The higher-plant shoot meristem is a dynamic structure whose maintenance depends on the coordination of two antagonistic processes, organ initiation and self-renewal of the stem cell population. In Arabidopsis shoot and floral meristems, the WUSCHEL (WUS) gene is required for stem cell identity, whereas the CLAVATA1, 2, and 3 (CLV) genes promote organ initiation. Our analysis of the interactions between these key regulators indicates that (1) the CLV genes repress WUS at the transcript level and that (2) WUS expression is sufficient to induce meristem cell identity and the expression of the stem cell marker CLV3. Our data suggest that the shoot meristem has properties of a self-regulatory system in which WUS/CLV interactions establish a feedback loop between the stem cells and the underlying organizing center.
The shoot meristem gives rise to the aerial parts of higher plants by continuously initiating new organs. The basis of this activity is its ability to maintain a pool of pluripotent stem cells, which are the ultimate source of all tissues of the shoot. In Arabidopsis plants mutant for the WUSCHEL (WUS) gene, the stem cells are misspecified and appear to undergo differentiation. Here, we show that WUS encodes a novel homeodomain protein which presumably acts as a transcriptional regulator. The pattern of WUS expression suggests that stem cells in the shoot meristem are specified by an underlying cell group which is established in the 16-cell embryo and becomes localized to its prospective domain of function by asymmetric cell divisions.
Throughout the lifespan of a plant, which in some cases can last more than one thousand years, the stem cell niches in the root and shoot apical meristems provide cells for the formation of complete root and shoot systems, respectively. Both niches are superficially different and it has remained unclear whether common regulatory mechanisms exist. Here we address whether root and shoot meristems use related factors for stem cell maintenance. In the root niche the quiescent centre cells, surrounded by the stem cells, express the homeobox gene WOX5 (WUSCHEL-RELATED HOMEOBOX 5), a homologue of the WUSCHEL (WUS) gene that non-cell-autonomously maintains stem cells in the shoot meristem. Loss of WOX5 function in the root meristem stem cell niche causes terminal differentiation in distal stem cells and, redundantly with other regulators, also provokes differentiation of the proximal meristem. Conversely, gain of WOX5 function blocks differentiation of distal stem cell descendents that normally differentiate. Importantly, both WOX5 and WUS maintain stem cells in either a root or shoot context. Together, our data indicate that stem cell maintenance signalling in both meristems employs related regulators.
During embryonic pattern formation, the main body axes are established and cells of different developmental fates are specified from a single-cell zygote. Despite the fundamental importance of this process, in plants, the underlying mechanisms are largely unknown. We show that expression dynamics of novel WOX (WUSCHEL related homeobox) gene family members reveal early embryonic patterning events in Arabidopsis. WOX2 and WOX8 are co-expressed in the egg cell and zygote and become confined to the apical and basal daughter cells of the zygote, respectively, by its asymmetric division. WOX2 not only marks apical descendants of the zygote, but is also functionally required for their correct development,suggesting that the asymmetric division of the plant zygote separates determinants of apical and basal cell fates. WOX9 expression is initiated in the basal daughter cell of the zygote and subsequently shifts into the descendants of the apical daughter apparently in response to signaling from the embryo proper. Expression of WOX5 shows that identity of the quiescent center is initiated very early in the hypophyseal cell, and highlights molecular and developmental similarities between the stem cell niches of root and shoot meristems. Together, our data suggest that during plant embryogenesis region-specific transcription programs are initiated very early in single precursor cells and that WOX genes play an important role in this process.
Floral meristems and shoot apical meristems (SAMs) are homologous, self-maintaining stem cell systems. Unlike SAMs, floral meristems are determinate, and stem cell maintenance is abolished once all floral organs are initiated. To investigate the underlying regulatory mechanisms, we analyzed the interactions between WUSCHEL (WUS), which specifies stem cell identity, and AGAMOUS (AG), which is required for floral determinacy. Our results show that repression of WUS by AG is essential for terminating the floral meristem and that WUS can induce AG expression in developing flowers. Together, this suggests that floral determinacy depends on a negative autoregulatory mechanism involving WUS and AG, which terminates stem cell maintenance.
Axis formation is one of the earliest patterning events in plant and animal embryogenesis. In Arabidopsis, the main axis of the embryo is evident at the asymmetric division of the zygote into a small, embryonic apical cell and a large extraembryonic basal cell. Here we show that the homeobox genes WOX2 and WOX8, which are initially coexpressed in the zygote, act as complementary cell fate regulators in the apical and basal lineage, respectively. Furthermore, WOX8 expression in the basal cell lineage is required for WOX2 expression and normal development of the proembryo, suggesting an inductive mechanism. The identified WOX cascade is required for normal expression of a reporter gene of the auxin efflux carrier PIN1 and for the formation of auxin response maxima in the proembryo. Thus, our results link the spatial separation of WOX transcription factors to localized auxin response and the formation of the main body axis in the embryo.
The function of the SHOOT MERISTEMLESS (STM) gene in shoot and floral meristems throughout Arabidopsis development has been analyzed. The results show that STM plays a major role in maintaining shoot and floral meristems. In an allelic series of stm mutants the shoot meristem was either reduced or completely absent in mature embryos and mutant seedling cotyledons showed partial fusion, indicating that the STM gene affects embryonic shoot meristem development and spacing of cotyledons. Postembryonically, stm mutants initiated adventitious shoot development at a position corresponding to the shoot meristem in wild-type. Repetitively initiated defective mutant shoot and floral meristems were consumed during primordia formation and typically terminated prematurely in fused ectopic primordia, indicating that STM is required for continuous shoot and floral meristem function. Analogous defects were observed in stm embryonic and postembryonic development suggesting that similar mechanisms are employed in embryonic and postembryonic organ primordia initiation. Allelic combination suggest different thresholds for STM requirement during plant development. STM requirement could not be bypassed by standard growth factor regimes or by shoot regeneration from calli. The results suggest that STM functions by preventing incorporation of cells in the meristem center into differentiating organ primordia and that this role can completely account for all defects observed in stm mutants. Mutations in the WUSCHEL (WUS) and ZWILLE (ZLL) genes result in defective organization and premature termination of shoot meristems. Genetic interactions between STM, WUS and ZLL were analyzed and the results indicate that STM acts upstream of WUS and ZLL. Therefore, while STM appears to function in keeping central meristem cells undifferentiated, WUS and ZLL seem to be subsequently required for proper function of these cells.
During leaf development in flowering plants, adaxial (upper) and abaxial (lower) side-specific genes are responsible for blade outgrowth, which takes places predominantly in the lateral direction, and for margin development as well as differentiation of adaxial and abaxial tissues. However, the underlying mechanisms are poorly understood. Here, we show that two WUSCHEL-RELATED HOMEOBOX (WOX) genes, PRESSED FLOWER (PRS)/WOX3 and WOX1, encoding homeobox transcription factors, act in blade outgrowth and margin development downstream of adaxial/abaxial polarity establishment. The expression of PRS and WOX1 defines a hitherto undescribed middle domain, including two middle mesophyll layers and the margin, as a center that organizes the outgrowth of leaf blades. The expression of PRS and WOX1 is repressed in the abaxial leaf domain by the abaxial-specific transcription factor KANADI. Furthermore, PRS and WOX1 coordinate adaxial/abaxial patterning together with adaxial-and abaxial-specific genes. Our data suggest a model of blade outgrowth and adaxial/abaxial patterning via the middle domain-specific WOX genes in Arabidopsis thaliana leaves.
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