Plant Carbonic Anhydrases: Structures, Locations, Evolution, and Physiological Roles

© 2017 The Authors Carbonic anhydrases (CAs) are zinc metalloenzymes that catalyze the interconversion of CO2 and HCO3− and are ubiquitous in nature. Higher plants contain three evolutionarily distinct CA families, αCAs, βCAs, and γCAs, where each family is represented by multiple isoforms in all species. Alternative splicing of CA transcripts appears common; consequently, the number of functional CA isoforms in a species may exceed the number of genes. CAs are expressed in numerous plant tissues and in different cellular locations. The most prevalent CAs are those in the chloroplast, cytosol, and mitochondria. This diversity in location is paralleled in the many physiological and biochemical roles that CAs play in plants. In this review, the number and types of CAs in C3, C4, and crassulacean acid metabolism (CAM) plants are considered, and the roles of the α and γCAs are briefly discussed. The remainder of the review focuses on plant βCAs and includes the identification of homologs between species using phylogenetic approaches, a consideration of the inter- and intracellular localization of the proteins, along with the evidence for alternative splice forms. Current understanding of βCA tissue-specific expression patterns and what controls them are reviewed, and the physiological roles for which βCAs have been implicated are presented

Multiple photosynthetic transitions, polyploidy, and lateral gene transfer in the grass subtribe Neurachninae

The Neurachninae is the only grass lineage known to contain C3, C4, and C3–C4 intermediate species, and as such has been suggested as a model system for studies of photosynthetic pathway evolution in the Poaceae; however, a lack of a robust phylogenetic framework has hindered this possibility. In this study, plastid and nuclear markers were used to reconstruct evolutionary relationships among Neurachninae species. In addition, photosynthetic types were determined with carbon isotope ratios, and genome sizes with flow cytometry. A high frequency of autopolyploidy was found in the Neurachninae, including in Neurachne munroi F.Muell. and Paraneurachne muelleri S.T.Blake, which independently evolved C4 photosynthesis. Phylogenetic analyses also showed that following their separate C4 origins, these two taxa exchanged a gene encoding the C4 form of phosphoenolpyruvate carboxylase. The C3–C4 intermediate Neurachne minor S.T.Blake is phylogenetically distinct from the two C4 lineages, indicating that intermediacy in this species evolved separately from transitional stages preceding C4 origins. The Neurachninae shows a substantial capacity to evolve new photosynthetic pathways repeatedly. Enablers of these transitions might include anatomical pre-conditions in the C3 ancestor, and frequent autopolyploidization. Transfer of key C4 genetic elements between independently evolved C4 taxa may have also facilitated a rapid adaptation of photosynthesis in these grasses that had to survive in the harsh climate appearing during the late Pliocene in Australia

Loss of the chloroplast transit peptide from an ancestral C3 carbonic anhydrase is associated with C4 evolution in the grass genus Neurachne

Neurachne is the only known grass lineage containing closely related C3, C3-C4intermediate, and C4species, making it an ideal taxon with which to study the evolution of C4photosynthesis in the grasses. To begin dissecting the molecular changes that led to the evolution of C4photosynthesis in this group, the complementary DNAs encoding four distinct β-carbonic anhydrase (CA) isoforms were characterized from leaf tissue of Neurachne munroi (C4), Neurachne minor (C3-C4), and Neurachne alopecuroidea (C3). Two genes (CA1 and CA2) each encode two different isoforms: CA1a/CA1b and CA2a/CA2b. Transcript analyses found that CA1 messenger RNAs were significantly more abundant than transcripts from the CA2 gene in the leaves of each species examined, constituting ∼99% of all β-CA transcripts measured. Localization experiments using green fluorescent protein fusion constructs showed that, while CA1b is a cytosolic CA in all three species, the CA1a proteins are differentially localized. The N. alopecuroidea and N. minor CA1a isoforms were imported into chloroplasts of Nicotiana benthamiana leaf cells, whereas N. munroi CA1a localized to the cytosol. Sequence analysis indicated an 11-amino acid deletion in the amino terminus of N. munroi CA1a relative to the C3and C3-C4proteins, suggesting that chloroplast targeting of CA1a is the ancestral state and that loss of a functional chloroplast transit peptide in N. munroi CA1a is associated with the evolution of C4photosynthesis in Neurachne spp. Remarkably, this mechanism is homoplastic with the evolution of the C4-associated CA in the dicotyledonous genus Flaveria, although the actual mutations in the two lineages differ

Mouse apolipoprotein J: characterization of a gene implicated in atherosclerosis.

Apolipoprotein J (apoJ), a glycoprotein associated with subclasses of plasma high density lipoproteins (HDL), was found to accumulate in aortic lesions in a human subject with transplantation-associated arteriosclerosis and in mice fed a high-fat atherogenic diet. Foam cells present in mouse aortic valve lesions expressed apoJ mRNA, suggesting local synthesis contributes to apoJ\u27s localization in atherosclerotic plaque. As a prerequisite for elucidating the physiological function of apoJ by using a mouse model, cDNA clones representing the mouse homolog of apoJ were isolated, characterized, and sequenced. The nucleotide sequence predicts a 448 amino acid, 50,260 dalton protein. There was 81% nucleotide sequence similarity between mouse and human apoJ, and 75% similarity at the amino acid level. Mouse apoJ contains six potential N-glycosylation sites, a potential Arg-Ser cleavage site to generate alpha and beta subunits, a cluster of five cysteine residues in each subunit, three putative amphipathic helices, and four potential heparin-binding domains. Southern blot analysis indicates that the gene encompasses approximately 23 kb of DNA. Recombinant inbred strains were used to map apoJ to mouse chromosome 14, tightly linked to Mtv-11. All of the transcribed portions of the gene were cloned and analyzed, and all intron-exon boundaries were defined. The first of the 9 exons is untranslated. Single exons encode the signal peptide, the cysteine-rich domain in the alpha subunit, two potential amphipathic helices flanking a heparin-binding consensus sequence, and a potential amphipathic helix overlapping a heparin-binding domain, supporting their potential functional significance in apoJ. A variety of mouse tissues constitutively express a 1.9 kb apoJ mRNA, with apparently identical transcriptional start sites utilized in all tissues tested. ApoJ mRNA was most abundant in stomach, liver, brain, and testis, with intermediate levels in heart, ovary, and kidney. The high degree of similarity between mouse and human apoJ, in structure and distribution of the gene product, gene structure, and deposition in atherosclerotic plaques, suggests that the mouse is an ideal model with which to elucidate the role of apoJ in HDL metabolism and atherogenesis

One thousand plant transcriptomes and the phylogenomics of green plants

Abstract: Green plants (Viridiplantae) include around 450,000–500,000 species1, 2 of great diversity and have important roles in terrestrial and aquatic ecosystems. Here, as part of the One Thousand Plant Transcriptomes Initiative, we sequenced the vegetative transcriptomes of 1,124 species that span the diversity of plants in a broad sense (Archaeplastida), including green plants (Viridiplantae), glaucophytes (Glaucophyta) and red algae (Rhodophyta). Our analysis provides a robust phylogenomic framework for examining the evolution of green plants. Most inferred species relationships are well supported across multiple species tree and supermatrix analyses, but discordance among plastid and nuclear gene trees at a few important nodes highlights the complexity of plant genome evolution, including polyploidy, periods of rapid speciation, and extinction. Incomplete sorting of ancestral variation, polyploidization and massive expansions of gene families punctuate the evolutionary history of green plants. Notably, we find that large expansions of gene families preceded the origins of green plants, land plants and vascular plants, whereas whole-genome duplications are inferred to have occurred repeatedly throughout the evolution of flowering plants and ferns. The increasing availability of high-quality plant genome sequences and advances in functional genomics are enabling research on genome evolution across the green tree of life