Encounter networks from collective mitochondrial dynamics support the emergence of effective mtDNA genomes in plant cells

TL;DR

This study investigates how mitochondrial encounter networks in plant cells facilitate the exchange and collection of mitochondrial DNA fragments, leading to the emergence of complete genomes within individual mitochondria over time.

Contribution

It combines experimental imaging, network analysis, and modeling to show that biological encounter networks are highly suited for genome collection, outperforming theoretical models.

Findings

Biological encounter networks support full genome collection.

Network degree distribution influences genome emergence.

Mitochondrial dynamics facilitate genetic exchange.

Abstract

Mitochondria in plant cells form strikingly dynamic populations of largely individual organelles. Each mitochondrion contains on average less than a full copy of the mitochondrial DNA (mtDNA) genome. Here, we asked whether mitochondrial dynamics may allow individual mitochondria to `collect' a full copy of the mtDNA genome over time, by facilitating exchange between individuals. Akin to trade on a social network, exchange of mtDNA fragments across organelles may lead to the emergence of full `effective' genomes in individuals over time. We characterise the collective dynamics of mitochondria in \emph{Arabidopsis thaliana} hypocotyl cells using a recent approach combining single-cell timelapse microscopy, video analysis, and network science. We then use a quantitative model to predict the capacity for the sharing and accumulation of genetic information through the networks of encounters between mitochondria. We find that biological encounter networks are strikingly well predisposed to support the collection of full genomes over time, outperforming a range of other networks generated from theory and simulation. Using results from the coupon collector's problem, we show that the upper tail of the degree distribution is a key determinant of an encounter network's performance at this task and discuss how features of mitochondrial dynamics observed in biology facilitate the emergence of full effective genomes.