Unifying Genetic Canalization, Genetic Constraint, and Genotype-by-Environment Interaction: QTL by Genomic Background by Environment Interaction of Flowering Time in Boechera stricta

Abstract

Natural populations exhibit substantial variation in quantitative traits. A quantitative trait is typically defined by its mean and variance, and to date most genetic mapping studies focus on loci altering trait means but not (co)variances. For single traits, the control of trait variance across genetic backgrounds is referred to as genetic canalization. With multiple traits, the genetic covariance among different traits in the same environment indicates the magnitude of potential genetic constraint, while genotype-by-environment interaction (GxE) concerns the same trait across different environments. While some have suggested that these three attributes of quantitative traits are different views of similar concepts, it is not yet clear, however, whether they have the same underlying genetic mechanism. Here, we detect quantitative trait loci (QTL) influencing the (co)variance of phenological traits in six distinct environments in Boechera stricta, a close relative of Arabidopsis. We identified nFT as the QTL altering the magnitude of phenological trait canalization, genetic constraint, and GxE. Both the magnitude and direction of nFT's canalization effects depend on the environment, and to our knowledge, this reversibility of canalization across environments has not been reported previously. nFT's effects on trait covariance structure (genetic constraint and GxE) likely result from the variable and reversible canalization effects across different traits and environments, which can be explained by the interaction among nFT, genomic backgrounds, and environmental stimuli. This view is supported by experiments demonstrating significant nFT by genomic background epistatic interactions affecting phenological traits and expression of the candidate gene, FT. In contrast to the well-known canalization gene Hsp90, the case of nFT may exemplify an alternative mechanism: Our results suggest that (at least in traits with major signal integrators such as flowering time) genetic canalization, genetic constraint, and GxE may have related genetic mechanisms resulting from interactions among major QTL, genomic backgrounds, and environments.

Differential regulation of cryptic genetic variation shapes the genetic interactome underlying complex traits

“…To estimate the difference in phenotypic variance between the two genotypic groups, i.e., to identify vQTL in each environment, the standard Brown–Forsythe (BF) statistic (Rönnegård and Valdar 2011; Lee et al 2014) and the corresponding LOD score were calculated for each genetic marker in each environment (supplementary file S1, Supplementary Material online). The BF-test is equivalent to an F-test performed on the deviations of the phenotypic values from their respective genotypic medians (or the means).…”

“…Whereas vQTL with significant effect on variation have been identified, viz. MOT1 (Forsberg et al 2015) and nFT (Lee et al 2014) in plants, these loci tend to be small effect when compared with conventional QTL (Shen et al 2012). In addition, while vQTL mapping has been proposed to be a predictor of prevalence of gene-gene interactions (Paré et al 2010; Rönnegård and Valdar 2012), thereby supporting our hypothesis of differential regulation of CGV by these loci, empirical evidence for this remains scarce.…”

The Modular Adaptive Ribosome

“…The F-test statistic, BF-test statistic [28], P values and variances were computed on the standardized phenotype data derived from the above-standardized Hillenmeyer dataset. Genes in each cluster in each condition were compared to their respective YPD control condition.…”

Canalization of Tomato Fruit Metabolism

“…It is now known that the extent to which a phenotype is canalized is under genetic control, although few studies have investigated the molecular basis of canalization in plants (Hall et al, 2007;JimenezGomez et al, 2011;Lee et al, 2014). Under specific conditions, trait canalization may be beneficial to the organism, leading to the increase of the allele frequencies contributing to the appearance of the canalized phenotype; on the other hand, there might be cases where the plasticity of a specific trait could confer an adaptive advantage, especially in environments subjected to unpredictable fluctuations (Lachowiec et al, 2016).…”

“…It additionally provided evidence of genotypic selection both for increased and decreased canalization. Recently, another study in Boechera stricta (a close relative of Arabidopsis) included mapping of, among others, a QTL associated with genetic canalization of flowering time (Lee et al, 2014). Similarly, treatment of Arabidopsis ecotypes and recombinant inbred lines with pharmacological inhibitors of Hsp90 suggests that this protein acts as a capacitor of phenotypic variation in plants as well as in the fruit fly (Rutherford and Lindquist, 1998;Queitsch et al, 2002).…”