Jia Yong, Wong Darren C J, Sweetman Crystal, Bruning John B, Ford Christopher M
School of Agriculture, Food and Wine, University of Adelaide, Adelaide, 5005, Australia.
Present address: Wine Research Center, Faculty of Land and Food Systems, University of British Columbia, Vancouver, V6T 1Z4, BC, Canada.
BMC Plant Biol. 2015 Apr 12;15:101. doi: 10.1186/s12870-015-0478-5.
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.
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).
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.
山梨醇脱氢酶（SDH，EC 1.1.1.14）是高等植物中山梨醇代谢的关键酶。一些蔷薇科物种中的SDH基因可分为两组。L-艾杜糖酸-5-脱氢酶（LIDH，EC 1.1.1.264）参与酿酒葡萄中酒石酸（TA）的合成，并且与植物SDH高度同源。尽管人们努力了解植物SDH的生物学功能，但植物SDH基因的进化历史及其与酿酒葡萄LIDH基因的系统发育关系尚未得到明确。
从42种被子植物物种中总共鉴定出92个SDH基因。SDH基因在蔷薇科家族中高度重复，而单子叶植物、十字花科和大多数菊类物种呈现单个SDH基因。核心真双子叶植物的SDH已分化为两个系统发育谱系，现在分类为SDH I类和SDH II类。酿酒葡萄LIDH被鉴定为II类SDH。串联重复在植物SDH家族的扩展中起主导作用，并且在几个植物基因组中，II类SDH基因与I类SDH基因串联定位。酿酒葡萄SDH的蛋白质建模分析揭示了19个假定的活性位点残基，其中三个在I类和II类SDH之间表现出氨基酸替换，并且在SDH II类谱系中受到正自然选择的影响。基因表达分析还表明，酿酒葡萄和甜橙（橙子）中I类和II类SDH基因之间存在明显的转录差异。
系统发育、自然选择和共线性分析为核心真双子叶植物共同祖先中串联重复后通过正自然选择产生II类SDH提供了有力支持。三个假定活性位点残基的替换可能是酿酒葡萄LIDH独特酶活性的原因，酿酒葡萄LIDH属于II类SDH，代表了SDH在酿酒葡萄中的一种新功能，其他II类SDH可能也是如此。基因表达分析也支持II类SDH在表达水平上的差异。这项研究将有助于未来对理解植物SDH生物学功能的研究。
