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New insights into the evolutionary history of plant sorbitol dehydrogenase.

Jia Y, Wong DC, Sweetman C, Bruning JB, Ford CM - BMC Plant Biol. (2015)

Bottom Line: V. vinifera LIDH was identified as a Class II SDH.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.

View Article: PubMed Central - PubMed

Affiliation: School of Agriculture, Food and Wine, University of Adelaide, Adelaide, 5005, Australia. yong.jia@adelaide.edu.au.

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.

No MeSH data available.


Related in: MedlinePlus

Distribution of SDH homologous genes in higher plants. Closely related species were specified accordingly. The gene abundance heat map was based on the total copy number of SDH genes in each species. SDHs of P. bretschneideri [39] and E. japonica (loquat) [35] were obtained from literature; additional SDHs may be identified in these two species when complete genome information becomes available. The classification of SDH Class I and SDH Class II was based on the phylogenetic analysis carried out in the present study.
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Fig1: Distribution of SDH homologous genes in higher plants. Closely related species were specified accordingly. The gene abundance heat map was based on the total copy number of SDH genes in each species. SDHs of P. bretschneideri [39] and E. japonica (loquat) [35] were obtained from literature; additional SDHs may be identified in these two species when complete genome information becomes available. The classification of SDH Class I and SDH Class II was based on the phylogenetic analysis carried out in the present study.

Mentions: A database homology search identified 92 SDH homologous genes from 42 species (Figure 1; See Additional file 2: Table S1 for identified gene IDs and Additional file 3 for gene sequences in corresponding species). At least one putative SDH gene was present in each plant genome studied, consistent with previous studies [17] that suggested the ubiquity of SDH and its functional importance across all life forms. However, the distribution of SDH homologous genes varied dramatically across species. Monocot species (n = 8) uniformly presented a single SDH gene, and this same observation was made with Brassicaceae plants (n = 7) from the Eudicot group. It was recently reported that there are 2 SDH genes in both rice (monocot) and A.thaliana (Brassicaceae) [50], however, in both cases these SDH genes were found to be alternative transcripts of a single gene. All except one species from the Asterid clade and the Leguminosae family had one SDH gene, the exceptions being Solanum tuberosum (potato) and Glycine max (soybean), respectively, which both had two copies. By contrast, numerous copies of SDH genes were found in Rosaceae species, which employ sorbitol as the major transported carbohydrate [25]. Malus × domestica (apple) contained 16 putative SDH genes, the highest number among all species investigated. A previous study [50] identified 17 SDH genes in the apple genome, however, the extra putative SDH (MDP0000506359) was only a partial gene (177 residues) and was excluded from the present study. In addition to apple, other Rosaceae species such as Prunus persica (peach), Prunus mume (Chinese plum), Eriobotrya japonica (loquat) and Pyrus bretschneideri (pear) had 4, 3, 1 and 5 putative SDH genes respectively. It should be noted that the information of SDH numbers in loquat [35] and pear [39] was retrieved from earlier reports, and that more SDH genes may be found when complete genome data for these species become available. Although Fragaria vesca (strawberry) belongs to the Rosaceae family, only one SDH gene was present in this species. Unlike other Rosaceae fruit species, F. vesca utilizes sucrose instead of sorbitol as the main translocated carbohydrate [51]. According to a recent development in the evolution by duplication theory, a proper gene dosage should be kept to maintain a stoichiometric balance in macromolecular complexes such as functional proteins, thereby ensuring the normal functioning of a particular biological process [41,52]. Transportation and assimilation of sorbitol is a Rosaceae-specific metabolism. The retention of highly duplicated SDH genes in Rosaceae species suggests that a higher dosage of SDH transcription or enzyme activity is needed to facilitate sorbitol metabolism in these species.Figure 1


New insights into the evolutionary history of plant sorbitol dehydrogenase.

Jia Y, Wong DC, Sweetman C, Bruning JB, Ford CM - BMC Plant Biol. (2015)

Distribution of SDH homologous genes in higher plants. Closely related species were specified accordingly. The gene abundance heat map was based on the total copy number of SDH genes in each species. SDHs of P. bretschneideri [39] and E. japonica (loquat) [35] were obtained from literature; additional SDHs may be identified in these two species when complete genome information becomes available. The classification of SDH Class I and SDH Class II was based on the phylogenetic analysis carried out in the present study.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4404067&req=5

Fig1: Distribution of SDH homologous genes in higher plants. Closely related species were specified accordingly. The gene abundance heat map was based on the total copy number of SDH genes in each species. SDHs of P. bretschneideri [39] and E. japonica (loquat) [35] were obtained from literature; additional SDHs may be identified in these two species when complete genome information becomes available. The classification of SDH Class I and SDH Class II was based on the phylogenetic analysis carried out in the present study.
Mentions: A database homology search identified 92 SDH homologous genes from 42 species (Figure 1; See Additional file 2: Table S1 for identified gene IDs and Additional file 3 for gene sequences in corresponding species). At least one putative SDH gene was present in each plant genome studied, consistent with previous studies [17] that suggested the ubiquity of SDH and its functional importance across all life forms. However, the distribution of SDH homologous genes varied dramatically across species. Monocot species (n = 8) uniformly presented a single SDH gene, and this same observation was made with Brassicaceae plants (n = 7) from the Eudicot group. It was recently reported that there are 2 SDH genes in both rice (monocot) and A.thaliana (Brassicaceae) [50], however, in both cases these SDH genes were found to be alternative transcripts of a single gene. All except one species from the Asterid clade and the Leguminosae family had one SDH gene, the exceptions being Solanum tuberosum (potato) and Glycine max (soybean), respectively, which both had two copies. By contrast, numerous copies of SDH genes were found in Rosaceae species, which employ sorbitol as the major transported carbohydrate [25]. Malus × domestica (apple) contained 16 putative SDH genes, the highest number among all species investigated. A previous study [50] identified 17 SDH genes in the apple genome, however, the extra putative SDH (MDP0000506359) was only a partial gene (177 residues) and was excluded from the present study. In addition to apple, other Rosaceae species such as Prunus persica (peach), Prunus mume (Chinese plum), Eriobotrya japonica (loquat) and Pyrus bretschneideri (pear) had 4, 3, 1 and 5 putative SDH genes respectively. It should be noted that the information of SDH numbers in loquat [35] and pear [39] was retrieved from earlier reports, and that more SDH genes may be found when complete genome data for these species become available. Although Fragaria vesca (strawberry) belongs to the Rosaceae family, only one SDH gene was present in this species. Unlike other Rosaceae fruit species, F. vesca utilizes sucrose instead of sorbitol as the main translocated carbohydrate [51]. According to a recent development in the evolution by duplication theory, a proper gene dosage should be kept to maintain a stoichiometric balance in macromolecular complexes such as functional proteins, thereby ensuring the normal functioning of a particular biological process [41,52]. Transportation and assimilation of sorbitol is a Rosaceae-specific metabolism. The retention of highly duplicated SDH genes in Rosaceae species suggests that a higher dosage of SDH transcription or enzyme activity is needed to facilitate sorbitol metabolism in these species.Figure 1

Bottom Line: V. vinifera LIDH was identified as a Class II SDH.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.

View Article: PubMed Central - PubMed

Affiliation: School of Agriculture, Food and Wine, University of Adelaide, Adelaide, 5005, Australia. yong.jia@adelaide.edu.au.

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.

No MeSH data available.


Related in: MedlinePlus