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Shpak, E. D.

Publications and source records attributed to Shpak, E. D..

4 recordsLinked to original sources

ERECTA family signaling controls cell fate specification during ovule initiation in Arabidopsis.

The number of seeds produced by a plant depends on the number of ovules initiated within the carpels by a meristematic tissue, the placenta. Previous studies indicated that ERECTA-LIKE1 (ERL1) and ERL2 receptors and their extracellular ligand EPIDERMAL PATTERNING FACTOR-LIKE2 (EPFL2) promote seed density while ERECTA inhibits it. Here, we show that all three receptors and two ligands, EPFL1 and EPFL2, promote ovule initiation. After initiation, EPFL1 and EPFL2 redundantly regulate the elongation of nascent ovules and promote the growth of the funiculus. The synergy of EPFL1 and EPFL2 with CUP-SHAPED COTYLEDON boundary genes in the regulation of ovule number and shape suggests cooperation in their function. Ovule initiation starts with the specification of ovule founder cells that are separated by boundary cells. During ovule bulging, a new cell type, characterized by a high proliferative rate, forms between ovule founder and boundary cells. In the epfl1 epfl2 mutant, marker genes for ovule founder and boundary cells are expressed much more broadly. Our data indicate that ERECTA family signaling is necessary for efficient cell fate separation at the earliest stages of ovule initiation. Later, it promotes the formation of a zone of high proliferation at the base of the ovule.

plant biology↗

An updated model of shoot apical meristem regulation by ERECTA family and CLAVATA3 signaling pathways

The shoot apical meristem (SAM) gives rise to above-ground organs. The size of the SAM is relatively constant due to the balance of stem cell replenishment versus cell recruitment into developing organs. In angiosperms, the transcription factor WUSCHEL (WUS) promotes stem cell identity in the central zone of the SAM. WUS forms a negative feedback loop with a signaling pathway activated by CLAVATA3 (CLV3). In the periphery of the SAM, the ERECTA family (ERf) receptors promote cell differentiation and constrain the expression of WUS and CLV3. Here, we show that four ligands of ERfs redundantly inhibit CLV3 and WUS expression. Transcriptome analysis confirmed that WUS and CLV3 are the main targets of ERf signaling and uncovered several new ones. Analysis of promoter reporters indicated that in the vegetative meristem, the WUS expression domain mostly overlapped with the CLV3 domain and did not shift along the apical-basal axis in clv3. A 3D mathematical model reproduced the experimentally observed CLV3 and WUS expression patterns with fewer assumptions than earlier models. Based on these findings, we propose that CLV3 regulates cellular levels of WUS expression through autocrine signaling, while ERfs regulate WUS spatial expression, preventing its encroachment into the peripheral zone. One Sentence SummaryThrough autocrine signaling, CLV3 regulates the level of WUS expression in the vegetative SAM but not its location, while ERfs regulate the WUS spatial pattern, preventing its expansion into the peripheral zone.

plant biology↗

Initiation of aboveground organ primordia depends on combined action of auxin, ERECTA family genes, and PINOID.

Leaves and flowers are produced by the shoot apical meristem (SAM) at a certain distance from its center, a process that requires the hormone auxin. The amount of auxin and the pattern of its distribution in the initiation zone determine the size and spatial arrangement of organ primordia. Auxin gradients in the SAM are formed by PIN-FORMED (PIN) auxin efflux carriers whose polar localization in the plasma membrane depends on the protein kinase PINOID (PID). Previous work determined that ERECTA family genes (ERfs) control initiation of leaves. ERfs are plasma membrane receptors that enable cell-to-cell communications by sensing extracellular small proteins from Epidermal Patterning Factor/EPF-like (EPF/EPFL) family. Here, we investigate whether ERfs regulate initiation of organs by altering auxin distribution or signaling. Genetic and pharmacological data suggest that ERfs do not regulate organogenesis through PINs while transcriptomics data show ERfs do not alter primary transcriptional responses to auxin. Our results indicate that in the absence of ERf signaling, the peripheral zone cells inefficiently initiate leaves in response to auxin signals and that increased accumulation of auxin in the er erl1 erl2 SAM can partially rescue organ initiation defects. We propose that both auxin and ERfs are essential for leaf initiation, and that they have common downstream targets. Genetic data also indicate that the role of PID in initiation of cotyledons and leaves cannot be attributed solely to regulation of PIN polarity, and PID is likely to have other functions in addition to regulation of auxin distribution. Summary statementAuxin is unable to promote cotyledon and leaf initiation in the absence of signaling by ERECTA family receptor kinases and the kinase PINOID.

plant biology↗

ERECTA family signaling constrains CLAVATA3 and WUSCHEL to the center of the shoot apical meristem.

The shoot apical meristem (SAM) is a reservoir of stem cells that gives rise to all post-embryonic aboveground plant organs. The size of the SAM remains stable over time due to a precise balance of stem cell replenishment versus cell incorporation into organ primordia. The WUSCHEL (WUS)/CLAVATA (CLV) negative feedback loop is central to SAM size regulation. Its correct function depends on accurate spatial expression of WUS and CLV3. A signaling pathway, consisting of ERECTA family (ERf) receptors and EPIDERMAL PATTERNING FACTOR LIKE (EPFL) ligands, restricts SAM width and promotes leaf initiation. While ERf receptors are expressed throughout the SAM, EPFL ligands are expressed in its periphery. Our genetic analysis demonstrated that ERfs and CLV3 synergistically regulate the size of the SAM, and wus is epistatic to erfs. Furthermore, activation of ERf signaling with exogenous EPFLs resulted in a rapid decrease of CLV3 and WUS expression. ERf-EPFL signaling inhibits expression of WUS and CLV3 in the periphery of the SAM, confining them to the center. These findings establish the molecular mechanism for stem cell positioning along the radial axis. Summary statementERf signaling restricts the width of the shoot apical meristem, a structure which generates aboveground plant organs, by inhibiting expression of two principal regulators, CLV3 and WUS, at its periphery.

developmental biology↗