Organ geometry channels cell fate in the Arabidopsis ovule primordium
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Curated by eLife
Evaluation Summary:
The authors use imaging analysis of Arabidopsis developing ovule primordia until the onset of meiosis to clarify the importance of organ morphogenesis in cell fate. They first document the growth of ovule cells in three dimensions, then use computational modelling to predict factors underlying ovule growth, shape and spore mother cell (SMC) differentiation. They test this model through analysis of a mutant of Katanin, encoding a microtubule-severing protein. Overall, this work is elegant, adds new information and confirms previous hypotheses for the field. A well appreciated feature of this paper is OvuleViz, an R-based software tool that they developed, which will provide a consistent way for others to analyze mutants with similar phenotypic abnormalities.
(This preprint has been reviewed by eLife. We include the joint public review from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
In multicellular organisms, sexual reproduction requires the separation of the germline from the soma. In flowering plants, the first cells of the germline, so-called spore mother cells (SMCs), differentiate as the reproductive organs form. Here, we explored how organ growth influences and contributes to SMC differentiation. We generated a collection of 92 annotated 3D images capturing ovule primordium ontogeny at cellular resolution in Arabidopsis. We identified a spatio-temporal pattern of cell divisions that acts in a domain-specific manner as the primordium forms, which is coupled with the emergence of a single SMC. Using tissue growth models, we uncovered plausible morphogenetic principles involving a spatially confined growth signal, differential mechanical properties, and cell growth anisotropy. Our analysis also reveals that SMC characteristics first arise in more than one cell but SMC fate becomes progressively restricted to a single cell during organ growth. Altered primordium geometry coincided with a delay in this fate restriction process in katanin mutants. Altogether, our study suggests that tissue geometry canalizes and modulates reproductive cell fate in the Arabidopsis ovule primordium.
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Joint Public Review:
This is an elegant study that delves into germline initiation and ovule development at a resolution not previously reported. The topic is of general significance for developmental biologists, and particularly interesting for groups studying the basis for germline development. Using a multitude of assays, starting from 3D segmentation analysis, progressing to modelling, reporter line analysis and mutant characterization, the authors document cellular components of ovule primordium growth and uncover new aspects of spore mother cell (SMC) emergence, in which ovule geometry appears to play a relevant role. The authors concluded that anisotropic growth is one of important factors to drive overall development of ovules, especially in Phase I, and that the L1 dome and the basal domain, but not the SMC and neighboring L2 …
Joint Public Review:
This is an elegant study that delves into germline initiation and ovule development at a resolution not previously reported. The topic is of general significance for developmental biologists, and particularly interesting for groups studying the basis for germline development. Using a multitude of assays, starting from 3D segmentation analysis, progressing to modelling, reporter line analysis and mutant characterization, the authors document cellular components of ovule primordium growth and uncover new aspects of spore mother cell (SMC) emergence, in which ovule geometry appears to play a relevant role. The authors concluded that anisotropic growth is one of important factors to drive overall development of ovules, especially in Phase I, and that the L1 dome and the basal domain, but not the SMC and neighboring L2 companion cells, are consecutive sites of cell proliferation, thus contributing to morphological changes of ovules in Phases I and II. In terms of novelty, this work identified growth principles conducive to ovule primordium growth, added a layer of complexity to the nucellar epidermis towards SMC specification, and provided a new concept of SMC development: SMC fate emergence and SMC singleness resolution, where cell geometry plays a very active role
The katanin mutant is an interesting choice since it has been reported previously to impact cell growth. As expected, in katanin mutants, the primordium became enlarged in size and was more isotropic (lower height/width ratio) in shape. A reduced anisotropy also induced aberrant enlargement of SMC companion L2 cells in katanin mutant ovules. From PCNA and CYCB1.1 expression patterns, which are S- and M-phase markers, respectively, the authors found that the SMC precursor and its companion cells showed a highly frequent S-phase pattern. Taken together with infrequent divisions, the SMC and its neighbors have properties distinct to other ovular cells in longer S-phase duration. In addition, SMC singleness was suggested to be determined partly by Katanin-dependent anisotropic condition.
The claims made through the work are well documented and supported. In terms of experimental clarity and composition, the authors describe very well how the samples were obtained/how they were named, the statistical analysis appears robust and well described, and several of the markers analyzed provide a comprehensive landscape of what is occurring in the ectopic cells.
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Evaluation Summary:
The authors use imaging analysis of Arabidopsis developing ovule primordia until the onset of meiosis to clarify the importance of organ morphogenesis in cell fate. They first document the growth of ovule cells in three dimensions, then use computational modelling to predict factors underlying ovule growth, shape and spore mother cell (SMC) differentiation. They test this model through analysis of a mutant of Katanin, encoding a microtubule-severing protein. Overall, this work is elegant, adds new information and confirms previous hypotheses for the field. A well appreciated feature of this paper is OvuleViz, an R-based software tool that they developed, which will provide a consistent way for others to analyze mutants with similar phenotypic abnormalities.
(This preprint has been reviewed by eLife. We include the …
Evaluation Summary:
The authors use imaging analysis of Arabidopsis developing ovule primordia until the onset of meiosis to clarify the importance of organ morphogenesis in cell fate. They first document the growth of ovule cells in three dimensions, then use computational modelling to predict factors underlying ovule growth, shape and spore mother cell (SMC) differentiation. They test this model through analysis of a mutant of Katanin, encoding a microtubule-severing protein. Overall, this work is elegant, adds new information and confirms previous hypotheses for the field. A well appreciated feature of this paper is OvuleViz, an R-based software tool that they developed, which will provide a consistent way for others to analyze mutants with similar phenotypic abnormalities.
(This preprint has been reviewed by eLife. We include the joint public review from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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