Legume Cytosolic and Plastid Acetyl-Coenzyme—A Carboxylase Genes Differ by Evolutionary Patterns and Selection Pressure Schemes Acting before and after Whole-Genome Duplications

Abstract

Acetyl-coenzyme A carboxylase (ACCase, E.C.6.4.1.2) catalyzes acetyl-coenzyme A carboxylation to malonyl coenzyme A. Plants possess two distinct ACCases differing by cellular compartment and function. Plastid ACCase contributes to de novo fatty acid synthesis, whereas cytosolic enzyme to the synthesis of very long chain fatty acids, phytoalexins, flavonoids, and anthocyanins. The narrow leafed lupin (Lupinus angustifolius L.) represents legumes, a plant family which evolved by whole-genome duplications (WGDs). The study aimed on the contribution of these WGDs to the multiplication of ACCase genes and their further evolutionary patterns. The molecular approach involved bacterial artificial chromosome (BAC) library screening, fluorescent in situ hybridization, linkage mapping, and BAC sequencing. In silico analysis encompassed sequence annotation, comparative mapping, selection pressure calculation, phylogenetic inference, and gene expression profiling. Among sequenced legumes, the highest number of ACCase genes was identified in lupin and soybean. The most abundant plastid ACCase subunit genes were accB. ACCase genes in legumes evolved by WGDs, evidenced by shared synteny and Bayesian phylogenetic inference. Transcriptional activity of almost all copies was confirmed. Gene duplicates were conserved by strong purifying selection, however, positive selection occurred in Arachis (accB2) and Lupinus (accC) lineages, putatively predating the WGD event(s). Early duplicated accA and accB genes underwent transcriptional sub-functionalization.

Photoperiod and Vernalization Control of Flowering-Related Genes: A Case Study of the Narrow-Leafed Lupin (Lupinus angustifolius L.)

“…L. angustifolius genome contains two FTa and two FTc genes, which putatively arose from single copies by lineage-specific duplication, whereas the whole FTb subclade is absent (Ksiażkiewicz et al, 2016). Indeed, L. angustifolius was recently used as a reference species in several phylogenetic studies addressing the influence of wholegenome and local duplications on the evolutionary fate of selected legume-specific and plant-wide gene clades (Przysiecka et al, 2015;Narożna et al, 2017;Szczepaniak et al, 2018;Czyż et al, 2020). The differences in the expression profiles for FTa and FTc genes, as established in the present study, provided novel evidence supporting the hypothesis on a functional divergence of particular duplicates.…”

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

“…Hane et al estimated the Papilionoideae radiation at 58 mya with genistoid lineage separation from the other Papilionoideae legumes at 54.6 mya, followed by whole-genome triplication in the genistoid lineage at 24.6 mya [11]. Additionally, the ancient polyploidy event has been confirmed based on an analysis of several genes, such as chalcone isomerases (CHI) [62], phosphatidylethanolamine binding proteins (PEBP) [30], isoflavone synthetases (IFS) [63], and cytosolic and plastid acetyl-coenzyme A carboxylases (ACCase) [64]. All listed genes are present in the narrow-leafed lupin genome in multiple variants and evolved by WGDs, evidenced by shared synteny and Bayesian phylogenetic inference.…”

“…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].…”

Allelic Diversity of Acetyl Coenzyme A Carboxylase accD/bccp Genes Implicated in Nuclear-Cytoplasmic Conflict in the Wild and Domesticated Pea (Pisum sp.)

“…The heteromeric form of ACCase is found in prokaryotes and the plastids of Viridiplantae. Presumably, all genes encoding ACCase subunits initially resided in the plastid genome after the original endosymbiotic event in algae and underwent sequential transfer to the nuclear genome [42]. Plastid ACCase participates in fatty acid synthesis, whereas the cytosolic enzyme is engaged in the synthesis of very long chain fatty acids, phytoalexins, flavonoids, and anthocyanins.…”

“…The plastid ACCase of legumes (Papilionoideae) consists of four subunits, each coded by a separate gene: biotin carboxylase ( accC ), biotin carboxyl carrier protein ( accB=bccp ), alpha-carboxyltransferase ( accA ), and beta-carboxyltransferase ( accD ). The genes coding accC, accB, and accA are localized in the nuclear genome, whereas the accD gene is localized in the plastid genome [42]. Multiple independent lineages have experienced accelerated rates of substitution in similar subsets of non-photosynthetic genes, including accD (in legumes [43,44,45] and in Oleaceae [46]).…”