LBD29-Involved Auxin Signaling Represses NAC Master Regulators and Fiber Wall Biosynthesis

NAM, ATAF1/2 and CUC2 (NAC) domain transcription factors function as master switches in regulating secondary cell wall (SCW) biosynthesis in Arabidopsis ( Arabidopsis thaliana ) stems. Despite the importance of these NACs in fiber development, the upstream signal is still elusive. Using a large-scale mutant screening, we identified a dominant activation-tagging mutant, fiberless-d ( fls-d ), showing defective SCW development in stem fibers, similar to that of the nac secondary wall thickening promoting factor1-1 ( nst1-1 ) nst3-3 double mutant. Overexpression of LATERAL ORGAN BOUNDARIES DOMAIN29 ( LBD29 ) is responsible for the fls-d mutant phenotypes. By contrast, loss-of-function of LBD29 , either in the dominant repression transgenic lines or in the transfer-DNA (T-DNA) insertion mutant lbd29-1 , enhanced SCW development in fibers. Genetic analysis and transgenic studies demonstrated LBD29 depends on master regulators in mediating SCW biosynthesis, specifically NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 ( NST1 ), NST 2, and NST 3. Increasing indole-3-acetic acid (IAA) levels, either in stem tissues above a N -1-naphthylphthalamic acid-treated region or in plants directly sprayed with IAA, inhibits fiber wall thickening. The inhibition effect of naphthylphthalamic acid treatment and exogenous IAA application depends on a known auxin signaling pathway involving AUXIN RESPONSE FACTOR7 (ARF7)/ARF19 and LBD29. These results demonstrate auxin is upstream of LBD29 in repressing NAC master regulators, and therefore shed new light on the regulation of SCW biosynthesis in Arabidopsis.