Stem cells serve as the source of new cells for plant development. A group of stem cells form a stem cell niche (SCN) at the root tip and in the center of the SCN are slowly dividing cells called the quiescent center (QC). QC is thought to function as a signaling hub that inhibits differentiation of surrounding stem cells. Although it has been generally assumed that cell-to-cell communication provides positional information for QC and SCN maintenance, the tools for testing this hypothesis have long been lacking. Here we exploit a system that effectively blocks plasmodesmata (PD)-mediated signaling to explore how cell-to-cell communication functions in the SCN. We showed that the symplastic signaling between the QC and adjacent cells directs the formation of local auxin maxima and establishment of AP2-domain transcription factors, PLETHORA gradients. Interestingly we found symplastic signaling is essential for local auxin biosynthesis, which acts together with auxin polar transport to provide the guidance for local auxin enrichment. Therefore, we demonstrate the crucial role of cell-to-cell communication in the SCN maintenance and further uncover a mechanism by which symplastic signaling initiates and reinforces the positional information during stem cell maintenance via auxin regulation.
Cell-to-cell communication is essential for the development and patterning of multicellular organisms. In plants, plasmodesmata (PD) provide direct routes for intercellular signaling. However, the role that PD-mediated signaling plays in plant development has not been fully investigated. To gain a comprehensive view of the role that symplastic signaling plays in Arabidopsis thaliana, we have taken advantage of a synthetic allele of CALLOSE SYNTHASE3 (icals3m) that inducibly disrupts cell-to-cell communication specifically at PD. Our results show that loss of symplastic signaling to and from the endodermis has very significant effects on the root, including an increase in the number of cell layers in the root and a misspecification of stele cells, as well as ground tissue. Surprisingly, loss of endodermal signaling also results in a loss of anisotropic elongation in all cells within the root, similar to what is seen in radially swollen mutants. Our results suggest that symplastic signals to and from the endodermis are critical in the coordinated growth and development of the root.A n enduring question in developmental biology is how cellular patterning and specification of cell fate are achieved. How are the processes of cell division, cell expansion, and cell differentiation coordinated over multiple cell distances to produce a functional organ? In plants, where nearly all cells are connected to their neighbors by plasmodesmata (PD; intercellular bridges), coordination of cellular patterning with growth and development could occur symplastically (through PD). Indeed, numerous groups have shown that proteins and RNAs are able to move between PD and that this movement is correlated with predictable changes in plant growth and development (reviewed in ref. 1). For example, in the patterning of root hairs, a mobile signal, CAPRICE (CPC) moves from the stele and from nonhair cells into the hair cells where it is sequestered by GLABRA3 to inhibit the nonhair cell fate (2-4). Likewise, during flowering, the mobile signal FLOWERING LOCUS T (FT) moves from leaf tissue into the shoot apical meristem to induce floral development (5-7). Consistent with an essential role for PD in plant development, rather mild increases or decreases in PD-mediated signaling are associated with seedling and/or embryonic lethality (e.g., INCREASED SIZE EXCUSION LIMIT 1 and 2 and GFP ARRESTED TRAFFICKING 1) (8-12). Tissue-specific defects in PD-mediated protein movement are associated with defects in stomatal patterning and spacing and defects in root patterning and cellular specification (13,14).One of the obstacles to understanding the function of PD in plant development has been a lack of tools for specifically modifying PD-mediated protein movement. There are no drugs that specifically inhibit PD-mediated protein trafficking, as there are for other processes like secretion and endocytosis. Recently, however, Vatén et al. designed a synthetic form of CALLOSE SYNTHASE 3 (icals3m) that can be used to inducibly block movement of proteins and R...
Tissue organization and pattern formation within a multicellular organism rely on coordinated cell division and cell-fate determination. In animals, cell fates are mainly determined by a cell lineage-dependent mechanism, whereas in plants, positional information is thought to be the primary determinant of cell fates. However, our understanding of cell-fate regulation in plants mostly relies on the histological and anatomical studies on Arabidopsis (Arabidopsis thaliana) roots, which contain a single layer of each cell type in nonvascular tissues. Here, we investigate the dynamic cell-fate acquisition in modified Arabidopsis roots with additional cell layers that are artificially generated by the misexpression of SHORT-ROOT (SHR). We found that cell-fate determination in Arabidopsis roots is a dimorphic cascade with lineage inheritance dominant in the early stage of pattern formation. The inherited cell identity can subsequently be removed or modified by positional information. The instruction of cell-fate conversion is not a fast readout during root development. The final identity of a cell type is determined by the synergistic contribution from multiple layers of regulation, including symplastic communication across tissues. Our findings underline the collaborative inputs during cell-fate instruction.Organogenesis in plants requires a tight spatiotemporal regulation of cell division and cell-type specification (Bennett and Scheres, 2010; ten Hove et al
Vascular tissues are surrounded by an apoplastic barrier formed of endodermis that is vital for selective absorption of water and nutrients. Lignification and suberization of endodermal cell walls are fundamental processes in establishing the apoplastic barrier. Endodermal suberization in Arabidopsis (Arabidopsis thaliana) roots is presumed to be the integration of developmental regulation and stress responses. In root endodermis, the suberization level is enhanced when the casparian strip, the lignified structure, is defective. However, it is not entirely clear how lignification and suberization interplay and how they interact with stress signaling. Here, in Arabidopsis, we constructed a hierarchical network mediated by SHORT-ROOT (SHR), a master regulator of endodermal development, and identified 13 key MYB transcription factors that form multiple sub-networks. Combined with functional analyses, we further uncovered MYB transcription factors that mediate feedback or feed-forward loops, thus balancing lignification and suberization in Arabidopsis roots. In addition, sub-networks comprising nine MYB transcription factors were identified that interact with abscisic acid (ABA) signaling to integrate stress response and root development. Our data provide insights into the mechanisms that enhance plant adaptation to changing environments.
The stomatal complex is critical for gas and water exchange between plants and the atmosphere. Originating over 400 million years ago, the structure of the stomata has evolved to facilitate the adaptation of plants to various environments. Although the molecular mechanism of stomatal development in Arabidopsis has been widely studied, the evolution of stomatal structure and its molecular regulators in different species remains to be answered. In this study, we examined stomatal development and the orthologues of Arabidopsis stomatal genes in a basal angiosperm plant, Nymphaea colorata, and a member of the eudicot CAM family, Kalanchoe laxiflora, which represent the adaptation to aquatic and drought environments, respectively. Our results showed that despite the conservation of core stomatal regulators, a number of critical genes were lost in the N. colorata genome, including EPF2, MPK6, and AP2C3 and the polarity regulators BASL and POLAR. Interestingly, this is coincident with the loss of asymmetric divisions during the stomatal development of N. colorata. In addition, we found that the guard cell in K. laxiflora is surrounded by three or four small subsidiary cells in adaxial leaf surfaces. This type of stomatal complex is formed via repeated asymmetric cell divisions and cell state transitions. This may result from the doubled or quadrupled key genes controlling stomatal development in K. laxiflora. Our results show that loss or duplication of key regulatory genes is associated with environmental adaptation of the stomatal complex.
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