Splice variant of the SND1 transcription factor is a dominant negative of SND1 members and their regulation in Populus trichocarpa

Abstract

Secondary Wall-Associated NAC Domain 1s (SND1s) are transcription factors (TFs) known to activate a cascade of TF and pathway genes affecting secondary cell wall biosynthesis (xylogenesis) in Arabidopsis and poplars. Elevated SND1 transcriptional activation leads to ectopic xylogenesis and stunted growth. Nothing is known about the upstream regulators of SND1. Here we report the discovery of a stem-differentiating xylem (SDX)-specific alternative SND1 splice variant, PtrSND1-A2IR, that acts as a dominant negative of SND1 transcriptional network genes in Populus trichocarpa. PtrSND1-A2IR derives from PtrSND1-A2, one of the four fully spliced PtrSND1 gene family members (PtrSND1-A1, -A2, -B1, and -B2). Each full-size PtrSND1 activates its own gene, and all four full-size members activate a common MYB gene (PtrMYB021). PtrSND1-A2IR represses the expression of its PtrSND1 member genes and PtrMYB021. Repression of the autoregulation of a TF family by its only splice variant has not been previously reported in plants. PtrSND1-A2IR lacks DNA binding and transactivation abilities but retains dimerization capability. PtrSND1-A2IR is localized exclusively in cytoplasmic foci. In the presence of any full-size PtrSND1 member, PtrSND1-A2IR is translocated into the nucleus exclusively as a heterodimeric partner with full-size PtrSND1s. Our findings are consistent with a model in which the translocated PtrSND1-A2IR lacking DNA-binding and transactivating abilities can disrupt the function of full-size PtrSND1s, making them nonproductive through heterodimerization, and thereby modulating the SND1 transcriptional network. PtrSND1-A2IR may contribute to transcriptional homeostasis to avoid deleterious effects on xylogenesis and plant growth.