An Emerging Role for Chloroplasts in Disease and Defense

Chloroplasts are key players in plant immune signaling, contributing to not only de novo synthesis of defensive phytohormones but also the generation of reactive oxygen and nitrogen species following activation of pattern recognition receptors or resistance (R) proteins. The local hypersensitive response (HR) elicited by R proteins is underpinned by chloroplast-generated reactive oxygen species. HR-induced lipid peroxidation generates important chloroplast-derived signaling lipids essential to the establishment of systemic immunity. As a consequence of this pivotal role in immunity, pathogens deploy effector complements that directly or indirectly target chloroplasts to attenuate chloroplast immunity (CI). Our review summarizes the current knowledge of CI signaling and highlights common pathogen chloroplast targets and virulence strategies. We address emerging insights into chloroplast retrograde signaling in immune responses and gaps in our knowledge, including the importance of understanding chloroplast heterogeneity and chloroplast involvement in intraorganellular interactions in host immunity.

Everything Is Faster: How Do Land-Grant University–Based Plant Diagnostic Laboratories Keep Up with a Rapidly Changing World?

Plant diagnostic laboratories (PDLs) are at the heart of land-grant universities (LGUs) and their extension mission to connect citizens with research-based information. Although research and technological advances have led to many modern methods and technologies in plant pathology diagnostics, the pace of adopting those methods into services at PDLs has many complexities we aim to explore in this review. We seek to identify current challenges in plant disease diagnostics, as well as diagnosticians' and administrators'perceptions of PDLs' many roles. Surveys of diagnosticians and administrators were conducted to understand the current climate on these topics. We hope this article reaches researchers developing diagnostic methods with modern and new technologies to foster a better understanding of PDL diagnosticians’ perspective on method implementation. Ultimately, increasing researchers’ awareness of the factors influencing method adoption by PDLs encourages support, collaboration, and partnerships to advance plant diagnostics.

Mycotoxin Production in Fusarium According to Contemporary Species Concepts

Fusarium is one of the most important genera of plant-pathogenic fungi in the world and arguably the world's most important mycotoxin-producing genus. Fusarium species produce a staggering array of toxic metabolites that contribute to plant disease and mycotoxicoses in humans and other animals. A thorough understanding of the mycotoxin potential of individual species is crucial for assessing the toxicological risks associated with Fusarium diseases. There are thousands of reports of mycotoxin production by various species, and there have been numerous attempts to summarize them. These efforts have been complicated by competing classification systems based on morphology, sexual compatibility, and phylogenetic relationships. The current depth of knowledge of Fusarium genomes and mycotoxin biosynthetic pathways provides insights into how mycotoxin production is distributed among species and multispecies lineages (species complexes) in the genus as well as opportunities to clarify and predict mycotoxin risks connected with known and newly described species. Here, we summarize mycotoxin production in the genus Fusarium and how mycotoxin risk aligns with current phylogenetic species concepts. Expected final online publication date for the Annual Review of Phytopathology, Volume 59 is August 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Small RNAs in Plant Immunity and Virulence of Filamentous Pathogens

Gene silencing guided by small RNAs governs a broad range of cellular processes in eukaryotes. Small RNAs are important components of plant immunity because they contribute to pathogen-triggered transcription reprogramming and directly target pathogen RNAs. Recent research suggests that silencing of pathogen genes by plant small RNAs occurs not only during viral infection but also in nonviral pathogens through a process termed host-induced gene silencing, which involves trans-species small RNA trafficking. Similarly, small RNAs are also produced by eukaryotic pathogens and regulate virulence. This review summarizes the small RNA pathways in both plants and filamentous pathogens, including fungi and oomycetes, and discusses their role in host–pathogen interactions. We highlight secondary small interfering RNAs of plants as regulators of immune receptor gene expression and executors of host-induced gene silencing in invading pathogens. The current status and prospects of small RNAs trafficking at the host–pathogen interface are discussed. Expected final online publication date for the Annual Review of Phytopathology, Volume 59 is August 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Rice stripe virus: Exploring Molecular Weapons in the Arsenal of a Negative-Sense RNA Virus

Rice stripe disease caused by Rice stripe virus (RSV) is one of the most devastating plant viruses of rice and causes enormous losses in production. RSV is transmitted from plant to plant by the small brown planthopper ( Laodelphax striatellus) in a circulative–propagative manner. The recent reemergence of this pathogen in East Asia since 2000 has made RSV one of the most studied plant viruses over the past two decades. Extensive studies of RSV have resulted in substantial advances regarding fundamental aspects of the virus infection. Here, we compile and analyze recent information on RSV with a special emphasis on the strategies that RSV has adopted to establish infections. These advances include RSV replication and movement in host plants and the small brown planthopper vector, innate immunity defenses against RSV infection, epidemiology, and recent advances in the management of rice stripe disease. Understanding these issues will facilitate the design of novel antiviral therapies for management and contribute to a more detailed understanding of negative-sense virus–host interactions at the molecular level. Expected final online publication date for the Annual Review of Phytopathology, Volume 59 is August 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Host Adaptation and Virulence in Heteroecious Rust Fungi

Rust fungi (Pucciniales, Basidiomycota) are obligate biotrophic pathogens that cause rust diseases in plants, inflicting severe damage to agricultural crops. Pucciniales possess the most complex life cycles known in fungi. These include an alternation of generations, the development of up to five different sporulating stages, and, for many species, the requirement of infecting two unrelated host plants during different parts of their life cycle, termed heteroecism. These fungi have been extensively studied in the past century through microscopy and inoculation studies, providing precise descriptions of their infection processes, although the molecular mechanisms underlying their unique biology are poorly understood. In this review, we cover recent genomic and life cycle transcriptomic studies in several heteroecious rust species, which provide insights into the genetic tool kits associated with host adaptation and virulence, opening new avenues for unraveling their unique evolution. Expected final online publication date for the Annual Review of Phytopathology, Volume 59 is August 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Genomic Approaches to Plant-Pathogen Epidemiology and Diagnostics

Diseases have a significant cost to agriculture. Findings from analyses of whole-genome sequences show great promise for informing strategies to mitigate risks from diseases caused by phytopathogens. Genomic approaches can be used to dramatically shorten response times to outbreaks and inform disease management in novel ways. However, the use of these approaches requires expertise in working with big, complex data sets and an understanding of their pitfalls and limitations to infer well-supported conclusions. We suggest using an evolutionary framework to guide the use of genomic approaches in epidemiology and diagnostics of plant pathogens. We also describe steps that are necessary for realizing these as standard approaches in disease surveillance. Expected final online publication date for the Annual Review of Phytopathology, Volume 59 is August 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Harnessing Eco-Evolutionary Dynamics of Xanthomonads on Tomato and Pepper to Tackle New Problems of an Old Disease

Bacterial spot is an endemic seedborne disease responsible for recurring outbreaks on tomato and pepper around the world. The disease is caused by four diverse species, Xanthomonas gardneri, Xanthomonas euvesicatoria, Xanthomonas perforans, and Xanthomonas vesicatoria. There are no commercially available disease-resistant tomato varieties, and the disease is managed by chemical/biological control options, although these have not reduced the incidence of outbreaks. The disease on peppers is managed by disease-resistant cultivars that are effective against X. euvesicatoria but not X. gardneri. A significant shift in composition and prevalence of different species and races of the pathogen has occurred over the past century. Here, I attempt to review ecological and evolutionary processes associated with the population dynamics leading to disease emergence and spread. The goal of this review is to integrate the knowledge on population genomics and molecular plant–microbe interactions for this pathosystem to tailor disease management strategies. Expected final online publication date for the Annual Review of Phytopathology, Volume 59 is August 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Models of Plant Resistance Deployment

Owing to their evolutionary potential, plant pathogens are able to rapidly adapt to genetically controlled plant resistance, often resulting in resistance breakdown and major epidemics in agricultural crops. Various deployment strategies have been proposed to improve resistance management. Globally, these rely on careful selection of resistance sources and their combination at various spatiotemporal scales (e.g., via gene pyramiding, crop rotations and mixtures, landscape mosaics). However, testing and optimizing these strategies using controlled experiments at large spatiotemporal scales are logistically challenging. Mathematical models provide an alternative investigative tool, and many have been developed to explore resistance deployment strategies under various contexts. This review analyzes 69 modeling studies in light of specific model structures (e.g., demographic or demogenetic, spatial or not), underlying assumptions (e.g., whether preadapted pathogens are present before resistance deployment), and evaluation criteria (e.g., resistance durability, disease control, cost-effectiveness). It highlights major research findings and discusses challenges for future modeling efforts. Expected final online publication date for the Annual Review of Phytopathology, Volume 59 is August 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Characterization of Effector–Target Interactions in Necrotrophic Pathosystems Reveals Trends and Variation in Host Manipulation

Great strides have been made in defining the details of the plant defense response involving biotrophic fungal and bacterial pathogens. The groundwork for the current model was laid by H.H. Flor and others who defined the gene-for-gene hypothesis, which is now known to involve effector-triggered immunity (ETI). PAMP-triggered immunity (PTI) is also a highly effective response to most pathogens because of the recognition of common pathogen molecules by pattern recognition receptors. In this article, we consider the three pathogens that make up the foliar disease complex of wheat, Zymoseptoria tritici, Pyrenophora tritici-repentis, and Parastagonospora nodorum, to review the means by which necrotrophic pathogens circumvent, or outright hijack, the ETI and PTI pathways to cause disease. Expected final online publication date for the Annual Review of Phytopathology, Volume 59 is August 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.