Plant secondary cell-wall (SCW) deposition and lignification are affected by both seasonal factors and abiotic stress, and these responses may involve the hormone abscisic acid (ABA). However, the mechanisms involved are not clear. Here we show that mutations that limit ABA synthesis or signaling reduce the extent of SCW thickness and lignification in Arabidopsis thaliana through the core ABA-signaling pathway involving SnRK2 kinases. SnRK2.2. 3 and 6 physically interact with the SCW regulator NAC SECONDARY WALL THICKENING PROMOTING FACTOR 1 (NST1), a NAC family transcription factor that orchestrates the transcriptional activation of a suite of downstream SCW biosynthesis genes, some of which are involved in the biosynthesis of cellulose and lignin. This interaction leads to phosphorylation of NST1 at Ser316, a residue that is highly conserved among NST1 proteins from dicots, but not monocots, and is required for transcriptional activation of downstream SCW-related gene promoters. Loss of function of NST1 in the snd1 mutant background results in lack of SCWs in the interfascicular fiber region of the stem, and the Ser316Ala mutant of NST1 fails to complement this phenotype and ABA-induced lignin pathway gene expression. The discovery of NST1 as a key substrate for phosphorylation by SnRK2 suggests that the ABA-mediated core-signaling cascade provided land plants with a hormone-modulated, competitive desiccation-tolerance strategy allowing them to differentiate water-conducting and supporting tissues built of cells with thicker cell walls.

A wide range of biological processes are regulated by sumoylation, a post-translational modification involving the conjugation of SUMO (Small Ubiquitin-Like Modifier) to protein. In Arabidopsis thaliana, AtSIZ1 encodes a SUMO E3 ligase for SUMO modification. siz1 mutants displayed defective secondary cell walls (SCWs) in inflorescence fiber cells. Such defects were caused by repression of SND1/NST1-mediated transcriptional networks. Yeast two-hybrid assay indicated that SIZ1 interacts with the LBD30 C-terminal domain, which was further confirmed using bimolecular fluorescence complementation and immunoprecipitation. Mass spectrometry and co-immunoprecipitation indicated that SIZ1 mediates SUMO conjugation to LBD30 at the K226 residue. Genes controlling SCW formation were activated by the overexpression of LBD30, but not in the LBD30(K226R) mutant. LBD30 enhancement of SCW formation resulted from upregulation of SND1/NST1-mediated transcriptional networks. This study presents a mechanism by which sumoylation of LBD30, mediated by SIZ1, regulates SCW formation in A. thaliana.