Systems genetics reveals a transcriptional network associated with susceptibility in the maize-gray leaf spot pathosystem

Abstract

We used a systems genetics approach to elucidate molecular mechanisms of maize responses to gray leaf spot (GLS) disease, caused by Cercospora zeina, a threat to maize production globally. Expression analysis of earleaf samples in a sub-tropical maize RIL population (CML444 X SC Malawi) subjected in field to C. zeina infection allowed detection of 20,206 expression QTLs (eQTL). Four trans-eQTL hotspots coincided with GLS disease QTLs mapped in the same field experiment. Co-expression network analysis identified three expression modules correlated with GLS disease scores. The module (GY-s) most highly correlated with susceptibility (r = 0.71; 179 genes) was enriched for the glyoxylate pathway, lipid metabolism, diterpenoid biosynthesis and responses to pathogen molecules such as chitin. The GY-s module was enriched for genes with transeQTLs in hotspots on chromosomes 9 and 10, which also coincided with phenotypic QTLs for GLS susceptibility. This transcriptional network has significant overlap with the GLS susceptibility response of maize line B73, and may reflect pathogen manipulation for nutrient acquisition and/or unsuccessful defense responses, such as kauralexin production by the diterpenoid biosynthesis pathway. The co-expression module that correlated best with resistance (TQ-r; 1498 genes) was enriched for genes with trans-eQTLs in hotspots coinciding with GLS resistance QTLs on chromosome 9. Jasmonate responses were implicated in resistance to GLS through co-expression of COI-1 and enrichment of genes with the GO term “cullin-RING ubiquitin ligase complex” in the TQ-r module. Consistent with this, JAZ repressor expression was highly correlated with GLS disease severity in the GY-s susceptibility network.