Cargando…
Changes in morphogen kinetics and pollen grain size are potential mechanisms of aberrant pollen aperture patterning in previously observed and novel mutants of Arabidopsis thaliana
Pollen provides an excellent system to study pattern formation at the single-cell level. Pollen surface is covered by the pollen wall exine, whose deposition is excluded from certain surface areas, the apertures, which vary between the species in their numbers, positions, and morphology. What determ...
Autores principales: | , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2019
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6394904/ https://www.ncbi.nlm.nih.gov/pubmed/30817762 http://dx.doi.org/10.1371/journal.pcbi.1006800 |
_version_ | 1783398982058246144 |
---|---|
author | Plourde, Shayne M. Amom, Prativa Tan, Michelle Dawes, Adriana T. Dobritsa, Anna A. |
author_facet | Plourde, Shayne M. Amom, Prativa Tan, Michelle Dawes, Adriana T. Dobritsa, Anna A. |
author_sort | Plourde, Shayne M. |
collection | PubMed |
description | Pollen provides an excellent system to study pattern formation at the single-cell level. Pollen surface is covered by the pollen wall exine, whose deposition is excluded from certain surface areas, the apertures, which vary between the species in their numbers, positions, and morphology. What determines aperture patterns is not understood. Arabidopsis thaliana normally develops three apertures, equally spaced along the pollen equator. However, Arabidopsis mutants whose pollen has higher ploidy and larger volume develop four or more apertures. To explore possible mechanisms responsible for aperture patterning, we developed a mathematical model based on the Gierer-Meinhardt system of equations. This model was able to recapitulate aperture patterns observed in the wild-type and higher-ploidy pollen. We then used this model to further explore geometric and kinetic factors that may influence aperture patterns and found that pollen size, as well as certain kinetic parameters, like diffusion and decay of morphogens, could play a role in formation of aperture patterns. In conjunction with mathematical modeling, we also performed a forward genetic screen in Arabidopsis and discovered two mutants with aperture patterns that had not been previously observed in this species but were predicted by our model. The macaron mutant develops a single ring-like aperture, matching the unusual ring-like pattern produced by the model. The doughnut mutant forms two pore-like apertures at the poles of the pollen grain. Further tests on these novel mutants, motivated by the modeling results, suggested the existence of an area of inhibition around apertures that prevents formation of additional apertures in their vicinity. This work demonstrates the ability of the theoretical model to help focus experimental efforts and to provide fundamental insights into an important biological process. |
format | Online Article Text |
id | pubmed-6394904 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-63949042019-03-08 Changes in morphogen kinetics and pollen grain size are potential mechanisms of aberrant pollen aperture patterning in previously observed and novel mutants of Arabidopsis thaliana Plourde, Shayne M. Amom, Prativa Tan, Michelle Dawes, Adriana T. Dobritsa, Anna A. PLoS Comput Biol Research Article Pollen provides an excellent system to study pattern formation at the single-cell level. Pollen surface is covered by the pollen wall exine, whose deposition is excluded from certain surface areas, the apertures, which vary between the species in their numbers, positions, and morphology. What determines aperture patterns is not understood. Arabidopsis thaliana normally develops three apertures, equally spaced along the pollen equator. However, Arabidopsis mutants whose pollen has higher ploidy and larger volume develop four or more apertures. To explore possible mechanisms responsible for aperture patterning, we developed a mathematical model based on the Gierer-Meinhardt system of equations. This model was able to recapitulate aperture patterns observed in the wild-type and higher-ploidy pollen. We then used this model to further explore geometric and kinetic factors that may influence aperture patterns and found that pollen size, as well as certain kinetic parameters, like diffusion and decay of morphogens, could play a role in formation of aperture patterns. In conjunction with mathematical modeling, we also performed a forward genetic screen in Arabidopsis and discovered two mutants with aperture patterns that had not been previously observed in this species but were predicted by our model. The macaron mutant develops a single ring-like aperture, matching the unusual ring-like pattern produced by the model. The doughnut mutant forms two pore-like apertures at the poles of the pollen grain. Further tests on these novel mutants, motivated by the modeling results, suggested the existence of an area of inhibition around apertures that prevents formation of additional apertures in their vicinity. This work demonstrates the ability of the theoretical model to help focus experimental efforts and to provide fundamental insights into an important biological process. Public Library of Science 2019-02-28 /pmc/articles/PMC6394904/ /pubmed/30817762 http://dx.doi.org/10.1371/journal.pcbi.1006800 Text en © 2019 Plourde et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Plourde, Shayne M. Amom, Prativa Tan, Michelle Dawes, Adriana T. Dobritsa, Anna A. Changes in morphogen kinetics and pollen grain size are potential mechanisms of aberrant pollen aperture patterning in previously observed and novel mutants of Arabidopsis thaliana |
title | Changes in morphogen kinetics and pollen grain size are potential mechanisms of aberrant pollen aperture patterning in previously observed and novel mutants of Arabidopsis thaliana |
title_full | Changes in morphogen kinetics and pollen grain size are potential mechanisms of aberrant pollen aperture patterning in previously observed and novel mutants of Arabidopsis thaliana |
title_fullStr | Changes in morphogen kinetics and pollen grain size are potential mechanisms of aberrant pollen aperture patterning in previously observed and novel mutants of Arabidopsis thaliana |
title_full_unstemmed | Changes in morphogen kinetics and pollen grain size are potential mechanisms of aberrant pollen aperture patterning in previously observed and novel mutants of Arabidopsis thaliana |
title_short | Changes in morphogen kinetics and pollen grain size are potential mechanisms of aberrant pollen aperture patterning in previously observed and novel mutants of Arabidopsis thaliana |
title_sort | changes in morphogen kinetics and pollen grain size are potential mechanisms of aberrant pollen aperture patterning in previously observed and novel mutants of arabidopsis thaliana |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6394904/ https://www.ncbi.nlm.nih.gov/pubmed/30817762 http://dx.doi.org/10.1371/journal.pcbi.1006800 |
work_keys_str_mv | AT plourdeshaynem changesinmorphogenkineticsandpollengrainsizearepotentialmechanismsofaberrantpollenaperturepatterninginpreviouslyobservedandnovelmutantsofarabidopsisthaliana AT amomprativa changesinmorphogenkineticsandpollengrainsizearepotentialmechanismsofaberrantpollenaperturepatterninginpreviouslyobservedandnovelmutantsofarabidopsisthaliana AT tanmichelle changesinmorphogenkineticsandpollengrainsizearepotentialmechanismsofaberrantpollenaperturepatterninginpreviouslyobservedandnovelmutantsofarabidopsisthaliana AT dawesadrianat changesinmorphogenkineticsandpollengrainsizearepotentialmechanismsofaberrantpollenaperturepatterninginpreviouslyobservedandnovelmutantsofarabidopsisthaliana AT dobritsaannaa changesinmorphogenkineticsandpollengrainsizearepotentialmechanismsofaberrantpollenaperturepatterninginpreviouslyobservedandnovelmutantsofarabidopsisthaliana |