Philosophical Transactions of the Royal Society B: Biological Sciences最新文献

Immense chemical diversity is one of the hallmark features of plants. This chemo-diversity is mainly underpinned by a highly complex and biodiverse biochemical machinery. Plant metabolic enzymes originated and were inherited from their eukaryotic and prokaryotic ancestors and further diversified by the unprecedentedly high rates of gene duplication and functionalization experienced in land plants. Unlike prokaryotic microbes, which display frequent horizontal gene transfer events and multiple inputs of energy and organic carbon, land plants predominantly rely on organic carbon generated from CO₂ and have experienced relatively few gene transfers during their recent evolutionary history. As such, plant metabolic networks have evolved in a stepwise manner using existing networks as a starting point and under various evolutionary constraints. That said, until recently, the evolution of only a handful of metabolic traits had been extensively investigated and as such, the evolution of metabolism has received a fraction of the attention of, the evolution of development, for example. Advances in metabolomics and next-generation sequencing have, however, recently led to a deeper understanding of how a wide range of plant primary and specialized (secondary) metabolic pathways have evolved both as a consequence of natural selection and of domestication and crop improvement processes. This article is part of the theme issue 'The evolution of plant metabolism'.

Vitamin B₁₂, also known as cobalamin, is an essential organic cofactor for methionine synthase (METH), and is only synthesized by a subset of bacteria. Plants and fungi have an alternative methionine synthase (METE) that does not need B₁₂ and are typically considered not to utilize it. Some algae facultatively utilize B₁₂ because they encode both METE and METH, while other algae are dependent on B₁₂ as they encode METH only. We performed phylogenomic analyses of METE, METH and 11 further proteins involved in B₁₂ metabolism across more than 1600 plant and algal genomes and transcriptomes (e.g. from OneKp), demonstrating the presence of B₁₂-associated metabolism deep into the streptophytes. METH and five further accessory proteins (MTRR, CblB, CblC, CblD and CblJ) were detected in the hornworts (Anthocerotophyta), and two (CblB and CblJ) were identified in liverworts (Marchantiophyta) in the bryophytes, suggesting a retention of B₁₂-metabolism in the last common land plant ancestor. Our data further show more limited distributions for other B₁₂-related proteins (MCM and RNR-II) and B₁₂ dependency in several algal orders. Finally, considering the collection sites of algae that have lost B₁₂ metabolism, we propose freshwater-to-land transitions and symbiotic associations to have been constraining factors for B₁₂ availability in early plant evolution. This article is part of the theme issue 'The evolution of plant metabolism'.

Plant chemical diversity is largely owing to a number of enzymes which catalyse reactions involved in the assembly, and in the subsequent chemical modifications, of the core structures of major classes of plant specialized metabolites. One such reaction is acylation. With this in mind, to study the deep evolutionary history of BAHD and the serine-carboxypeptidase-like (SCPL) acyltransferase genes, we assembled phylogenomic synteny networks based on a large-scale inference analysis of orthologues across whole-genome sequences of 126 species spanning Stramenopiles and Archaeplastida, including Arabidopsis thaliana, tomato (Solanum lycopersicum) and maize (Zea mays). As such, this study combined the study of genomic location with changes in gene sequences. Our analyses revealed that serine-carboxypeptidase (SCP)/serine-carboxypeptidase-like (SCPL) genes had a deeper evolutionary origin than BAHD genes, which expanded massively on the transition to land and with the development of the vascular system. The two gene families additionally display quite distinct patterns of copy number variation across phylogenies as well as differences in cross-phylogenetic syntenic network components. In unlocking the above observations, our analyses demonstrate the possibilities afforded by modern phylogenomic (syntenic) networks, but also highlight their current limitations, as demonstrated by the inability of phylogenetic methods to separate authentic SCPL acyltransferases from standard SCP peptide hydrolases.This article is part of the theme issue 'The evolution of plant metabolism'.

A diverse array of plant aromatic compounds contributes to the tremendous chemical diversity in the plant kingdom that cannot be seen in microbes or animals. Such chemodiversity of aromatic natural products has emerged, occasionally in a lineage-specific manner, to adopt to challenging environmental niches, as various aromatic specialized metabolites play indispensable roles in plant development and stress responses (e.g. lignin, phytohormones, pigments and defence compounds). These aromatic natural products are synthesized from aromatic amino acids (AAAs), l-tyrosine, l-phenylalanine and l-tryptophan. While amino acid metabolism is generally assumed to be conserved between animals, microbes and plants, recent phylogenomic, biochemical and metabolomic studies have revealed the diversity of the AAA metabolism that supports efficient carbon allocation to downstream biosynthetic pathways of AAA-derived metabolites in plants. This review showcases the intra- and inter-kingdom diversification and origin of committed enzymes involved in plant AAA biosynthesis and catabolism and their potential application as genetic tools for plant metabolic engineering. I also discuss evolutionary trends in the diversification of plant AAA metabolism that expands the chemical diversity of AAA-derived aromatic natural products in plants. This article is part of the theme issue 'The evolution of plant metabolism'.

Carotenoids are essential components of the photosynthetic apparatus and precursors of plant hormones, such as strigolactones (SLs). SLs are involved in various aspects of plant development and stress-response processes, including the establishment of root and shoot architecture. SL biosynthesis begins with the reversible isomerization of all-trans-carotene into 9-cis-β-carotene, catalysed by DWARF27 β-carotene isomerase (D27). Sequence comparisons have revealed the presence of D27-related proteins in photosynthetic eukaryotes and cyanobacteria lacking SLs. To gain insight into the evolution of SL biosynthesis, we characterized the activity of a cyanobacterial D27 protein (CaD27) from Cyanobacterim aponinum, using carotenoid-accumulating Escherichia coli cells and in vitro enzymatic assays. Our results demonstrate that CaD27 is an all-trans/cis and cis/cis-β-carotene isomerase, with a cis/cis conversion preference. CaD27 catalysed 13-cis/15-cis-, all-trans/9-cis-β-carotene, and neurosporene isomerization. Compared with plant enzymes, it exhibited a lower 9-cis-/all-trans-β-carotene conversion ratio. A comprehensive genome survey revealed the presence of D27 as a single-copy gene in the genomes of 20 out of 200 cyanobacteria species analysed. Phylogenetic and enzymatic analysis of CaD27 indicated that cyanobacterial D27 genes form a single orthologous group, which is considered an ancestral type of those found in photosynthetic eukaryotes. This article is part of the theme issue 'The evolution of plant meta‌bolism'.

Studies of enzymes in modern-day plants have documented the diversity of metabolic activities retained by species today but only provide limited insight into how those properties evolved. Ancestral sequence reconstruction (ASR) is an approach that provides statistical estimates of ancient plant enzyme sequences which can then be resurrected to test hypotheses about the evolution of catalytic activities and pathway assembly. Here, I review the insights that have been obtained using ASR to study plant metabolism and highlight important methodological aspects. Overall, studies of resurrected plant enzymes show that (i) exaptation is widespread such that even low or undetectable levels of ancestral activity with a substrate can later become the apparent primary activity of descendant enzymes, (ii) intramolecular epistasis may or may not limit evolutionary paths towards catalytic or substrate preference switches, and (iii) ancient pathway flux often differs from modern-day metabolic networks. These and other insights gained from ASR would not have been possible using only modern-day sequences. Future ASR studies characterizing entire ancestral metabolic networks as well as those that link ancient structures with enzymatic properties should continue to provide novel insights into how the chemical diversity of plants evolved. This article is part of the theme issue 'The evolution of plant metabolism'.

Phenolic compounds of land plants are varied: they are chemodiverse, are sourced from different biosynthetic routes and fulfil a broad spectrum of functions that range from signalling phytohormones, to protective shields against stressors, to structural compounds. Their action defines the biology of land plants as we know it. Often, their roles are tied to environmental responses that, however, impacted already the algal progenitors of land plants, streptophyte algae. Indeed, many streptophyte algae successfully dwell in terrestrial habitats and have homologues for enzymatic routes for the production of important phenolic compounds, such as the phenylpropanoid pathway. Here, we synthesize what is known about the production of specialized phenolic compounds across hundreds of millions of years of streptophyte evolution. We propose an evolutionary scenario in which selective pressures borne out of environmental cues shaped the chemodiversity of phenolics in streptophytes. This article is part of the theme issue 'The evolution of plant metabolism'.

Plants are chemical engineers par excellence. Collectively they make a vast array of structurally diverse specialized metabolites. The raw materials for building new pathways (genes encoding biosynthetic enzymes) are commonly recruited directly or indirectly from primary metabolism. Little is known about how new metabolic pathways and networks evolve in plants, or what key nodes contribute to branches that lead to the biosynthesis of diverse chemicals. Here we review the molecular mechanisms underlying the generation of biosynthetic branchpoints. We also consider examples in which new metabolites are formed through the joining of precursor molecules arising from different biosynthetic routes, a scenario that greatly increases both the diversity and complexity of specialized metabolism. Given the emerging importance of metabolic gene clustering in helping to identify new enzymes and pathways, we further cover the significance of biosynthetic gene clusters in relation to metabolic networks and dedicated biosynthetic pathways. In conclusion, an improved understanding of the branchpoints between metabolic pathways will be key in order to be able to predict and illustrate the complex structure of metabolic networks and to better understand the plasticity of plant metabolism. This article is part of the theme issue 'The evolution of plant metabolism'.

Sexual reproduction in Charophyceae abounds in complex traits. Their gametangia develop as intricate structures, with oogonia spirally surrounded by envelope cells and richly pigmented antheridia. The red-probably protectant-pigmentation of antheridia is conserved across Charophyceae. Chara tomentosa is, however, unique in exhibiting this pigmentation and also in vegetative tissue. Here, we investigated the two sympatric species, C. tomentosa and Chara baltica, and compared their molecular chassis for pigmentation. Using reversed phase C₃₀ high performance liquid chromatography (RP-C₃₀-HPLC), we uncover that the major pigments are β-carotene, δ-carotene and γ-carotene; using headspace solid-phase microextraction coupled to gas chromatography equipped with a mass spectrometer (HS-SPME-GC-MS), we pinpoint that the unusually large carotenoid pool in C. tomentosa gives rise to diverse volatile apocarotenoids, including abundant 6-methyl-5-hepten-2-one. Based on transcriptome analyses, we uncover signatures of the unique biology of Charophycaee and genes for pigment production, including monocyclized carotenoids. The rich carotenoid pool probably serves as a substrate for diverse carotenoid-derived metabolites, signified not only by (i) the volatile apocarotenoids we detected but (ii) the high expression of a gene coding for a cytochrome P450 enzyme related to land plant proteins involved in the biosynthesis of carotenoid-derived hormones. Overall, our data shed light on a key protection strategy of sexual reproduction in the widespread group of macroalgae. The genetic underpinnings of this are shared across hundreds of millions of years of plant and algal evolution. This article is part of the theme issue 'The evolution of plant metabolism'.

Purine alkaloids are naturally occurring nitrogenous methylated derivatives of purine nucleotide degradation products, having essential roles in medicine, food and various other aspects of our daily lives. They are generated through convergent evolution in different plant species. The pivotal reaction steps within the purine alkaloid metabolic pathways have been largely elucidated, and the convergent evolution of purine alkaloids has been substantiated through bioinformatic, biochemical and other research perspectives within S-adenosyl-ʟ-methionine-dependent N-methyltransferases. Currently, the biological and ecological roles of purine alkaloids, further refinement of the purine alkaloid metabolic pathways and the investigation of purine alkaloid adaptive evolutionary mechanisms continue to attract widespread research interest. The exploration of the purine alkaloid metabolic pathways also enhances our comprehension of the biochemical mechanism, providing insights into inter-species interactions and adaptive evolution and offering potential value in drug development and agricultural applications. Here, we review the progress of research in the distribution, metabolic pathway elucidation and regulation, evolutionary mechanism and ecological roles of purine alkaloids in plants. The opportunities and challenges involved in elucidating the biochemical basis and evolutionary mechanisms of the purine alkaloid metabolic pathways, as well as other research aspects, are also discussed. This article is part of the theme issue 'The evolution of plant meta-bolism'.