CLE peptide signaling during plant development

Abstract

Peptide signaling in plants is a rapid developing area of research which focuses on so called peptide hormones. These signaling molecules are utilized for inter-cellular communication in different developmental processes, beside the usage of the more well-known phytohormones. Probably the best studied peptide ligands in plants are the CLAVATA3 (CLV3)/ENDOSPERM SURROUNDING REGION (ESR)-related (CLE) proteins. This family of signaling polypeptides is comprised of 32 members in Arabidopsis and, with the exception of the presence of related proteins in some parasitic worms, is restricted to the plant kingdom. CLV3 is one of the founding CLE genes and is involved in stem cell niche maintenance in apical meristems during plant development. While the CLV signaling pathway is well characterized with the identification of three receptors and a stem-cell-promoting transcription factor as target, the functioning of other family members is not or poorly understood. The recent discoveries of a new type of receptor involved in CLV signaling and a functional pathway for CLE40 in root development mark the rapid progress that is made in the area of CLE peptide signaling. This review gives an overview how CLE peptides are used as signaling molecules, and how they are involved in cell-to-cell communication in concert with different known and unknown receptors in a range of developmental processes during plant development.

Fig. 1

Schematic representation of the shoot apical meristem expressed CLE genes and genes involved in the CLV pathway in the SAM. The central zone (CZ) harbors the stem cells that are specified by CLV3 expression and the organizing center is marked by WUS expression and surrounded by CLV1 expression. Next to the CZ are the peripheral zones (PZ) where organ primordia are initiated. CLE19 is specifically expressed in the periphery of the SAM where the new primordia will be formed and CLE27 is expressed in the developing organs. CLE41 is expressed in the SAM but excluded from the CZ whereas CLE40, CRN, CLV2, and the BAM receptors are expressed throughout the SAM. Expression data from CLE27 and CLE41 are based on the data from Yadav et al. (2009)

Fig. 2

Alignment of several CLE proteins from different plants and organisms including the mature peptide of CLV3 and TDIF. The signal sequences are underlined and the CLE box is framed. Note the four extra CLE domains in OsCLE32. MCLV3 and TDIF represent the mature peptides, in which the first and second proline is hydroxylated (as indicated by asterisks) and in case of MCLV3 the second proline is arbinosylated (indicated by a)

Fig. 3

Structure of the root with all CLE genes expressed in the meristematic area and any known receptors and targets of CLE signaling. The BAM3 receptor is mainly expressed in the stele while BAM1 and BAM2 are expressed throughout the root. The expression data from CLE2, CLE4, CLE12, CLE17, and the BAM receptors are based on the data from Birnbaum et al. (2003), combining the expression of stage 1 and 2 in root development with a cutoff of 40