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Biosynthesis and Function of Plant Specialized Metabolites

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A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Phytochemistry".

Deadline for manuscript submissions: closed (31 December 2023) | Viewed by 25105

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Dr. Rebecca Dauwe

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Guest Editor

Biologie des plantes et innovation (BIOPI) EA3900, UFR des Sciences, Université de Picardie Jules Verne, 80000 Amiens, France
Interests: plant specialized metabolism; LC-MS; metabolomics; structural characterization by MSn

Special Issue Information

Dear Colleagues,

Plants synthesize an extremely large array of small molecules. The large majority of plant compounds are not essential for life-sustaining processes, such as energy acquisition or photosynthesis. They were for a long time referred to as “secondary” metabolites. The overwhelming structural diversity in secondary metabolites found throughout the plant kingdom results from their strong taxonomic restriction, and from the specificity within species to certain cell types, developmental stages or environmental stimuli. Therefore these compounds are now referred to as specialized metabolites. They are also no longer considered “secondary”, as their role in plant physiology and in the interaction with the biotic and abiotic environment is difficult to overestimate. The diversity among specialized metabolites evolved through adaptations to ever-changing challenges of the environment and often led to large biosynthetic multigene families. The specific role of many secondary metabolism biosynthesis enzymes remains to be characterized and the regular discovery of new enzymes shows how incomplete our knowledge of the pathways remains. Likewise, the high rate of discovery of new plant secondary metabolites, induced by the recent developments in metabolomics, shows the limitations of our current understanding of the plant secondary metabolome and it’s functioning. For most known secondary metabolites the specific role in physiological processes or in the resistance to stress conditions has not been established. However, due to their biological activity, color, odor, or other commercially or pharmaceutically exploitable characteristics, there is notable interest in enhancing the production of plant specialized metabolites through biotechnological approaches. Metabolic engineering can benefit from a profound knowledge of the biosynthetic pathways. This Special Issue will be dedicated to the study of both the biosynthesis and the role of plant specialized metabolites.

Topics of interest include:

functional characterization of biosynthetic enzymes;
flux analysis through biosynthesis pathways;
functional characterization of specialized metabolites in physiological processes or in the interaction with the environment;
studies of the modulation of the specialized metabolome in function of endogenous or exogenous stimuli;
metabolic engineering.

Original research papers and reviews related to these items will be considered for publication.

Dr. Rebecca Dauwe
Guest Editor

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Keywords

plant specialized metabolites
biosynthesis enzymes
biosynthesis pathways
metabolic engineering

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Published Papers (8 papers)

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Research

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21 pages, 1837 KiB

Open AccessArticle

A New Fluorescence Detection Method for Tryptophan- and Tyrosine-Derived Allelopathic Compounds in Barley and Lupin

by Sara Leite Dias, Adriana Garibay-Hernández, Fabian Leon Brendel, Benjamin Gabriel Chavez, Elena Brückner, Hans-Peter Mock, Jakob Franke and John Charles D’Auria

Plants 2023, 12(10), 1930; https://doi.org/10.3390/plants12101930 - 9 May 2023

Cited by 5 | Viewed by 2784

Abstract

Barley (Hordeum vulgare) is one of the most widely cultivated crops for feedstock and beer production, whereas lupins (Lupinus spp.) are grown as fodder and their seeds are a source of protein. Both species produce the allelopathic alkaloids gramine and hordenine. These plant-specialized metabolites may be of economic interest for crop protection, depending on their tissue distribution. However, in high concentrations they pose a health risk to humans and animals that feed on them. This study was carried out to develop and validate a new method for monitoring these alkaloids and their related metabolites using fluorescence detection. Separation was performed on an HSS T3 column using slightly acidified water-acetonitrile eluents. Calibration plots expressed linearity over the range 0.09–100 pmol/µL for gramine. The accuracy and precision ranged from 97.8 to 123.4%, <7% RSD. The method was successfully applied in a study of the natural range of abundance of gramine, hordenine and their related metabolites, AMI, tryptophan and tyramine, in 22 barley accessions and 10 lupin species. This method provides accurate and highly sensitive chromatographic separation and detection of tryptophan- and tyrosine-derived allelochemicals and is an accessible alternative to LC-MS techniques for routine screening. Full article

(This article belongs to the Special Issue Biosynthesis and Function of Plant Specialized Metabolites)

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15 pages, 3195 KiB

Open AccessArticle

Integrated Analysis of microRNA and RNA-Seq Reveals Phenolic Acid Secretion Metabolism in Continuous Cropping of Polygonatum odoratum

by Yan Wang, Kaitai Liu, Yunyun Zhou, Yong Chen, Chenzhong Jin and Yihong Hu

Plants 2023, 12(4), 943; https://doi.org/10.3390/plants12040943 - 19 Feb 2023

Cited by 3 | Viewed by 1783

Abstract

Polygonatum odoratum (Mill.) Druce is an essential Chinese herb, but continuous cropping (CC) often results in a serious root rot disease, reducing the yield and quality. Phenolic acids, released through plant root exudation, are typical autotoxic substances that easily cause root rot in CC. To better understand the phenolic acid biosynthesis of P. odoratum roots in response to CC, this study performed a combined microRNA (miRNA)-seq and RNA-seq analysis. The phenolic acid contents of the first cropping (FC) soil and CC soil were determined by HPLC analysis. The results showed that CC soils contained significantly higher levels of p-coumaric acid, phenylacetate, and caffeic acid than FC soil, except for cinnamic acid and sinapic acid. Transcriptome identification and miRNA sequencing revealed 15,788 differentially expressed genes (DEGs) and 142 differentially expressed miRNAs (DEMs) in roots from FC and CC plants. Among them, 28 DEGs and eight DEMs were involved in phenolic acid biosynthesis. Meanwhile, comparative transcriptome and microRNA-seq analysis demonstrated that eight miRNAs corresponding to five target DEGs related to phenolic acid synthesis were screened. Among them, ath-miR172a, ath-miR172c, novel_130, sbi-miR172f, and tcc-miR172d contributed to phenylalanine synthesis. Osa-miR528-5p and mtr-miR2673a were key miRNAs that regulate syringyl lignin biosynthesis. Nta-miR156f was closely related to the shikimate pathway. These results indicated that the key DEGs and DEMs involved in phenolic acid anabolism might play vital roles in phenolic acid secretion from roots of P. odoratum under the CC system. As a result of the study, we may have a better understanding of phenolic acid biosynthesis during CC of roots of P. odoratum. Full article

(This article belongs to the Special Issue Biosynthesis and Function of Plant Specialized Metabolites)

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19 pages, 6035 KiB

Open AccessArticle

RNA-Seq Dissects Incomplete Activation of Phytoalexin Biosynthesis by the Soybean Transcription Factors GmMYB29A2 and GmNAC42-1

by Jie Lin, Ivan Monsalvo, Melissa Ly, Md Asraful Jahan, Dasol Wi, Izabella Martirosyan and Nik Kovinich

Plants 2023, 12(3), 545; https://doi.org/10.3390/plants12030545 - 25 Jan 2023

Cited by 5 | Viewed by 2615

Abstract

Glyceollins, isoflavonoid-derived antimicrobial metabolites, are the major phytoalexins in soybean (Glycine max). They play essential roles in providing resistance to the soil-borne pathogen Phytophthora sojae and have unconventional anticancer and neuroprotective activities that render them desirable for pharmaceutical development. Our previous studies revealed that the transcription factors GmMYB29A2 and GmNAC42-1 have essential roles in activating glyceollin biosynthesis, yet each cannot activate the transcription of all biosynthesis genes in the absence of a pathogen elicitor treatment. Here, we report that co-overexpressing both transcription factors is also insufficient to activate glyceollin biosynthesis. To understand this insufficiency, we compared the transcriptome profiles of hairy roots overexpressing each transcription factor with glyceollin-synthesizing roots treated with wall glucan elicitor (WGE) from P. sojae. GmMYB29A2 upregulated most of the WGE-regulated genes that encode enzymatic steps spanning from primary metabolism to the last step of glyceollin biosynthesis. By contrast, GmNAC42-1 upregulated glyceollin biosynthesis genes only when overexpressed in the presence of WGE treatment. This is consistent with our recent discovery that, in the absence of WGE, GmNAC42-1 is bound by GmJAZ1 proteins that inhibit its transactivation activity. WGE, and not GmMYB29A2 or GmNAC42-1, upregulated the heat shock family gene GmHSF6-1, the homolog of Arabidopsis HSFB2a that directly activated the transcription of several glyceollin biosynthesis genes. Our results provide important insights into what biosynthesis genes will need to be upregulated to activate the entire glyceollin biosynthetic pathway. Full article

(This article belongs to the Special Issue Biosynthesis and Function of Plant Specialized Metabolites)

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15 pages, 2161 KiB

Open AccessArticle

The Combination of Monochromatic LEDs and Elicitation with Stressors Enhances the Accumulation of Glucosinolates in Mustard Sprouts with Species-Dependency

by Carla Guijarro-Real, Lorena Hernández-Cánovas, Ángel Abellán-Victorio, Oumaima Ben-Romdhane and Diego A. Moreno

Plants 2022, 11(21), 2961; https://doi.org/10.3390/plants11212961 - 2 Nov 2022

Cited by 5 | Viewed by 1426

Abstract

This work studies the enhancement of glucosinolates (GSLs) in mustard sprouts as health promoters. Sprouts of Sinapis alba, Brassica nigra, and B. carinata were grown under broad-spectrum, monochromatic blue or red light-emitting diode (LED) lamps, irrigated with 0–100 mM sodium chloride (NaCl), and sprayed with 0–250 µM methyl jasmonate (MeJA) as elicitor. The use of LEDs did not result in increased sprout biomass in any case. The effect of the applied treatments on the GSLs depended on the species and were restricted to Brassica spp. The red LEDs produced an overall increase in GSLs over 500% in B. carinata (from 12 to 81 mg 100 g⁻¹ F.W.), compared to the white broad-spectrum lights, although the highest increase in content was obtained in treated sprouts with 250 µM MeJA (104 an 105 mg 101 g⁻¹ F.W., under the red and blue LEDs, respectively). The combination of blue LEDs, 100 mM NaCl, and 250 µM MeJA enhanced the levels of GLSs in B. nigra to the maximum (81 mg 100 g⁻¹ F.W.). Overall, these results indicate that by modifying the growing conditions for a given sprout, enhancement in the accumulation of GSLs as health promoters is possible. The use of these treatments is a sustainable alternative to genetic modification when looking for bioactive-enriched foods, delivering natural plant foods rich in bioactive ingredients (e.g., glucosinolates). Nevertheless, the response to the treatments varies among species, indicating that treatments will require adjustment across sprouts. Further research continues with producing cruciferous sprouts to obtain GSL-enriched formulas for further studying the effects of their bioavailability and bioactivity on health-promotion. Full article

(This article belongs to the Special Issue Biosynthesis and Function of Plant Specialized Metabolites)

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19 pages, 1071 KiB

Open AccessArticle

Unravelling the Effect of Provitamin A Enrichment on Agronomic Performance of Tropical Maize Hybrids

by Abebe Menkir, Ibnou Dieng, Wende Mengesha, Silvestro Meseka, Bussie Maziya-Dixon, Oladeji Emmanuel Alamu, Bunmi Bossey, Oyekunle Muhyideen, Manfred Ewool and Mmadou Mory Coulibaly

Plants 2021, 10(8), 1580; https://doi.org/10.3390/plants10081580 - 31 Jul 2021

Cited by 6 | Viewed by 2843

Abstract

Maize is consumed in different traditional diets as a source of macro- and micro-nutrients across Africa. Significant investment has thus been made to develop maize with high provitamin A content to complement other interventions for alleviating vitamin A deficiencies. The current breeding focus on increasing β-carotene levels to develop biofortified maize may affect the synthesis of other beneficial carotenoids. The changes in carotenoid profiles, which are commonly affected by environmental factors, may also lead to a trade-off with agronomic performance. The present study was therefore conducted to evaluate provitamin A biofortified maize hybrids across diverse field environments. The results showed that the difference in accumulating provitamin A and other beneficial carotenoids across variable growing environments was mainly regulated by the genetic backgrounds of the hybrids. Many hybrids, accumulating more than 10 µg/g of provitamin A, produced higher grain yields (>3600 kg/ha) than the orange commercial maize hybrid (3051 kg/ha). These hybrids were also competitive, compared to the orange commercial maize hybrid, in accumulating lutein and zeaxanthins. Our study showed that breeding for enhanced provitamin A content had no adverse effect on grain yield in the biofortified hybrids evaluated in the regional trials. Furthermore, the results highlighted the possibility of developing broadly adapted hybrids containing high levels of beneficial carotenoids for commercialization in areas with variable maize growing conditions in Africa. Full article

(This article belongs to the Special Issue Biosynthesis and Function of Plant Specialized Metabolites)

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15 pages, 2449 KiB

Open AccessArticle

Identification and Functional Characterization of Genes Encoding Phenylacetaldehyde Reductases That Catalyze the Last Step in the Biosynthesis of Hydroxytyrosol in Olive

by Rosario Sánchez, Cristina Bahamonde, Carlos Sanz and Ana G. Pérez

Plants 2021, 10(7), 1268; https://doi.org/10.3390/plants10071268 - 22 Jun 2021

Cited by 5 | Viewed by 2761

Abstract

Hydroxytyrosol derivatives are the most important phenolic components in virgin olive oil due to their well-demonstrated biological activities. In this regard, two phenyl acetaldehyde reductase genes, OePAR1.1 and OePAR1.2, involved in hydroxytyrosol synthesis, have been identified from an olive transcriptome. Both genes were synthesized and expressed in Escherichia coli, and their encoded proteins were purified. The recombinant enzymes display high substrate specificity for 2,4-dihydroxyphenylacetaldehyde (3,4-DHPAA) to form hydroxytyrosol. The reaction catalyzed by OePAR constitutes the second, and last, biochemical step in the formation of hydroxytyrosol from the amino acid L-3,4-dihydroxyphenylalanine (L-DOPA) in olive. OePAR1.1 and OePAR1.2 enzymes exhibit high thermal stability, similar pH optima (pH 6.5), and high affinity for 3,4-DHPAA (apparent Km 0.6 and 0.8 µmol min⁻¹ mg⁻¹, respectively). However, OePAR1.2 exhibited higher specific activity and higher expression levels in all the olive cultivars under study. The expression analyses indicate that both OePAR1.1 and OePAR1.2 genes are temporally regulated in a cultivar-dependent manner. The information provided here could be of interest for olive breeding programs searching for new olive genotypes with the capacity to produce oils with higher levels of hydroxytyrosol derivatives. Full article

(This article belongs to the Special Issue Biosynthesis and Function of Plant Specialized Metabolites)

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25 pages, 10354 KiB

Open AccessArticle

Cellular and Subcellular Compartmentation of the 2C-Methyl-D-Erythritol 4-Phosphate Pathway in the Madagascar Periwinkle

by Grégory Guirimand, Anthony Guihur, Catalina Perello, Michael Phillips, Samira Mahroug, Audrey Oudin, Thomas Dugé de Bernonville, Sébastien Besseau, Arnaud Lanoue, Nathalie Giglioli-Guivarc’h, Nicolas Papon, Benoit St-Pierre, Manuel Rodríguez-Concepcíon, Vincent Burlat and Vincent Courdavault

Plants 2020, 9(4), 462; https://doi.org/10.3390/plants9040462 - 7 Apr 2020

Cited by 19 | Viewed by 4723

Abstract

The Madagascar periwinkle (Catharanthus roseus) synthesizes the highly valuable monoterpene indole alkaloids (MIAs) through a long metabolic route initiated by the 2C-methyl-D-erythritol 4-phosphate (MEP) pathway. In leaves, a complex compartmentation of the MIA biosynthetic pathway occurs at both the cellular and subcellular levels, notably for some gene products of the MEP pathway. To get a complete overview of the pathway organization, we cloned four genes encoding missing enzymes involved in the MEP pathway before conducting a systematic analysis of transcript distribution and protein subcellular localization. RNA in situ hybridization revealed that all MEP pathway genes were coordinately and mainly expressed in internal phloem-associated parenchyma of young leaves, reinforcing the role of this tissue in MIA biosynthesis. At the subcellular level, transient cell transformation and expression of fluorescent protein fusions showed that all MEP pathway enzymes were targeted to plastids. Surprisingly, two isoforms of 1-deoxy-D-xylulose 5-phosphate synthase and 1-deoxy-D-xylulose 5-phosphate reductoisomerase initially exhibited an artifactual aggregated pattern of localization due to high protein accumulation. Immunogold combined with transmission electron microscopy, transient transformations performed with a low amount of transforming DNA and fusion/deletion experiments established that both enzymes were rather diffuse in stroma and stromules of plastids as also observed for the last six enzymes of the pathway. Taken together, these results provide new insights into a potential role of stromules in enhancing MIA precursor exchange with other cell compartments to favor metabolic fluxes towards the MIA biosynthesis. Full article

(This article belongs to the Special Issue Biosynthesis and Function of Plant Specialized Metabolites)

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Review

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25 pages, 1933 KiB

Open AccessReview

Origin and Function of Structural Diversity in the Plant Specialized Metabolome

by Sandrien Desmet, Kris Morreel and Rebecca Dauwe

Plants 2021, 10(11), 2393; https://doi.org/10.3390/plants10112393 - 6 Nov 2021

Cited by 24 | Viewed by 3897

Abstract

The plant specialized metabolome consists of a multitude of structurally and functionally diverse metabolites, variable from species to species. The specialized metabolites play roles in the response to environmental changes and abiotic or biotic stresses, as well as in plant growth and development. At its basis, the specialized metabolism is built of four major pathways, each starting from a few distinct primary metabolism precursors, and leading to distinct basic carbon skeleton core structures: polyketides and fatty acid derivatives, terpenoids, alkaloids, and phenolics. Structural diversity in specialized metabolism, however, expands exponentially with each subsequent modification. We review here the major sources of structural variety and question if a specific role can be attributed to each distinct structure. We focus on the influences that various core structures and modifications have on flavonoid antioxidant activity and on the diversity generated by oxidative coupling reactions. We suggest that many oxidative coupling products, triggered by initial radical scavenging, may not have a function in se, but could potentially be enzymatically recycled to effective antioxidants. We further discuss the wide structural variety created by multiple decorations (glycosylations, acylations, prenylations), the formation of high-molecular weight conjugates and polyesters, and the plasticity of the specialized metabolism. We draw attention to the need for untargeted methods to identify the complex, multiply decorated and conjugated compounds, in order to study the functioning of the plant specialized metabolome. Full article

(This article belongs to the Special Issue Biosynthesis and Function of Plant Specialized Metabolites)

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