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

item CHRISTIE, NANETTE - University Of Pretoria
item MYBURG, ALEXANDER - University Of Pretoria
item JOUBERT, FOURIE - University Of Pretoria
item MURRAY, SHANE - University Of Cape Town
item CARSTENS, MARYKE - University Of Pretoria
item LIN, YAO-CHENG - University Of Pretoria
item MEYER, JACQUELINE - University Of Pretoria
item CRAMPTON, BRIDGET - University Of Pretoria
item Christensen, Shawn
item NTULI, JEAN - University Of Cape Town
item WIGHARD, SARA - University Of Cape Town
item VAN DE PEER, YVES - Ghent University
item BERGER, DAVE - University Of Pretoria

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/4/2016
Publication Date: 2/13/2017
Citation: Christie, N., Myburg, A.A., Joubert, F., Murray, S.L., Carstens, M., Lin, Y., Meyer, J., Crampton, B.G., Christensen, S.A., Ntuli, J.F., Wighard, S.S., Van De Peer, Y., Berger, D.K. 2017. Systems genetics reveals a transcriptional network associated with susceptibility in the maize-grey leaf spot pathosystem. Plant Journal. 89(4):746–763. doi:10.1111/tpj.13419.

Interpretive Summary: Crop loss due to pathogen threats is a recurring global problem leading to billions of dollars in reduced yield and revenue annually. Gray leaf spot (GLS) is a damaging foliar disease of maize that has been documented in many sub-tropical and tropical regions of the world. Symptoms are matchstick-shaped necrotic lesions with a gray tint on the leaf surface. Resistance to GLS and other maize pathogens often requires the action of many defensive genes (e.g. fungal cell wall damaging and antibiotic producing genes), a phenomenon referred to as quantitative disease resistance. While many studies have described the genetic regions responsible for disease resistance, identifying the specific genes that confer quantitative disease resistance in maize is currently a major challenge. Scientists at the Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL, in collaboration with researchers from South Africa and Belgium, investigated the genetics of a large population of maize derived from resistant (CML444) and susceptible (SC Malawi) parent lines in search for specific genes responsible for resistance and susceptibility to GLS. As a result of our analysis, we identified a specific maize gene, termed COI-1, which plays a significant role in controlling GLS disease severity. The screening for and incorporation of this gene into germplasm will contribute to strategies that improve disease resistance in maize.

Technical Abstract: 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 that 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.