Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system

Abstract

Land plants evolved a long-distance transport system of water and nutrients composed of the xylem and phloem, both of which are generated from the procambium-and cambium-comprising vascular stem cells. However, little is known about the molecular mechanism of cell communication governing xylem-phloem patterning. Here, we show that a dodecapeptide (HEVHypSGHypN-PISN; Hyp, 4-hydroxyproline), TDIF (tracheary element differentiation inhibitory factor), is secreted from the phloem and suppresses the differentiation of vascular stem cells into xylem cells through a leucine-rich repeat receptor-like kinase (LRR-RLK). TDIF binds in vitro specifically to the LRR-RLK, designated TDR (putative TDIF receptor), whose expression is restricted to procambial cells. However, the combined analysis of TDIF with a specific antibody and the expression profiles of the promoters of two genes encoding TDIF revealed that TDIF is synthesized mainly in, and secreted from, the phloem and its neighboring cells. The observation that TDIF is capable of promoting proliferation of procambial cells while suppressing xylem differentiation suggests that this small peptide functions as a phloem-derived, non-cellautonomous signal that controls stem cell fate in the procambium. Our results indicate that we have discovered a cell communication system governing phloem-xylem cross-talk.CLV3/ESR-related (CLE) ͉ leucine-rich repeat receptor-like kinase ͉ phloem ͉ procambium ͉ xylem

Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF–TDR signalling

“…In hypocotyls, TDIF did not reduce xylem cell numbers (Fig. 6e), which is consistent with results reported previously 16,31,32 . This might result from a counterbalance between TDIF-dependent reduced xylem cells and ectopic xylem formation as a secondary effect arising from TDIF-induced random procambial cell proliferation (Fig.…”

“…To investigate roles of SKI and II members in TDIF signalling, TDIF sensitivity was examined by genetic analysis using loss-of-function mutants for GSK3s. Previous physiological and genetic studies have shown that TDIF has two distinct effects on vascular development; inhibition of xylem differentiation and promotion of vascular cell division 15,16,18 . In the WT, exogenous TDIF application suppresses xylem differentiation from procambial cells, resulting in discontinuous xylem formation in Arabidopsis leaf veins 16,18 ( Fig.…”

“…7c-e). The adjacency phenotype in tdr results from the exhaustion of procambial cells by a combination of the inhibition of procambial cell proliferation and the consumption of procambial cells via enhanced xylem differentiation 16,18 . wox4-1 mutant, which shows only a defect in TDIF-dependent promotion of procambial cell proliferation in contrast to gsk3 mutants 18,32 , exhibits the reduction of procambial cell layers but not the adjacency of xylem and phloem cells 18,32 .…”

“…Genetic and biochemical analyses identified TDIF receptor (TDR)/PHLOEM INTERCALATED WITH XYLEM (PXY), which belongs to the leucine-rich repeat receptor-like kinase (LRR-RLK) class XI, as a specific membrane-associated receptor for TDIF 16,17 . TDIF both suppresses the differentiation of procambial cells into xylem cells and promotes their proliferation through TDR 15,16 . These dual functions of TDIF-TDR are considered to be separated by downstream components 18 .…”

RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana

“…TRACHEARY ELEMENT DIFFERENTIATION INHIBITORY FACTOR (TDIF)/ CLE41/CLE44 peptide regulates vascular development in Arabidopsis. TDIF peptide derived from CLE41 or CLE44 is perceived by PHLOEM INTERCALATED WITH XYLEM (PXY), an LRR-RLK [21][22][23][24].…”