Jared M. LeBoldus, Shannon C. Lynch, Andrew E. Newhouse, Kelsey L. Søndreli, George Newcombe, Patrick I. Bennett, Wellington Muchero, Jin-Gui Chen, Posy E. Busby, Michael Gordon, Haiying Liang
{"title":"Biotechnology and Genomic Approaches to Mitigating Disease Impacts on Forest Health","authors":"Jared M. LeBoldus, Shannon C. Lynch, Andrew E. Newhouse, Kelsey L. Søndreli, George Newcombe, Patrick I. Bennett, Wellington Muchero, Jin-Gui Chen, Posy E. Busby, Michael Gordon, Haiying Liang","doi":"10.1146/annurev-phyto-021622-114434","DOIUrl":"https://doi.org/10.1146/annurev-phyto-021622-114434","url":null,"abstract":"Outbreaks of insects and diseases are part of the natural disturbance regime of all forests. However, introduced pathogens have had outsized impacts on many dominant forest tree species over the past century. Mitigating these impacts and restoring these species are dilemmas of the modern era. Here, we review the ecological and economic impact of introduced pathogens, focusing on examples in North America. We then synthesize the successes and challenges of past biotechnological approaches and discuss the integration of genomics and biotechnology to help mitigate the effects of past and future pathogen invasions. These questions are considered in the context of the transgenic American chestnut, which is the most comprehensive example to date of how biotechnological tools have been used to address the impacts of introduced pathogens on naïve forest ecosystems.","PeriodicalId":8251,"journal":{"name":"Annual review of phytopathology","volume":"5 1","pages":""},"PeriodicalIF":10.2,"publicationDate":"2024-09-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142178829","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
V. Fiorilli, A. Martínez-Medina, Maria J. Pozo, L. Lanfranco
{"title":"Plant Immunity Modulation in Arbuscular Mycorrhizal Symbiosis and Its Impact on Pathogens and Pests","authors":"V. Fiorilli, A. Martínez-Medina, Maria J. Pozo, L. Lanfranco","doi":"10.1146/annurev-phyto-121423-042014","DOIUrl":"https://doi.org/10.1146/annurev-phyto-121423-042014","url":null,"abstract":"Arbuscular mycorrhizal (AM) symbiosis is the oldest and most widespread mutualistic association on Earth and involves plants and soil fungi belonging to Glomeromycotina. A complex molecular, cellular, and genetic developmental program enables partner recognition, fungal accommodation in plant tissues, and activation of symbiotic functions such as transfer of phosphorus in exchange for carbohydrates and lipids. AM fungi, as ancient obligate biotrophs, have evolved strategies to circumvent plant defense responses to guarantee an intimate and long-lasting mutualism. They are among those root-associated microorganisms able to boost plants’ ability to cope with biotic stresses leading to mycorrhiza-induced resistance (MIR), which can be effective across diverse hosts and against different attackers. Here, we examine the molecular mechanisms underlying the modulation of plant immunity during colonization by AM fungi and at the onset and display of MIR against belowground and aboveground pests and pathogens. Understanding the MIR efficiency spectrum and its regulation is of great importance to optimizing the biotechnological application of these beneficial microbes for sustainable crop protection.","PeriodicalId":8251,"journal":{"name":"Annual review of phytopathology","volume":"81 1","pages":""},"PeriodicalIF":10.2,"publicationDate":"2024-09-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142178832","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jelle Spooren, Sietske van Bentum, Linda S Thomashow, Corné M J Pieterse, David M Weller, Roeland L Berendsen
{"title":"Plant-Driven Assembly of Disease-Suppressive Soil Microbiomes.","authors":"Jelle Spooren, Sietske van Bentum, Linda S Thomashow, Corné M J Pieterse, David M Weller, Roeland L Berendsen","doi":"10.1146/annurev-phyto-021622-100127","DOIUrl":"10.1146/annurev-phyto-021622-100127","url":null,"abstract":"<p><p>Plants have coevolved together with the microbes that surround them and this assemblage of host and microbes functions as a discrete ecological unit called a holobiont. This review outlines plant-driven assembly of disease-suppressive microbiomes. Plants are colonized by microbes from seed, soil, and air but selectively shape the microbiome with root exudates, creating microenvironment hot spots where microbes thrive. Using plant immunity for gatekeeping and surveillance, host-plant genetic properties govern microbiome assembly and can confer adaptive advantages to the holobiont. These advantages manifest in disease-suppressive soils, where buildup of specific microbes inhibits the causal agent of disease, that typically develop after an initial disease outbreak. Based on disease-suppressive soils such as take-all decline, we developed a conceptual model of how plants in response to pathogen attack cry for help and recruit plant-protective microbes that confer increased resistance. Thereby, plants create a soilborne legacy that protects subsequent generations and forms disease-suppressive soils.</p>","PeriodicalId":8251,"journal":{"name":"Annual review of phytopathology","volume":" ","pages":"1-30"},"PeriodicalIF":9.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141299872","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Markéta Vlková-Žlebková, Fang Wei Yuen, Honour C McCann
{"title":"Evolving Archetypes: Learning from Pathogen Emergence on a Nonmodel Host.","authors":"Markéta Vlková-Žlebková, Fang Wei Yuen, Honour C McCann","doi":"10.1146/annurev-phyto-021622-095110","DOIUrl":"10.1146/annurev-phyto-021622-095110","url":null,"abstract":"<p><p>Research initiatives undertaken in response to disease outbreaks accelerate our understanding of microbial evolution, mechanisms of virulence and resistance, and plant-pathogen coevolutionary interactions. The emergence and global spread of <i>Pseudomonas syringae</i> pv. <i>actinidiae</i> (Psa) on kiwifruit (<i>Actinidia chinensis</i>) showed that there are parallel paths to host adaptation and antimicrobial resistance evolution, accelerated by the movement of mobile elements. Significant progress has been made in identifying type 3 effectors required for virulence and recognition in <i>A. chinensis</i> and <i>Actinidia arguta</i>, broadening our understanding of how host-mediated selection shapes virulence. The rapid development of <i>Actinidia</i> genomics after the Psa3 pandemic began has also generated new insight into molecular mechanisms of immunity and resistance gene evolution in this recently domesticated, nonmodel host. These findings include the presence of close homologs of known resistance genes <i>RPM1</i> and <i>RPS2</i> as well as the novel expansion of CC<sub>G10</sub>-NLRs (nucleotide-binding leucine-rich repeats) in <i>Actinidia</i> spp. The advances and approaches developed during the pandemic response can be applied to new pathosystems and new outbreak events.</p>","PeriodicalId":8251,"journal":{"name":"Annual review of phytopathology","volume":" ","pages":"49-68"},"PeriodicalIF":9.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141417523","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Regulation of Bacterial Growth and Behavior by Host Plant.","authors":"Satoru Nakagami, Zhe Wang, Xiaowei Han, Kenichi Tsuda","doi":"10.1146/annurev-phyto-010824-023359","DOIUrl":"10.1146/annurev-phyto-010824-023359","url":null,"abstract":"<p><p>Plants are associated with diverse bacteria in nature. Some bacteria are pathogens that decrease plant fitness, and others are beneficial bacteria that promote plant growth and stress resistance. Emerging evidence also suggests that plant-associated commensal bacteria collectively contribute to plant health and are essential for plant survival in nature. Bacteria with different characteristics simultaneously colonize plant tissues. Thus, plants need to accommodate bacteria that provide service to the host plants, but they need to defend against pathogens at the same time. How do plants achieve this? In this review, we summarize how plants use physical barriers, control common goods such as water and nutrients, and produce antibacterial molecules to regulate bacterial growth and behavior. Furthermore, we highlight that plants use specialized metabolites that support or inhibit specific bacteria, thereby selectively recruiting plant-associated bacterial communities and regulating their function. We also raise important questions that need to be addressed to improve our understanding of plant-bacteria interactions.</p>","PeriodicalId":8251,"journal":{"name":"Annual review of phytopathology","volume":" ","pages":"69-96"},"PeriodicalIF":9.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141299873","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
A C Newton, H E Creissen, I A Erreguerena, N D Havis
{"title":"Disease Management in Regenerative Cropping in the Context of Climate Change and Regulatory Restrictions.","authors":"A C Newton, H E Creissen, I A Erreguerena, N D Havis","doi":"10.1146/annurev-phyto-121423-042037","DOIUrl":"10.1146/annurev-phyto-121423-042037","url":null,"abstract":"<p><p>Regenerative agriculture as a term and concept has gained much traction over recent years. Many farmers are convinced that by adopting these principles they will be able to address the triple crisis of biodiversity loss, climate change, and food security. However, the impact of regenerative agriculture practices on crop pathogens and their management has received little attention from the scientific community. Significant changes to cropping systems may result in certain diseases presenting more or less of a threat. Shifts in major diseases may have significant implications regarding optimal integrated pest management (IPM) strategies that aim to improve profitability and productivity in an environmentally sensitive manner. In particular, many aspects of regenerative agriculture change risk levels and risk management in ways that are central to effective IPM. This review outlines some of the challenges, gaps, and opportunities in our understanding of appropriate approaches for managing crop diseases in regenerative cropping systems.</p>","PeriodicalId":8251,"journal":{"name":"Annual review of phytopathology","volume":" ","pages":"337-356"},"PeriodicalIF":9.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141475795","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sara Garcia-Figuera, Sarah R Lowder, Mark N Lubell, Walter F Mahaffee, Neil McRoberts, David H Gent
{"title":"Free-Riding in Plant Health: A Social-Ecological Systems Approach to Collective Action.","authors":"Sara Garcia-Figuera, Sarah R Lowder, Mark N Lubell, Walter F Mahaffee, Neil McRoberts, David H Gent","doi":"10.1146/annurev-phyto-121423-041950","DOIUrl":"10.1146/annurev-phyto-121423-041950","url":null,"abstract":"<p><p>Plant disease epidemics often transcend land management boundaries, creating a collective-action problem where a group must cooperate in a common effort to maximize individual and group benefits. Drawing upon the social-ecological systems framework and associated design principles, we review variables of resource systems, resource units, actors, and governance systems relevant to collective action in plant health. We identify a need to better characterize how attributes of epidemics determine the usefulness of collective management, what influences actors' decisions to participate, what governance systems fit different plant health threats, and how these subsystems interact to lead to plant health outcomes. We emphasize that there is not a single governance structure that ensures collective action but rather a continuum of structures that depend on the key system variables identified. An integrated social-ecological systems approach to collective action in plant health should enable institutional designs to better fit specific plant health challenges.</p>","PeriodicalId":8251,"journal":{"name":"Annual review of phytopathology","volume":" ","pages":"357-384"},"PeriodicalIF":9.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140896976","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Theories for Understanding the Effect of Impact Assessment and Project Evaluation on the Practice of Science.","authors":"Neil McRoberts, Samuel Brinker, Kaity Coleman","doi":"10.1146/annurev-phyto-080417-050125","DOIUrl":"10.1146/annurev-phyto-080417-050125","url":null,"abstract":"<p><p>We examine the phenomenon of impact assessment in the practice of scientific research, paying attention to the context in which project evaluation is used in federally funded research on plant health in the United States. Our analysis, which is derived from systems theory, carries out a particular view of the research process. For the purposes of this review, our use of the term systems theory references the body of interdisciplinary work that deals with the organization and function of complex structures in nature and human society. Key concepts in this body of theory are that both the components and the interactions among components are important in understanding behavior and that, frequently, systems are seen to be hierarchical in structure. The aim of our analysis is to bring to the attention of the plant health community several concepts from the social sciences that might help in understanding how researchers have responded to the increased expectations from funders to provide project evaluations and impact assessments. We generate a synthesis of these theories, which have not previously been used in a unified way, to explain choices in response to newly imposed goals. Although our analysis is motivated by a specific disciplinary focus on plant health, the issues we discuss are general. Thus, we hope the review is useful to a wide range of scientists, science program managers, and policymakers.</p>","PeriodicalId":8251,"journal":{"name":"Annual review of phytopathology","volume":" ","pages":"385-400"},"PeriodicalIF":9.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141299875","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Francisco M Ayala, Itzell Eurídice Hernández-Sánchez, Monika Chodasiewicz, Brande B H Wulff, Radim Svačina
{"title":"Engineering a One Health Super Wheat.","authors":"Francisco M Ayala, Itzell Eurídice Hernández-Sánchez, Monika Chodasiewicz, Brande B H Wulff, Radim Svačina","doi":"10.1146/annurev-phyto-121423-042128","DOIUrl":"10.1146/annurev-phyto-121423-042128","url":null,"abstract":"<p><p>Wheat is the predominant crop worldwide, contributing approximately 20% of protein and calories to the human diet. However, the yield potential of wheat faces limitations due to pests, diseases, and abiotic stresses. Although conventional breeding has improved desirable traits, the use of modern transgenesis technologies has been limited in wheat in comparison to other crops such as maize and soybean. Recent advances in wheat gene cloning and transformation technology now enable the development of a super wheat consistent with the One Health goals of sustainability, food security, and environmental stewardship. This variety combines traits to enhance pest and disease resistance, elevate grain nutritional value, and improve resilience to climate change. In this review, we explore ways to leverage current technologies to combine and transform useful traits into wheat. We also address the requirements of breeders and legal considerations such as patents and regulatory issues.</p>","PeriodicalId":8251,"journal":{"name":"Annual review of phytopathology","volume":" ","pages":"193-215"},"PeriodicalIF":9.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141299871","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The Use of <i>Caenorhabditis elegans</i> as a Model for Plant-Parasitic Nematodes: What Have We Learned?","authors":"Mirela C Coke, Christopher A Bell, P E Urwin","doi":"10.1146/annurev-phyto-021622-113539","DOIUrl":"10.1146/annurev-phyto-021622-113539","url":null,"abstract":"<p><p>Nematoda is a diverse phylum that is estimated to contain more than a million species. More than 4,100 of these species have the ability to parasitize plants and cause agricultural losses estimated at US $173 billion annually. This has led to considerable research into their biology to minimize crop losses via control methods. At the infancy of plant-parasitic nematode molecular biology, researchers compared nematode genomes, genes, and biological processes to the model nematode species <i>Caenorhabditis elegans</i>, which is a free-living bacterial feeder<i>.</i> This well-annotated and researched model nematode assisted the molecular biology research, e.g., with genome assemblies, of plant-parasitic nematodes. However, as research into these plant parasites progressed, the necessity of relying on the free-living relative as a reference has reduced. This is partly driven by revealing the considerable divergence between the two types of nematodes both genomically and anatomically, forcing comparisons to be redundant as well as the increased quality of molecular plant nematology proposing more suitable model organisms for this clade of nematode. The major irregularity between the two types of nematodes is the unique anatomical structure and effector repertoire that plant nematodes utilize to establish parasitism, which <i>C. elegans</i> lacks, therefore reducing its value as a heterologous system to investigate parasitic processes. Despite this, <i>C. elegans</i> remains useful for investigating conserved genes via its utility as an expression system because of the current inability to transform plant-parasitic nematodes. Unfortunately, owing to the expertise that this requires, it is not a common and/or accessible tool. Furthermore, we believe that the application of <i>C. elegans</i> as an expression system for plant nematodes will be redundant once tools are established for stable reverse-genetics in these plant parasites. This will remove the restraints on molecular plant nematology and allow it to excel on par with the capabilities of <i>C. elegans</i> research.</p>","PeriodicalId":8251,"journal":{"name":"Annual review of phytopathology","volume":" ","pages":"157-172"},"PeriodicalIF":9.1,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141287618","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}