The evolution of plant responses underlying specialized metabolism in host-pathogen interactions.

In the course of plant evolution from aquatic to terrestrial environments, land plants (embryophytes) acquired a diverse array of specialized metabolites, including phenylpropanoids, flavonoids and cuticle components, enabling adaptation to various environmental stresses. While embryophytes and their closest algal relatives share candidate enzymes responsible for producing some of these compounds, the complete genetic network for their biosynthesis emerged in embryophytes. In this review, we analysed genomic data from chlorophytes, charophytes and embryophytes to identify genes related to phenylpropanoid, flavonoid and cuticle biosynthesis. By integrating published research, transcriptomic data and metabolite studies, we provide a comprehensive overview on how these specialized metabolic pathways have contributed to plant defence responses to pathogens in non-vascular bryophytes and vascular plants throughout evolution. The evidence suggests that these biosynthetic pathways have provided land plants with a repertoire of conserved and lineage-specific compounds, which have shaped immunity against invading pathogens. The discovery of additional enzymes and metabolites involved in bryophyte responses to pathogen infection will provide evolutionary insights into these versatile pathways and their impact on environmental terrestrial challenges.This article is part of the theme issue 'The evolution of plant metabolism'.

Molecular Evolution of RAMOSA1 (RA1) in Land Plants.

RAMOSA1 (RA1) is a Cys2-His2-type (C2H2) zinc finger transcription factor that controls plant meristem fate and identity and has played an important role in maize domestication. Despite its importance, the origin of RA1 is unknown, and the evolution in plants is only partially understood. In this paper, we present a well-resolved phylogeny based on 73 amino acid sequences from 48 embryophyte species. The recovered tree topology indicates that, during grass evolution, RA1 arose from two consecutive SUPERMAN duplications, resulting in three distinct grass sequence lineages: RA1-like A, RA1-like B, and RA1; however, most of these copies have unknown functions. Our findings indicate that RA1 and RA1-like play roles in the nucleus despite lacking a traditional nuclear localization signal. Here, we report that copies diversified their coding region and, with it, their protein structure, suggesting different patterns of DNA binding and protein-protein interaction. In addition, each of the retained copies diversified regulatory elements along their promoter regions, indicating differences in their upstream regulation. Taken together, the evidence indicates that the RA1 and RA1-like gene families in grasses underwent subfunctionalization and neofunctionalization enabled by gene duplication.

Significant nonsymbiotic nitrogen fixation in Patagonian ombrotrophic bogs.

Nitrogen (N) nutrition in pristine peatlands relies on the natural input of inorganic N through atmospheric deposition or biological dinitrogen (N2 ) fixation. However, N2 fixation and its significance for N cycling, plant productivity, and peat buildup are mostly associated with the presence of Sphagnum mosses. Here, we report high nonsymbiotic N2 -fixation rates in two pristine Patagonian bogs with diversified vegetation and natural N deposition. Nonsymbiotic N2 fixation was measured in samples from 0 to 10, 10 to 20, and 40 to 50 cm depth using the (15) N2 assay as well as the acetylene reduction assay (ARA). The ARA considerably underestimated N2 fixation and can thus not be recommended for peatland studies. Based on the (15) N2 assay, high nonsymbiotic N2 -fixation rates of 0.3-1.4 µmol N2  g(-1)  day(-1) were found down to 50 cm under micro-oxic conditions (2 vol.%) in samples from plots covered by Sphagnum magellanicum or by vascular cushion plants, latter characterized by dense and deep aerenchyma roots. Peat N concentrations point to greater potential of nonsymbiotic N2 fixation under cushion plants, likely because of the availability of easily decomposable organic compounds and oxic conditions in the rhizosphere. In the Sphagnum plots, high N2 fixation below 10 cm depth rather reflects the potential during dry periods or low water level when oxygen penetrates the top peat layer and triggers peat mineralization. Natural abundance of the (15) N isotope of live Sphagnum (5.6 δ‰) from 0 to 10 cm points to solely N uptake from atmospheric deposition and nonsymbiotic N2 fixation. A mean (15) N signature of -0.7 δ‰ of peat from the cushion plant plots indicates additional N supply from N mineralization. Our findings suggest that nonsymbiotic N2 fixation overcomes N deficiency in different vegetation communities and has great significance for N cycling and peat accumulation in pristine peatlands.

Different patterns of chromosomal histone H3 phosphorylation in land plants.

The chromosomal phosphorylation of histone H3 during mitosis and meiosis seems to play a fundamental role in the control of cell division in all eukaryotes. In plants, the temporal and spatial distribution of H3S10 phosphorylated (H3S10ph) is currently known only for chromosomes of a few angiosperms. In the present study, we analyzed the pattern of H3S10ph in mitotic chromosomes of 14 plant species, including 2 bryophytes and 12 tracheophytes. In all species, the phosphorylation of H3S10 was cytologically detected first in prophase and disappeared in late anaphase. Two patterns of chromosomal phosphorylation were observed: (1) only the pericentromeric regions were hyperphosphorylated, whereas the remaining chromosome arms appeared weakly and diffusely immunolabeled, and (2) the whole chromosomes appear uniformly phosphorylated, increasing the labeling intensity at metaphase. The first pattern was observed in all tracheophytes with monocentric chromosomes, whereas the second one was restricted to the bryophytes and angiosperms with holokinetic chromosomes. In both cases, no particular kind of chromatin such as NORs or heterochromatic bands were differentially labeled. Based on this data and previous analyses in other eukaryotes, we suggest that hyperphosphorylation of the whole mitotic metaphase chromosome represents the ancestral condition for eukaryotic chromosomes, and the change to the pericentromeric pattern occurred in the transition from bryophytes to tracheophytes. The meaning and possible implications of these results are discussed in the light of recent and classical experiments.

The evolution of land plant hemoglobins.

This review discusses the evolution of land plant hemoglobins within the broader context of eukaryote hemoglobins and the three families of bacterial globins. Most eukaryote hemoglobins, including metazoan globins and the symbiotic and non-symbiotic plant hemoglobins, are homologous to the bacterial 3/3-fold flavohemoglobins. The remaining plant hemoglobins are homologous to the bacterial 2/2-fold group 2 hemoglobins. We have proposed that all eukaryote globins were acquired via horizontal gene transfer concomitant with the endosymbiotic events responsible for the origin of mitochondria and chloroplasts. Although the 3/3 hemoglobins originated in the ancestor of green algae and plants prior to the emergence of embryophytes at about 450 mya, the 2/2 hemoglobins appear to have originated via horizontal gene transfer from a bacterium ancestral to present day Chloroflexi. Unlike the 2/2 hemoglobins, the evolution of the 3/3 hemoglobins was accompanied by duplication, diversification, and functional adaptations. Duplication of the ancestral plant nshb gene into the nshb-1 and nshb-2 lineages occurred prior to the monocot-dicot divergence at ca. 140 mya. It was followed by the emergence of symbiotic hemoglobins from a non-symbiotic hemoglobin precursor and further specialization, leading to leghemoglobins in N2-fixing legume nodules concomitant with the origin of nodulation at ca. 60 mya. The transition of non-symbiotic to symbiotic hemoglobins (including to leghemoglobins) was accompanied by the alteration of heme-Fe coordination from hexa- to penta-coordination. Additional genomic information about Charophyte algae, the sister group to land plants, is required for the further clarification of plant globin phylogeny.