucial for understanding pathogenesis. Therefore, we performed meta-analysis and co-expression gene network analyses of the barley transcriptome in response to fungus and aphid based on hormone signaling pathways. We selected 13 studies, including 380 fungal infection samples, 48 aphid-attack samples, and 34 hormone-treated samples. We showed that 1.1% of DEGs were common between fungal and aphid-related datasets, while only 0.1% of DEGs were shared among all datasets. In addition, 70% of common DEGs were uniquely regulated by JA or SA signaling. In contrast, 30% of DEGs were regulated by both JA and SA simultaneously. Regulatory element analysis revealed that 85% of DEGs contained at least one binding site from AP2/EREBP or C2H2 zinc-finger factors that show substantial roles in SAR/ISR pathways during plant defense. Gene network analysis identified key hub genes, including SSI2, PAD2, RPS1, RPS17, SHM1, CYP5, and RPL21C, which influence plant host preference in response to pathogens. Moreover, we identified novel hub genes with unknown functions that potentially interact with the genes involved in defense responses and host preference. This study presents the first systems biology analysis of barley transcriptomic responses to heterotroph/biotroph cross-talk focusing on the preference and performance of Rhopalosiphum padi. Our findings suggest critical insights into the molecular mechanisms underlying barley defense responses and identify valuable candidate genes to developing pathogen resistance genotypes in agricultural systems.