Information processing without brains--the power of intercellular regulators in plants

Abstract

Plants exhibit different developmental strategies than animals; these are characterized by a tight linkage between environmental conditions and development. As plants have neither specialized sensory organs nor a nervous system, intercellular regulators are essential for their development. Recently, major advances have been made in understanding how intercellular regulation is achieved in plants on a molecular level. Plants use a variety of molecules for intercellular regulation: hormones are used as systemic signals that are interpreted at the individual-cell level; receptor peptide-ligand systems regulate local homeostasis; moving transcriptional regulators act in a switch-like manner over small and large distances. Together, these mechanisms coherently coordinate developmental decisions with resource allocation and growth.

Fig. 1.

Schematic representation of two different specimens of white oak (Quercus alba). The specimen on the left is a free-standing tree, whereas the tall slender tree on the right grew in a forest. Reproduced with permission from Holdrege (Holdrege, 2005).

Fig. 2.

Modes of intercellular movement. (A) The apoplastic transport of molecules occurs by diffusion in the extracellular space. (B) Transcellular transport involves passage through two plasma membranes and can occur by secretion and subsequent endocytosis, diffusion or transporter activity. (C) Symplastic transport is facilitated by plasmodesmata that connect adjacent cells. They consist of endoplasmic reticulum (ER) that is appressed into the central axial desmotubule (DM) and flanked by the plasma membrane (PM). Transport can occur through the cytoplasmic sleeve between DM and PM.

Fig. 3.

The CLAVATA signaling module in the shoot apical meristem. The action of the transcription factor WUSCHEL (WUS) leads to the production of an unknown signal (X) that results in the transcription of CLV3 in neighboring cells. CLV3 protein is processed into the mature CLV3 peptide (mCLV3), which subsequently binds to CLV1 and to CLV2/CRN receptor complexes. This event eventually causes the repression of WUS.

Fig. 4.

FLOWERING LOCUS T (FT) protein movement. In suitable conditions, FT is transcribed in the phloem companion cells (CC) of leaves (left). FT is then transported into the sieve elements (SE). There, long-distance transport of FT occurs toward sink tissues. In the shoot apex (right), FT is unloaded from the phloem and acts together with FLOWERING LOCUS D (FD) to induce APETALA 1 (AP1) expression. FM, floral meristem; IM, inflorescence meristem; LP, leaf primordium.

Fig. 5.

Some pathogens can usurp intercellular regulatory pathways. Three strategies through which pathogens alter plant development are shown. (A) Xanthomonas bacteria secrete AvrBs3 protein into plant cells. This directly induces upregulated by AvrBs3 (UPA) genes that eventually lead to hypertrophy. (B) The Rhodococcus bacteria produce cytokinin, which activates class-I KNOTTED-like homeobox genes (KNOX) that convert differentiated tissue into a meristematic state. (C) Root-knot nematode worms invade the root (a) and excrete CLE peptides that lead to the dedifferentiation and the enlargement of cells that develop into feeding cells (large cells in green) for the nematodes (b).