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New insights into the evolutionary history of plant sorbitol dehydrogenase

Identifieur interne : 000527 ( Main/Exploration ); précédent : 000526; suivant : 000528

New insights into the evolutionary history of plant sorbitol dehydrogenase

Auteurs : Yong Jia [Australie] ; Darren Cj Wong [Australie] ; Crystal Sweetman [Australie] ; John B. Bruning [Australie] ; Christopher M. Ford [Australie]

Source :

RBID : PMC:4404067

English descriptors

Abstract

Background

Sorbitol dehydrogenase (SDH, EC 1.1.1.14) is the key enzyme involved in sorbitol metabolism in higher plants. SDH genes in some Rosaceae species could be divided into two groups. L-idonate-5-dehydrogenase (LIDH, EC 1.1.1.264) is involved in tartaric acid (TA) synthesis in Vitis vinifera and is highly homologous to plant SDHs. Despite efforts to understand the biological functions of plant SDH, the evolutionary history of plant SDH genes and their phylogenetic relationship with the V. vinifera LIDH gene have not been characterized.

Results

A total of 92 SDH genes were identified from 42 angiosperm species. SDH genes have been highly duplicated within the Rosaceae family while monocot, Brassicaceae and most Asterid species exhibit singleton SDH genes. Core Eudicot SDHs have diverged into two phylogenetic lineages, now classified as SDH Class I and SDH Class II. V. vinifera LIDH was identified as a Class II SDH. Tandem duplication played a dominant role in the expansion of plant SDH family and Class II SDH genes were positioned in tandem with Class I SDH genes in several plant genomes. Protein modelling analyses of V. vinifera SDHs revealed 19 putative active site residues, three of which exhibited amino acid substitutions between Class I and Class II SDHs and were influenced by positive natural selection in the SDH Class II lineage. Gene expression analyses also demonstrated a clear transcriptional divergence between Class I and Class II SDH genes in V. vinifera and Citrus sinensis (orange).

Conclusions

Phylogenetic, natural selection and synteny analyses provided strong support for the emergence of SDH Class II by positive natural selection after tandem duplication in the common ancestor of core Eudicot plants. The substitutions of three putative active site residues might be responsible for the unique enzyme activity of V. vinifera LIDH, which belongs to SDH Class II and represents a novel function of SDH in V. vinifera that may be true also of other Class II SDHs. Gene expression analyses also supported the divergence of SDH Class II at the expression level. This study will facilitate future research into understanding the biological functions of plant SDHs.

Electronic supplementary material

The online version of this article (doi:10.1186/s12870-015-0478-5) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/s12870-015-0478-5
PubMed: 25879735
PubMed Central: 4404067


Affiliations:


Links toward previous steps (curation, corpus...)


Le document en format XML

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<title xml:lang="en" level="a" type="main">New insights into the evolutionary history of plant sorbitol dehydrogenase</title>
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<name sortKey="Jia, Yong" sort="Jia, Yong" uniqKey="Jia Y" first="Yong" last="Jia">Yong Jia</name>
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<nlm:aff id="Aff1">School of Agriculture, Food and Wine, University of Adelaide, Adelaide, 5005 Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
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<wicri:noRegion>Adelaide</wicri:noRegion>
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<name sortKey="Wong, Darren Cj" sort="Wong, Darren Cj" uniqKey="Wong D" first="Darren Cj" last="Wong">Darren Cj Wong</name>
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<nlm:aff id="Aff1">School of Agriculture, Food and Wine, University of Adelaide, Adelaide, 5005 Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
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<name sortKey="Sweetman, Crystal" sort="Sweetman, Crystal" uniqKey="Sweetman C" first="Crystal" last="Sweetman">Crystal Sweetman</name>
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<title level="j">BMC Plant Biology</title>
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<term>Amino Acid Sequence</term>
<term>Angiosperms (genetics)</term>
<term>Angiosperms (metabolism)</term>
<term>Biological Evolution</term>
<term>Evolution, Molecular</term>
<term>Gene Expression Regulation, Plant</term>
<term>L-Iditol 2-Dehydrogenase (genetics)</term>
<term>L-Iditol 2-Dehydrogenase (metabolism)</term>
<term>Molecular Sequence Data</term>
<term>Phylogeny</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Sequence Alignment</term>
<term>Vitis (genetics)</term>
<term>Vitis (metabolism)</term>
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<term>L-Iditol 2-Dehydrogenase</term>
<term>Plant Proteins</term>
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<term>Angiosperms</term>
<term>Vitis</term>
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<term>Angiosperms</term>
<term>L-Iditol 2-Dehydrogenase</term>
<term>Plant Proteins</term>
<term>Vitis</term>
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<term>Amino Acid Sequence</term>
<term>Biological Evolution</term>
<term>Evolution, Molecular</term>
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<term>Phylogeny</term>
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<div type="abstract" xml:lang="en">
<sec>
<title>Background</title>
<p>Sorbitol dehydrogenase (SDH, EC 1.1.1.14) is the key enzyme involved in sorbitol metabolism in higher plants. SDH genes in some
<italic>Rosaceae</italic>
species could be divided into two groups. L-idonate-5-dehydrogenase (LIDH, EC 1.1.1.264) is involved in tartaric acid (TA) synthesis in
<italic>Vitis vinifera</italic>
and is highly homologous to plant SDHs. Despite efforts to understand the biological functions of plant SDH, the evolutionary history of plant SDH genes and their phylogenetic relationship with the
<italic>V. vinifera</italic>
LIDH gene have not been characterized.</p>
</sec>
<sec>
<title>Results</title>
<p>A total of 92 SDH genes were identified from 42 angiosperm species. SDH genes have been highly duplicated within the
<italic>Rosaceae</italic>
family while monocot,
<italic>Brassicaceae</italic>
and most
<italic>Asterid</italic>
species exhibit singleton SDH genes. Core Eudicot SDHs have diverged into two phylogenetic lineages, now classified as SDH Class I and SDH Class II.
<italic>V. vinifera</italic>
LIDH was identified as a Class II SDH. Tandem duplication played a dominant role in the expansion of plant SDH family and Class II SDH genes were positioned in tandem with Class I SDH genes in several plant genomes. Protein modelling analyses of
<italic>V. vinifera</italic>
SDHs revealed 19 putative active site residues, three of which exhibited amino acid substitutions between Class I and Class II SDHs and were influenced by positive natural selection in the SDH Class II lineage. Gene expression analyses also demonstrated a clear transcriptional divergence between Class I and Class II SDH genes in
<italic>V. vinifera</italic>
and
<italic>Citrus sinensis</italic>
(orange).</p>
</sec>
<sec>
<title>Conclusions</title>
<p>Phylogenetic, natural selection and synteny analyses provided strong support for the emergence of SDH Class II by positive natural selection after tandem duplication in the common ancestor of core Eudicot plants. The substitutions of three putative active site residues might be responsible for the unique enzyme activity of
<italic>V. vinifera</italic>
LIDH, which belongs to SDH Class II and represents a novel function of SDH in
<italic>V. vinifera</italic>
that may be true also of other Class II SDHs. Gene expression analyses also supported the divergence of SDH Class II at the expression level. This study will facilitate future research into understanding the biological functions of plant SDHs.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12870-015-0478-5) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
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