The role of cytonuclear interactions in plant adaptation across a Populus hybrid zone

Co-adaptation of cytoplasmic and nuclear genomes is critical to physiological function for many species. Despite this understanding, hybridization can disrupt co-adaptation, leading to a mismatch between maternally-inherited cytoplasmic genomes and biparentally inherited nuclear genomes. Few studies have examined the consequences of cytonuclear interactions on physiological function across environments. Here, we quantify the degree of co-introgression between chloroplast and nuclear-chloroplast (N-cp) genes across repeated hybrid zones and their consequences to physiological function across environments. We use whole-genome resequencing and common garden experiments with clonally replicated genotypes sampled across the natural hybrid zone between Populus trichocarpa and P. balsamifera. We use geographic clines to test for co-introgression of the chloroplast genome with N-cp and non-interacting nuclear genes. Co-introgression of chloroplast and N-cp genes was limited, although contact zone-specific patterns suggest that local environments may influence co-introgression. Combining ancestry estimates with phenotypic data across common gardens revealed that mismatches between chloroplast and nuclear ancestry can influence physiological performance, but the strength and direction of these effects vary depending on the environment. Overall, this study highlights the importance of cytonuclear interactions to adaptation and the role of the environment in modifying the effect of those interactions.

细胞质基因组与细胞核基因组的共适应对诸多物种的生理功能至关重要。尽管学界已达成这一共识，但杂交作用会破坏共适应状态，导致母系遗传的细胞质基因组与双亲遗传的细胞核基因组间出现错配。目前针对核质互作在不同环境下对生理功能产生的影响的相关研究仍较为稀缺。本研究以毛果杨（*Populus trichocarpa*）与香脂杨（*Populus balsamifera*）的自然杂交带为研究对象，对采自该区域的无性繁殖重复基因型开展全基因组重测序（whole-genome resequencing）与同质园实验（common garden experiments），量化了重复杂交带内叶绿体基因与核-叶绿体（N-cp）基因的共渐渗程度，并分析其在不同环境下对生理功能的影响。研究借助地理渐变群（geographic clines）检验叶绿体基因组与N-cp基因、非互作核基因的共渐渗情况。结果显示，叶绿体与N-cp基因的共渐渗程度有限，但不同杂交带的特有分布模式表明，局部环境可能会对共渐渗过程产生影响。结合同质园实验中的祖先成分估计结果与表型数据可知，叶绿体与细胞核祖先成分间的错配会影响生理表现，但此类效应的强度与方向会因环境而异。综上，本研究凸显了核质互作对物种适应的重要性，以及环境在修饰此类互作效应中发挥的关键作用。