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

We have applied a systems genetics approach to elucidate molecular mechanisms of maize responses to gray leaf spot (GLS) disease, caused by Cercospora zeina, a major threat to maize production globally. We conducted expression QTL (eQTL) analysis of gene expression variation measured in earleaf samples in a sub-tropical maize RIL population (CML444 X SC Malawi) subjected to C. zeina infection in the field. A total of 20,206 eQTLs were identified from 19,281 microarray reporters. Four trans-eQTL hotspots coincided with phenotypic QTLs for GLS disease mapped in the same field experiment. Weighted gene co-expression network analysis identified three gene co-expression modules correlated with GLS disease scores. The module (termed 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 trans-eQTLs in hotspots on maize chromosomes 9 and 10, which also coincided with phenotypic QTLs for GLS susceptibility. This represents a transcriptional network that has significant overlap with the susceptible response of maize line B73, and may reflect pathogen manipulation for nutrient acquisition and/or ineffective defense responses. The co-expression module that correlated with resistance (termed TQ-r; 1564 genes) was enriched for maize 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, expression of JAZ repressors were highly correlated with GLS disease in the GY-s susceptibility network.

Christie, K.R., Myburg, A.A., Joubert, Y., Murray, S.L., Carstens, M., Lin, Y.-C., Meyer, J., Crampton, B.G., Christensen, S.A., Ntuli, J.F., Wighard, S.S., Van de Peer, Y., Berger, D.K. (2016) Systems genetics reveals a transcriptional network associated with susceptibility in the maize-gray leaf spot pathosystem. The Plant Journal 89(4):746-763.

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