Abstract

Peptide signals mediate a variety of cell-to-cell communication crucial for plant growth and development. During Arabidopsis thaliana vascular development, a CLE (CLAVATA3/EMBRYO SURROUNDING REGION-related) family peptide hormone, TDIF (tracheary element differentiation inhibitory factor), regulates procambial cell fate by its inhibitory activity on xylem differentiation. To address if this activity is conserved among vascular plants, we performed comparative analyses of TDIF signaling in non-flowering vascular plants (gymnosperms, ferns and lycophytes). We identified orthologs of TDIF/CLE as well as its receptor TDR/PXY (TDIF RECEPTOR/PHLOEM INTERCALATED WITH XYLEM) in Ginkgo biloba, Adiantum aethiopicum, and Selaginella kraussiana by RACE-PCR. The predicted TDIF peptide sequences in seed plants and ferns were identical to that of A. thaliana TDIF. We examined the effects of exogenous CLE peptide-motif sequences of TDIF in these species. We found that liquid culturing of dissected leaves or shoots was useful for examining TDIF activity during vascular development. TDIF treatment suppressed xylem/tracheary element differentiation of procambial cells in G. biloba and A. aethiopicum leaves. In contrast, neither TDIF nor putative endogenous TDIF inhibited xylem differentiation in developing shoots and rhizophores of S. kraussiana. These data suggest that activity of TDIF in vascular development is conserved among extant euphyllophytes. In addition to the conserved function, via liquid culturing of its bulbils, we found a novel inhibitory activity on root growth in the fern Asplenium × lucrosum suggesting lineage-specific co-option of peptide signaling occurred during the evolution of vascular plant organs.

Highlights

  • Recent advances in biochemical, genetic and bioinformatic analyses have unveiled the importance of peptide hormones in plant growth and development (Matsubayashi, 2014)

  • TDIF genes in non-flowering vascular plants were identified by searching the Genbank and 1 KP databases using the amino acid sequence of TDIF, HEVPSGPNPISN, as a query

  • CLE peptide motifs identical to TDIF were found in Picea sitchensis, Pseudotsuga menziesii, Taxus baccata, Sequoia sempervirens, Gnetum gnemon, G. biloba, Equisetum giganteum (Table S1)

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Summary

Introduction

Genetic and bioinformatic analyses have unveiled the importance of peptide hormones in plant growth and development (Matsubayashi, 2014). The R-type CLE includes CLV3 (CLAVATA3), which plays a significant role in the maintenance of shoot apical meristem in Arabidopsis thaliana, while the Htype CLE includes TDIF, an important regulator of vascular cell differentiation (Brand et al, 2000; Schoof et al, 2000; Ito et al, 2006; Hirakawa et al, 2008). The TDIF-TDR pair mediates a phloem-derived signal that inhibits differentiation of procambial cells into xylem cells, which is important during secondary growth of vasculature in A. thaliana floral stems (Hirakawa et al, 2008, 2010; Whitford et al, 2008; Etchells and Turner, 2010)

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