Mechanisms of Pathogenicity and Host Specificity of the Oomycete Plant Pathogen Phytophthora palmivora

棕榈疫霉菌是一种类似真菌的真核微生物，会导致许多农业和生态上重要植物的毁灭性疾病，包括可可，这是一种热带多年生树木，是价值数十亿美元的巧克力产业的主要组成部分。全球每年因棕榈食性疫病造成的可可损失至少10亿美元。作为一种侵袭性很强的病原菌，棕榈疫霉通常能够侵染寄主的几乎所有植物部位，这使得它的控制变得极其困难。因此，它对农业生产和生态系统构成了越来越大的威胁。棕榈疫霉菌引起的疾病是通过频繁使用杀菌剂来控制的，但收效甚微。该项目的长期目标是在对棕榈原虫感染机制的基本了解的基础上，开发新的、有效的和环境友好的策略来控制棕榈食性巴氏杆菌。为此，本项目的具体目标是确定棕榈食性巴氏杆菌的关键致病因素，这些因素如何作用于植物细胞成分而导致疾病，以及它们在棕榈食性巴氏杆菌分离物中的存在/缺失如何决定感染哪些植物物种。该项目预计将产生对制定合乎需要的疾病控制措施至关重要的重要基础知识，从而大大促进粮食安全、自然生态系统的可持续性和生物经济。此外，该项目将通过向研究生、本科生和高中生提供培训机会，并向初中/高中教师介绍植物病理学和基因编辑技术，以吸引新一代进入农业和生命科学，从而促进STEM劳动力的可持续性。卵菌形成了真核生物独特的系统发育谱系，许多真核生物会导致植物和动物的毁灭性疾病。棕榈疫霉菌是一种侵染范围广的卵菌类植物病原菌，具有寄主专一性。棕榈食单胞菌提供了一系列不同的效应器来操纵宿主细胞的过程以促进感染，包括RxLR效应器超家族，它由一个N端信号肽和一个规范的RxLR(或RxLR-EER)易位基序组成，介导进入宿主细胞。棕榈疫霉RxLR效应子PpalRxLR1含有一个具有潜在DNA结合活性的功能性核定位信号，是可可致病的关键因子。在从可可感染中获得的所有被检查的棕榈食性巴氏杆菌分离株中都存在它，但在整个物种中表现出存在/不存在的多态，这表明它可能是宿主范围和特异性的决定因素。本研究的目的是：1)通过测定PpalRxLR1在可可上的核定位分子相互作用动力学和被颠覆的寄主细胞过程，确定其致病机制；2)通过分析PpalRxLR1相对于物种的进化和与寄主范围的关联，确定PpalRxLR1在棕榈疫霉寄主范围进化中的关键作用；3)利用棕榈疫霉分离物的自然变异，识别在特定或广泛寄主上致病的其他关键效应物。跨特定目标的整合有望改变对棕榈食性疫霉致病性和寄主范围进化的分子基础的理解，这是植物与微生物相互作用的关键方面。这一奖项反映了NSF的法定使命，并通过使用基金会的智力优势和更广泛的影响审查标准进行评估，被认为值得支持。

Phytophthora palmivora is a fungus-like eukaryotic microorganism that causes devastating diseases of numerous agriculturally and ecologically important plants, including cacao, a tropical perennial tree that produces the major component of the multi-billion-dollar chocolate industry. The annual global loss on cacao due to diseases caused by P. palmivora is at least one billion U.S. dollars. As a very aggressive pathogen, P. palmivora is often capable of infecting almost all plant parts of a host, rendering its control extremely challenging. As a result, it has become an increasing threat to agricultural production and ecosystems. Diseases caused by P. palmivora are managed by frequent application of fungicides with limited success. The long-term goal of this project is to develop novel, effective and environmentally friendly strategies to control P. palmivora based on the fundamental understandings of its infection mechanisms. To this end, the specific objectives of this project are to identify the key pathogenicity factors of P. palmivora, how these factors act on plant cellular components to contribute to disease, and how their presence/absence in a P. palmivora isolate determines which plant species to infect. This project is expected to generate significant foundational knowledge essential for developing desirable disease control measures, thereby significantly contributing to food security, sustainability of natural ecosystems and the bioeconomy. In addition, the project will contribute to STEM workforce sustainability by providing training opportunities to graduate, undergraduate and high school students, and introducing plant pathology and gene-editing technology to middle/high-school teachers to attract a new generation into agriculture and life sciences. Oomycetes form a distinct phylogenetic lineage of eukaryotes, with many causing devastating diseases of plants and animals. Phytophthora palmivora is a destructive broad-host-range oomycete plant pathogen with host specificity. P. palmivora delivers a diverse array of effectors to manipulate the host cellular processes to facilitate infection, including the superfamily of RxLR effectors that are defined by an N-terminal signal peptide followed by a canonical RxLR (or RxLR-EER) translocation motif that mediates entry into host cells. The P. palmivora RxLR effector designated PpalRxLR1 contains a functional nuclear localization signal with potential DNA-binding activities and was identified as a key pathogenicity factor on cacao. It is present in all examined P. palmivora isolates obtained from cacao infections, but exhibits presence/absence polymorphisms across the species, suggesting that it may be a determinant of host range and specificity. This project is to: 1) determine the mechanisms by which PpalRxLR1 confers pathogenicity on cacao by determining its nuclear-localized molecular interaction dynamics and the subverted host cellular processes during infection, 2) determine the role of PpalRxLR1 as a key component in host range evolution of P. palmivora by analyzing its evolution relative to the species and association with host range, 3) identify additional effectors with key roles in pathogenicity of P. palmivora on specific or a broad range of hosts using the natural variation of P. palmivora isolates. Integrating across specific aims is expected to transform understanding of the molecular basis of pathogenicity and host range evolution of P. palmivora, key aspects of plant-microbe interactions.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.