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

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'.

Plants started to colonize land around 500 million years ago. It meant dealing with new challenges like absence of buoyancy, water and nutrients shortage, increased light radiation, reproduction on land, and interaction with new microorganisms. This obviously required the acquisition of novel functions and metabolic capacities. Cytochrome P450 (CYP) monooxygenases form the largest superfamily of enzymes and are present to catalyse critical and rate-limiting steps in most plant-specific pathways. The different families of CYP enzymes are typically associated with specific functions. CYP family emergence and evolution in the green lineage thus offer the opportunity to obtain a glimpse into the timing of the evolution of the critical functions that were required (or became dispensable) for the plant transition to land. Based on the analysis of currently available genomic data, this review provides an evolutionary history of plant CYPs in the context of plant terrestrialization and describes the associated functions in the different lineages. Without surprise it highlights the relevance of the biosynthesis of antioxidants and UV screens, biopolymers, and critical signalling pathways. It also points to important unsolved questions that would deserve to be answered to improve our understanding of plant adaptation to challenging environments and the management of agricultural traits. This article is part of the theme issue 'The evolution of plant metabolism'.

The flavonoid pathway is characteristic of land plants and a central biosynthetic component enabling life in a terrestrial environment. Flavonoids provide tolerance to both abiotic and biotic stresses and facilitate beneficial relationships, such as signalling to symbiont microorganisms, or attracting pollinators and seed dispersal agents. The biosynthetic pathway shows great diversity across species, resulting principally from repeated biosynthetic gene duplication and neofunctionalization events during evolution. Such events may reflect a selection for new flavonoid structures with novel functions that enable occupancy of varied ecological niches. However, the biochemical and genetic diversity of the pathway also likely resulted from evolution along parallel trends across land plant lineages, producing variant compounds with similar biological functions. Analyses of the wide range of whole-plant genome sequences now available, particularly for archegoniate plants, have enabled proposals on which genes were ancestral to land plants and which arose within the land plant lineages. In this review, we discuss the emerging proposals for how the flavonoid pathway may have evolved and diversified. This article is part of the theme issue 'The evolution of plant metabolism'.

Plant glutathione transferases (GSTs) constitute a large and diverse family of enzymes that are involved in plant stress response, metabolism and defence, yet their physiological functions remain largely elusive. Consistent with the traditional view on GSTs across organisms as detoxification enzymes, in vitro most plant GSTs catalyse glutathionylation, conjugation of the tripeptide glutathione (GSH; γ-Glu-Cys-Gly) onto reactive molecules. However, when it comes to elucidating GST functions, it remains a key challenge that the endogenous plant glutathione conjugates (GS-conjugates) that would result from such glutathionylation reactions are rarely reported. Furthermore, GSTs often display high substrate promiscuity, and their proposed substrates are prone to spontaneous chemical reactions with GSH; hence, single-gene knockouts rarely provide clear chemotypes or phenotypes. In a few cases, GS-conjugates are demonstrated to be biosynthetic intermediates that are rapidly further metabolized towards a pathway end product, explaining their low abundance and rare detection. In this review, we summarize the current knowledge of plant GST functions and how and possibly why evolution has resulted in a broad and extensive expansion of the plant GST family. Finally, we demonstrate that endogenous GS-conjugates are more prevalent in plants than assumed and suggest they are overlooked as clues towards the identification of plant GST functions. This article is part of the theme issue 'The evolution of plant metabolism'.

Recent research on a special type of sexual reproduction and zygospore formation in Zygnematophyceae, the sister group of land plants, is summarized. Within this group, gamete fusion occurs by conjugation. Zygospore development in Mougeotia, Spirogyra and Zygnema is highlighted, which has recently been studied using Raman spectroscopy, allowing chemical imaging and detection of changes in starch and lipid accumulation. Three-dimensional reconstructions after serial block-face scanning electron microscopy (SBF-SEM) or focused ion beam SEM (FIB-SEM) made it possible to visualize and quantify cell wall and organelle changes during zygospore development. The zygospore walls undergo strong modifications starting from uniform thin cell walls to a multilayered structure. The mature cell wall is composed of a cellulosic endospore and exospore and a central mesospore built up by aromatic compounds. In Spirogyra, the exospore and endospore consist of thick layers of helicoidally arranged cellulose fibrils, which are otherwise only known from stone cells of land plants. While starch is degraded during maturation, providing building blocks for cell wall formation, lipid droplets accumulate and fill large parts of the ripe zygospores, similar to spores and seeds of land plants. Overall, data show similarities between streptophyte algae and embryophytes, suggesting that the genetic toolkit for many land plant traits already existed in their shared algal ancestor. This article is part of the theme issue 'The evolution of plant metabolism'.

Autophagy is a highly conserved 'self-digesting' mechanism used in eukaryotes to degrade and recycle cellular components by enclosing them in a double membrane compartment and delivering them to lytic organelles (lysosomes or vacuoles). Extensive studies in plants have revealed how autophagy is intricately linked to essential aspects of metabolism and growth, in both normal and stress conditions, including cellular and organelle homeostasis, nutrient recycling, development, responses to biotic and abiotic stresses, senescence and cell death. However, knowledge regarding autophagic processes in other photosynthetic organisms remains limited. In this review, we attempt to summarize the current understanding of autophagy in algae from a metabolic, molecular and evolutionary perspective. We focus on the composition and conservation of the autophagy molecular machinery in eukaryotes and discuss the role of autophagy in metabolic regulation, cellular homeostasis and stress adaptation in algae. This article is part of the theme issue 'The evolution of plant metabolism'.