Heterosis is a systemic property emerging from nonlinear genotype-phenotype relationships: evidence fromin vitrogenetics and computer simulations

Abstract

Heterosis, the superiority of hybrids over their parents for quantitative traits, represents a crucial issue in plant and animal breeding. Heterosis has given rise to countless genetic, genomic and molecular studies, but has rarely been investigated from the point of view of systems biology. We hypothesized that heterosis is an emergent property of living systems resulting from frequent concave relationships between genotypic variables and phenotypes, or between different phenotypic levels. We chose the enzyme-flux relationship as a model of the concave genotype-phenotype (GP) relationship, and showed that heterosis can be easily created in the laboratory. First, we reconstituted in vitro the upper part of glycolysis. We simulated genetic variability of enzyme activity by varying enzyme concentrations in test tubes. Mixing the content of ”parental” tubes resulted in ”hybrids”, whose fluxes were compared to the parental fluxes. Frequent heterotic fluxes were observed, under conditions that were determined analytically and confirmed by computer simulation. Second, to test this model in a more realistic situation, we modeled the glycolysis/fermentation network in yeast by considering one input flux, glucose, and two output fluxes, glycerol and acetaldehyde. We simulated genetic variability by randomly drawing parental enzyme concentrations under various conditions, and computed the parental and hybrid fluxes using a system of differential equations. Again we found that a majority of hybrids exhibited positive heterosis for metabolic fluxes. Cases of negative heterosis were due to local convexity between certain enzyme concentrations and fluxes. In both approaches, heterosis was maximized when the parents were phenotypically close and when the distributions of parental enzyme concentrations were contrasted and constrained. These conclusions are not restricted to metabolic systems: they only depend on the concavity of the GP relationship, which is commonly observed at various levels of the phenotypic hierarchy, and could account for the pervasiveness of heterosis. Author summary Heterosis, or hybrid vigor, is a genetic phenomenon that is widespread in the living world and is extensively exploited in domesticated species. First described more than 200 years ago, it has only been elucidated on a case-by-case basis. We propose a unifying principle of heterosis, hypothesizing that its pervasiveness reflects the general non-linearity of genotype-phenotype relationships. To corroborate this model, we first used theoretical developments that established the link between heterosis and the curvature of the genotype-phenotype relationship. Then we reconstituted in vitro a small metabolic pathway and mixed the content of different “parental” test tubes to simulate crossings. We showed that reaction rates in hybrid tubes were frequently faster than in parental tubes. The conditions for having heterosis were analyzed using computer simulations of this system, and proved to be direct consequences of the curvature of the enz...

Disentangling genetic variation and heterosis pattern for sexual compatibility and key nut traits within self, single and double hybrid crosses of kola [Cola nitida (Vent) Schott and Endl.]

“…Heterosis is the expression of dominance deviation, a variance from mid parent value, which may be explained by the additive effects of several desired dominant alleles, or as 'overdominance' the combined effect of two different alleles at the same gene locus, or a combination of both [109][110][111][112] . From the de nition, heterosis helps a breeder to make more stringent selections.…”

Review on the Importance and Breeding History of Spider Plant (<i>Gynandropsisgynandra (L.) Briq</i>.)

“…Heterosis, defined as the superiority of hybrids over their parents for quantitative traits, represents by crossbreed organisms as compared with inbred, as the results of dissimilar in the constitution of the uniting parental gametes [70,22]. Heterosis exploitation is the most important in agriculture, which was added improved genotype in the production of crops and animals during the last of 20 th century [18,62].…”

“…It might be due to different factors of genetic effects; namely: dominance, overdominance and epistasis effects. While substantial debated on dominance or over-dominance effects, evidence of different studies indicated that both are not mutually exclusive [22].…”

Decoupling the variances of heterosis and inbreeding effects is evidenced in yeast’s life-history and proteomic traits

“…The respective parts of the various genetics effects in heterosis depends on the trait, the species and the genetic material (Xiao et al 1995;Huang et al 2016;Seymour et al 2016). Altogether, heterosis appears to be a pervasive phenomenon, accounted for by the common non-linearity of the genotype-phenotype map (Wright 1934;Omholt et al 2000;Fiévet et al 2018).…”