Ion signaling oscillatory patterns as integrators of chemotropic responses in pollen tubes

离子信号振荡模式作为花粉管趋化反应的积分器

• 批准号: 1930165
• 负责人: Jose Feijo
• 金额: $ 90万
• 依托单位: University of Maryland, College Park
• 依托单位国家: 美国
• 项目类别: Standard Grant
• 财政年份: 2019
• 资助国家: 美国
• 起止时间: 2019-08-01 至 2023-07-31
• 项目状态: 已结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=1930165&HistoricalAwards=false
• 关键词: Ion; signaling; oscillatory; patterns; integrators

Periodic oscillations are present at all levels of biology, from ecology and circadian clocks, to neural function and molecular phenomena. Oscillatory phenomena in the minute/hour range are, however, particularly intriguing since they have important roles in cellular and organ physiology but are poorly understood in terms of mechanisms. Pollen tubes are the male gametophytes of plants, indispensable for the formation of seeds, hence food, and display conspicuous oscillations of small inorganic ions in the minute range when grown in vitro. Previous work has identified these oscillations as implied in intracellular coordination and/or cell-cell communication and this project builds on previous research supported by the National Science Foundation that resulted in the development of a suite of statistical tools to study such oscillations with quantitative precision. Besides pollen tubes, these tools are being applied to phenomena ranging from circadian clocks to astrophysics, revealing unsuspected oscillatory patterns and their underlying mechanisms. The prevalence of oscillations associated with such widespread phenomena and different areas of scientific knowledge, make them attractive topics for any STEM education program, bridging mathematics and physics with biology at various levels. This project will have extensive training opportunities for students at all levels in the quantitative analysis of these oscillations in cellular function.Pollen tubes, reach to the female gametophyte by chemotropism, which is the ability of some cells to grow towards or against an external stimuli. The present project will focus on the surprising finding that mutation of two genes coding for proteins that exchanges potassium against protons in the cell membrane of pollen tubes affect their chemotropic response to an extent that the mutant plant barely produces any seed. It thus unveils a mechanism which is essential for food production. Preliminary evidence showed that the mutant pollen tubes have distinct oscillatory "signatures", which were taken as representing information about specific aspects of cell physiology. The present project will dissect quantitatively the nature of these oscillations when challenged with various negative and positive chemotropic molecules in different genetic backgrounds. Researchers will utilize state-of-the-art methods of cell imaging, molecular genetics, biophysics and mathematical biology. The project is crafted around the hypothesis that the disturbances in proton or potassium concentration resulting from these mutations will affect cell physiology by perturbing some basal level or property of the cell membrane, namely its electric potential, which in turn will render the signaling underlining the chemotropic reaction null. This stringent theoretical framework will be tested, on one hand, through the elaboration of mathematical models that can predict the robustness of key features of cell growth and, on the other hand, by direct proof that the electric potential of the cell membrane is affected is different ways in the mutant and the wildtype pollen tubes. Maintenance of electric potential potentials through cell membrane is a vital property of all living cells and has been evolutionarily co-opted for many fundamental physiological processes, e.g. excitability in the nervous system. The major transducers of energy to create such electric potentials in nature are proton-ATPases, proteins that "pump" protons out of the cell, thus creating a pH gradient used by numerous other proteins to transport molecules into and out of cells. This project will genetically dissect the proton-ATPase family of proteins to determine the boundaries of electric potential in the cell membrane outside of which chemotropism signaling becomes mute.The widespread relevance of chemosensing in biology and the expected mechanistic advances, suggests the present project has a high potential to generate new fundamental models for understanding these phenomena by bridging cell biology, biophysics and mathematical biology.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.

周期振荡存在于生物学的各个层面，从生态学和生物钟，到神经功能和分子现象。然而，分钟/小时范围内的振荡现象特别有趣，因为它们在细胞和器官生理学中起着重要作用，但在机制方面却知之甚少。花粉管是植物的雄性配子体，对种子的形成是必不可少的，因此是食物，在离体培养时，花粉管表现出微小的无机离子振荡。先前的工作已经确定这些振荡隐含在细胞内协调和/或细胞-细胞通信中，该项目建立在美国国家科学基金会支持的先前研究的基础上，该研究开发了一套统计工具，以定量精确地研究这种振荡。除了花粉管，这些工具还被应用于从生物钟到天体物理学的各种现象，揭示了意想不到的振荡模式及其潜在机制。与这种普遍现象和不同科学知识领域相关的振荡的流行，使它们成为任何STEM教育计划的有吸引力的主题，在各个层面上架起数学和物理与生物学的桥梁。这个项目将为各个层次的学生提供大量的训练机会，以定量分析细胞功能中的这些振荡。花粉管通过趋化作用到达雌性配子体，这是一些细胞向着或反对外界刺激生长的能力。目前的项目将集中在一个令人惊讶的发现，即编码花粉管细胞膜中钾与质子交换的蛋白质的两个基因突变会影响它们的趋化反应，以至于突变植物几乎不产生任何种子。因此，它揭示了一种对粮食生产至关重要的机制。初步证据表明，突变体花粉管具有明显的振荡“特征”，这些特征被认为代表了细胞生理的特定方面的信息。本项目将定量剖析这些振荡的性质，当挑战与各种负和正的趋化分子在不同的遗传背景。研究人员将利用最先进的细胞成像、分子遗传学、生物物理学和数学生物学方法。该项目是围绕这样一个假设进行的，即由这些突变引起的质子或钾浓度的干扰将通过扰乱细胞膜的一些基础水平或特性（即其电位）来影响细胞生理学，这反过来将使趋化反应的信号通路失效。这一严格的理论框架将得到检验，一方面，通过阐述数学模型来预测细胞生长的关键特征的稳健性，另一方面，通过直接证明，在突变型和野生型花粉管中，细胞膜的电位受到不同方式的影响。通过细胞膜维持电势电位是所有活细胞的重要特性，并且在进化过程中被许多基本生理过程所选择，例如神经系统的兴奋性。在自然界中产生这种电位的主要能量传感器是质子- atp酶，这种蛋白质将质子“泵”出细胞，从而产生一种pH梯度，许多其他蛋白质利用这种梯度将分子运送进和运出细胞。该项目将对质子- atp酶家族的蛋白质进行遗传剖析，以确定细胞膜上的电位边界，在该边界外，趋化性信号变得沉默。化学传感在生物学中的广泛相关性和预期的机制进展表明，本项目具有很高的潜力，可以通过桥接细胞生物学，生物物理学和数学生物学来产生新的基本模型来理解这些现象。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

项目成果

Ethylene-independent signaling by the ethylene precursor ACC in Arabidopsis ovular pollen tube attraction

• DOI: 10.1038/s41467-020-17819-9
• 发表时间: 2020-08-14
• 期刊: NATURE COMMUNICATIONS
• 影响因子: 16.6
• 作者: Mou, Wangshu;Kao, Yun-Ting;Chang, Caren
• 通讯作者: Chang, Caren

Bioelectricity and the Control of Apical Growth in Pollen Tubes

生物电与花粉管顶端生长的控制

• DOI: 10.1089/bioe.2023.0006
• 发表时间: 2023
• 期刊: Bioelectricity
• 影响因子: 2.3
• 作者: Oliveira Nunes, Custódio de;Feijó, José A.
• 通讯作者: Feijó, José A.

Plasma membrane H+-ATPases sustain pollen tube growth and fertilization

• DOI: 10.1038/s41467-020-16253-1
• 发表时间: 2020-05-14
• 期刊: NATURE COMMUNICATIONS
• 影响因子: 16.6
• 作者: Hoffmann, Robert D.;Portes, Maria Teresa;Palmgren, Michael
• 通讯作者: Palmgren, Michael

Structure of the Arabidopsis thaliana glutamate receptor-like channel GLR3.4.

• DOI: 10.1016/j.molcel.2021.05.025
• 发表时间: 2021-08-05
• 期刊: Molecular cell
• 影响因子: 16
• 作者: Green MN;Gangwar SP;Michard E;Simon AA;Portes MT;Barbosa-Caro J;Wudick MM;Lizzio MA;Klykov O;Yelshanskaya MV;Feijó JA;Sobolevsky AI
• 通讯作者: Sobolevsky AI

Bioelectricity in Plants: From So Simple a Beginning

植物中的生物电：从如此简单的开始

• DOI: 10.1089/bioe.2023.0011.editorial
• 发表时间: 2023
• 期刊: Bioelectricity
• 影响因子: 2.3
• 作者: Feijó, José A.