An official website of the United States government
Abstract Vascular plants direct large amounts of carbon to produce the aromatic amino acid phenylalanine to support the production of lignin and other phenylpropanoids. Uniquely, grasses, which include many major crops, can synthesize lignin and phenylpropanoids from both phenylalanine and tyrosine. However, how grasses regulate aromatic amino acid biosynthesis to feed this dual lignin pathway is unknown. Here we show, by stable-isotope labeling, that grasses produce tyrosine >10-times faster than Arabidopsis without compromising phenylalanine biosynthesis. Detailed in vitro enzyme characterization and combinatorialin plantaexpression uncovered that coordinated expression of specific enzyme isoforms at the entry and exit steps of the aromatic amino acid pathway enables grasses to maintain high production of both tyrosine and phenylalanine, the precursors of the dual lignin pathway. These findings highlight the complex regulation of plant aromatic amino acid biosynthesis and provide novel genetic tools to engineer the interface of primary and specialized metabolism in plants.
more »
« less
Traditional medicinal use is linked with apparency, not specialized metabolite profiles in the order Caryophyllales
Abstract PremiseBetter understanding of the relationship between plant specialized metabolism and traditional medicine has the potential to aid in bioprospecting and untangling of cross‐cultural use patterns. However, given the limited information available for metabolites in most plant species, understanding medicinal use–metabolite relationships can be difficult. The order Caryophyllales has a unique pattern of lineages of tyrosine‐ or phenylalanine‐dominated specialized metabolism, represented by mutually exclusive anthocyanin and betalain pigments, making Caryophyllales a compelling system to explore the relationship between medicine and metabolites by using pigment as a proxy for dominant metabolism. MethodsWe compiled a list of medicinal species in select tyrosine‐ or phenylalanine‐dominant families of Caryophyllales (Nepenthaceae, Polygonaceae, Simmondsiaceae, Microteaceae, Caryophyllaceae, Amaranthaceae, Limeaceae, Molluginaceae, Portulacaceae, Cactaceae, and Nyctaginaceae) by searching scientific literature until no new uses were recovered. We then tested for phylogenetic clustering of uses using a “hot nodes” approach. To test potential non‐metabolite drivers of medicinal use, like how often humans encounter a species (apparency), we repeated the analysis using only North American species across the entire order and performed phylogenetic generalized least squares regression (PGLS) with occurrence data from the Global Biodiversity Information Facility (GBIF). ResultsWe hypothesized families with tyrosine‐enriched metabolism would show clustering of different types of medicinal use compared to phenylalanine‐enriched metabolism. Instead, wide‐ranging, apparent clades in Polygonaceae and Amaranthaceae are overrepresented across nearly all types of medicinal use. ConclusionsOur results suggest that apparency is a better predictor of medicinal use than metabolism, although metabolism type may still be a contributing factor.
more »
« less
- Award ID(s):
- 1939226
- PAR ID:
- 10502611
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- American Journal of Botany
- Volume:
- 111
- Issue:
- 4
- ISSN:
- 0002-9122
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Plants produce an astonishingly diverse array of specialized metabolites. A crucial step in understanding the origin of such chemodiversity is describing how chemodiversity manifests across the spatial and ontogenetic scales relevant to plant–biotic interactions.Focusing on 21 sympatric species ofPsychotriaandPalicourea sensu lato(Rubiaceae), we describe patterns of specialized metabolite diversity across spatial and ontogenetic scales using a combination of field collections, untargeted metabolomics, and ecoinformatics. We compare α, β, and γ diversity of specialized metabolites in expanding leaves, unripe pulp, immature seed, ripe pulp, mature seed, and fine roots.Within species, fruit tissues from across ontogenetic stages had ≥α diversity than leaves, and ≤β diversity than leaves. Pooled across species, fruit tissues and ontogenetic stages had the highest γ diversity of all organs, and fruit tissues and ontogenetic stages combined had a higher incidence of organ‐specific mass spectral features than leaves. Roots had ≤α diversity than leaves and the lowest β and γ diversity of all organs. Phylogenetic correlations of chemical distance varied by plant organ and chemical class.Our results describe patterns of specialized metabolite diversity across organs and species and provide support for organ‐specific contributions to plant chemodiversity. This study contributes to the growing understanding within plant evolutionary ecology of the biological scales of specialized metabolite diversification. Future studies combining our data on specialized metabolite diversity with biotic interaction data and experiments can test existing hypotheses on the roles of ecological interactions in the evolution of chemodiversity.more » « less
-
Abstract Premise The specialized metabolites of plants are recognized as key chemical traits in mediating the ecology and evolution of sundry plant–biotic interactions, from pollination to seed predation. Intra‐ and interspecific patterns of specialized metabolite diversity have been studied extensively in leaves, but the diverse biotic interactions that contribute to specialized metabolite diversity encompass all plant organs. Focusing on two species of Psychotria shrubs, we investigated and compared patterns of specialized metabolite diversity in leaves and fruit with respect to each organ's diversity of biotic interactions. Methods To evaluate associations between biotic interaction diversity and specialized metabolite diversity, we combined UPLC‐MS metabolomic analysis of foliar and fruit specialized metabolites with existing surveys of leaf‐ and fruit‐centered biotic interactions. We compared patterns of specialized metabolite richness and variance among vegetative and reproductive tissues, among plants, and between species. Results In our study system, leaves interact with a far larger number of consumer species than do fruit, while fruit‐centric interactions are more ecologically diverse in that they involve antagonistic and mutualistic consumers. This aspect of fruit‐centric interactions was reflected in specialized metabolite richness—leaves contained more than fruit, while each organ contained over 200 organ‐specific specialized metabolites. Within each species, leaf‐ and fruit‐specialized metabolite composition varied independently of one another across individual plants. Contrasts in specialized metabolite composition were stronger between organs than between species. Conclusions As ecologically disparate plant organs with organ‐specific specialized metabolite traits, leaves and fruit can each contribute to the tremendous overall diversity of plant specialized metabolites.more » « less
-
null (Ed.)Plants produce diverse metabolites to cope with the challenges presented by complex and ever-changing environments. These challenges drive the diversification of specialized metabolites within and between plant species. However, we are just beginning to understand how frequently new alleles arise controlling specialized metabolite diversity and how the geographic distribution of these alleles may be structured by ecological and demographic pressures. Here we measure the variation in specialized metabolites across a population of 797 natural Arabidopsis thaliana accessions. We show a combination of geography, environmental parameters, demography, and different genetic processes all combine to influence the specific chemotypes and their distribution. This showed that causal loci in specialized metabolism contain frequent independently generated alleles with patterns suggesting potential within species convergence. This provides a new perspective about the complexity of the selective forces and mechanisms that shape the generation and distribution of allelic variation that may influence local adaptation.more » « less
-
Plants collectively synthesize a huge repertoire of metabolites. General metabolites, also referred to as primary metabolites, are conserved across the plant kingdom and are required for processes essential to growth and development. These include amino acids, sugars, lipids, and organic acids. In contrast, specialized metabolites, historically termed secondary metabolites, are structurally diverse, exhibit lineage-specific distribution and provide selective advantage to host species to facilitate reproduction and environmental adaptation. Due to their potent bioactivities, plant specialized metabolites attract considerable attention for use as flavorings, fragrances, pharmaceuticals, and bio-pesticides. The Solanaceae (Nightshade family) consists of approximately 2700 species and includes crops of significant economic, cultural, and scientific importance: these include potato, tomato, pepper, eggplant, tobacco, and petunia. The Solanaceae has emerged as a model family for studying the biochemical evolution of plant specialized metabolism and multiple examples exist of lineage-specific metabolites that influence the senses and physiology of commensal and harmful organisms, including humans. These include, alcohols, phenylpropanoids, and carotenoids that contribute to fruit aroma and color in tomato (fruity), glandular trichome-derived terpenoids and acylsugars that contribute to plant defense (stinky & sticky, respectively), capsaicinoids in chilli-peppers that influence seed dispersal (spicy), and steroidal glycoalkaloids (bitter) from Solanum, nicotine (addictive) from tobacco, as well as tropane alkaloids (deadly) from Deadly Nightshade that deter herbivory. Advances in genomics and metabolomics, coupled with the adoption of comparative phylogenetic approaches, resulted in deeper knowledge of the biosynthesis and evolution of these metabolites. This review highlights recent progress in this area and outlines opportunities for – and challenges of-developing a more comprehensive understanding of Solanaceae metabolism.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1002/ajb2.16308
