Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene

Abstract

Plants are attacked by pathogens representing diverse taxonomic groups, such that genes providing multiple disease resistance (MDR) are expected to be under positive selection pressure. To address the hypothesis that naturally occurring allelic variation conditions MDR, we extended the framework of structured association mapping to allow for the analysis of correlated complex traits and the identification of pleiotropic genes. The multivariate analytical approach used here is directly applicable to any species and set of traits exhibiting correlation. From our analysis of a diverse panel of maize inbred lines, we discovered high positive genetic correlations between resistances to three globally threatening fungal diseases. The maize panel studied exhibits rapidly decaying linkage disequilibrium that generally occurs within 1 or 2 kb, which is less than the average length of a maize gene. The positive correlations therefore suggested that functional allelic variation at specific genes for MDR exists in maize. Using a multivariate test statistic, a glutathione S -transferase ( GST ) gene was found to be associated with modest levels of resistance to all three diseases. Resequencing analysis pinpointed the association to a histidine (basic amino acid) for aspartic acid (acidic amino acid) substitution in the encoded protein domain that defines GST substrate specificity and biochemical activity. The known functions of GSTs suggested that variability in detoxification pathways underlie natural variation in maize MDR.

Unraveling Genomic Complexity at a Quantitative Disease Resistance Locus in Maize

“…Significant associations within the qNLB1.06 Tx303 fine-mapping interval were detected using both the NAM and Goodman diversity panels (Flint-Garcia et al 2005;Poland et al 2011;Wisser et al 2011;Chia et al 2012). The most significant association within this region in the NAM was an intergenic copy number variation, which had a BPP value of 44 (P-value = 0.0000737), one of the most highly significant associations from the analysis Chia et al 2012).…”

“…This polymorphism is close to the Stewart's wilt fine-mapping interval, lending support to the hypothesis that a region present in Tx303 but not B73 may contain gene(s) for resistance to both diseases. Association analysis using the Goodman diversity panel revealed a significant intergenic SNP within the fine-mapping interval, 800 kb from the NAM CNV (Flint-Garcia et al 2005;Wisser et al 2011). The NLBassociated CNV and SNP polymorphisms may be in linkage disequilibrium with one or more genes in the vicinity.…”

“…The smaller confidence interval for Stewart's wilt may Figure 4 Diversity panel association. Shown is association analysis for NLB in the fine-mapping region using the Goodman diversity panel (Flint-Garcia et al 2005;Wisser et al 2011). The significant SNP at 188,018,070 bp (Pvalue = 1.72 3 10 24 , q-value = 0.136) is highlighted in blue.…”

“…Each locus has a unique profile, with some loci contributing broadspectrum protection against diverse pathogen species and strains. Investigating these intricacies offers the opportunity to understand the diverse ways in which plants defend themselves against microbial assault.Correlated responses to multiple diseases have been observed in various germplasm panels, implying that there are loci and genes that condition broad-spectrum resistance (Rossi et al 2006;Gurung et al 2009;Wisser et al 2011). At the chromosomal segment level, disease and insect resistance loci colocalize in a nonrandom fashion (McMullen and Simcox 1995;Williams 2003;Wisser et al 2005) and loci have been identified that confer resistance to diverse pathogen isolates and taxa (Zwonitzer et al 2010;Chung et al 2011;Belcher et al 2012).…”

A Connected Set of Genes Associated with Programmed Cell Death Implicated in Controlling the Hypersensitive Response in Maize

“…Lines with highest membership probability, Q k , 0.8 for all k, were considered to result from admixture and hence were classified as "mixed. "Genotypic correlation analysis: We estimated genotypic correlations among lesion mimic traits measured in this study and previously derived quantitative resistance scores for three different diseases of maize measured on the same association panel but evaluated in different environment sets (Wisser et al 2011): southern leaf blight (SLB), northern leaf blight (NLB), and gray leaf spot (GLS). To reduce the impact of population structure on genotypic correlation estimates, we estimated correlations among inbred line residual values obtained after fitting population structure covariates (b k for each Q k ) to least square means (for lesion mimic traits) or best linear unbiased predictors (for disease scores) for each trait.…”