Gene duplication accelerates the pace of protein gain and loss from plant organelles.

Abstract

Introductory paragraphA hallmark of eukaryotic cells is the compartmentalisation of intracellular processes into specialised membrane-bound compartments known as organelles. Plant cells contain several such organelles including the nucleus, chloroplast, mitochondrion, peroxisome, golgi, endoplasmic reticulum and vacuole. Organelle biogenesis and function is dependent on the concerted action of numerous nuclear-encoded proteins which must be imported from the cytosol (or endoplasmic reticulum) where they are made. Using phylogenomic approaches coupled to ancestral state estimation we show that the rate of change in plant organellar proteome content is proportional to the rate of molecular sequence evolution such that the proteomes of chloroplasts and mitochondria lose or gain ~3.2 proteins per million years. We show that these changes in protein targeting have predominantly occurred in genes with regulatory rather than metabolic functions, and thus altered regulatory capacity rather than metabolic function has been the major theme of plant organellar evolution. Finally we show gain and loss of protein targeting occurs at a higher rate following gene duplication events, revealing that gene and genome duplication are a key facilitator of organelle evolution.