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de Vienne, D.

Publications and source records attributed to de Vienne, D..

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Non-linear phenotypic variation uncovers the emergence of heterosis in Arabidopsis thaliana

Heterosis describes the phenotypic superiority of hybrids over their parents in traits related to fitness. Understanding and predicting non-additive inheritance such as heterosis is crucial for evolutionary biology, as well as for plant and animal breeding. However, the physiological bases of heterosis remain debated. Moreover, empirical data in various species have shown that diverse genetic and molecular mechanisms are likely to explain heterosis, making it difficult to predict its emergence and amplitude from parental genotypes alone. In this study, we evaluated a model of physiological dominance proposed by Sewall Wright to explain the non-additive inheritance of metabolic fluxes at the cellular level. We used 450 hybrids derived from crosses among natural inbred accessions of Arabidopsis thaliana to test Wrights model for two fitness-related traits at the whole-plant level: growth rate and fruit number. We found that allometric relationships between traits constrain phenotypic variation in hybrids and inbreds to a similar extent. These allometric relationships behave predictably, in a non-linear manner, explaining up to 75% of heterosis amplitude, while genetic distance among parents at best explains 7%. Thus, our findings are consistent with Wrights model of physiological dominance on plant performance, and suggest that the emergence of heterosis is an intrinsic property of non-linear relationships between traits. Furthermore, our study highlights the potential of a geometric approach of phenotypic relationships for predicting heterosis of two major components of crop productivity and yield.

evolutionary biology

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

Heterosis (hybrid vigor) and inbreeding depression, commonly considered as corollary phenomena, could nevertheless be decoupled under certain assumptions according to theoretical population genetics works. In order to explore this issue on real data, we analyzed the components of genetic variation in a population derived from a half-diallel cross between strains from Saccharomyces cerevisiae and S. uvarum, two related yeast species involved in alcoholic fermentation. A large number of phenotypic traits, either molecular (coming from quantitative proteomics) or related to fermentation and life-history, were measured during alcoholic fermentation. Because the parental strains were included in the design, we were able to distinguish between inbreeding effects, which measures phenotypic differences between inbred and hybrids, and heterosis, which measures phenotypic differences between a specific hybrid and the other hybrids sharing a common parent. The sources of phenotypic variation differed depending on the temperature, indicating the predominance of genotype by environment interactions. Decomposing the total genetic variance into variances of additive (intra- and inter-specific) effects, of inbreeding effects and of heterosis (intra- and inter-specific) effects, we showed that the distribution of variance components defined clear-cut groups of proteins and traits. Moreover, it was possible to cluster fermentation and life-history traits into most proteomic groups. Within groups, we observed positive, negative or null correlations between the variances of heterosis and inbreeding effects. To our knowledge, such a decoupling had never been experimentally demonstrated. This result suggests that, despite a common evolutionary history of individuals within a species, the different types of traits have been subject to different selective pressures.

systems biology

The geometry of heterosis

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.

systems biology