PRISEs (progesterone 5β-reductase and/or iridoid synthase-like 1,4-enone reductases): Catalytic and substrate promiscuity allows for realization of multiple pathways in plant metabolism

Schmidt, Karin; Petersen, Jan; Munkert, Jennifer; Egerer-Sieber, C.; Hörnig, Michael; Muller, Yves A.; Kreis, Wolfgang

doi:10.1016/j.phytochem.2018.08.012

Cited by 18 publications

(22 citation statements)

References 44 publications

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“…This was paralleled by a transient boost in cardenolide formation. Homology-based screening in the available gene databases indicated the presence of more than two progesterone reductases in D. purpurea and D. lanata (Schmidt et al 2018 ). We here focused on the two known genes only, accepting that the knockdown of them might not silence progesterone reductase activity completely.…”

Section: Resultsmentioning

confidence: 99%

“…Moreover, P5βR-like enzymes (termed iridoid synthases; ISY) are involved in iridoid biosynthesis (Geu-Flores et al 2012 ), and Munkert et al ( 2015a , b ) reported that iridoid synthase activity is common among the plant progesterone 5β-reductase family. More recently, the enzymes progesterone 5β-reductase/iridoid synthase-like enzymes were termed PRISEs (Schmidt et al 2018 ) and described as a catalytic reservoir for specialized metabolism across land plants (Nguyen and O’Connor 2020 ). Progesterone in cardenolide biosynthesis and 8-oxogeranial in iridoid synthesis are not the only substrates for PRISEs.…”

Section: Introductionmentioning

confidence: 99%

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RNAi-mediated gene knockdown of progesterone 5β-reductases in Digitalis lanata reduces 5β-cardenolide content

et al. 2021

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Key message Studying RNAi-mediated DlP5βR1 and DlP5βR2 knockdown shoot culture lines of Digitalis lanata, we here provide direct evidence for the participation of PRISEs (progesterone 5β-reductase/iridoid synthase-like enzymes) in 5β-cardenolide formation. Abstract Progesterone 5β-reductases (P5βR) are assumed to catalyze the reduction of progesterone to 5β-pregnane-3,20-dione, which is a crucial step in the biosynthesis of the 5β-cardenolides. P5βRs are encoded by VEP1-like genes occurring ubiquitously in embryophytes. P5βRs are substrate-promiscuous enone-1,4-reductases recently termed PRISEs (progesterone 5β-reductase/iridoid synthase-like enzymes). Two PRISE genes, termed DlP5βR1 (AY585867.1) and DlP5βR2 (HM210089.1) were isolated from Digitalis lanata. To give experimental evidence for the participation of PRISEs in 5β-cardenolide formation, we here established several RNAi-mediated DlP5βR1 and DlP5βR2 knockdown shoot culture lines of D. lanata. Cardenolide contents were lower in D. lanata P5βR-RNAi lines than in wild-type shoots. We considered that the gene knockdowns may have had pleiotropic effects such as an increase in glutathione (GSH) which is known to inhibit cardenolide formation. GSH levels and expression of glutathione reductase (GR) were measured. Both were higher in the Dl P5βR-RNAi lines than in the wild-type shoots. Cardenolide biosynthesis was restored by buthionine sulfoximine (BSO) treatment in Dl P5βR2-RNAi lines but not in Dl P5βR1-RNAi lines. Since progesterone is a precursor of cardenolides but can also act as a reactive electrophile species (RES), we here discriminated between these by comparing the effects of progesterone and methyl vinyl ketone, a small RES but not a precursor of cardenolides. To the best of our knowledge, we here demonstrated for the first time that P5βR1 is involved in cardenolide formation. We also provide further evidence that PRISEs are also important for plants dealing with stress by detoxifying reactive electrophile species (RES).

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

RNAi-mediated gene knockdown of progesterone 5β-reductases in Digitalis lanata reduces 5β-cardenolide content

et al. 2021

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“…The gene harbouring SNP117 was assigned to the GO category progesterone 5β-reductase (P5βR) . In spite of being a family first described in animals, PRISEs (progesterone 5 β -reductase and/or iridoid synthase-like 1,4-enone reductases) are ubiquitous in plants and are involved in cardenolide and iridoid biosynthesis in many species [ 32 ]. The occurrence of species with these enzymes but not producing cardenolides or iridoids may indicate a more general role in the scavenging and detoxification of reactive carbonyl compounds [ 32 ].…”

Section: Discussionmentioning

confidence: 99%

“…In spite of being a family first described in animals, PRISEs (progesterone 5 β -reductase and/or iridoid synthase-like 1,4-enone reductases) are ubiquitous in plants and are involved in cardenolide and iridoid biosynthesis in many species [ 32 ]. The occurrence of species with these enzymes but not producing cardenolides or iridoids may indicate a more general role in the scavenging and detoxification of reactive carbonyl compounds [ 32 ]. In agreement with this proposal, members of this family showed to be sensitive to abiotic and mechanical stressors, with their expression being regulated by ethylene and hydrogen peroxide [ 33 ].…”

Section: Discussionmentioning

confidence: 99%

Unveiling the genetic basis of Sclerotinia head rot resistance in sunflower

et al. 2020

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Background: Sclerotinia sclerotiorum is a necrotrophic fungus that causes Sclerotinia head rot (SHR) in sunflower, with epidemics leading to severe yield losses. In this work, we present an association mapping (AM) approach to investigate the genetic basis of natural resistance to SHR in cultivated sunflower, the fourth most widely grown oilseed crop in the world. Results: Our association mapping population (AMP), which comprises 135 inbred breeding lines (ILs), was genotyped using 27 candidate genes, a panel of 9 Simple Sequence Repeat (SSR) markers previously associated with SHR resistance via bi-parental mapping, and a set of 384 SNPs located in genes with molecular functions related to stress responses. Moreover, given the complexity of the trait, we evaluated four disease descriptors (i.e, disease incidence, disease severity, area under the disease progress curve for disease incidence, and incubation period). As a result, this work constitutes the most exhaustive AM study of disease resistance in sunflower performed to date. Mixed linear models accounting for population structure and kinship relatedness were used for the statistical analysis of phenotype-genotype associations, allowing the identification of 13 markers associated with disease reduction. The number of favourable alleles was negatively correlated to disease incidence, disease severity and area under the disease progress curve for disease incidence, whereas it was positevily correlated to the incubation period. Conclusions: Four of the markers identified here as associated with SHR resistance (HA1848, HaCOI_1, G33 and G34) validate previous research, while other four novel markers (SNP117, SNP136, SNP44, SNP128) were consistently associated with SHR resistance, emerging as promising candidates for marker-assisted breeding. From the germplasm point of view, the five ILs carrying the largest combination of resistance alleles provide a valuable resource for sunflower breeding programs worldwide.

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“… 13 − 17 Earlier reports showed that both PRISEs from Catharanthus roseus , an iridoid-producing species, and PRISEs from the Brassicaceae, including those that do not produce iridoids and/or cardenolides, had different reductase activities toward 8-oxogeranial and progesterone. 16 , 18 , 19 Promiscuous enzymatic activities are likely starting points for specialization under different conditions, as demonstrated by several examples in enzyme evolution. 20 − 24 To determine whether such a process within the PRISE family played a role in iridoid metabolism evolution, we identified PRISE homologues from an encompassing range of plant lineages.…”

Section: Introductionmentioning

confidence: 99%

The Progesterone 5β-Reductase/Iridoid Synthase Family: A Catalytic Reservoir for Specialized Metabolism across Land Plants

Nguyen

O’Connor

2020

ACS Chem. Biol.

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Iridoids are plant-derived terpenoids with a rich array of bioactivities. The key step in iridoid skeleton formation is the reduction of 8-oxogeranial by certain members of the progesterone 5β-reductase/iridoid synthase (PRISE) family of short-chain alcohol dehydrogenases. Other members of the PRISE family have previously been implicated in the biosynthesis of the triterpenoid class of cardenolides, which requires the reduction of progesterone. Here, we explore the occurrence and activity of PRISE across major lineages of plants. We observed trace activities toward either 8-oxogeranial or progesterone in all PRISEs, including those from nonseed plants and green algae. Phylogenetic analysis, coupled with enzymatic assays, show that these activities appear to have become specialized in specific angiosperm lineages. This broad analysis of the PRISE family provides insight into how these enzymes evolved in plants and also suggests that iridoid synthase activity is an ancestral trait in all land plants, which might have contributed to the rise of iridoid metabolites.

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PRISEs (progesterone 5β-reductase and/or iridoid synthase-like 1,4-enone reductases): Catalytic and substrate promiscuity allows for realization of multiple pathways in plant metabolism

Cited by 18 publications

References 44 publications

RNAi-mediated gene knockdown of progesterone 5β-reductases in Digitalis lanata reduces 5β-cardenolide content

RNAi-mediated gene knockdown of progesterone 5β-reductases in Digitalis lanata reduces 5β-cardenolide content

Unveiling the genetic basis of Sclerotinia head rot resistance in sunflower

The Progesterone 5β-Reductase/Iridoid Synthase Family: A Catalytic Reservoir for Specialized Metabolism across Land Plants

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