MYC2 mediated regulation of xylan substitution patterns

Abstract

O-Acetylation is the most abundant xylan decoration in eudicot plants and plays a critical role in determining xylan conformation and its interactions with cellulose and lignin, thereby contributing to secondary cell wall (SCW) integrity. In Arabidopsis, loss of the xylan O-acetyltransferase TBL29/ESK1 causes collapsed xylem and growth defects that can be suppressed by mutations in strigolactone (SL) biosynthesis genes such as MAX3. However, the molecular basis of this suppression remains unknown. Hypoacetylated xylan in tbl29 has a higher frequency of methyl glucuronic acid (MeGlcA) substituents, while the ratio of GlcA/MeGlcA is recovered in tbl29 max3. Furthermore, gene expression analyses reveal that the three xylan glucuronoxylan methyltransferases (GXM1/2/3) involved in xylan MeGlcA modification are upregulated in tbl29 SCWs but downregulated in tbl29 max3. Genetic analysis shows that the transcription factor MYC2 is required for max3-mediated suppression: the loss of MYC2 in tbl29 max3 prevents growth recovery and reverts GXM genes expression and xylan MeGlcA substitution levels. We propose a model where SL deficiency enhances MYC2 transcription, which in turn represses GXMs, thereby fine-tuning xylan methylation and re-establishing the MeGlcA/GlcA substitution balance under conditions of reduced O-acetylation. Our findings identify a MYC2-dependent regulatory module linking SL signalling to xylan methylation and reveal a genetically encoded compensatory mechanism that mitigates the consequences of defective xylan O-acetylation. More broadly, this work demonstrates that plants can preserve SCW function through adaptive remodelling of polysaccharide substitution patterns, highlighting an unexpected plasticity in SCW biosynthesis. Significance StatementSecondary cell wall integrity depends on the coordinated modification of xylan. We show that defects caused by reduced xylan O-acetylation can be alleviated through a strigolactone- and MYC2-dependent pathway that alters xylan methylglucuronidation. Rather than restoring the original wall composition, this mechanism appears to compensate for the loss of O-acetyl groups by remodelling polysaccharide substitution patterns to maintain cell wall function, revealing a new layer of plasticity in secondary wall biosynthesis.