The invention of WUS-like stem cell-promoting functions in plants predates leptosporangiate ferns

The growth of land plants depends on stem cell-containing meristems which show major differences in their architecture from basal to higher plant species. In Arabidopsis, the stem cell niches in the shoot and root meristems are promoted by WUSCHEL (WUS) and WOX5, respectively. Both genes are members of a non-ancestral clade of the WUS-related homeobox (WOX) gene family, which is absent in extant bryophytes and lycophytes. Our analyses of five fern species suggest that a single WUS orthologue was present in the last common ancestor (LCA) of leptosporangiate ferns and seed plants. In the extant fern Ceratopteris richardii, the WUS pro-orthologue marks the pluripotent cell fate of immediate descendants of the root apical initial, so-called merophytes, which undergo a series of stereotypic cell divisions and give rise to all cell types of the root except the root cap. The invention of a WUS-like function within the WOX gene family in an ancestor of leptosporangiate ferns and seed plants and its amplification and sub-functionalisation to different stem cell niches might relate to the success of seed plants, especially angiosperms.     

Decoding ABA and osmostress signalling in plants from an evolutionary point of view

The plant hormone abscisic acid (ABA) is fundamental for land plant adaptation to water-limited conditions. Osmostress, such as drought, induces ABA accumulation in angiosperms, triggering physiological responses such as stomata closure. The core components of angiosperm ABA signalling are soluble ABA receptors, group A protein phosphatase type 2C and SNF1-related protein kinase2 (SnRK2). ABA also has various functions in non-angiosperms, however, suggesting that its role in adaptation to land may not have been angiosperm-specific. Indeed, among land plants, the core ABA signalling components are evolutionarily conserved, implying their presence in a common ancestor. Results of ongoing functional genomics studies of ABA signalling components in bryophytes and algae have expanded our understanding of the evolutionary role of ABA signalling, with genome sequencing uncovering the ABA core module even in algae. In this review, we describe recent discoveries involving the ABA core module in non-angiosperms, tracing the footprints of how ABA evolved as a phytohormone. We also cover the latest findings on Raf-like kinases as upstream regulators of the core ABA module component SnRK2. Finally, we discuss the origin of ABA signalling from an evolutionary perspective.     

ABA in bryophytes: how a universal growth regulator in life became a plant hormone?

Abscisic acid (ABA) is not a plant-specific compound but one found in organisms across kingdoms from bacteria to animals, suggesting that it is a ubiquitous and versatile substance that can modulate physiological functions of various organisms. Recent studies have shown that plants developed an elegant system for ABA sensing and early signal transduction mechanisms to modulate responses to environmental stresses for survival in terrestrial conditions. ABA-induced increase in stress tolerance has been reported not only in vascular plants but also in non-vascular bryophytes. Since bryophytes are the key group of organisms in the context of plant evolution, clarification of their ABA-dependent processes is important for understanding evolutionary adaptation of land plants. Molecular approaches using Physcomitrella patens have revealed that ABA plays a role in dehydration stress tolerance in mosses, which comprise a major group of bryophytes. Furthermore, we recently reported that signaling machinery for ABA responses is also conserved in liverworts, representing the most basal members of extant land plant lineage. Conservation of the mechanism for ABA sensing and responses in angiosperms and basal land plants suggests that acquisition of this mechanism for stress tolerance in vegetative tissues was one of the critical evolutionary events for adaptation to the land. This review describes the role of ABA in basal land plants as well as non-land plant organisms and further elaborates on recent progress in molecular studies of model bryophytes by comparative and functional genomic approaches.     

Identification,expression, and taxonomic distribution of alternative oxidases in non-angiosperm plants

Alternative oxidase (AOX) is a terminal ubiquinol oxidase present in the respiratory chain of all angiosperms investigated to date, but AOX distribution in other members of the Viridiplantae is less clear. We assessed the taxonomic distribution of AOX using bioinformatics. Multiple sequence alignments compared AOX proteins and examined amino acid residues involved in AOX catalytic function and post-translational regulation. Novel AOX sequences were found in both Chlorophytes and Streptophytes and we conclude that AOX is widespread in the Viridiplantae. AOX multigene families are common in non-angiosperm plants and the appearance of AOX1 and AOX2 subtypes pre-dates the divergence of the Coniferophyta and Magnoliophyta. Residues involved in AOX catalytic function are highly conserved between Chlorophytes and Streptophytes, while AOX post-translational regulation likely differs in these two lineages. We demonstrate experimentally that an AOX gene is present in the moss Physcomitrella patens and that the gene is transcribed. Our findings suggest that AOX will likely exert an influence on plant respiration and carbon metabolism in non-angiosperms such as green algae, bryophytes, liverworts, lycopods, ferns, gnetophytes, and gymnosperms and that further research in these systems is required.     

Portrait of the expansin superfamily in Physcomitrella patens: comparisons with angiosperm expansins

BACKGROUND AND AIMS: Expansins are plant cell wall loosening proteins important in a variety of physiological processes. They comprise a large superfamily of genes consisting of four families (EXPA, EXPB, EXLA and EXLB) whose evolutionary relationships have been well characterized in angiosperms, but not in basal land plants. This work attempts to connect the expansin superfamily in bryophytes with the evolutionary history of this superfamily in angiosperms. METHODS: The expansin superfamily in Physcomitrella patens has been assembled from the Physcomitrella sequencing project data generated by the Joint Genome Institute and compared with angiosperm expansin superfamilies. Phylogenetic, motif, intron and distance analyses have been used for this purpose. KEY RESULTS: A gene superfamily is revealed that contains similar numbers of genes as found in arabidopsis, but lacking EXLA or EXLB genes. This similarity in gene numbers exists even though expansin evolution in Physcomitrella diverged from the angiosperm line approx. 400 million years ago. Phylogenetic analyses suggest that there were a minimum of two EXPA genes and one EXPB gene in the last common ancestor of angiosperms and Physcomitrella. Motif analysis seems to suggest that EXPA protein function is similar in bryophytes and angiosperms, but that EXPB function may be altered. CONCLUSIONS: The EXPA genes of Physcomitrella are likely to have maintained the same biochemical function as angiosperm expansins despite their independent evolutionary history. Changes seen at normally conserved residues in the Physcomitrella EXPB family suggest a possible change in function as one mode of evolution in this family.     

Biological implications of the occurrence of 32 members of the XTH (xyloglucan endotransglucosylase/hydrolase) family of proteins in the bryophyte Physcomitrella patens

This comprehensive overview of the xyloglucan endotransglucosylase/hydrolase (XTH) family of genes and proteins in bryophytes, based on research using genomic resources that are newly available for the moss Physcomitrella patens, provides new insights into plant evolution. In angiosperms, the XTH genes are found in large multi‐gene families, probably reflecting the diverse roles of individual XTHs in various cell types. As there are fewer cell types in P. patens than in angiosperms such as Arabidopsis and rice, it is tempting to deduce that there are fewer XTH family genes in bryophytes. However, the present study unexpectedly identified as many as 32 genes that potentially encode XTH family proteins in the genome of P. patens, constituting a fairly large multi‐gene family that is comparable in size with those of Arabidopsis and rice. In situ localization of xyloglucan endotransglucosylase activity in this moss indicates that some P. patens XTH proteins exhibit biochemical functions similar to those found in angiosperms, and that their expression profiles are tissue‐dependent. However, comparison of structural features of families of XTH genes between P. patens and angiosperms demonstrated the existence of several bryophyte‐specific XTH genes with distinct structural and functional features that are not found in angiosperms. These bryophyte‐specific XTH genes might have evolved to meet morphological and functional needs specific to the bryophyte. These findings raise interesting questions about the biological implications of the XTH family of proteins in non‐seed plants.     

Fundamental mechanisms of the stem cell regulation in land plants: lesson from shoot apical cells in bryophytes

Plant Molecular Biology - This review compares the molecular mechanisms of stem cell control in the shoot apical meristems of mosses and angiosperms and reveals the conserved features and evolution...     

The branching pattern of major groups of land plants inferred from parsimony analysis of ribosomal RNA sequences

The parsimony and bootstrap branching pattern of major groups of land plants derived from relevant 5S rRNA sequence trees have been discussed in the light of paleobotanical and morphological evidences. Although 5S rRNA sequence information is not useful for dileneating angiosperm relationships, it does capture the earlier phase of land plant evolution. The consensus branching pattern indicates an ancient split of bryophytes and vascular plants from the charophycean algal stem. Among the bryophytes,Marchantia andLophocolea appear to be phylogenetically close and together withPlagiomnium form a monophyletic group.Lycopodium andPsilotum arose early in vascular land plant evolution, independent of fem-sphenopsid branch. Gymnosperms are polyphyletic; conifers, Gnetales and cycads emerge in that order with ginkgo joiningCycas. Among the conifers,Metasequoia,Juniperus andTaxus emerge as a branch independent ofPinus which joins Gnetales. The phylogeny derived from the available ss-RNA sequences shows that angiosperms are monophyletic with monocots and dicots diverging from a common stem. The nucleotide replacements during angiosperm descent from the gymnosperm ancestor which presumably arose around 370 my ago indicates that monocots and dicots diverged around 180 my ago, which is compatible with the reported divergence estimate of around 200 my ago deduced from chloroplast DNA sequences. Since deceased.     

Evolution of shoot apical meristem structures in vascular plants with respect to plasmodesmatal network

Vascular plants have evolved shoot apical meristems (SAMs), whose structures differ among plant groups. To clarify the evolutionary course of the different structural types of SAMs, we compared plasmodesmatal networks in the SAMs for 17 families and 24 species of angiosperms, gymnosperms, and pteridophytes, using transmission electron microscopy (TEM). The plasmodesmata (PD) in almost all cell walls in median longitudinal sections of SAMs were counted, and the PD density per unit area was calculated for each cell wall. Angiosperm and gymnosperm SAMs have low densities, with no difference between stratified (tunica-corpus) and unstratified structures. SAMs of ferns, including Psilotum and Equisetum, have average densities that are more than three times higher than those of seed plants. Interestingly, microphyllous lycopods have both the fern and seed-plant types of PD networks; Selaginellaceae SAMs with single apical cells have high PD densities, while SAMs of Lycopodiaceae and Isoetaceae with plural initial cells have low PD densities, equivalent to those of seed plants. In summary, PD networks are strongly correlated to SAM organizations-SAMs with single and plural initial cells have the fern and seed-plant types of PD, respectively. The two SAM organizations may have evolved separately in lycophytes and euphyllophytes and may be associated with gain or loss of the ability to form secondary PD.     

Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants

Borate ester cross-linking of the cell wall pectic polysaccharide rhamnogalacturonan II (RG-II) is required for the growth and development of angiosperms and gymnosperms. Here, we report that the amounts of borate cross-linked RG-II present in the sporophyte primary walls of members of the most primitive extant vascular plant groups (Lycopsida, Filicopsida, Equisetopsida, and Psilopsida) are comparable with the amounts of RG-II in the primary walls of angiosperms. By contrast, the gametophyte generation of members of the avascular bryophytes (Bryopsida, Hepaticopsida, and Anthocerotopsida) have primary walls that contain small amounts (approximately 1% of the amounts of RG-II present in angiosperm walls) of an RG-II-like polysaccharide. The glycosyl sequence of RG-II is conserved in vascular plants, but these RG-IIs are not identical because the non-reducing L-rhamnosyl residue present on the aceric acid-containing side chain of RG-II of all previously studied plants is replaced by a 3-O-methyl rhamnosyl residue in the RG-IIs isolated from Lycopodium tristachyum, Ceratopteris thalictroides, Platycerium bifurcatum, and Psilotum nudum. Our data indicate that the amount of RG-II incorporated into the walls of plants increased during the evolution of vascular plants from their bryophyte-like ancestors. Thus, the acquisition of a boron-dependent growth habit may be correlated with the ability of vascular plants to maintain upright growth and to form lignified secondary walls. The conserved structures of pteridophyte, lycophyte, and angiosperm RG-IIs suggests that the genes and proteins responsible for the biosynthesis of this polysaccharide appeared early in land plant evolution and that RG-II has a fundamental role in wall structure.     

The sequenced genomes of nonflowering land plants reveal the innovative evolutionary history of peptide signaling

An understanding of land plant evolution is a prerequisite for in-depth knowledge of plant biology. Here we extract and explore information hidden in the increasing number of sequenced plant genomes, from bryophytes to angiosperms, to elucidate a specific biological question—how peptide signaling evolved. To conquer land and cope with changing environmental conditions, plants have gone through transformations that must have required innovations in cell-to-cell communication. We discuss peptides mediating endogenous and exogenous changes by interaction with receptors activating intracellular molecular signaling. Signaling peptides were discovered in angiosperms and operate in tissues and organs such as flowers, seeds, vasculature, and 3D meristems that are not universally conserved across land plants. Nevertheless, orthologs of angiosperm peptides and receptors have been identified in nonangiosperms. These discoveries provoke questions regarding coevolution of ligands and their receptors, and whether de novo interactions in peptide signaling pathways may have contributed to generate novel traits in land plants. The answers to such questions will have profound implications for the understanding of the evolution of cell-to-cell communication and the wealth of diversified terrestrial plants. Under this perspective, we have generated, analyzed, and reviewed phylogenetic, genomic, structural, and functional data to elucidate the evolution of peptide signaling.

The identification of orthologs of Arabidopsis signaling peptides and their receptors in nonflowering plants suggest their importance in cell-to-cell communication in all land plants.     

Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS.

Floral meristems and shoot apical meristems (SAMs) are homologous, self-maintaining stem cell systems. Unlike SAMs, floral meristems are determinate, and stem cell maintenance is abolished once all floral organs are initiated. To investigate the underlying regulatory mechanisms, we analyzed the interactions between WUSCHEL (WUS), which specifies stem cell identity, and AGAMOUS (AG), which is required for floral determinacy. Our results show that repression of WUS by AG is essential for terminating the floral meristem and that WUS can induce AG expression in developing flowers. Together, this suggests that floral determinacy depends on a negative autoregulatory mechanism involving WUS and AG, which terminates stem cell maintenance.     

Evolution of DNA amounts across land plants (embryophyta)

BACKGROUND AND AIMS: DNA C-values in land plants (comprising bryophytes, lycophytes, monilophytes, gymnosperms and angiosperms) vary approximately 1000-fold from approx. 0.11 to 127.4 pg. To understand the evolutionary significance of this huge variation it is essential to evaluate the phylogenetic component. Recent increases in C-value data (e.g. Plant DNA C-values database; release 2.0, January 2003; http://www.rbgkew.org.uk/cval/homepage.html) together with improved consensus of relationships between and within land plant groups makes such an analysis timely. METHODS: Insights into the distribution of C-values in each group of land plants were gained by superimposing available C-value data (4119 angiosperms, 181 gymnosperms, 63 monilophytes, 4 lycophytes and 171 bryophytes) onto phylogenetic trees. To enable ancestral C-values to be reconstructed for clades within land plants, character-state mapping with parsimony and MacClade was also applied. KEY RESULTS AND CONCLUSIONS: Different land plant groups are characterized by different C-value profiles, distribution of C-values and ancestral C-values. For example, the large ( approximately 1000-fold) range yet strongly skewed distribution of C-values in angiosperms contrasts with the very narrow 12-fold range in bryophytes. Further, character-state mapping showed that the ancestral genome sizes of both angiosperms and bryophytes were reconstructed as very small (i.e. < or =1.4 pg) whereas gymnosperms and most branches of monilophytes were reconstructed with intermediate C-values (i.e. >3.5, <14.0 pg). More in-depth analyses provided evidence for several independent increases and decreases in C-values; for example, decreases in Gnetaceae (Gymnosperms) and heterosperous water ferns (monilophytes); increases in Santalales and some monocots (both angiosperms), Pinaceae, Sciadopityaceae and Cephalotaxaceae (Gymnosperms) and possibly in the Psilotaceae + Ophioglossaceae clade (monilophytes). Thus, in agreement with several focused studies within angiosperm families and genera showing that C-values may both increase and decrease, it is apparent that this dynamic pattern of genome size evolution is repeated on a broad scale across land plants.     

Phylogenomic analysis of gene co‐expression networks reveals the evolution of functional modules

Molecular evolutionary studies correlate genomic and phylogenetic information with the emergence of new traits of organisms. These traits are, however, the consequence of dynamic gene networks composed of functional modules, which might not be captured by genomic analyses. Here, we established a method that combines large‐scale genomic and phylogenetic data with gene co‐expression networks to extensively study the evolutionary make‐up of modules in the moss Physcomitrella patens, and in the angiosperms Arabidopsis thaliana and Oryza sativa (rice). We first show that younger genes are less annotated than older genes. By mapping genomic data onto the co‐expression networks, we found that genes from the same evolutionary period tend to be connected, whereas old and young genes tend to be disconnected. Consequently, the analysis revealed modules that emerged at a specific time in plant evolution. To uncover the evolutionary relationships of the modules that are conserved across the plant kingdom, we added phylogenetic information that revealed duplication and speciation events on the module level. This combined analysis revealed an independent duplication of cell wall modules in bryophytes and angiosperms, suggesting a parallel evolution of cell wall pathways in land plants. We provide an online tool allowing plant researchers to perform these analyses at http://www.gene2function.de .