Tension and resolution: Dynamic, evolving populations of organelle genomes within plant cells

Mitochondria and plastids form dynamic, evolving populations physically embedded in the fluctuating environment of the plant cell. Their evolutionary heritage has shaped how the cell controls the genetic structure and the physical behaviour of its organelle populations. While the specific genes involved in these processes are gradually being revealed, the governing principles underlying this controlled behaviour remain poorly understood. As the genetic and physical dynamics of these organelles are central to bioenergetic performance and plant physiology, this challenges both fundamental biology and strategies to engineer better-performing plants. This article will review current knowledge of the physical and genetic behaviour of mitochondria and chloroplasts in plant cells. An overarching hypothesis is proposed, whereby organelles face a tension between genetic robustness and individual control and responsiveness, and different species resolve this tension in different ways. As plants are immobile and therefore subject to fluctuating environments, their organelles are proposed to favour individual responsiveness, sacrificing genetic robustness. Several notable features of plant organelle dynamics including mtDNA recombination and plastid/mitochondrial differences may be explained by this hypothesis. Finally, the article highlights how tools from quantitative and systems biology can help shed light on the plethora of open questions in this field.