Class I KNOX transcription factors promote differentiation of cambial derivatives into xylem fibers in the Arabidopsis hypocotyl

Abstract

The class I KNOX transcription factors SHOOT MERISTEMLESS (STM) and KNAT1 are important regulators of meristem maintenance in shoot apices, with a dual role of promoting cell proliferation and inhibiting differentiation. We examined whether they control stem cell maintenance in the cambium of Arabidopsis hypocotyls, a woodforming lateral meristem, in a similar fashion as in the shoot apical meristem. Weak loss-of-function alleles of KNAT1 and STM led to reduced formation of xylem fibers -highly differentiated cambial derivatives -whereas cell proliferation in the cambium was only mildly affected. In a knat1;stm double mutant, xylem fiber differentiation was completely abolished, but residual cambial activity was maintained. Expression of early and late markers of xylary cell differentiation was globally reduced in the knat1;stm double mutant. KNAT1 and STM were found to act through transcriptional repression of the meristem boundary genes BLADE-ON-PETIOLE 1 (BOP1) and BOP2 on xylem fiber differentiation. Together, these data indicate that, in the cambium, KNAT1 and STM, contrary to their function in the shoot apical meristem, promote cell differentiation through repression of BOP genes.

Vascular Cambium Development

“…BOP1 and BOP2 are normally expressed only in the pedicel axils, but in the bp pny mutant their expression pattern expands from the pedicel to the main stem. Similarly, BOP1 and BOP2 expression is also upregulated in the weak stm mutant (Liebsch et al, 2014). The defective sectors in bp are rescued in the bop1 bop2 bp triple mutant (Fig.…”

“…Three interacting homeodomain transcription factors, the KNOX protein BREVI-PEDICELLUS/KNOTTED-LIKE FROM ARABIDOPSIS THALI-ANA 1 (BP/KNAT1; At4g08150), SHOOT MERISTEMLESS (STM; At1g62360) and the BELL family protein PENNYWISE/ BELLRINGER/VAANAMA (PNY/BLR/VAN; At5g02030) function in the regulation of Arabidopsis shoot architecture and vascular development (Bhatt et al, 2004;Etchells et al, 2012;Khan et al, 2012a;Khan et al, 2012b;Liebsch et al, 2014). It is wellestablished that various KNOX and BELL family proteins interact during meristem development; these interactions determine their subcellular localization and DNA binding affinity (reviewed by Hay and Tsiantis, 2010).…”

“…These sectors are associated with stripes of ectopically lignified cortical tissue and appear as gaps in the vascular ring (Khan et al, 2012a;Khan et al, 2012b). Vascular bundles with deficient xylem fiber differentiation also frequently appear in the shoot of the weak stm loss-of-function mutant (Liebsch et al, 2014). By contrast, single loss-of-function mutants of pny have an increased number of vascular bundles which appear relatively normal (Smith and Hake, 2003;Etchells et al, 2012).…”

Overexpression of ARBORKNOX1 delays the differentiation of induced somatic sector analysis (ISSA) derived xylem fibre cells in poplar stems

“…However, a recent study in Arabidopsis hypocotyls in mildly downregulated STM mutants and double mutants with KNAT1, another KNOX1 family member, showed phenotypes that where contrary to their proposed role in the SAM, including a reduction and/or loss of fibre differentiation, hinting different roles for this gene in the cambium (Liebsch et al 2014).…”

“…ARK1 targets also share high similarity with binding targets of other closely related transcription factors ARBORKNOX 2 and BELLRINGER (Liu et al 2015a, b). In addition, when overexpressed in transgenic plants, only a small proportion of target genes are shown to be differentially expressed suggesting that on its own, it is not able to significantly modulate target gene expression (Liu et al 2015b;Liebsch et al 2014). These findings highlight the complex way ARK1 interacts at a molecular level to regulate cambial processes.…”