Novel Cytonuclear Combinations Modify Arabidopsis thaliana Seed Physiology and Vigor

Abstract

Dormancy and germination vigor are complex traits of primary importance for adaptation and agriculture. Intraspecific variation in cytoplasmic genomes and cytonuclear interactions were previously reported to affect germination in Arabidopsis using novel cytonuclear combinations that disrupt co-adaptation between natural variants of nuclear and cytoplasmic genomes. However, specific aspects of dormancy and germination vigor were not thoroughly explored, nor the parental contributions to the genetic effects. Here, we specifically assessed dormancy, germination performance and longevity of seeds from Arabidopsis plants with natural and new genomic compositions. All three traits were modified by cytonuclear reshuffling. Both depth and release rate of dormancy could be modified by a changing of cytoplasm. Significant changes on dormancy and germination performance due to specific cytonuclear interacting combinations mainly occurred in opposite directions, consistent with the idea that a single physiological consequence of the new genetic combination affected both traits oppositely. However, this was not always the case. Interestingly, the ability of parental accessions to contribute to significant cytonuclear interactions modifying the germination phenotype was different depending on whether they provided the nuclear or cytoplasmic genetic compartment. The observed deleterious effects of novel cytonuclear combinations (in comparison with the nuclear parent) were consistent with a contribution of cytonuclear interactions to germination adaptive phenotypes. More surprisingly, we also observed favorable effects of novel cytonuclear combinations, suggesting suboptimal genetic combinations exist in natural populations for these traits. Reduced sensitivity to exogenous ABA and faster endogenous ABA decay during germination were observed in a novel cytonuclear combination that also exhibited enhanced longevity and better germination performance, compared to its natural nuclear parent. Taken together, our results strongly support that cytoplasmic genomes represent an additional resource of natural variation for breeding seed vigor traits.

Cytonuclear Genetic Incompatibilities in Plant Speciation

“…A significant effect of the cytoplasm genotype on seed germination efficiency was identified, suggesting a role of the selection on the plasmotype geographical distribution and its role in A. thaliana populations adaptation [36]. Another study conducted on the same cytolines concluded that cytonuclear interactions and coevolution had an impact on adaptive traits linked to seed vigor [78]. For example, the creation of novel CN combinations in cytolines, leading to the disruption of CN coadaptation, had a deleterious effect on adaptive dormancy and germination, consistent with a contribution of CN co-adaptation and cytoplasmic variation on complex traits involved in plant adaptation [78].…”

“…Another study conducted on the same cytolines concluded that cytonuclear interactions and coevolution had an impact on adaptive traits linked to seed vigor [78]. For example, the creation of novel CN combinations in cytolines, leading to the disruption of CN coadaptation, had a deleterious effect on adaptive dormancy and germination, consistent with a contribution of CN co-adaptation and cytoplasmic variation on complex traits involved in plant adaptation [78].…”

Time‐resolved dissection of the molecular crosstalk driving Fusarium head blight in wheat provides new insights into host susceptibility determinism

“…The FDR was <0.01 corresponding to P values <0.003 for Fg proteins and to P values <0.002, <0.0018, and < 0.0006 for wheat proteins in the T, D, and T × D effects, respectively. Within all significant order 2 interactions, we computed a contrast test procedure to identify significant T × D interactions (Boussardon et al, 2018).…”

DiCoExpress: a tool to process multifactorial RNAseq experiments from quality controls to co-expression analysis through differential analysis based on contrasts inside GLM models

“…When the number of observations is two times greater than the number of parameters of the model, we advise to include interaction terms between the biological factors. Such terms in the gene expression definition might reveal meaningful interactions such as genotype-environment interaction and answer in a direct way to some biological questions [39][40][41]. The (3) GLM_Contrasts function automatically writes a list of contrasts based on the model specified by the user.…”