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

Abstract

Although the contribution of cytonuclear interactions to plant fitness variation is relatively well documented at the interspecific level, the prevalence of cytonuclear interactions at the intraspecific level remains poorly investigated. In this study, we set up a field experiment to explore the range of effects that cytonuclear interactions have on fitness-related traits in Arabidopsis thaliana.To do so, we created a unique series of 56 cytolines resulting from cytoplasmic substitutions among eight natural accessions reflecting within-species genetic diversity. An assessment of these cytolines and their parental lines scored for 28 adaptive whole-organism phenotypes showed that a large proportion of phenotypic traits (23 of 28) were affected by cytonuclear interactions. The effects of these interactions varied from slight but frequent across cytolines to strong in some specific parental pairs. Two parental pairs accounted for half of the significant pairwise interactions. In one parental pair, Ct-1/Sha, we observed symmetrical phenotypic responses between the two nuclear backgrounds when combined with specific cytoplasms, suggesting nuclear differentiation at loci involved in cytonuclear epistasis. In contrast, asymmetrical phenotypic responses were observed in another parental pair, Cvi-0/Sha. In the Cvi-0 nuclear background, fecundity and phenology-related traits were strongly affected by the Sha cytoplasm, leading to a modified reproductive strategy without penalizing total seed production. These results indicate that natural variation in cytoplasmic and nuclear genomes interact to shape integrative traits that contribute to adaptation, thereby suggesting that cytonuclear interactions can play a major role in the evolutionary dynamics of A. thaliana.cytolines | cytoplasm × nucleus interactions | fitness-related traits | plant adaptation | organelles T he genomes of eukaryotes originate from ancient endosymbiotic associations that eventually led to energy-harnessing organelles: mitochondria, common to all eukaryotes, and chloroplasts in the "green" lineage. The evolution of endosymbionts into cellular organelles was accompanied by massive gene loss, with a large proportion being transferred to the nucleus (1, 2). Nevertheless, mitochondria and chloroplasts retained a few (30-80) protein-encoding genes that play crucial roles in energy metabolism (respiration and photosynthesis). Mitochondrion and chloroplast metabolisms rely on the proper interaction of nuclear-encoded proteins and their counterparts encoded in the organelle genome. Consequently, the genes in nuclear and organellar compartments are expected to be coadapted (3).Cytonuclear coadaptation has been demonstrated by altered phenotypes observed on interspecific exchanges of cytoplasm between related species in mammals (4), yeast (5), arthropods (6), and plants, whose interspecific crosses are frequently successful (7). These alterations affect organelle function and even the organism phenotype, indicating epistasis between nuclear and cytoplasmic gen...

Cytonuclear incompatibility contributes to the early stages of speciation

“…In contrast, lineages with more typical rates of plastid evolution may be unlikely to exhibit strong cytonuclear incompatibility. This expectation may explain the lack of cytonuclear incompatibility found in several studies that have combined nuclear and cytoplasmic backgrounds from different populations to examine the role of cytonuclear interactions in local adaptation (e.g., Galloway and Fenster 1999;Roux et al 2016). Cytonuclear incompatibility is also likely to play a substantial role in the early stages of speciation in species with rapid mitochondrial evolution (Burton and Barreto 2012).…”

Thermal plasticity of the circadian clock is under nuclear and cytoplasmic control in wild barley

“…A recent work demonstrated that variation in the organellar genome can contribute to phenotypic or metabolomic differences between individuals, although the relative contribution of organellar versus nuclear genes remains unclear (Joseph, Corwin, Li, Atwell, & Kliebenstein, ). Effects of the cytoplasm on plant fitness and agronomic traits are described from many plant systems (Greiner & Bock, ; Roux et al, ). For example, disease resistance can be influenced by the genotype of the cytoplasm (plasmotype), as can be yield and grain quality (Frei, Peiretti, & Wenzel, ; Sanetomo & Gebhardt, ).…”

Production of a desirable Brassica oleraceaCMS line using an alloplasmic B. rapaCMS line carrying Diplotaxis erucoides cytoplasm as a bridge plant

“…In addition to the B. oleracea De ‐CMS lines, alloplasmic B. rapa line and B. juncea line carrying D. erucoides cytoplasm also showed improvements of growth in plant size and seed size, respectively (Malik et al., ; Peng et al., ). Similarly, variations in phenotype caused by the interactions between the nuclear and organellar genomes have also been observed in other plant species, such as wheat (Soltani et al., ), maize (Allen, ), rice (Wang, Tang, & Tang, ) and Arabidopsis (Moison et al., ; Roux et al., ). These examples indicate that nuclear–cytoplasm interactions have the potential to contribute to crop breeding.…”