Peptide signaling in plant development

Abstract

Cell-to-cell communication is integral to the evolution of multicellularity. In plant development, peptide signals relay information coordinating cell proliferation and differentiation. These peptides are often encoded by gene families and bind to corresponding families of receptors. The precise spatiotemporal expression of signals and their cognate receptors underlies developmental patterning, and expressional and biochemical changes over evolutionary time have likely contributed to the refinement and complexity of developmental programs. Here, we discuss two major plant peptide families which have central roles in plant development: the CLAVATA3/ENDOSPERM SURROUNDING REGION (CLE) peptide family and the EPIDERMAL PATTERNING FACTOR (EPF) family. We discuss how specialization has enabled the CLE peptides to modulate stem cell differentiation in various tissue types, and how differing activities of EPF peptides precisely regulate the stomatal developmental program, and we examine the contributions of these peptide families to plant development from an evolutionary perspective.

Figure 1. Scheme of CLE and EPF structure and maturation

(A) Full length CLE is processed to release the active CLEp consisting of the CLE motif (here represented by CLV3). Stars represent sites of post-translational modifications (B) Consensus sequences of A-type and B-type CLE peptide sequences and activities of each class are shown. Sequence alignments were generated by ClustalW2 and logos were made with WebLogo. (C,D) EPF family protein structure using STOMAGEN as a representative example. (C) Full length STO MAGEN is processed to produce a cysteinerich active peptide (conserved cysteines shown in blue). (D) Experimentally determined structure of STOMAGEN with conserved cysteines (blue) and intramolecular disulfide bonds (green). The variable loop residues exposed at the surface are highlighted in yellow. Image modeled after [62].

Figure 2. Models for CLE-dependent stem cell maintenance in the shoot, root, and vascular meristems

(A) Upper panel: WUS expression in the organizing center (turqoise) is required for expression of CLV3 in the stem cells (red), and CLV3 in turn restricts the expression of WUS. The CLV1 receptor (blue) is largely expressed underneath the two outermost cell layers of the shoot meristem. Lower panel: CLV3p interaction with several receptor complexes which repress the expression of WUS via repressing POL/PLL. (B) CLE40 expression in the columella root cap (blue) acts through ACR4 to restrict WOX5 expression to the quiescent center (turquoise). Columella stem cells are indicated in red. (C) CLE41 is secreted by phloem cells and perceived by TDR, which represses differentiation and upregulates the expression of WOX4 to support stem cell proliferation (red). The dashed green line indicates the plane of division set up by the adjacent CLE41 expression. Where CLE41 concentration is low, the procambial stem cell daughter undergoes differentiation.

Figure 3. Model of stomatal development and proposed receptor–ligand interactions

(A) Scheme of Arabidopsis stomatal development illustrated in isolated cells, and in the context of the developing leaf below. A protodermal cell (grey) enters the stomatal lineage via an asymmetric division generating a meristemoid (purple) and larger daughter cell known as a stomatal lineage ground cell (SLGC). The meristemoid may undergo additional asymmetric ‘amplifying’ divisions (producing additional SLGCs) and neighboring cells that undergo asymmetric divisions will orient their division such that two meristemoids are not physically adjacent to each other. The meristemoid differentiates into a guard mother cell (yellow) and the subsequent symmetric division gives rise to two guard cells (green). (B) Summary of EPF ligand–receptor interactions. EPF1 and EPF2 inhibit stomatal development through TMM and ERf receptors. STOMAGEN promotes stomatal development and may compete with EPF1 and EPF2 to do so. CHAL inhibits stomatal development through ERf receptors, and TMM dampens CHAL signaling.

Figure 4. Alignment of EPFs

CLUSTAL_W2 alignment of characterized Arabidopsis EPFs and homologues in Physcomitrella patens (Pp), Selaginella moellindorffii (Sm), and Oryza sativa (Os). Alignment uses the putative active peptides based on the mature STOMAGEN sequence.