Evolutionary Diversification of Primary Metabolism and Its Contribution to Plant Chemical Diversity

Abstract

Plants produce a diverse array of lineage-specific specialized (secondary) metabolites, which are synthesized from primary metabolites. Plant specialized metabolites play crucial roles in plant adaptation as well as in human nutrition and medicine. Unlike well-documented diversification of plant specialized metabolic enzymes, primary metabolism that provides essential compounds for cellular homeostasis is under strong selection pressure and generally assumed to be conserved across the plant kingdom. Yet, some alterations in primary metabolic pathways have been reported in plants. The biosynthetic pathways of certain amino acids and lipids have been altered in specific plant lineages. Also, two alternative pathways exist in plants for synthesizing primary precursors of the two major classes of plant specialized metabolites, terpenoids and phenylpropanoids. Such primary metabolic diversities likely underlie major evolutionary changes in plant metabolism and chemical diversity by acting as enabling or associated traits for the evolution of specialized metabolic pathways.

Harnessing evolutionary diversification of primary metabolism for plant synthetic biology

“…Here, I discuss one promising approach to achieve this goal by learning from millions of years of experimentations that nature has done. Although primary metabolism is generally assumed to be conserved across the plant kingdom, unlike highly-diversified specialized metabolism (45-48), there are some examples of evolutionary diversification of primary metabolic pathways, especially at the interface between primary and specialized metabolism (49). Exploring and harnessing such relatively-rare but key evolutionary innovations of plant metabolism will provide useful tools and strategies to optimize plant primary metabolism in coordination with downstream specialized metabolic pathways, in order to achieve efficient production of plant natural products in carefully-selected plant hosts.…”

A Tale of Two Families: Whole Genome and Segmental Duplications Underlie Glutamine Synthetase and Phosphoenolpyruvate Carboxylase Diversity in Narrow-Leafed Lupin (Lupinus angustifolius L.)

“…Usually, genes encoding enzymes located at the top of the metabolic pathway are under stronger purifying selection than downstream ones [87]. An association between the selective pressure acting on a gene and the position of an encoded enzyme in the pathway was revealed in a wide metabolic context [88,89], including L. angustifolius genes encoding isoflavone synthase and acetyl-coenzyme A carboxylase [63,64]. A higher selection pressure acts on central and highly connected enzymes, enzymes with high metabolic flux, and enzymes catalyzing reactions that are difficult to bypass through alternative pathways [88].…”

“…A higher selection pressure acts on central and highly connected enzymes, enzymes with high metabolic flux, and enzymes catalyzing reactions that are difficult to bypass through alternative pathways [88]. Moreover, enzymes participating in primary metabolism are usually under a constant strong selective pressure, whereas enzymes performing specified metabolism are under weaker negative selection [89]. One of the postulated explanations for the above pattern is that these specified metabolism genes initially experienced positive selection (higher rate than primary metabolism genes) [90].…”

Network Analysis Provides Insight into Tomato Lipid Metabolism

“…Plants produce a wide variety of biochemical compounds, starting at the central or primary metabolism which generates compounds absolutely vital for plant survival and continuing through the pathways of specialized or secondary metabolism [1][2][3][4][5]. Specialized metabolites display a tremendous diversity, are often specific to certain plant lineages, and play many different roles in adaptation to the environment [6]. Volatile organic compounds (VOCs) are often discussed as a subgroup of secondary metabolites, with their low molecular weight enabling movement across cell membranes and release into the surrounding environment [7].…”