Abstract
The degradation of damaged proteins is essential for cell viability. Lon is a highly conserved ATP-dependent serine-lysine protease that maintains proteostasis. We performed a comparative genome-wide analysis to determine the evolutionary history of Lon proteases. Prokaryotes and unicellular eukaryotes retained a single Lon copy, whereas multicellular eukaryotes acquired a peroxisomal copy, in addition to the mitochondrial gene, to sustain the evolution of higher order organ structures. Land plants developed small Lon gene families. Despite the Lon2 peroxisomal paralog, Lon genes triplicated in the Arabidopsis lineage through sequential evolutionary events including whole-genome and tandem duplications. The retention of Lon1, Lon4, and Lon3 triplicates relied on their differential and even contrasting expression patterns, distinct subcellular targeting mechanisms, and functional divergence. Lon1 seems similar to the pre-duplication ancestral gene unit, whereas the duplication of Lon3 and Lon4 is evolutionarily recent. In the wider context of plant evolution, papaya is the only genome with a single ancestral Lon1-type gene. The evolutionary trend among plants is to acquire Lon copies with ambiguous pre-sequences for dual-targeting to mitochondria and chloroplasts, and a substrate recognition domain that deviates from the ancestral Lon1 type. Lon genes constitute a paradigm of dynamic evolution contributing to understanding the functional fate of gene duplicates.
Highlights
Energy metabolism relies on the decomposition of polyunsaturated fatty acids and carbohydrates during storage reserve mobilization
Eukaryotic genomes have large numbers of duplicated genes that can evolve expression divergence, which might represent an important evolutionary mechanism for retention of duplicated genes (Haberer et al, 2004; Liu et al, 2011).To test whether Lon genes differentiate in terms of the expression profile, we analyzed data obtained by independent high-throughput approaches of the Arabidopsis transcriptome
The differential expression pattern between the Lon genes was confirmed by meta-analysis of microarray data for Arabidopsis (Fig. 1B; Zimmermann et al, 2004)
Summary
Energy metabolism relies on the decomposition of polyunsaturated fatty acids and carbohydrates during storage reserve mobilization. This process is performed by intricately interconnected biochemical pathways, functional in more than one plant organelle including mitochondria, chloroplasts, and peroxisomes. While energy production is efficient, it often results in harmful by-products. In these eukaryotic organelles, the accumulation of oxidants creates an oxidative environment and causes irreversible modification of proteins (Møller et al, 2007, 2011). Proteome homeostasis in plant organelles is preserved by energy-driven processive proteases that maintain protein quality control by removing defective or damaged proteins, preventing the formation of insoluble and deleterious protein aggregates.
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