Functional Modules in the Meristems: "Tinkering" in Action

Abstract

Background: A feature of higher plants is the modular principle of body organisation. One of these conservative morphological modules that regulate plant growth, histogenesis and organogenesis is meristems-structures that contain pools of stem cells and are generally organised according to a common principle. Basic content: The development of meristems is under the regulation of molecular modules that contain conservative interacting components and modulate the expression of target genes depending on the developmental context. In this review, we focus on two molecular modules that act in different types of meristems. The WOX-CLAVATA module, which includes the peptide ligand, its receptor and the target transcription factor, is responsible for the formation and control of the activity of all meristem types studied, but it has its own peculiarities in different meristems. Another regulatory module is the so-called florigen-activated complex, which is responsible for the phase transition in the shoot vegetative meristem (e.g., from the vegetative shoot apical meristem to the inflorescence meristem).

Conclusions: The review considers the composition and functions of these two functional modules in different developmental programmes, as well as their appearance, evolution and use in plant breeding.

Keywords: evo-devo; functional module; land plants; meristem; peptide/protein ligand; phase transition; regulation of transcription.

Figure 1

Examples of functional modules operating in meristems. A functional model could include (1) a peptide ligand and its receptor, (2) transcription factors, their cofactors and target genes, and (3) small RNAs and their target transcripts. Simpler modules can be combined into a more complex one, such as the WOX-CLAVATA module, including the mobile signalling peptides CLE, their receptors, LRR-RLKs, and the target genes encoding TFs of the WOX family, some of which could regulate the CLE gene expression through a feedback mechanism.

Figure 2

The WOX-CLAVATA module in the control of three major meristems. Left—zonation of meristems; middle—components of WOX-CLAVATA systems and other ways of regulating WOX expression; right—targets of WOX TFs. The obligate parts of the SAM, RAM and the cambium are the stem cell pool (SC) and the organising centre (OC). In the SAM and RAM, these parts represent local groups of cells, and in the cambium—cell layers. The WOX-CLAVATA system is a complex regulatory module involving the same families of proteins operating in different meristems. The WOX transcription factors (TFs), WUS in the SAM, WOX5 in the RAM, and WOX4 and WOX14 in the cambium, regulate OC maintenance and repression of SC differentiation. The expression levels of the WOX genes are controlled by CLE peptides and their receptors: the CLV3 and CLE40 peptides and their receptors CLV1 and BAM1 in the SAM, the CLE40 peptide and its receptors ACR4 and CLV1 in the RAM, and the CLE41/42/44 peptides and the PXY family receptors in the cambium. There are also transcriptional regulators which control WOX expression: ROW1 in the SAM and RAM, the complex SCR-TCP20/21-PLT1/3 in the RAM and certain ARFs and HD-ZIPIIIs in the cambium. An additional target of the PXY receptor, GSK3 kinase, was found in the cambium. The WOX TFs have different direct target genes in the meristems (see details in the text). To modulate their binding efficiency to their promoters, the WOX TFs can form homodimers or interact with other TFs: e.g., the STM TF enhances the binding of the WUS TF to the promoter of CLV3, while the HAM family TFs in the whole meristem and PLT3 in the RAM block the mobility of the WOX proteins.

Figure 3

Scheme illustrating the role of alternative FAC-like complexes in the phase transitions of vegetative SAM. The FAC is a hexameric complex consisting of two molecules of FT-like mobile proteins; two molecules of 14-3-3 family proteins, conservative molecular adaptors; and two molecules of the FD transcription factor. This complex binds to G-box-containing motifs (CCACGTGG) in the promoters of target genes. During flowering induction, FT, as part of the FAC, acts as a co-activator of target genes responsible for the floral meristem development (AP1, LFY, SOC1). The TFL1 (“antiflorigen”) acts as a transcriptional co-repressor when it replaces FT in the FAC complex. In poplar, bud dormancy release is activated by FT in the complex with 14-3-3 and FD proteins (StFDL1), whereas CEN1, a TFL1-like poplar protein, inhibits this process. Potato tuber formation is stimulated by the FT-like protein SP6A, which forms a complex with the 14-3-3 and FD proteins (known as tuberigen-activating complex), whereas another FT-like protein, SP5G, suppresses tuber formation by inhibiting the action of SP6A. The induction of tuber formation in Allium cepa is stimulated by the FT-like protein AcFT1. This process is suppressed by another FT-like protein, AcFT4, and it is proposed that these proteins form alternative complexes with the 14-3-3 proteins and the FD TF and probably with other partners.

Figure 4

Proposed scheme for the evolutionary acquisition of the WOX-CLAVATA and FAC modules in land plants. Bryophytes: The only meristem is the unicellular gametophytic SAM. In liverworts and hornworts, two types of CLEs (TDIF and R-CLE) regulate the gametophytic SAM development in opposite directions and bind to PXY-like and BAM-like receptors, respectively. The TDIF lineage is lost in mosses. In all bryophytes, WOX do not play a role in SAM development. Lycophytes: Acquisition of vasculature and RAM; multicellular SAM and RAM in Lycopodiacea and Isoetacea. Monilophytes: unicellular SAM and RAM. In Lycophytes and Monilophytes, the TDIF-TDR pathway regulates vascular system, and R-CLEs stimulate SAM and RAM activity via PXY-like and BAM-like receptors. T3-type WOX is expressed in the RAM and vasculature, but not in the SAM. TDIF-PXY and R-CLE-BAMs are thought to be associated with T3WOX in the vasculature and RAM. Gymnosperms: Seed capture. Only multicellular SAM and RAM. T3 WOXs are expressed in the SAM, RAM and cambium; WOX4 regulates cambium, WUS/WOX5 in some species or separate WUS and WOX5 in others—SAM and RAM. TDIF-TDR signalling regulates cambium; R-CLEs stimulate SAM and RAM activity via PXY-like and BAM-like receptors. Presumably, this regulation is mediated by WUS/WOX5 pro-ortholog. Angiosperms: Flower acquisition. Only multicellular SAM and RAM. TDIF-TDR-WOX4 signalling regulates cambium, CLE40-CLV1/ACR4-WOX5—RAM; CLV3-CLV1-WUS and CLE40-BAM-X-WUS alternatively regulate SAM.