From algae to vascular plants: The multistep evolutionary trajectory of the ALDH superfamily towards functional promiscuity and the emergence of structural characteristics

Abstract

Aldehyde dehydrogenases (ALDHs) constitute an evolutionary conserved superfamily of oxidoreductases, which convert a large array of aldehydes to carboxylic acids. Plant ALDHs caught attention in the last two decades after the discovery of their central role in the adaptive responses to abiotic stress. Recent advances in next-generation sequencing and genome assembly enabled us to identify many ALDH genes of plants from diverse lineages. This provided valuable clues to trace their evolutionary trajectory. The ALDH superfamily has ancient origins that go back to the chromista kingdom. Major evolutionary events like the conquest of land by plants, and later their vascularization, along with the acquisition of developmental complexity coincide with important changes in the abundance, expansion, and diversification of ALDH genes and proteins. Plant ALDH sequences divergence led to the emergence of functions, absent in their algal ancestors. The most evolved, higher plant ALDHs have functional promiscuity which positioned them as important ‘hubs’ at the crossroads of the primary/basal and the stress-related metabolism. Stress-responsive ALDHs mitigate the harmful effect of cytotoxic aldehydes resulting from lipid peroxidation occurring during oxidative stress and contribute to the synthesis of osmolytes, like glycine betaine. Other isoforms play significant roles in glycolysis, TCA cycle, and amino acid catabolism. Therefore, plant ALDHs are attractive targets for molecular breeding of stress tolerant plants. The overall three-dimensional structures and the catalytic mechanism of ALDHs are conserved in prokaryotes, mammalians, and plants. However, some amino acids at specific locations, underwent progressive changes in the course of the evolution of plantae, yielding shifts in the enzymatic properties, including substrate and cofactor specificities. We explore data related to the evolutionary history of ALDHs, gather information about their biochemical functions, and discuss their physiological relevance.