Abstract
Phosphoenolpyruvate carboxylase (PEPC) plays pivotal roles in the carbon fixation of photosynthesis and a variety of metabolic and stress pathways. Suaeda aralocaspica belongs to a single-cellular C4 species and carries out a photosynthetic pathway in an unusually elongated chlorenchyma cell, which is expected to have PEPCs with different characteristics. To identify the different isoforms of PEPC genes in S. aralocaspica and comparatively analyze their expression and regulation patterns as well as the biochemical and enzymatic properties in this study, we characterized a bacterial-type PEPC (BTPC; SaPEPC-4) in addition to the two plant-type PEPCs (PTPCs; SaPEPC-1 and SaPEPC-2) using a genome-wide identification. SaPEPC-4 presented a lower expression level in all test combinations with an unknown function; two SaPTPCs showed distinct subcellular localizations and different spatiotemporal expression patterns but positively responded to abiotic stresses. Compared to SaPEPC-2, the expression of SaPEPC-1 specifically in chlorenchyma cell tissues was much more active with the progression of development and under various stresses, particularly sensitive to light, implying the involvement of SaPEPC-1 in a C4 photosynthetic pathway. In contrast, SaPEPC-2 was more like a non-photosynthetic PEPC. The expression trends of two SaPTPCs in response to light, development, and abiotic stresses were also matched with the changes in PEPC activity in vivo (native) or in vitro (recombinant), and the biochemical properties of the two recombinant SaPTPCs were similar in response to various effectors while the catalytic efficiency, substrate affinity, and enzyme activity of SaPEPC-2 were higher than that of SaPEPC-1 in vitro. All the different properties between these two SaPTPCs might be involved in transcriptional (e.g., specific cis-elements), posttranscriptional [e.g., 5′-untranslated region (5′-UTR) secondary structure], or translational (e.g., PEPC phosphorylation/dephosphorylation) regulatory events. The comparative studies on the different isoforms of the PEPC gene family in S. aralocaspica may help to decipher their exact role in C4 photosynthesis, plant growth/development, and stress resistance.
Highlights
Phosphoenolpyruvate carboxylase (PEPC, EC 4.1.1.31) is widely distributed in photosynthetic organisms such as vascular plants, algae, and photosynthetic bacteria
A total of three putative PEPC genes were identified by a local BLASTP search of S. aralocaspica genome, the deduced proteins were subjected to Pfam, SMART, and InterProScan databases to analyze the domains and active sites
Three nonredundant genes (GOSA_00009595-RA, GOSA_00006741-RA, and GOSA_00018957-RA) were confirmed as SaPEPCs, the first two were recognized as SaPEPC-1 (GenBank: KP985714.1) and SaPEPC-2 (GenBank: KX009562.1), respectively, which were identified in our previous work; the third one was similar to AtPPC4 in Arabidopsis and denominated as SaPEPC-4
Summary
Phosphoenolpyruvate carboxylase (PEPC, EC 4.1.1.31) is widely distributed in photosynthetic organisms such as vascular plants, algae, and photosynthetic bacteria. Plant PEPCs consist of a small gene family, which encodes several plant-type PEPCs (PTPCs) and at least one “distant relative” – bacterial-type PEPC (BTPC; Sánchez and Cejudo, 2003). With the completion of plant genome project and gene sequencing, numerous PEPC genes of different plant species have been identified, e.g., four PEPCs in Arabidopsis (Sánchez and Cejudo, 2003), five in tomato (Waseem and Ahmad, 2019), 10 in soybean (Wang et al, 2016), 5–9 in different peanut species (Yu et al, 2010; Pan et al, 2017; Tu et al, 2018), 6–11 among different cotton cultivars (Zhao et al, 2019), etc., limited information is available concerning PEPC from C4 species without Kranz anatomy. The introduction of the draft genome assembly of S. aralocaspica makes it possible to identify genomewide PEPC genes in S. aralocaspica (Wang et al, 2019)
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