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

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
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DOI:
10.1371/journal.pcbi.1006800
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发表时间:
2019-02-01
影响因子:
4.3
通讯作者:
Dobritsa, Anna A.
Dobritsa, Anna A.
中科院分区:
生物学2区
文献类型:
--
作者:
Plourde, Shayne M.;Amom, Prativa;Dobritsa, Anna A.

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花粉提供了一个很好的系统来研究单细胞水平上的图案形成。花粉表面由花粉壁外壁覆盖,其沉积被排除在某些表面积之外,这些表面积在物种之间在数量,位置和形态上有所不同。是什么决定了孔径模式还不清楚。拟南芥通常发育三个孔,沿着花粉赤道等距分布。然而,拟南芥突变体的花粉具有更高的倍性和更大的体积发展四个或更多的孔。为了探索可能的机制负责光圈图案,我们开发了一个数学模型的基础上的Gierer-Meinhardt方程组。该模型能够概括在野生型和高倍性花粉中观察到的孔径模式。然后,我们使用这个模型,进一步探讨几何和动力学因素,可能会影响孔径图案,并发现花粉大小,以及某些动力学参数,如扩散和衰减的形态发生剂,可以发挥作用,在孔径图案的形成。结合数学建模,我们还在拟南芥中进行了正向遗传筛选,发现了两个突变体,其孔径模式以前在该物种中没有观察到,但我们的模型预测。马卡龙突变体形成了一个单一的环状孔,与模型产生的不寻常的环状图案相匹配。甜甜圈突变体在花粉粒的两极形成两个孔状孔。对这些新的突变体的进一步测试,由建模结果的动机,建议存在的抑制孔周围的区域,防止在其附近形成额外的孔。这项工作证明了理论模型的能力,以帮助集中实验工作,并提供一个重要的生物过程的基本见解。
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.