A sucrose ferulate cycle linchpin for ferulyolation of arabinoxylans in plant commelinids

IF 15.8 1区 生物学 Q1 PLANT SCIENCES Nature Plants Pub Date : 2024-09-04 DOI:10.1038/s41477-024-01781-1
Dalin Yang, Hui Liu, Xiaojie Li, Yafeng Zhang, Xingwang Zhang, Huanhuan Yang, Mingyu Liu, Karen E. Koch, Donald R. McCarty, Shengying Li, Bao-Cai Tan
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Abstract

A transformation in plant cell wall evolution marked the emergence of grasses, grains and related species that now cover much of the globe. Their tough, less digestible cell walls arose from a new pattern of cross-linking between arabinoxylan polymers with distinctive ferulic acid residues. Despite extensive study, the biochemical mechanism of ferulic acid incorporation into cell walls remains unknown. Here we show that ferulic acid is transferred to arabinoxylans via an unexpected sucrose derivative, 3,6-O-diferuloyl sucrose (2-feruloyl-O-α-d-glucopyranosyl-(1′→2)-3,6-O-feruloyl-β-d-fructofuranoside), formed by a sucrose ferulate cycle. Sucrose gains ferulate units through sequential transfers from feruloyl-CoA, initially at the O-3 position of sucrose catalysed by a family of BAHD-type sucrose ferulic acid transferases (SFT1 to SFT4 in maize), then at the O-6 position by a feruloyl sucrose feruloyl transferase (FSFT), which creates 3,6-O-diferuloyl sucrose. An FSFT-deficient mutant of maize, disorganized wall 1 (dow1), sharply decreases cell wall arabinoxylan ferulic acid content, causes accumulation of 3-O-feruloyl sucrose (α-d-glucopyranosyl-(1′→2)-3-O-feruloyl-β-d-fructofuranoside) and leads to the abortion of embryos with defective cell walls. In vivo, isotope-labelled ferulic acid residues are transferred from 3,6-O-diferuloyl sucrose onto cell wall arabinoxylans. This previously unrecognized sucrose ferulate cycle resolves a long-standing mystery surrounding the evolution of the distinctive cell wall characteristics of cereal grains, biofuel crops and related commelinid species; identifies an unexpected role for sucrose as a ferulate group carrier in cell wall biosynthesis; and reveals a new paradigm for modifying cell wall polymers through ferulic acid incorporation. A key feature of the evolutionary transformation of grass cell walls is the cross-linking of interwoven arabinoxylans via ferulate units. This study discovered an unexpected sucrose ferulate cycle that mediates the feruloylation of arabinoxylan.

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蔗糖阿魏酸酯循环中的一个关键环节,用于植物纤毛虫体内阿魏酸酯的分解
植物细胞壁进化的转变标志着禾本科植物、谷物和相关物种的出现,它们现在覆盖了全球大部分地区。它们坚韧、不易消化的细胞壁是由具有独特阿魏酸残基的阿拉伯木聚糖聚合物之间新的交联模式产生的。尽管进行了广泛的研究,但阿魏酸融入细胞壁的生化机制仍然未知。在这里,我们发现阿魏酸是通过一种意想不到的蔗糖衍生物--3,6-O-二阿魏酰蔗糖(2-阿魏酰-O-α-d-吡喃葡萄糖基-(1′→2)-3,6-O-阿魏酰-β-d-呋喃果糖苷)转移到阿拉伯木聚糖中的,这种蔗糖衍生物是由蔗糖阿魏酸酯循环形成的。蔗糖通过从阿魏酰-CoA 顺序转移获得阿魏酸单位,最初是在 BAHD 型蔗糖阿魏酸转移酶家族(玉米中为 SFT1 至 SFT4)的催化下在蔗糖的 O-3 位进行转移,然后在 O-6 位由阿魏酰蔗糖阿魏酰转移酶(FSFT)进行转移,从而产生 3,6-O-diferuloyl 蔗糖。缺乏 FSFT 的玉米突变体 "无组织壁 1(dow1)"会使细胞壁阿拉伯木聚糖阿魏酸含量急剧下降,导致 3-O-阿魏酰蔗糖(α-d-吡喃葡萄糖基-(1′→2)-3-O-阿魏酰-β-d-呋喃果糖苷)积累,并导致细胞壁有缺陷的胚胎流产。在体内,同位素标记的阿魏酸残基从 3,6-O-二阿魏酰基蔗糖转移到细胞壁阿拉伯木聚糖上。这种以前未被发现的蔗糖阿魏酸酯循环解开了围绕谷物、生物燃料作物和相关软骨鱼类物种独特细胞壁特征进化的一个长期谜团;确定了蔗糖作为阿魏酸酯基团载体在细胞壁生物合成中的一个意想不到的作用;并揭示了通过阿魏酸掺入改变细胞壁聚合物的一个新范例。
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来源期刊
Nature Plants
Nature Plants PLANT SCIENCES-
CiteScore
25.30
自引率
2.20%
发文量
196
期刊介绍: Nature Plants is an online-only, monthly journal publishing the best research on plants — from their evolution, development, metabolism and environmental interactions to their societal significance.
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