Plasmodesmata and chloroplasts in integrative defense signaling

阻止传染病传播的最有效方法之一是自我隔离。然而，如果不及时进行自我隔离，疾病的传播可能会失控。在细胞水平上也是如此，无论是动物还是植物系统。一旦成功识别入侵的病原体，宿主细胞就会部署防御程序来对抗病原体。这通常涉及一种称为程序性细胞死亡的现象，这是一种有效的免疫反应。然而，如果一个细胞或一组细胞在没有与邻近细胞进行适当沟通的情况下死亡，则可能导致整个生物体的不必要死亡。因此，了解细胞如何调节细胞死亡或健康信号的传递不仅对提高我们的知识至关重要，而且有助于设计增强宿主免疫力的新方法。在植物中，各种免疫信号在叶绿体中产生，并且已知叶绿体和称为胞间连丝的细胞间桥梁对植物防御至关重要。本项目拟通过多学科研究，研究植物感染细胞如何将叶绿体免疫信号传递给胞间连丝，并与周围细胞进行通信，在正确的时间和地点差异传递死亡和健康信号。这些研究将使用最先进的活细胞成像技术和基因编码荧光传感器，将其引入叶绿体移动性或plasmodesmal功能改变的突变植物中。病原菌感染后，植物可引发超敏反应（hypersensitive response， HR），引发被感染细胞的程序性细胞死亡（programmed cell death， PCD），同时保持周围细胞的健康。HR-PCD是一种非常有效的植物免疫形式，有可能为在不严重依赖杀菌剂的情况下提高农业生产力提供新的解决方案。然而，目前尚不清楚HR-PCD如何仅被包含在感染部位内和附近的那些细胞中。在这里，研究小组提出探索HR-PCD细胞与其周围健康细胞之间的信号传递。具体来说，他们将重点关注过氧化氢（H2O2），这是HR-PCD所需的活性氧（ROS）的关键类型。研究小组将追踪细胞内叶绿体爆发的H2O2是如何通过连接HR-PCD位点内细胞和周围健康细胞的胞间连丝来限制分子运动的。主要研究目标包括：1)建立H2O2突发与PD状态之间的时间轴；2)研究PD局部H2O2爆发的可能性；3)探索HR-PCD细胞内外PD调控模式。研究小组设想首次提供高分辨率、实时的胞间连丝通透性图，显示叶绿体-胞间连丝如何在细胞内和细胞间水平发生相互作用。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。

One of the most effective ways to stop spreading a contagious disease is self-isolation. However, when self-isolation does not happen at the right timing, the spread of disease could go unruly. This is also true at the cellular level whether it concerns an animal or plant system. Upon a successful recognition of invading pathogen, host cells deploy defense programs to fight off pathogens. This often involves a phenomenon called programmed cell death, which is an effective immune response. However, if a cell or group of cells undergo cell death without appropriately communicating for neighboring cells to survive, it could result in an unwanted death of the whole organism. Therefore, understanding how cells regulate the relay of cell death or health signal is not only critical to advance our knowledge but also to help engineer new ways to boost host immunity. In plants, various immune signals are produced in chloroplasts, and it is known that both chloroplasts and the intercellular bridges called plasmodesmata are vital for plant defense. Through multi-disciplinary research proposed in this project, the research team aims to investigate how infected cells in plants might deliver chloroplastic immune signals to plasmodesmata and communicate with their surrounding cells to differentially relay death and health signals at the right time and right place. These investigations will be performed using state-of-the-art live-cell imaging techniques and genetically encoded fluorescent sensors introduced into mutant plants that are altered in chloroplasts mobility or plasmodesmal function.Upon pathogen infection, plants can elicit the hypersensitive response (HR), triggering programmed cell death (PCD) of the infected cells while preserving the health of the surrounding cells. HR-PCD is a highly effective form of plant immunity that can potentially lead to new solutions for boosting agricultural productivity without relying heavily on biocides. However, it remains unknown how HR-PCD is contained to just those cells within and near the infection sites. Here, the research team proposes to explore the signal relay between the HR-PCD cells and the healthy cells bordering them. Specifically, they will focus on hydrogen peroxide (H2O2), which is a key type of reactive oxygen species (ROS) required for HR-PCD. The team will track how the H2O2 burst from intracellular chloroplasts is delivered to restrict molecular movement through the plasmodesmata connecting cells within the HR-PCD site and healthy cells surrounding it. Major research aims include: 1) Establishing the timeline between H2O2 burst and PD status; 2) Investigating the potential of a localized H2O2 burst at PD; 3) Exploring the modes of PD regulation within and outside HR-PCD cells. The research team envisions delivering, for the first time, a high-resolution, real-time plasmodesmal permeability map displaying how chloroplast-plasmodesmata interactions may occur at the intra- and intercellular levels.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.