Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Science, Shandong University, Qingdao, China.
Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China.
Nat Plants. 2024 Sep;10(9):1389-1399. doi: 10.1038/s41477-024-01781-1. Epub 2024 Sep 4.
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.
植物细胞壁演化的一次变革标志着草类、谷物和相关物种的出现，这些物种现在覆盖了全球的大部分地区。它们坚韧、不易消化的细胞壁是由阿拉伯木聚糖聚合物与具有独特阿魏酸残基的交联新模式产生的。尽管进行了广泛的研究，但阿魏酸掺入细胞壁的生化机制仍然未知。在这里，我们表明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-果糖呋喃糖苷）转移到阿拉伯木聚糖中的，该衍生物是由蔗糖阿魏酸循环形成的。蔗糖通过顺序从阿魏酰辅酶 A 转移阿魏酸单元，最初在蔗糖被一系列 BAHD 型蔗糖阿魏酸转移酶（玉米中的 SFT1 到 SFT4）催化的 O-3 位置，然后在 O-6 位置由阿魏酰蔗糖阿魏酰转移酶（FSFT）催化，该酶生成 3,6-O-二阿魏酰蔗糖。玉米的 FSFT 缺陷突变体 disorganized wall 1（dow1），显著降低细胞壁阿拉伯木聚糖阿魏酸含量，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-果糖呋喃糖苷）积累，并导致细胞壁有缺陷的胚胎夭折。在体内，同位素标记的阿魏酸残基从 3,6-O-二阿魏酰蔗糖转移到细胞壁阿拉伯木聚糖上。这个以前未被认识的蔗糖阿魏酸循环解决了一个长期存在的谜团，即谷物、生物燃料作物和相关鸭跖草科物种的独特细胞壁特征的演化；确定了蔗糖作为细胞壁生物合成中阿魏酸基团载体的意外作用；并揭示了通过阿魏酸掺入修饰细胞壁聚合物的新范例。
