A Group of O-Acetyltransferases Catalyze Xyloglucan Backbone Acetylation and Can Alter Xyloglucan Xylosylation Pattern and Plant Growth When Expressed in Arabidopsis

A Group of O-Acetyltransferases Catalyze Xyloglucan Backbone Acetylation and Can Alter Xyloglucan Xylosylation Pattern and Plant Growth When Expressed in Arabidopsis
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DOI:
10.1093/pcp/pcaa031
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发表时间:
2020-06-01
影响因子:
4.9
通讯作者:
Ye, Zheng-Hua
Ye, Zheng-Hua
中科院分区:
生物学2区
文献类型:
--
作者:
Zhong, Ruiqin;Cui, Dongtao;Ye, Zheng-Hua

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木葡聚糖是植物细胞壁中的主要半纤维素,并且以两种不同的类型XXXG和XXGG存在。虽然来自双子叶植物物种的XXXG型木葡聚糖仅在侧链半乳糖(Gal)残基上含有0-乙酰基,但来自禾本科(禾本科)和茄科的XXGG型木葡聚糖在主链葡糖基(Glc)残基上具有0-乙酰基。虽然负责木葡聚糖Gal乙酰化的0-乙酰基转移酶已经被表征,但是木葡聚糖主链乙酰化的生物化学机制仍有待阐明。在这项研究中,我们发现,一组DUF 231成员从水稻和番茄的重组蛋白能够转移乙酰基到O-6的葡萄糖残基的纤维低聚物受体,表明他们是木葡聚糖骨架60-乙酰基转移酶(XyBAT)。我们进一步证明了XyBAT-乙酰化的纤维六糖低聚物可以容易地被AtXXT 1(拟南芥木葡聚糖木糖基转移酶1)木糖基化以产生乙酰化的木糖基化的纤维低聚物,而AtXXT 1-木糖基化的纤维六糖低聚物被XyBAT乙酰化的效率低得多。水稻XyBAT在拟南芥中的异源表达导致细胞扩增和植物生长的严重减少以及木葡聚糖木糖基化模式的急剧改变,形成乙酰化XXGG型单元,包括XGG、XGGG、XXGG、XXGGG和XXGGG(C表示乙酰化Glc)。此外,两个拟南芥XyBAT同源物的重组蛋白也表现出O-乙酰转移酶对纤维六糖的活性,这表明它们可能在体内介导木葡聚糖骨架乙酰化的作用。我们的研究结果为木葡聚糖主链乙酰化的生化机制提供了新的见解,并表明了维持细胞壁功能中常规木葡聚糖木糖基化模式的重要性。
Xyloglucan is a major hemicellulose in plant cell walls and exists in two distinct types, XXXG and XXGG. While the XXXG-type xyloglucan from dicot species only contains O-acetyl groups on side-chain galactose (Gal) residues, the XXGG-type xyloglucan from Poaceae (grasses) and Solanaceae bears O-acetyl groups on backbone glucosyl (Glc) residues. Although O-acetyltransferases responsible for xyloglucan Gal acetylation have been characterized, the biochemical mechanism underlying xyloglucan backbone acetylation remains to be elucidated. In this study, we showed that recombinant proteins of a group of DUF231 members from rice and tomato were capable of transferring acetyl groups onto O-6 of Glc residues in cello-oligomer acceptors, indicating that they are xyloglucan backbone 60-acetyltransferases (XyBATs). We further demonstrated that XyBAT-acetylated cellohexaose oligomers could be readily xylosylated by AtXXT1 (Arabidopsis xyloglucan xylosyltransferase 1) to generate acetylated, xylosylated cello-oligomers, whereas AtXXT1-xylosylated cellohexaose oligomers were much less effectively acetylated by XyBATs. Heterologous expression of a rice XyBAT in Arabidopsis led to a severe reduction in cell expansion and plant growth and a drastic alteration in xyloglucan xylosylation pattern with the formation of acetylated XXGG-type units, including XGG, XGGG, XXGG, XXGG,XXGGG and XXGGG (C denotes acetylated Glc). In addition, recombinant proteins of two Arabidopsis XyBAT homologs also exhibited O-acetyltransferase activity toward cellohexaose, suggesting their possible role in mediating xyloglucan backbone acetylation in vivo. Our findings provide new insights into the biochemical mechanism underlying xyloglucan backbone acetylation and indicate the importance of maintaining the regular xyloglucan xylosylation pattern in cell wall function.