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.

评估叶绿体DNA与线粒体DNA（二者统称为质体基因组（plasmotype））的变异对植物表型的影响颇具挑战，这是因为难以将其效应与核来源变异（核型基因组（nucleotype））的效应区分开来。单倍体诱导系可作为高效的质体基因组供体，用于构建全新的质体基因组-核型基因组组合（即胞质杂种（cybrids））。本研究构建了涵盖7个拟南芥（Arabidopsis thaliana）生态型所有可能胞质杂种的组合群体，并在稳定与波动环境条件下，对这些株系开展了1859项表型的系统性鉴定。研究表明，质体基因组的自然变异在所有表型类别中均可产生加性效应与上位性效应。能引发更强表型加性改变的质体基因组，同时也会诱导更为显著的上位性效应，这提示加性效应与上位性效应可能存在共同的分子基础。平均而言，上位性互作对表型方差的解释度是质体基因组加性效应的两倍。在波动与胁迫环境条件下，质体基因组变异的影响更为显著。综上，质体基因组变异的表型效应是核型基因组-质体基因组-环境多级互作的结果，因此质体基因组很可能是一类仅在特定条件下才会显现其变异效应的遗传变异储备库。利用单倍体诱导系制备胞质杂种，是评估细胞器基因组自然变异表型效应的快速精准方法。该方法将助力高效筛选独特的核型基因组-质体基因组组合，既有助于加深我们对核型-质体互作自然变异的理解，也能鉴定出可优化植物表现的优良组合。