EPFL Signals in the Boundary Region of the SAM Restrict Its Size and Promote Leaf Initiation

Kosentka, Pawel Z; Overholt, Alexander M; Maradiaga, Richard; Mitoubsi, Omar; Shpak, Elena D.

doi:10.1104/pp.18.00714

Cited by 40 publications

(57 citation statements)

References 71 publications

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“…However, expression was not noted in carpels of stage 8 flowers (Figure 4C, D). As previously reported 44 , EPFL2 seems to be preferentially expressed at the boundary between ovules.…”

Section: Resultssupporting

confidence: 85%

A peptide pair coordinates regular ovule initiation patterns with seed number and fruit size

Kawamoto

Carpio

Hofmann

et al. 2019

Preprint

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Ovule development in Arabidopsis thaliana involves pattern formation which ensures that ovules are regularly arranged in the pistils to reduce competition for nutrients and space. Mechanisms underlying pattern formation in plants, such as phyllotaxis, flower morphogenesis or lateral root initiation, have been extensively studied, and genes controlling the initiation of ovules have been identified. However, how a regular spacing of ovules is achieved is not known. Using natural variation analysis combined with quantitative trait locus analysis, we found that the spacing of ovules in the developing fruits is controlled by two secreted peptides, EPFL2 and EPFL9 (also known as Stomagen), and their receptors from the ERECTA (ER) family that act from the carpel wall and the placental tissue. We found that a signalling pathway controlled by EPFL9 acting from the carpel wall through the LRR-receptor kinases ER, ERL1 and ERL2 promotes fruit growth. Regular spacing of ovules depends on EPFL2 expression in the carpel wall and in the inter-ovule spaces, where it acts through ERL1 and ERL2. Loss of EPFL2 signalling results in shorter fruits and irregular spacing of ovules or even ovule twinning. The EPFL2 expression pattern between ovules is under negative-feedback regulation by auxin, which accumulates in the arising ovule primordia. We propose that the auxin-EPFL2 signalling module evolved to control the initiation and regular, equidistant spacing of ovule primordia, which serves to minimise competition between developing seeds. Together, EPFL2 and EPFL9 coordinate ovule patterning and thereby seed number with fruit growth through a set of shared receptors.

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“…However, expression was not noted in carpels of stage 8 flowers (Figure 4C, D). As previously reported 44 , EPFL2 seems to be preferentially expressed at the boundary between ovules.…”

Section: Resultssupporting

confidence: 85%

A peptide pair coordinates regular ovule initiation patterns with seed number and fruit size

Kawamoto

Carpio

Hofmann

et al. 2019

Preprint

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“…In [42] it is discussed that a dose-dependent inhibitory effect of WUS on proliferation rates may play a role in this context. Furthermore, ERECTA signalling may be involved in confining the WUS and CLV3 expression to the meristem centre by repressing both signals [48,49]. These mechanisms could be compared in future extension of our model.…”

Section: Discussionmentioning

confidence: 98%

Mathematical modeling of plant cell fate transitions controlled by hormonal signals

Klawe

Stiehl

Bastian

et al. 2019

Preprint

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Coordination of fate transition and cell division is crucial to maintain the plant architecture and to achieve efficient production of plant organs. In this paper, we analysed the stem cell dynamics at the shoot apical meristem (SAM) that is one of the plant stem cells locations. We designed a mathematical model to elucidate the impact of hormonal signaling on the fate transition rates between different zones corresponding to slowly dividing stem cells and fast dividing transit amplifying cells. The model is based on a simplified two-dimensional disc geometry of the SAM and accounts for a continuous displacement towards the periphery of cells produced in the central zone. Coupling growth and hormonal signaling results in a nonlinear system of reaction-diffusion equations on a growing domain with the growth velocity depending on the model components. The model is tested by simulating perturbations in the level of key transcription factors that maintain SAM homeostasis. The model provides new insights on how the transcription factor HECATE is integrated in the regulatory network that governs stem cell differentiation. 1 SummaryPlants continuously generate new organs such as leaves, roots and flowers. This process is driven by stem cells which are located in specialized regions, so-called meristems. Dividing stem cells give rise to offspring that, during a process referred to as cell fate transition, become more specialized and give rise to organs. Plant architecture and crop yield crucially depend on the regulation of meristem dynamics. To better understand this regulation, we develop a computational model of the shoot meristem. The model describes the meristem as a two-dimensional disk that can grow and shrink over time, depending on the concentrations of the signalling factors in its interior. This allows studying how the non-linear interaction of multiple transcription factors is linked to cell division and fate-transition. We test the model by simulating perturbations of meristem signals and comparing them to experimental data. The model allows simulating different hypotheses about signal effects. Based on the model we study the specific role of the transcription factor HECATE and provide new insights in its action on cell dynamics and in its interrelation with other known transcription factors in the meristem. 4 ing molecules. Such models have been applied e.g., to investigate cytokinin signaling [11] and patterning of the shoot apical meristem [14,17]. To investigate the impact of HEC on fate transition and proliferation rates of cells in the CZ and PZ, we have recently proposed a model based on the population dynamics approach, in which dynamics of different cell subpopulations are described by ordinary differential equations [9]. Such approach allows tracking how changes in cell proliferation, fate transition, primordia formation and primordia separation affect the time evolution and steady-state size of the different SAM zones but does not take into account spatio-temporal dynamics of the underlying signal...

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“…In contrast, in A. thaliana the close homologs EPFL4 and EPFL6 have been shown to have distinct functions in inflorescence growth 62 , 63 . However, two very recent studies revealed that EPFL4 and EPFL6 are also expressed in the periphery of the shoot apical meristem (SAM) and function redundantly with EPFL1 and EPFL2 to regulate the meristem size and leaf initiation 64 , 65 . In particular, signaling downstream of EFPL ligands and their receptors confines the WUS-CLV3 pathway to the center of the SAM by inhibiting its expression in the meristem periphery 65 .…”

Section: Resultsmentioning

confidence: 99%

Transcriptome profiling and weighted gene co-expression network analysis of early floral development in Aquilegia coerulea

Min

Kramer

2020

Sci Rep

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The earliest phases of floral development include a number of crucial processes that lay the foundation for the subsequent morphogenesis of floral organs and success in reproduction. Currently, key transcriptional changes during this developmental window have been characterized in the model species Arabidopsis thaliana, but little is known about how transcriptional dynamics change over the course of these developmental processes in other plant systems. Here, we have conducted the first in-depth transcriptome profiling of early floral development in Aquilegia at four finely dissected developmental stages, with eight biological replicates per stage. Using differential gene expression analysis and weighted gene co-expression network analysis, we identified both crucial genes whose expression changes mark the transitions between developmental stages and hub genes in co-expression modules. Our results support the potential functional conservation of key genes in early floral development that have been identified in other systems, but also reveal a number of previously unknown or overlooked loci that are worthy of further investigation. In addition, our results highlight not only the dynamics of transcriptional regulation during early floral development, but also the potential involvement of the complex, essential networks of small RNA and post-translational regulation to these developmental stages.

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EPFL Signals in the Boundary Region of the SAM Restrict Its Size and Promote Leaf Initiation

Cited by 40 publications

References 71 publications

A peptide pair coordinates regular ovule initiation patterns with seed number and fruit size

A peptide pair coordinates regular ovule initiation patterns with seed number and fruit size

Mathematical modeling of plant cell fate transitions controlled by hormonal signals

Transcriptome profiling and weighted gene co-expression network analysis of early floral development in Aquilegia coerulea

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