Reciprocal cybrids reveal how organellar genomes affect plant phenotypes

Assessing the impact of variation in chloroplast and mitochondrial DNA
(collectively termed the plasmotype) on plant phenotypes is challenging
due to the difficulty in separating their effect from nuclear derived
variation (the nucleotype). Haploid inducer lines can be used as efficient
plasmotype donors to generate new plasmotype-nucleotype combinations
(cybrids). We generated a panel comprising all possible cybrids of seven
Arabidopsis thaliana accessions and extensively phenotyped these lines for
1859 phenotypes under stable and fluctuating conditions. We show that
natural variation in the plasmotype results in additive as well as
epistatic effects across all phenotypic categories. Plasmotypes which
induce more additive phenotypic changes also cause more significant
epistatic effects, suggesting a possible common basis for both additive
and epistatic effects. On average epistatic interactions explained twice
as much of the variance in phenotypes as additive plasmotype effects. The
impact of plasmotypic variation was also more pronounced under fluctuating
and stressful environmental conditions. Thus, the phenotypic impact of
variation in plasmotypes is the outcome of multilevel Nucleotype x
Plasmotype x Environment interactions and, as such, the plasmotype is
likely to serve as a reservoir of variation which is predominantly exposed
under certain conditions.  The production of cybrids using
haploid inducers is a quick and precise method for assessing the
phenotypic effects of natural variation in organellar genomes. It will
facilitate efficient screening of unique nucleotype-plasmotype
combinations to both improve our understanding of natural variation in
nucleotype-plasmotype interactions and identify favourable combinations to
improve plant performance.