Crossroads in the evolution of plant specialized metabolism

Rieseberg, Tim P; Dadras, Armin; Fürst-Jansen, Janine M R; Ashok, Amra Dhabalia; Darienko, Tatyana; Vries, Sophie de; Irisarri, Iker; Vries, Jan de

doi:10.1016/j.semcdb.2022.03.004

Cited by 48 publications

(46 citation statements)

References 328 publications

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“…The flavonoid biosynthetic pathway is a branch of the phenylpropanoid pathway, which produces flavonoids, lignins, lignans, stilbenes, and others (Davies et al., 2020; Vogt, 2010). Most core genes of the phenylpropanoid pathway are present in both streptophyte algae and land plants (de Vries et al., 2021; Rieseberg et al., 2022), suggesting that this pathway is deeply conserved in plant lineages and might have played critical roles in the stress responses of the earliest land plants (de Vries et al., 2020; Rieseberg et al., 2022). The key enzyme in flavonoid biosynthesis is chalcone synthase (CHS), which catalyzes the first step in the flavonoid pathway.…”

Section: Introductionmentioning

confidence: 99%

The type III polyketide synthase supergene family in plants: complex evolutionary history and functional divergence

et al. 2022

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Type III polyketide synthases (PKSs) are key enzymes involved in the biosynthesis of a variety of plant specialized metabolites, including flavonoids, stilbenes, and sporopollenin, to name a few. These enzymes likely played vital roles in plant adaptation during their transition from aquatic to terrestrial habitats and their colonization of specific ecological environments. Members of this supergene family have diverse functions, but how type III PKSs and their functions have evolved remains poorly understood. Here, we conducted comprehensive phylogenomics analysis of the type III PKS supergene family in 60 species representing the major plant lineages and elucidated the classification, origin, and evolutionary history of each class. Molecular evolutionary analysis of the typical chalcone synthase and stilbene synthase types revealed evidence for strong positive natural selection in both the Pinaceae and Fabaceae lineages. The positively selected sites of these proteins include residues at the catalytic tunnel entrance and homodimer interface, which might have driven the functional divergence between the two types. Our results also suggest that convergent evolution of enzymes involved in plant flavonoid biosynthesis is quite common. The results of this study provide new insights into the origin, evolution, and functional diversity of plant type III PKSs. In addition, they serve as a guide for the enzymatic engineering of plant polyketides.

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Section: Introductionmentioning

confidence: 99%

The type III polyketide synthase supergene family in plants: complex evolutionary history and functional divergence

et al. 2022

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“…Recent studies also discovered flavonoid-like pigments possessing UV-absorbing properties in Penium margaritaceum , which also occur in some species of Chlorophyta ( Goiris et al, 2014 ; Jiao et al, 2020 ). In addition to the detection of phenolic compounds and flavonoids, recent data suggest the presence of parts of the phenylpropanoid pathway in streptophyte algae ( Rieseberg et al, 2022 ; Serrano-Pérez et al, 2022 ). The phenylpropanoid pathway can be seen as central for numerous crucial land-plant structural components and stress responses, and has long been seen as a land-plant-specific adaptation (e.g., Dixon and Paiva, 1995 ; Thévenin et al, 2011 ; Lee et al, 2019 ; Rieseberg et al, 2022 ).…”

Section: Protection Strategies Against Light- and Ultraviolet Radiati...mentioning

confidence: 99%

Temperature- and light stress adaptations in Zygnematophyceae: The challenges of a semi-terrestrial lifestyle

2022

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Streptophyte green algae comprise the origin of land plants and therefore life on earth as we know it today. While terrestrialization opened new habitats, leaving the aquatic environment brought additional abiotic stresses. More-drastic temperature shifts and high light levels are major abiotic stresses in semi-terrestrial habitats, in addition to desiccation, which has been reviewed elsewhere. Zygnematophyceae, a species-rich class of streptophyte green algae, is considered a sister-group to embryophytes. They have developed a variety of avoidance and adaptation mechanisms to protect against temperature extremes and high radiation in the form of photosynthetically active and ultraviolet radiation (UV) radiation occurring on land. Recently, knowledge of transcriptomic and metabolomic changes as consequences of these stresses has become available. Land-plant stress-signaling pathways producing homologs of key enzymes have been described in Zygnematophyceae. An efficient adaptation strategy is their mat-like growth habit, which provides self-shading and protects lower layers from harmful radiation. Additionally, Zygnematophyceae possess phenolic compounds with UV-screening ability. Resting stages such as vegetative pre-akinetes tolerate freezing to a much higher extent than do young cells. Sexual reproduction occurs by conjugation without the formation of flagellated male gametes, which can be seen as an advantage in water-deficient habitats. The resulting zygospores possess a multilayer cell wall, contributing to their resistance to terrestrial conditions. Especially in the context of global change, understanding temperature and light tolerance is crucial.

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“…As such we can expect high sequence diversity. Then, specialized metabolism generates a plethora of chemically related compounds via parallel, diverging and converging pathways [29]. We envisage that promiscuous enzyme activity is often related to specialized metabolism and superfamily enzymes.…”

Section: Design Of the Performance Analysismentioning

confidence: 99%

“…We selected superfamilies involved in specialized metabolism since this provides a number of challenges. First, we argue that enzymes from specialized metabolism are under less functional constraint than enzymes from primary metabolism [29]. As such we can expect high sequence diversity.…”

Section: Introductionmentioning

confidence: 99%

Seqrutinator: Non-Functional Homologue Sequence Scrutiny for the Generation of large Datatsets for Protein Superfamily Analysis

Amalfitano

Stocchi

Atencio

et al. 2022

Preprint

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BackgroundIn recent years protein protein bioinformatics has resulted in much improved algorithms for multiple sequence alignment (MSA) and phylogeny. Few attention has been paid to sequence selection whereas particularly recently published complete proteomes often have many sequences that are partial or derive from pseudogenes. Not only do these sequences add noise to the MSA, phylogeny and other downstream computational analyses, they actually also instigate many errors in the processing of the MSAs and therewith all other downstream analyses, including the phylogeny.ObjectiveHere we aim to provide and test an objective, automated and flexible pipeline for the scrutiny of sequence sets from large, complex protein superfamilies, resulting in the classification of sequences into either functional or non-functional. The pipeline should identify few Swissprot sequences and result in an improved MSA.ResultsSeqrutinator is a pipeline that consists of five modules written in Python that identify and remove sequences that are likely Non-Functional Homologues. Here we tested the pipeline in its default order using default settings using three complex, related plant superfamilies (BAHD, CYP and UGT) that act in specialized metabolism, using the complete proteome of 16 plant species as input and using Swissprot as a control. Only 3.4% of Swissprot sequences were identified as NFH. Most NFH sequences are partial but, interestingly, their removal results in much shorter MSAs with many more reliable columns. Few but significant sequences that instigate gaps are found. The three superfamilies furthermore show similar scrutiny patterns.Conclusion and perspectiveSeqrutinator forms a consistent pipeline for sequence scrutiny that does result in sequence sets that generate high fidelity MSAs. Additional tests will be performed in order to further demonstrate Seqrutinators performance.

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Crossroads in the evolution of plant specialized metabolism

Cited by 48 publications

References 328 publications

The type III polyketide synthase supergene family in plants: complex evolutionary history and functional divergence

The type III polyketide synthase supergene family in plants: complex evolutionary history and functional divergence

Temperature- and light stress adaptations in Zygnematophyceae: The challenges of a semi-terrestrial lifestyle

Seqrutinator: Non-Functional Homologue Sequence Scrutiny for the Generation of large Datatsets for Protein Superfamily Analysis

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