A revised view on the evolution of glutamine synthetase isoenzymes in plants

Abstract

Glutamine synthetase (GS) is a key enzyme responsible for the incorporation of inorganic nitrogen in the form of ammonium into the amino acid glutamine. The genes encoding GS are among the oldest existing genes in living organisms. In plants, two groups of functional GS enzymes are found: eubacterial GSIIb (GLN2) and eukaryotic GSIIe (GLN1/GS). Phylogenetic analyses have shown that the GLN2 group originated from bacteria following horizontal gene transfer. Only GLN1/GS genes are found in vascular plants, which suggests that they are involved in the final adaptation of plants to terrestrial life. The present phylogenetic study reclassifies the different GS of seed plants into three clusters: GS1a, GS1b and GS2. The presence of genes encoding GS2 has been expanded to Cycadopsida gymnosperms, which suggests the origin of this gene in a common ancestor of Cycadopsida, Ginkgoopsida and angiosperms. GS1a genes have been identified in all gymnosperms, basal angiosperms and some Magnoliidae species. Previous studies in conifers and the gene expression profiles obtained in ginkgo and magnolia in the present work could explain the absence of GS1a in more recent angiosperm species (e.g., monocots and eudicots) due to the redundant roles of GS1a and GS2 in photosynthetic cells. Altogether, the results provide a better understanding of the evolution of plant GS isoenzymes and their physiological roles, which is valuable for improving crop nitrogen use efficiency and productivity.

Is plastidic glutamine synthetase essential for C3 plants? A tale of photorespiratory mutants, ammonium tolerance and conifers

“…Conifers and gnetales lack GS2 (Valderrama‐Martín et al ., 2022) but they have high photorespiratory rates (Hanawa et al ., 2017). As an alternative to GS2, gymnosperms possess GS1a, which, although cytosolic, performs a GS2‐like function, namely photorespiratory NH 4 + reassimilation (Cánovas et al ., 2007).…”

“…As an alternative to GS2, gymnosperms possess GS1a, which, although cytosolic, performs a GS2‐like function, namely photorespiratory NH 4 + reassimilation (Cánovas et al ., 2007). Indeed, as is the case with GS2, GS1a is mainly expressed in photosynthetic tissues, and its gene expression is light‐dependent (Cantón et al ., 1999; Valderrama‐Martín et al ., 2022). This fact, together with the findings regarding GLN2 mutants in Arabidopsis (Ferreira et al ., 2019; Hachiya et al ., 2021), demonstrate that GS subcellular location is not essential for plant survival, but probably for the coordination of GS gene expression with photosynthesis and photorespiration, as is the case for GS1a in conifers.…”

“… 1 DvGS2 is a homologue of the GLN2 gene from the green algae Chlamydomonas reinhardtii and thus corresponds to a different evolutionary lineage than GS2 from seed plants (Valderrama‐Martín et al ., 2022). …”

“…In seed plants, the GS family is composed of the cytosol‐localized GS1 and the plastid‐localized GS2. In a recent study, it was proposed that GS1 is divided into two evolutionary lineages, named according to their sequence and functional similarity to the gymnosperm GS1s: GS1a‐like and GS1b‐like (Valderrama‐Martín et al ., 2022). GS1b is found in all seed plants and GS1a is present exclusively in gymnosperms and basal angiosperms.…”

“…GS1b is found in all seed plants and GS1a is present exclusively in gymnosperms and basal angiosperms. GS2 is present in all seed plants except conifers and gnetales (Valderrama‐Martín et al ., 2022). In general, GS1 is encoded by multiple genes, whereas GS2 is, in diploid species, generally encoded by a single gene.…”