Plant Cells CLEave Their Way to Differentiation

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Science  11 Aug 2006:
Vol. 313, Issue 5788, pp. 773-774
DOI: 10.1126/science.1131833

Most plant cells are immobile and thus have to inform each other about their relative position through the exchange of chemical signals. Such cell-cell communication is particularly important during the development (differentiation) of stem cells to form specialized tissue cells. Two reports in this issue describe the isolation of small peptides that fulfill such short-range signaling functions (1, 2). Both peptides are derived from precursor proteins belonging to the (almost) plant-exclusive CLE family and are very similar in amino acid sequence, but one promotes and the other suppresses stem cell differentiation during shoot and vascular development.

Plant stem cells are found in tissues called meristems, which are found at the tips of both the shoots and the roots (see the figure). Here, new cells are generated that enter differentiation paths to form specialized tissue cells. Stem cell identity in the shoot meristem is controlled by signaling to neighboring cells via the CLAVATA (CLV) pathway (see the figure, left). The known components of this pathway are CLV1 (a leucine-rich repeat receptor-like kinase), CLV2 (a leucine-rich repeat receptor-like protein), and the predicted ligand CLV3 (35). Stem cells secrete CLV3 to activate the CLV1/CLV2 complex in adjacent cells. This complex then represses the expression of the transcription factor WUSCHEL (3, 6). Because this transcription factor is required for stem cell maintenance, increased CLV3 signaling induces stem cell differentiation.

The CLV3 protein is one of 31 proteins in the flowering plant Arabidopsis (a model organism for plant research) that contain the 14-amino acid CLE motif near their carboxyl terminus (7, 8). Several other members of the CLE family can activate CLV signaling if they are expressed at sufficient levels in the meristem (9). Even short peptides consisting only of the CLE motif retain this activity (10, 11). But it has been difficult to determine the exact nature of the CLV3 peptide, because this peptide is expressed in only a few cells (the stem cells) at the meristem tip. Overexpression of CLV3 causes rapid stem cell loss and developmental arrest.

What it takes to be different.

Effects of CLE peptide signaling on shoot and root meristems and on vascular stem cells (procambial cells). Stem cells are shown in orange, differentiated cells in green. (Left) Balancing stem cell numbers in the shoot. CLV3 is expressed in stem cells at the tip of the shoot meristem. The CLV3 precursor is processed into its active form, which contains only 12 amino acids of the CLE motif, as reported by Kondo et al. Extracellular CLV3 peptide is expected to bind to the CLV1/CLV2 receptor complex, leading to down-regulation of the transcription factor WUSCHEL, which in turn activates CLV3 expression and promotes stem cell fate. (Top right) Inhibition of xylem cell formation. Isolated mesophyll cells of Zinnia elegans first dedifferentiate, turn into procambial cells (PC) and then xylem precursor cells, and finally differentiate again into tracheary elements (TE). This differentiation process, mediated by the secreted factor xylogen, results in secondary cell-wall thickening and programmed cell death. Ito et al. isolated a small peptide homologous to CLE 41, 42, and 44 of Arabidopsis that inhibits this stage of differentiation in vitro, counteracting the xylogen differentiation signal. (Bottom right) Most other CLE peptides, including CLV3, can promote differentiation of Arabidopsis root meristem cells.

Kondo et al. have now acquired sufficient plant material for isolating the active CLV3 peptide. They did so by inducing leaf tissue of CLV3-overexpressing Arabidopsis plants to become callus tissue (which is not differentiated and can grow without restriction). They then applied matrix-assisted laser desorption/ionization time-of-flight mass spectrometry directly to this callus tissue. On page 845 (1), they report that the active CLV3 peptide consists of only 12 amino acids within the CLE motif and that it carries hydroxyl groups at two of the three proline residues. However, this hydroxylation is not required for signaling; its role may lie in controlling peptide stability.

To date, CLE peptides have been shown to promote the shift from the stem cell state to cellular differentiation in shoot and root meristems (see the figure, bottom right). On page 842, Ito et al. (2) show that CLE peptides can also inhibit differentiation.

The authors used plant vascular development as a model system to study the steps that control differentiation. The stem cells of the vascular system—the procambial cells—give rise to daughter cells (called xylem and phloem precursor cells) that subsequently differentiate into tracheary elements (see the figure, top right). This differentiation involves cell-wall thickening, loss of the nucleus, and ultimately cell death. To form a continuous tube system for liquid transport, the tracheary elements have to interconnect with each other, suggesting that their differentiation could be coordinated by short-range signaling.

This process can be studied in vitro using cultured leaf cells from Zinnia elegans plants. These cells differentiate into tracheary elements in the presence of the appropriate plant hormones. The resulting cells secrete factors into the medium that promote differentiation. One such secreted factor, xylogen, has previously been isolated from the cell walls of differentiating tracheary elements (12). Directed secretion of xylogen from one cell might coerce its next neighbor into vascular differentiation.

During the isolation of xylogen, Ito et al. also detected an inhibitory peptide, termed TDIF (tracheary element differentiation inhibitory factor), that suppressed the transition of procambial cells to tracheary elements and instead promoted cell division (2). The authors purified TDIF from conditioned medium and show that it is yet another hydroxyproline-carrying CLE peptide. Homologous CLE peptides from Arabidopsis have TDIF activity, but do not arrest root meristem development.

The identification of the active CLV3 peptide and of TDIF raises important questions: Where does processing of CLE peptides take place, which enzymes are involved, and how is it regulated? And how do processing and post-translational modifications contribute to determine the selectivity of CLE peptides for a specific signaling pathway? So far, CLE peptides have been shown to control the fates of shoot, root, and vascular stem cells. With 31 CLE peptides and more than 200 leucine-rich repeat receptor-like kinases as potential receptors in Arabidopsis alone, we have only seen the clef that starts the tune of differentiation.


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