Small signaling peptides in Arabidopsis development: how cells communicate over a short distance

Abstract

To sustain plants' postembryonic growth and development in a structure of cells fixed in cell walls, a tightly controlled short distance cell-cell communication is required. The focus on phytohormones, such as auxin, has historically overshadowed the importance of small peptide signals, but it is becoming clear that secreted peptide signals are important in cell-cell communication to coordinate and integrate cellular functions. However, of the more than 1000 potential secreted peptides, so far only very few have been functionally characterized or matched to a receptor. Here, we will describe our current knowledge on how small peptide signals can be identified, how they are modified and processed, which roles they play in Arabidopsis thaliana development, and through which receptors they act.

Figure 1.

Posttranslational Modifications and Processing of Small Signaling Peptides. (A) Following entry of the full-length mRNA-encoded prepropeptide to the secretory pathway, the N-terminal hydrophobic signal peptide is cleaved by a signal peptidase. Small posttranslationally modified peptides and Cys-rich peptides then follow different pathways to produce an active peptide. All small posttranslationally modified peptides discovered in plants thus far undergo one or more of three types of post translational modification: Tyr sulfation (yellow), Pro hydroxylation (red), and/or Hyp arabinosylation (green). Proteolytic cleavage of the modified peptide from the precursor sequence completes activation. Cys-rich peptides often do not require proteolytic processing from a precursor, though there are exceptions. Activation of Cys-rich peptides is completed upon formation of disulphide bonds between the conserved Cys residues of the peptide, thus bringing the peptide to an active conformation. Schematic is based on Matsubayashi et al. (2012) with permission. (B) The CLE18 precursor contains two motifs with sequence similarity to the canonical CLE motif. CLE18 is found within the variable region of the peptide at amino acid residues 35 to 48, rather than at the extreme C terminus, like other currently known CLE motifs. At the C terminus, there is a sequence of 13 amino acids with a CLEL sequence. At the N terminus is a region of hydrophobic amino acids, thought to act as a secretion signal (Meng et al., 2012). Overexpression of the full-length precursor gives a long root phenotype (Strabala et al., 2006); conversely, treatment with a synthetic peptide based on the CLE18 motif causes a short root phenotype (Ito et al., 2006). Overexpression of the CLEL8/RGF1 motif (derived from the CLE18 precursor) and related CLELs (RGF6/CLEL6, RGF5/CLEL7, and RGF9/GLV2/CLEL19), derived from other precursors, also results in a long root phenotype, suggesting that the extreme C-terminal motif represents the sequence of the active peptide (Matsuzaki et al., 2010; Meng et al., 2012; Whitford et al., 2012).

Figure 2.

SAM and RAM. (A) CLV3 (yellow) is expressed in the central zone (CZ) of the SAM and inhibits expression of WUS (red) in the OC. WUS itself promotes CLV3 expression. The CLV1 receptor is expressed below layers one and two of the SAM (L1 and L2). On the right is the proposed CLV3-CLV1-WUS signaling module. PZ, peripheral zone; RZ, rib zone. (B) Several peptides, such as CLE14, CLE40, and RGF4/GLV3, are expressed in the RAM in overlapping domains to control cell identity and meristematic activity. On the right is the proposed CLE40-ACR4-WOX5 signaling module. At present, there is no evidence for WOX5 controlling CLE40 expression (?). Red outline, stem cells and QC; purple, starch granules.

Figure 3.

Vascular Differentiation. Schematic of a stem section highlighting the vascular bundles (top left). Phloem cells (yellow) generate and secrete CLE41 peptides (peach) into procambial cells (green) where they are bound by membrane-localized TDR/PXY. TDR/PXY inhibits differentiation of procambium into xylem cells (blue) and upregulates the expression of the transcription factor WOX4, initiating stem cell proliferation (green). As CLE41 concentration lowers (toward plane of division: dashed line), procambial cells (green) can differentiate into xylem cells (blue) without inhibition from TDR. On the top right is the proposed CLE41-TDR/PXY-WOX4 signaling module. At present, there is no evidence for WOX4 controlling CLE41 expression (?).

Figure 4.

Stomatal Development. Stomatal development begins when protodermal cells differentiate into MMCs. Protodermal cells that do not differentiate into MMCs instead differentiate into epidermal pavement cells. The MMC then divides asymmetrically to form a small triangular meristemoid cell (red) and a larger type of daughter cell, a stomatal lineage ground cell (SLGC). At these early stages of stomatal development, cells secrete EPF2 (yellow); after these stages, there is a switch to EPF1 expression (purple). Meristemoids often further divide to amplify the number of cells in the stomatal lineage, before finally differentiating into GMCs. GMCs then divide symmetrically to form two guard cells surrounding a pore, completing stomatal development. Once guard cell maturation is complete, EPF1 secretion is terminated. STOMAGEN (light blue) is expressed in the mesophyll and diffuses to the epidermis, promoting stomatal development. CHAL (orange) is secreted by cells surrounding the vascular bundle and diffuses to the epidermis, restricting stomatal development.