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

TL;DR

This study explores how interactions between cytoplasmic and nuclear genes affect plant adaptation in hybrid zones of Populus species.

Contribution

The study provides new insights into cytonuclear co-introgression and its environmental context-dependent effects on physiological performance.

Findings

Co-introgression of chloroplast and nuclear–chloroplast genes is limited but shows regional variation.

Mismatch between chloroplast and nuclear ancestry influences physiological performance, with effects varying by environment.

Abstract

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 to 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 its 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. Geographic clines were used to test for co-introgression of the chloroplast genome with N-cp and non-interacting nuclear genes. Co-introgression of the chloroplast alongside N-cp genes was limited, although contact-zone specific patterns point to the importance of regional differences. 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 context-dependent role the environment may play influencing that interaction.

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