Exploiting Differential Gene Expression and Epistasis to Discover Candidate Genes for Drought-Associated QTLs in Arabidopsis thaliana

Abstract

Soil water availability represents one of the most important selective agents for plants in nature and the single greatest abiotic determinant of agricultural productivity, yet the genetic bases of drought acclimation responses remain poorly understood. Here, we developed a systems-genetic approach to characterize quantitative trait loci (QTLs), physiological traits and genes that affect responses to soil moisture deficit in the TSUxKAS mapping population of Arabidopsis thaliana. To determine the effects of candidate genes underlying QTLs, we analyzed gene expression as a covariate within the QTL model in an effort to mechanistically link markers, RNA expression, and the phenotype. This strategy produced ranked lists of candidate genes for several drought-associated traits, including water use efficiency, growth, abscisic acid concentration (ABA), and proline concentration. As a proof of concept, we recovered known causal loci for several QTLs. For other traits, including ABA, we identified novel loci not previously associated with drought. Furthermore, we documented natural variation at two key steps in proline metabolism and demonstrated that the mitochondrial genome differentially affects genomic QTLs to influence proline accumulation. These findings demonstrate that linking genome, transcriptome, and phenotype data holds great promise to extend the utility of genetic mapping, even when QTL effects are modest or complex.

Natural variation of plant metabolism: genetic mechanisms, interpretive caveats, evolutionary and mechanistic insights.

“…However, there is extensive evidence for genetic variation in the organelles altering adaptive phenotypes and interacting with nuclear loci (Greiner and Bock, 2013). Recent populations have been developed that are allowing quantitative assessment of the role of genetic variation in the organelle in quantitative phenotypes (McKay et al, 2008;Lovell et al, 2015). Analyzing metabolomic variation in the Arabidopsis Kas 3 Tsu population showed that genomic variation within the organelle altered the accumulation of nearly all metabolites (Joseph et al, 2013a(Joseph et al, , 2013b.…”

Drought responsive gene expression regulatory divergence between upland and lowland ecotypes of a perennial C4grass

“…5B)-DREBs are the most extensively studied drought-responsive group of genes in Arabidopsis (Sakuma et al 2002;Agarwal et al 2006;Xianjun et al 2011); (3) FT, a central gene in the flowering pathway (Fig. 5C)-several recent studies have implicated a physiological and genetic tie between drought-responsive and flowering pathways (McKay et al 2003;Lovell et al 2013Lovell et al , 2015Riboni et al 2013;Kimura et al 2015); (4) RLK1, the rice ortholog (OsLecRK4) which improves resistance to insect herbivory (Liu et al 2015), and (5) a rice ortholog (OSMate2) of the MATE efflux family gene AT1G71140, which, when overexpressed in A. thaliana, alters a variety of abiotic and biotic stress responses (Tiwari et al 2014). …”

Cytonuclear interactions affect adaptive traits of the annual plantArabidopsis thalianain the field

“…Although some studies have reported significant effects of cytonuclear epistasis (17,20,21,23,25), others have found additive cytoplasmic effects but with weak or no cytonuclear epistasis (22). Each of these studies (with the exception of ref.…”