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A proteoglycan mediates inductive interaction during plant vascular development

Abstract

Inductive cell–cell interactions are essential for controlling cell fate determination in both plants and animals1; however, the chemical basis of inductive signals in plants remains little understood. A proteoglycan-like factor named xylogen mediates local and inductive cell–cell interactions required for xylem differentiation in Zinnia cells cultured in vitro2,3. Here we describe the purification of xylogen and cloning of its complementary DNA, and present evidence for its role in planta. The polypeptide backbone of xylogen is a hybrid-type molecule with properties of both arabinogalactan proteins and nonspecific lipid-transfer proteins. Xylogen predominantly accumulates in the meristem, procambium and xylem. In the xylem, xylogen has a polar localization in the cell walls of differentiating tracheary elements. Double knockouts of Arabidopsis lacking both genes that encode xylogen proteins show defects in vascular development: discontinuous veins, improperly interconnected vessel elements and simplified venation. Our results suggest that the polar secretion of xylogen draws neighbouring cells into the pathway of vascular differentiation to direct continuous vascular development, thereby identifying a molecule that mediates an inductive cell–cell interaction involved in plant tissue differentiation.

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Figure 1: Xylogen is an arabinogalactan protein that induces xylem differentiation.
Figure 2: Characterization of xylogen.
Figure 3: Temporal and spatial profiles of xylogen expression.
Figure 4: Phenotypic analysis of Arabidopsis xylogen knockouts.

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Acknowledgements

We thank J. J. Harada for critically reading the manuscript; K. Roberts for JIM13; S. Hasezawa and T. Nagata for tobacco BY-2 cells; S. Sawa for advice on the protein–lipid overlay assay; N. Sassa, K. Iwamoto and C. Nishitani for advice on in situ hybridization; M. Fujita and N. Shinohara for advice on immunohistochemistry; the Salk Institute Genomic Analysis Laboratory for the sequence-indexed Arabidopsis T-DNA insertion mutants; the Kazusa DNA Research Institute for the Tag-line pool; A. Nagatani for xyp2-3 seeds; K. Ohashi-Ito and S. Sakamoto for the screening and isolation of xyp2-3. H.M. was supported in part by the Yamada Science Foundation. Funding for the SIGnAL indexed insertion mutant collection was provided by the National Science Foundation of USA. This work was supported in part by Grants-in-Aid from the Ministry of Education, Science, Sports and Culture of Japan, from the Japan Society for the Promotion of Science, and from the Mitsubishi Foundation.

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Correspondence to Hiroyasu Motose.

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Motose, H., Sugiyama, M. & Fukuda, H. A proteoglycan mediates inductive interaction during plant vascular development. Nature 429, 873–878 (2004). https://doi.org/10.1038/nature02613

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