Convergent molecular evolution of phosphoenolpyruvate carboxylase gene family in C₄ and crassulacean acid metabolism plants

Abstract

Phosphoenolpyruvate carboxylase (PEPC), as the key enzyme in initial carbon fixation of C4and crassulacean acid mechanism (CAM) pathways, was thought to undergo convergent adaptive changes resulting in the convergent evolution of C4 and CAM photosynthesis in vascular plants. However, the integral evolutionary history and convergence of PEPC in plants remain poorly understood. In the present study, we identified the members of PEPC gene family across green plants with seventeen genomic datasets, found ten conserved motifs and modeled three-dimensional protein structures of 90 plant-type PEPC genes. After reconstructing PEPC gene family tree and reconciled with species tree, we found PEPC genes underwent 71 gene duplication events and 16 gene loss events, which might result from whole-genome duplication events in plants. Based on the phylogenetic tree of the PEPC gene family, we detected four convergent evolution sites of PEPC in C4 species but none in CAM species. The PEPC gene family was ubiquitous and highly conservative in green plants. After originating from gene duplication of ancestral C3-PEPC, C4-PEPC isoforms underwent convergent molecular substitution that might facilitate the convergent evolution of C4 photosynthesis in Angiosperms. However, there was no evidence for convergent molecular evolution of PEPC genes between CAM plants. Our findings help to understand the origin and convergent evolution of C4 and CAM plants and shed light on the adaptation of plants in dry, hot environments.

Changes in Phytohormones and Transcriptomic Reprogramming in Strawberry Leaves under Different Light Qualities

“…Phosphoenolpyruvate carboxylase (CAPP) forms oxaloacetate through the carboxylation of phosphoenolpyruvate and CO 2 (atmospheric) [ 35 ], and malate dehydrogenase (MDHP or MDHG) catalyzes the NAD/NADH-dependent interconversion of the substrates malate and oxaloacetate [ 36 ]. Aspartate aminotransferase (AATC) is a bidirectional enzyme that exists between oxaloacetate and aspartate.…”

“…A high proportion of DEGs was associated with molecular functions, including photosynthesis antenna proteins (69), photosynthesis (68), carbon fixation in photosynthetic organisms (80), porphyrin and chlorophyll metabolisms (37), carotenoid biosynthesis (35), tryptophan metabolism (29), phenylalanine metabolism (19), zeatin biosynthesis (13), and alpha-linolenic acid metabolism (46) (Figure 1c).…”

Diurnal Rhythms in the Red Seaweed Gracilariopsis chorda are Characterized by Unique Regulatory Networks of Carbon Metabolism

“…chorda (pattern-e; Fig. 3 ), and likely plays an important role in the induction of cytosolic OAA ( Shi et al 2015 ; Walker et al 2021 ; Shu et al 2022 ). This enzyme is supported by carbonic anhydrase (CA) which catalyzes the interconversion of carbon dioxide to bicarbonate (CO 2 + H 2 O ←→ HCO 3 − + H + )—a major CO 2 -concentrating mechanism (CCM) in G .…”

Plasticity of Plantago lanceolata L. in Adaptation to Extreme Environmental Conditions

“…P. lanceolata is an obligate C 3 plant with primary photosynthetic CO 2 fixation via RubisCO; however, it is important to note that all the plants are also equipped with carboxylating PEPC, which is involved in a variety of non-photosynthetic anaplerotic roles, including nitrogen fixation [16,17,19]. Its carboxylating activity enabling catalysis of CO 2 into oxaloacetic acid is well described in the stomata of C 4 and CAM plants.…”

“…In the midribs of this plant, there is high electron transport rate (ETR) efficiency, and the resulting energy can support veinal tissues in their transport function. PEPC, which is responsible for β-carboxylation, also plays a crucial role in a variety of important non-photosynthetic anaplerotic functions [16][17][18], including nitrogen fixation, known as a process necessary for synthetizing proteins, nucleic acids and many other biomolecules [19]; thus, PEPC creates, at least partially, carbon-nitrogen interactions, and some PEPC isoforms are more specifically expressed in the roots [20]. As reported by Hibberd and Quick [9], and Brown et al [21], PEPC localized in the root tissues is responsible for significant CO 2 fixation in tobacco and Arabidopsis plants.…”