Codon usage bias and determining forces in green plant mitochondrial genomes

The phenomenon of codon usage bias has been observed in a wide range of organisms. As organisms evolve, how their codon usage pattern change is still an intriguing question. In this article, we focused on the green plant mitochondrial genomes to analyze the codon usage patterns in different lineages, and more importantly, to investigate the possible change of determining forces during the plant evolution. Two patterns were observed between the separate lineages of green plants: Chlorophyta and Streptophyta. In Chlorophyta lineages, their codon usages showed substantial variation (from strongly A, T-biased to strongly G, C-biased); while in Streptophyta lineages, especially in the land plants, the overall codon usages are interestingly stable. Further, based on the Nc-GC3s plots and Akashi's scaled χ(2) -tests, we found that lineages within Chlorophyta exhibit much stronger evidence of deviating from neutrality; while lineages within Streptophyta rarely do so. Such differences, together with previous reports based on the chloroplast data, suggests that after plants colonized the land, their codon usages in organellar genomes are more reluctant to be shaped by selection force.     

Unraveling the evolution of auxin signaling

Auxin signaling is central to plant growth and development, yet hardly anything is known about its evolutionary origin. While the presence of key players in auxin signaling has been analyzed in various land plant species, similar analyses in the green algal lineages are lacking. Here, we survey the key players in auxin biology in the available genomes of Chlorophyta species. We found that the genetic potential for auxin biosynthesis and AUXIN1 (AUX1)/LIKE AUX1- and P-GLYCOPROTEIN/ATP-BINDING CASSETTE subfamily B-dependent transport is already present in several single-celled and colony-forming Chlorophyta species. In addition, our analysis of expressed sequence tag libraries from Coleochaete orbicularis and Spirogyra pratensis, green algae of the Streptophyta clade that are evolutionarily closer to the land plants than those of the Chlorophyta clade, revealed the presence of partial AUXIN RESPONSE FACTORs and/or AUXIN/INDOLE-3-ACETIC ACID proteins (the key factors in auxin signaling) and PIN-FORMED-like proteins (the best-characterized auxin-efflux carriers). While the identification of these possible AUXIN RESPONSE FACTOR- and AUXIN/INDOLE-3-ACETIC ACID precursors and putative PIN-FORMED orthologs calls for a deeper investigation of their evolution after sequencing more intermediate genomes, it emphasizes that the canonical auxin response machinery and auxin transport mechanisms were, at least in part, already present before plants "moved" to land habitats.     

The glycosyltransferase repertoire of the spikemoss Selaginella moellendorffii and a comparative study of its cell wall

Spike mosses are among the most basal vascular plants, and one species, Selaginella moellendorffii, was recently selected for full genome sequencing by the Joint Genome Institute (JGI). Glycosyltransferases (GTs) are involved in many aspects of a plant life, including cell wall biosynthesis, protein glycosylation, primary and secondary metabolism. Here, we present a comparative study of the S. moellendorffii genome across 92 GT families and an additional family (DUF266) likely to include GTs. The study encompasses the moss Physcomitrella patens, a non-vascular land plant, while rice and Arabidopsis represent commelinid and non-commelinid seed plants. Analysis of the subset of GT-families particularly relevant to cell wall polysaccharide biosynthesis was complemented by a detailed analysis of S. moellendorffii cell walls. The S. moellendorffii cell wall contains many of the same components as seed plant cell walls, but appears to differ somewhat in its detailed architecture. The S. moellendorffii genome encodes fewer GTs (287 GTs including DUF266s) than the reference genomes. In a few families, notably GT51 and GT78, S. moellendorffii GTs have no higher plant orthologs, but in most families S. moellendorffii GTs have clear orthologies with Arabidopsis and rice. A gene naming convention of GTs is proposed which takes orthologies and GT-family membership into account. The evolutionary significance of apparently modern and ancient traits in S. moellendorffii is discussed, as is its use as a reference organism for functional annotation of GTs.     

Biochemical control of xylan biosynthesis - which end is up?

Xylans are major components of land plant secondary cell walls and are required for normal plant growth and development. Secondary walls also account for the bulk of lignocellulosic biomass, a potential feedstock for large-scale production of biofuels. Glucuronoxylan and arabinoxylan affect the conversion of lignocellulosic biomass to fermentable sugar, a crucial and expensive step in biofuel production. Thus, knowledge of xylan biosynthesis may provide tools to modify secondary cell wall structure and thereby improve the bioprocessing characteristics of biomass. Recent studies have shown that glucuronoxylan structure and biosynthesis are far more complex than previously appreciated and the number of glycosyltransferases implicated in this process continues to increase. New hypotheses regarding the mechanisms of glucuronoxylan biosynthesis challenge some widely held views.     

Mitochondrial Genome of Prasinophyte Alga Pyramimonas parkeae

Prasinophytes are a paraphyletic assemblage of nine heterogeneous lineages in the Chlorophyta clade of Archaeplastida. Until now, seven complete mitochondrial genomes have been sequenced from four prasinophyte lineages. Here, we report the mitochondrial genome of Pyramimonas parkeae, the first representative of the prasinophyte clade I. The circular‐mapping molecule is 43,294 bp long, AT rich (68.8%), very compact and it comprises two 6,671 bp long inverted repeat regions. The gene content is slightly smaller than the gene‐richest prasinophyte mitochondrial genomes. The single identified intron is located in the cytochrome c oxidase subunit 1 gene (cox1). Interestingly, two exons of cox1 are encoded on the same strand of DNA in the reverse order and the mature mRNA is formed by trans‐splicing. The phylogenetic analysis using the data set of 6,037 positions assembled from 34 mtDNA‐encoded proteins of 48 green algae and plants is not in compliance with the branching order of prasinophyte clades revealed on the basis of 18S rRNA genes and cpDNA‐encoded proteins. However, the phylogenetic analyses based on all three genomic elements support the sister position of prasinophyte clades Pyramimonadales and Mamiellales.     

Phylogenetic analyses of nuclear, mitochondrial, and plastid multigene data sets support the placement of Mesostigma in the Streptophyta

All extant green plants belong to 1 of 2 major lineages, commonly known as the Chlorophyta (most of the green algae) and the Streptophyta (land plants and their closest green algal relatives). The scaly green flagellate Mesostigma viride has an important place in the debate on the origin of green plants. However, there have been conflicting results from molecular systematics as to whether Mesostigma diverges before the Chlorophyta/Streptophyta split or is an early diverging flagellate member of the Streptophyta. Previous studies employed either a limited taxon sampling (plastid and mitochondrial genomes) or a small number of phylogenetically informative sites (single nuclear genes). Here, we use large data sets from the nuclear (125 proteins; 29,319 positions), mitochondrial (33 proteins; 6,622 positions), and plastid (50 proteins; 10,137 positions) genomes with an expanded taxon sampling (21, 13, and 28 species, respectively) to reevaluate the phylogenetic position of Mesostigma. Our study supports the placement of Mesostigma in the Streptophyta (as an early diverging lineage) and provides evidence that systematic biases have played a role in generating some of the previous conflicting results. Importantly, we demonstrate that using an increased taxon sampling as well as more realistic models of evolution allows increasing congruence among the nuclear, mitochondrial, and plastid data sets.     

Development of functional modules based on co-expression patterns for cell-wall biosynthesis related genes in rice

The functional elucidation of plant cell wall biosynthesis (CWB) related genes is important for understanding various stress tolerance responses as well as enhancing biomass in plants. Despite their significant role in physiology and growth of the plant, the function of a limited number of CWB related genes have been identified. Major obstacles such as functional redundancy and limited functional information pose challenges in the characterization of CWB genes. Here, a genome-wide analysis of CWB genes using meta-expression data revealed their roles in stress tolerance and developmental processes. The identification of coexpressed CWB genes suggests functional modules for plant cell wall biosynthesis associated with specific tissue types, biotic stress, abiotic stress, and hormone responses. More interestingly, we identified that glycosyl hydrolases are specialized for root and pollen development, glycosyltransferases for ubiquitous function and leaf development, and carbohydrate esterases for pollen development. A T-DNA insertional mutant of OsCESA9 showing internode preferred expression revealed severe dwarfism and a co-expression network analysis of OsCESA9 in oscesa9 mutant suggest downstream pathways for secondary cell wall biosynthesis and DNA repair processes. Data from our studies will facilitate functional genomic studies of CWB genes in rice and contribute to the enhancement of biomass and yield in crop plants.     

Three rings for the evolution of plastid shape: a tale of land plant FtsZ

Nuclear-encoded plant FtsZ genes are derived from endosymbiotic gene transfer of cyanobacteria-like genes. The green lineage (Chloroplastida) and red lineage (Rhodophyta) feature FtsZ1 and FtsZ2 or FtsZB and FtsZA, respectively, which are involved in plastid division. These two proteins show slight differences and seem to heteropolymerize to build the essential inner plastid division ring. A third gene, encoding FtsZ3, is present in glaucophyte and charophyte algae, as well as in land plants except ferns and angiosperms. This gene was probably present in the last common ancestor of the organisms united by having a primary plastid (Archaeplastida) and was lost during vascular plant evolution as well as in the red and green algae. The presence/absence pattern of FtsZ3 mirrors that of a full set of Mur genes and the peptidoglycan wall encoded by them. Based on these findings, we discuss a role for FtsZ3 in the establishment or maintenance of plastid peptidoglycan shells.     

The closest lineage of Archaeplastida is revealed by phylogenomics analyses that include Microheliella maris

By clarifying the phylogenetic positions of ‘orphan’ protists (unicellular micro-eukaryotes with no affinity to extant lineages), we may uncover the novel affiliation between two (or more) major lineages in eukaryotes. Microheliella maris was an orphan protist, which failed to be placed within the previously described lineages by pioneering phylogenetic analyses. In this study, we analysed a 319-gene alignment and demonstrated that M. maris represents a basal lineage of one of the major eukaryotic lineages, Cryptista. We here propose a new clade name ‘Pancryptista’ for Cryptista plus M. maris. The 319-gene analyses also indicated that M. maris is a key taxon to recover the monophyly of Archaeplastida and the sister relationship between Archaeplastida and Pancryptista, which is collectively called ‘CAM clade’ here. Significantly, Cryptophyceae tend to be attracted to Rhodophyta depending on the taxon sampling (ex., in the absence of M. maris and Rhodelphidia) and the particular phylogenetic ‘signal’ most likely hindered the stable recovery of the monophyly of Archaeplastida in previous studies.     

A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies

Background  

The Viridiplantae comprise two major phyla: the Streptophyta, containing the charophycean green algae and all land plants, and the Chlorophyta, containing the remaining green algae. Despite recent progress in unravelling phylogenetic relationships among major green plant lineages, problematic nodes still remain in the green tree of life. One of the major issues concerns the scaly biflagellate Mesostigma viride, which is either regarded as representing the earliest divergence of the Streptophyta or a separate lineage that diverged before the Chlorophyta and Streptophyta. Phylogenies based on chloroplast and mitochondrial genomes support the latter view. Because some green plant lineages are not represented in these phylogenies, sparse taxon sampling has been suspected to yield misleading topologies. Here, we describe the complete chloroplast DNA (cpDNA) sequence of the early-diverging charophycean alga Chlorokybus atmophyticus and present chloroplast genome-based phylogenies with an expanded taxon sampling.     

A genome-wide phylogenetic reconstruction of family 1 UDP-glycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land

For almost a decade, our knowledge on the organisation of the family 1 UDP‐glycosyltransferases (UGTs) has been limited to the model plant A. thaliana. The availability of other plant genomes represents an opportunity to obtain a broader view of the family in terms of evolution and organisation. Family 1 UGTs are known to glycosylate several classes of plant secondary metabolites. A phylogeny reconstruction study was performed to get an insight into the evolution of this multigene family during the adaptation of plants to life on land. The organisation of the UGTs in the different organisms was also investigated. More than 1500 putative UGTs were identified in 12 fully sequenced and assembled plant genomes based on the highly conserved PSPG motif. Analyses by maximum likelihood (ML) method were performed to reconstruct the phylogenetic relationships existing between the sequences. The results of this study clearly show that the UGT family expanded during the transition from algae to vascular plants and that in higher plants the clustering of UGTs into phylogenetic groups appears to be conserved, although gene loss and gene gain events seem to have occurred in certain lineages. Interestingly, two new phylogenetic groups, named O and P, that are not present in A. thaliana were discovered.     

XET activity is found near sites of growth and cell elongation in bryophytes and some green algae: new insights into the evolution of primary cell wall elongation

BACKGROUND AND AIMS: In angiosperms xyloglucan endotransglucosylase (XET)/hydrolase (XTH) is involved in reorganization of the cell wall during growth and development. The location of oligo-xyloglucan transglucosylation activity and the presence of XTH expressed sequence tags (ESTs) in the earliest diverging extant plants, i.e. in bryophytes and algae, down to the Phaeophyta was examined. The results provide information on the presence of an XET growth mechanism in bryophytes and algae and contribute to the understanding of the evolution of cell wall elongation in general. METHODS: Representatives of the different plant lineages were pressed onto an XET test paper and assayed. XET or XET-related activity was visualized as the incorporation of fluorescent signal. The Physcomitrella genome database was screened for the presence of XTHs. In addition, using the 3' RACE technique searches were made for the presence of possible XTH ESTs in the Charophyta. KEY RESULTS: XET activity was found in the three major divisions of bryophytes at sites corresponding to growing regions. In the Physcomitrella genome two putative XTH-encoding cDNA sequences were identified that contain all domains crucial for XET activity. Furthermore, XET activity was located at the sites of growth in Chara (Charophyta) and Ulva (Chlorophyta) and a putative XTH ancestral enzyme in Chara was identified. No XET activity was identified in the Rhodophyta or Phaeophyta. CONCLUSIONS: XET activity was shown to be present in all major groups of green plants. These data suggest that an XET-related growth mechanism originated before the evolutionary divergence of the Chlorobionta and open new insights in the evolution of the mechanisms of primary cell wall expansion.     

OsCD1 encodes a putative member of the cellulose synthase-like D sub-family and is essential for rice plant architecture and growth

The cell wall plays important roles in plant architecture and morphogenesis. The cellulose synthase-like super-families were reported to contain glycosyltransferases motif and are required for the biosynthesis of cell wall polysaccharides. Here, we describe a curled leaf and dwarf mutant, cd1, in rice, which exhibits multiple phenotypic traits such as the reduction of plant height and leaf width, curled leaf morphology and a decrease in the number of grains and in the panicle length. Map-based cloning indicates that a member of the cellulose synthase-like D (CSLD) group is a candidate for OsCD1. RNAi transgenic plants with the candidate CSLD gene display a similar phenotype to the cd1 mutant, suggesting that OsCD1 is a member of the CSLD sub-family. Furthermore, sequence analysis indicates that OsCD1 contains the common D,D,D,QXXRW motif, which is a feature of the cellulose synthase-like super-family. Analysis of OsCD1 promoter with GUS fusion expression shows that OsCD1 exhibits higher expression in young meristem tissues such as fresh roots, young panicle and stem apical meristem. Cell wall composition analysis reveals that cellulose content and the level of xylose are significantly reduced in mature culm owing to loss of OsCD1 function. Take together, the work presented here is useful for expanding the understanding of cell wall biosynthesis.     

The structure, function, and biosynthesis of plant cell wall pectic polysaccharides

Plant cell walls consist of carbohydrate, protein, and aromatic compounds and are essential to the proper growth and development of plants. The carbohydrate components make up ∼90% of the primary wall, and are critical to wall function. There is a diversity of polysaccharides that make up the wall and that are classified as one of three types: cellulose, hemicellulose, or pectin. The pectins, which are most abundant in the plant primary cell walls and the middle lamellae, are a class of molecules defined by the presence of galacturonic acid. The pectic polysaccharides include the galacturonans (homogalacturonan, substituted galacturonans, and RG-II) and rhamnogalacturonan-I. Galacturonans have a backbone that consists of α-1,4-linked galacturonic acid. The identification of glycosyltransferases involved in pectin synthesis is essential to the study of cell wall function in plant growth and development and for maximizing the value and use of plant polysaccharides in industry and human health. A detailed synopsis of the existing literature on pectin structure, function, and biosynthesis is presented.     

Epiphytic dinoflagellates associated with ciguatera in the northwestern coast of Cuba

The spatial and temporal abundance of epiphytic dinoflagellates associated with ciguatera was studied over two annual cycles (March 1999 to March 2000 and March 2001 to March 2002) in the northwestern coast of Cuba. From 14 species of macroalgae (Phaeophyta, Chlorophyta, and Rhodophyta), 1340 samples were obtained identifying seven species as potentially noxious; five of them are new reports for Cuba's phytobenthos: Prorocentrum belizeanum Faust, P. concavum Fukuyo, P. mexicanum Tafall, Coolia monotis Meunier, and Ostreopsis lenticularis Fukuyo. ANOVA/MANOVA analysis showed significant spatial differences: lower cell abundance near the shoreline adjacent to a river inlet and higher cell abundance in the deepest area. Prorocentrum lima (Ehrenberg) Dodge 1975 was found mainly on Phaeophyta followed by Chlorophyta and Rhodophyta. Gambierdiscus toxicus was found mainly on Phaeophyta followed by Rhodophyta and Chlorophyta. All the species reported in the study area were mainly on Padina spp. (Phaeophyta). Acanthophora spicifera (Rhodophyta) did not host dinoflagellate species. Environmental conditions in summer (higher temperature, more nutrients, greater water transparency, and low wind intensity) are suitable for macroalgae development, which serves as a substrate for potentially harmful dinoflagellates, and possibly the main vector for spreading ciguatera along the coast of Cuba.     

Cloning and characterization of cellulose synthase-like gene, PtrCSLD2 from developing xylem of aspen trees

Genetic improvement of cell wall polymer synthesis in forest trees is one of the major goals of forest biotechnology that could possibly impact their end product utilization. Identification of genes involved in cell wall polymer biogenesis is essential for achieving this goal. Among various candidate cell wall-related genes, cellulose synthase-like D (CSLD) genes are intriguing due to their hitherto unknown functions in cell wall polymer synthesis but strong structural similarity with cellulose synthases (CesAs) involved in cellulose deposition. Little is known about CSLD genes from trees. In the present article PtrCSLD2, a first CSLD gene from an economically important tree, aspen (Populus tremuloides) is reported. PtrCSLD2 cDNA was isolated from an aspen xylem cDNA library and encodes a protein that shares 90% similarity with Arabidopsis AtCSLD3 protein involved in root hair tip growth. It is possible that xylem fibers that also grow by intrusive tip growth may need expression of PtrCSLD2 for controlling the length of xylem fibers, a wood quality trait of great economical importance. PtrCSLD2 protein has a N-terminal cysteine-rich putative zinc-binding domain; eight transmembrane domains; alternating conserved and hypervariable domains; and a processive glycosyltransferases signature, D, D, D, QXXRW; all similar to aspen CesA proteins. However, PtrCSLD2 shares only 43-48% overall identity with the known aspen CesAs suggesting its distinct functional role in cell wall polymer synthesis perhaps other than cellulose biosynthesis. Based on Southern analysis, the aspen CSLD gene family consists of at least three genes and this gene copy estimate is supported by phylogenetic analysis of available CSLDs from plants. Moreover, gene expression studies using RT-PCR and in situ mRNA hybridization showed that PtrCSLD2 is expressed at a low level in all aspen tissues examined with a slightly higher expression level in secondary cell wall-enriched aspen xylem as compared to primary cell wall enriched tissues. Together, these observations suggest that PtrCSLD2 gene may be involved in the synthesis of matrix polysaccharides that are dominant in secondary cell walls of poplar xylem. Future molecular genetic analyses will clarify the functional significance of CSLD genes in the development of woody trees.