Syringyl lignin biosynthesis is directly regulated by a secondary cell wall master switch

Abstract

Lignin is a major component of plant secondary cell walls and is derived from p-hydroxyphenyl (H), guaiacyl (G), and syringyl (S) monolignols. Among higher plants, S lignin is generally considered to be restricted to angiosperms, which contain the S lignin-specific cytochrome P450-dependent monooxygenase, ferulic acid/coniferaldehyde/coniferyl alcohol 5-hydoxylase (F5H). The transcription factor MYB58 directly regulates expression of monolignol pathway genes except for F5H. Here we show that F5H expression is directly regulated by the secondary cell wall master switch NST1/SND1, which is known to regulate expression of MYB58. Deletion of NST1 expression in Medicago truncatula leads to a loss of S lignin associated with a more than 25-fold reduction of F5H expression but only around a 2-fold reduction in expression of other lignin pathway genes. A detailed phylogenetic analysis showed that gymnosperms lack both F5H and orthologs of NST1/SND1. We propose that both F5H and NST1 appeared at a similar time after the divergence of angiosperms and gymnosperms, with F5H possibly originating as a component of a defense mechanism that was recruited to cell wall biosynthesis through the evolution of NST1-binding elements in its promoter.ferulate 5-hydroxylase | NAC transcription factor | pathway evolution L ignin is an aromatic heteropolymer derived primarily from the hydroxycinnamyl alcohols p-coumaryl, coniferyl, and sinapyl alcohol, which give rise to p-hydroxyphenyl (H), guaiacyl (G) and syringyl (S) subunits, respectively (1). Lignin is one of the three main components of plant secondary cell walls and plays important roles in vascular plant growth by contributing to structural rigidity, facilitating water transport, and providing a defensive barrier against pathogens.Lignin monomer composition varies among plant species. Although S lignin has arisen more than once during evolution (2), it does not appear to exist in the majority of gymnosperms or in ferns, whereas angiosperms deposit S units in lignin polymers in secondary cell walls. A cytochrome P450 (CYP)-dependent monooxygenase, ferulic acid/coniferaldehyde/coniferyl alcohol 5-hydoxylase (F5H, CYP84A1) is specifically required for S lignin biosynthesis (3, 4) and diverts G monolignol intermediates into the S lignin branch pathway.The Arabidopsis lignin-specific transcription factor MYB58 can directly activate most lignin biosynthesis genes except F5H (5). This activation is through binding to AC elements, which are present in most of the promoters of lignin biosynthetic genes (6-9), although no AC element has been detected in the F5H gene (9). Two NAC transcription factors, NST1 and SND1 (NST3), act together as key regulators of the entire secondary cell wall biosynthesis program in Arabidopsis (10, 11) and activate a cascade of downstream transcription factors, which in turn activates the biosynthetic pathways for the individual secondary cell wall components cellulose, xylan, and lignin (12). MYB46 is a direct target of SND1 in Arabidopsis. Although downstream ...

The role of CCoAOMT1 and COMT1 in Arabidopsis anthers

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