The Plant Short-Chain Dehydrogenase (SDR) superfamily: genome-wide inventory and diversification patterns

Abstract

BackgroundShort-chain dehydrogenases/reductases (SDRs) form one of the largest and oldest NAD(P)(H) dependent oxidoreductase families. Despite a conserved ‘Rossmann-fold’ structure, members of the SDR superfamily exhibit low sequence similarities, which constituted a bottleneck in terms of identification. Recent classification methods, relying on hidden-Markov models (HMMs), improved identification and enabled the construction of a nomenclature. However, functional annotations of plant SDRs remain scarce.ResultsWide-scale analyses were performed on ten plant genomes. The combination of hidden Markov model (HMM) based analyses and similarity searches led to the construction of an exhaustive inventory of plant SDR. With 68 to 315 members found in each analysed genome, the inventory confirmed the over-representation of SDRs in plants compared to animals, fungi and prokaryotes. The plant SDRs were first classified into three major types — ‘classical’, ‘extended’ and ‘divergent’ — but a minority (10% of the predicted SDRs) could not be classified into these general types (‘unknown’ or ‘atypical’ types). In a second step, we could categorize the vast majority of land plant SDRs into a set of 49 families. Out of these 49 families, 35 appeared early during evolution since they are commonly found through all the Green Lineage. Yet, some SDR families — tropinone reductase-like proteins (SDR65C), ‘ABA2-like’-NAD dehydrogenase (SDR110C), ‘salutaridine/menthone-reductase-like’ proteins (SDR114C), ‘dihydroflavonol 4-reductase’-like proteins (SDR108E) and ‘isoflavone-reductase-like’ (SDR460A) proteins — have undergone significant functional diversification within vascular plants since they diverged from Bryophytes. Interestingly, these diversified families are either involved in the secondary metabolism routes (terpenoids, alkaloids, phenolics) or participate in developmental processes (hormone biosynthesis or catabolism, flower development), in opposition to SDR families involved in primary metabolism which are poorly diversified.ConclusionThe application of HMMs to plant genomes enabled us to identify 49 families that encompass all Angiosperms (‘higher plants’) SDRs, each family being sufficiently conserved to enable simpler analyses based only on overall sequence similarity. The multiplicity of SDRs in plant kingdom is mainly explained by the diversification of large families involved in different secondary metabolism pathways, suggesting that the chemical diversification that accompanied the emergence of vascular plants acted as a driving force for SDR evolution.

Structural Studies of Cinnamoyl-CoA Reductase and Cinnamyl-Alcohol Dehydrogenase, Key Enzymes of Monolignol Biosynthesis

“…The structural conservation of this binding pocket in CCR and CAD2 reflects most obviously the divergence of CCR and CAD2 from a progenitor reductase enzyme that was specific for a phenolic compound. Such an evolutionary ancestry is consistent with the predominance in the SDR108E/SDR115E family of enzymes that participate in phenylpropanoid and flavonoid metabolism (Moummou et al, 2012). Thus, the apparent binding by the CAD enzymes of taxifolin (a substrate of dihydroflavonol reductase, an enzyme belonging to the SDR115E branch) is likely due to recognition of the phenolic ring and propanaldehyde substituent in common with the true phenylpropenyl-aldehyde substrates.…”

“…Sequence comparisons, phylogenetic analyses, and our structure determination nevertheless unambiguously placed Mt-CAD2 within a distinct family (SDR108E/SDR115E; i.e., the SDR108E family together with a SDR115E daughter branch, as proposed by Moummou et al, 2012) of the SDR superfamily. More specifically, Mt-CAD2 resides in the flowering plant phenylacetaldehyde-reductase subgroup, which is notably distinct from the exclusive subgroup formed by the bona fide CCRs.…”

“…These two CCRs share 75% amino acid sequence identity and consequently have essentially identical polypeptide chain folds. CCR possesses a bilobal tertiary structure typical of the extended SDR family (Moummou et al, 2012), with distinct NADP (H) binding and substrate binding domains (Figure 2). The NADP (H) binding domain is an alternating a/b structure that forms a seven-stranded, parallel b-sheet (with strand topology 3-2-1-4-5-6-7) sandwiched between two layers of three a-helices.…”

Tropane and Granatane Alkaloid Biosynthesis: A Systematic Analysis

“…In solanaceous plants, two types of tropinone reductases exist, tropinone reductase I (TR I) and tropinone reductase II (TR II). They share a common tertiary "Rossman" fold structure, a conserved motif that consists of two pairs of α-helices and six parallel β-sheets, a catalytic active site with the motif YxxxK, and a dinucleotide cofactor-binding motif [91]. These enzymes share more than 50% of amino acid sequence similarity and are also assumed to have evolved from a common ancestor [90].…”

Antisense expression of Gossypium hirsutum UDP-glucuronate decarboxylase in Arabidopsis leads to changes in cell wall components

“…The UXS family belongs to the short-chain dehydrogenase/reductase superfamily (Moummou et al, 2012). In plants, different UXS isoforms occur in the cytosol and membrane-bound compartments (Harper and Bar-Peled, 2002).…”