Annual Review of Phytopathology - Volume 60, 2022

Early detection of pests and pathogens is of paramount importance in reducing agricultural losses. One approach to early detection is point-of-care (POC) diagnostics, which can provide early warning and therefore allow fast deployment of preventive measures to slow down the establishment of crop diseases. Among the available diagnostic technologies, nucleic acid amplification–based diagnostics provide the highest sensitivity and specificity, and those technologies that forego the requirement for thermocycling show the most potential for use at POC. In this review, I discuss the progress, advantages, and disadvantages of the established and most promising POC amplification technologies. The success and usefulness of POC amplification are ultimately dependent on the availability of POC-friendly nucleic acid extraction methods and amplification readouts, which are also briefly discussed in the review.

The most economically important biotic stresses in crop production are caused by fungi, oomycetes, insects, viruses, and bacteria. Often chemical control is still the most commonly used method to manage them. However, the development of resistance in the different pathogens/pests, the putative damage on the natural ecosystem, the toxic residues in the field, and, thus, the contamination of the environment have stimulated the search for saferalternatives such as the use of biological control agents (BCAs). Among BCAs, viruses, a major driver for controlling host populations and evolution, are somewhat underused, mostly because of regulatory hurdles that make the cost of registration of such host-specific BCAs not affordable in comparison with the limited potential market. Here, we provide a comprehensive overview of the state of the art of virus-based BCAs against fungi, bacteria, viruses, and insects, with a specific focus on new approaches that rely on not only the direct biocidal virus component but also the complex ecological interactions between viruses and their hosts that do not necessarily result in direct damage to the host.

Root-knot nematodes (RKNs; Meloidogyne spp.) engage in complex parasitic interactions with many different host plants around the world, initiating elaborate feeding sites and disrupting host root architecture. Although RKNs have been the focus of research for many decades, new molecular tools have provided useful insights into the biological mechanisms these pests use to infect and manipulate their hosts. From identifying host defense mechanisms underlying resistance to RKNs to characterizing nematode effectors that alter host cellular functions, the past decade of research has significantly expanded our understanding of RKN–plant interactions, and the increasing number of quality parasite and host genomes promises to enhance future research efforts into RKNs. In this review, we have highlighted recent discoveries, summarized the current understanding within the field, and provided links to new and useful resources for researchers. Our goal is to offer insights and tools to support the study of molecular RKN–plant interactions.

Although the phloem is a highly specialized tissue, certain pathogens, including phytoplasmas, spiroplasmas, and viruses, have evolved to access and live in this sequestered and protected environment, causing substantial economic harm. In particular, Candidatus Liberibacter spp. are devastating citrus in many parts of the world. Given that most phloem pathogens are vectored, they are not exposed to applied chemicals and are therefore difficult to control. Furthermore, pathogens use the phloem network to escape mounted defenses. Our review summarizes the current knowledge of phloem anatomy, physiology, and biochemistry relevant to phloem/pathogen interactions. We focus on aspects of anatomy specific to pathogen movement, including sieve plate structure and phloem-specific proteins. Phloem sampling techniques are discussed. Finally, pathogens that cause particular harm to the phloem of crop species are considered in detail.

Peptide signaling is an emerging paradigm in molecular plant–microbe interactions with vast implications for our understanding of plant–nematode interactions and beyond. Plant-like peptide hormones, first discovered in cyst nematodes, are now recognized as an important class of peptide effectors mediating several different types of pathogenic and symbiotic interactions. Here, we summarize what has been learned about nematode-secreted CLAVATA3/EMBRYO SURROUNDING REGION-RELATED (CLE) peptide effectors since the last comprehensive review on this topic a decade ago. We also highlight new discoveries of a diverse array of peptide effectors that go beyond the CLE peptide effector family in not only phytonematodes but in organisms beyond the phylum Nematoda.

Yellow dwarf viruses are the most economically important and widespread viruses of cereal crops. Although they share common biological properties such as phloem limitation and obligate aphid transmission, the replication machinery and associated cis-acting signals of these viruses fall into two unrelated taxa represented by Barley yellow dwarf virus and Cereal yellow dwarf virus. Here, we explain the reclassification of these viruses based on their very different genomes. We also provide an overview of viral protein functions and their interactions with the host and vector, replication mechanisms of viral and satellite RNAs, and the complex gene expression strategies. Throughout, we point out key unanswered questions in virus evolution, structural biology, and genome function and replication that, when answered, may ultimately provide new tools for virus management.

Plant-parasitic nematodes spend much of their lives inside or in contact with host tissue, and molecular interactions constantly occur and shape the outcome of parasitism. Eggs of these parasites generally hatch in the soil, and the juveniles must locate and infect an appropriate host before their stored energy is exhausted. Components of host exudate are evaluated by the nematode and direct its migration to its infection site. Host plants recognize approaching nematodes before physical contact through molecules released by the nematodes and launch a defense response. In turn, nematodes deploy numerous mechanisms to counteract plant defenses. This review focuses on these early stages of the interaction between plants and nematodes. We discuss how nematodes perceive and find suitable hosts, how plants perceive and mount a defense response against the approaching parasites, and how nematodes fight back against host defenses.

A group of aggressive pathogens have evolved to colonize the plant xylem. In this vascular tissue, where water and nutrients are transported from the roots to the rest of the plant, pathogens must be able to thrive under acropetal xylem sap flow and scarcity of nutrients while having direct contact only with predominantly dead cells. Nevertheless, a few bacteria have adapted to exclusively live in the xylem, and various pathogens may colonize other plant niches without causing symptoms unless they reach the xylem. Once established, the pathogens modulate its physicochemical conditions to enhance their growth and virulence. Adaptation to the restrictive lifestyle of the xylem leads to genome reduction in xylem-restricted bacteria, as they have a higher proportion of pseudogenes in their genome. The basis of xylem adaptation is not completely understood; therefore, a need still exists for model systems to advance the knowledge on this topic.

Biotechnological advances now permit broad exploration of past microbial communities preserved in diverse substrates. Despite biomolecular degradation, high-throughput sequencing of preserved materials can yield invaluable genomic and metagenomic data from the past. This line of research has expanded from its initial human- and animal-centric foci to include plant-associated microbes (viruses, archaea, bacteria, fungi, and oomycetes), for which historical, archaeological, and paleontological data illuminate past epidemics and evolutionary history. Genetic mechanisms underlying the acquisition of microbial pathogenicity, including hybridization, polyploidization, and horizontal gene transfer, can now be reconstructed, as can gene-for-gene coevolution with plant hosts. Epidemiological parameters, such as geographic origin and range expansion, can also be assessed. Building on published case studies with individual phytomicrobial taxa, the stage is now set for broader, community-wide studies of preserved plant microbiomes to strengthen mechanistic understanding of microbial interactions and plant disease emergence.

Pseudomonas syringae is an evolutionarily diverse bacterial species complex and a preeminent model for the study of plant–pathogen interactions due in part to its remarkably broad host range. A critical feature of P. syringae virulence is the employment of suites of type III secreted effector (T3SE) proteins, which vary widely in composition and function. These effectors act on a variety of plant intracellular targets to promote pathogenesis but can also be avirulence factors when detected by host immune complexes. In this review, we survey the phylogenetic diversity (PD) of the P. syringae effectorome, comprising 70 distinct T3SE families identified to date, and highlight how avoidance of host immune detection has shaped effectorome diversity through functional redundancy, diversification, and horizontal transfer. We present emerging avenues for research and novel insights that can be gained via future investigations of plant–pathogen interactions through the fusion of large-scale interaction screens and phylogenomic approaches.

Canola is an important oilseed crop, providing food, feed, and fuel around the world. However, blackleg disease, caused by the ascomycete Leptosphaeria maculans, causes significant yield losses annually. With the recent advances in genomic technologies, the understanding of the Brassica napus–L. maculans interaction has rapidly increased, with numerous Avr and R genes cloned, setting this system up as a model organism for studying plant–pathogen associations. Although the B. napus–L. maculans interaction follows Flor's gene-for-gene hypothesis for qualitative resistance, it also puts some unique spins on the interaction. This review discusses the current status of the host–pathogen interaction and highlights some of the future gaps that need addressing moving forward.

Bacterial diseases are a constant threat to crop production globally. Current management strategies rely on an array of tactics, including improved cultural practices; application of bactericides, plant activators, and biocontrol agents; and use of resistant varieties when available. However, effective management remains a challenge, as the longevity of deployed tactics is threatened by constantly changing bacterial populations. Increased scrutiny of the impact of pesticides on human and environmental health underscores the need for alternative solutions that are durable, sustainable, accessible to farmers, and environmentally friendly. In this review, we discuss the strengths and shortcomings of existing practices and dissect recent advances that may shape the future of bacterial disease management. We conclude that disease resistance through genome modification may be the most effective arsenal against bacterial diseases. Nonetheless, more research is necessary for developing novel bacterial disease management tactics to meet the food demand of a growing global population.

Our understanding of the ecological interactions between plant viruses, their insect vectors, and their host plants has increased rapidly over the past decade. The suite of viruses known collectively as the yellow dwarf viruses infect an extensive range of cultivated and noncultivated grasses worldwide and is one of the best-studied plant virus systems. The yellow dwarf viruses are ubiquitous in cereal crops, where they can significantly limit yields, and there is growing recognition that they are also ubiquitous in grassland ecosystems, where they can influence community dynamics. Here, we discuss recent research that has explored (a) the extent and impact of yellow dwarf viruses in a diversity of plant communities, (b) the role of vector behavior in virus transmission, and (c) the prospects for impacts of climate change—including rising temperatures, drought, and elevated CO2—on the epidemiology of yellow dwarf viruses.

High-throughput virome analyses with various fungi, from cultured or uncultured sources, have led to the discovery of diverse viruses with unique genome structures and even neo-lifestyles. Examples in the former category include splipalmiviruses and ambiviruses. Splipalmiviruses, related to yeast narnaviruses, have multiple positive-sense (+) single-stranded (ss) RNA genomic segments that separately encode the RNA-dependent RNA polymerase motifs, the hallmark of RNA viruses (members of the kingdom Orthornavirae). Ambiviruses appear to have an undivided ssRNA genome of 3∼5 kb with two large open reading frames (ORFs) separated by intergenic regions. Another narna-like virus group has two fully overlapping ORFs on both strands of a genomic segment that span more than 90% of the genome size. New virus lifestyles exhibited by mycoviruses include the yado-kari/yado-nushi nature characterized by the partnership between the (+)ssRNA yadokarivirus and an unrelated dsRNA virus (donor of the capsid for the former) and the hadaka nature of capsidless 10–11 segmented (+)ssRNA accessible by RNase in infected mycelial homogenates. Furthermore, dsRNA polymycoviruses with phylogenetic affinity to (+)ssRNA animal caliciviruses have been shown to be infectious as dsRNA–protein complexes or deproteinized naked dsRNA. Many previous phylogenetic gaps have been filled by recently discovered fungal and other viruses, which haveprovided interesting evolutionary insights. Phylogenetic analyses and the discovery of natural and experimental cross-kingdom infections suggest that horizontal virus transfer may have occurred and continue to occur between fungi and other kingdoms.

Tree planting and natural regeneration contribute to the ongoing effort to restore Earth's forests. Our review addresses how the plant microbiome can enhance the survival of planted and naturally regenerating seedlings and serve in long-term forest carbon capture and the conservation of biodiversity. We focus on fungal leaf endophytes, ubiquitous defensive symbionts that protect against pathogens. We first show that fungal and oomycetous pathogen richness varies greatly for tree species native to the United States (n = 0–876 known pathogens per US tree species), with nearly half of tree species either without pathogens in these major groups or with unknown pathogens. Endophytes are insurance against the poorly known and changing threat of tree pathogens. Next, we review studies of plant phyllosphere feedback, but knowledge gaps prevent us from evaluating whether adding conspecific leaf litter to planted seedlings promotes defensive symbiosis, analogous to adding soil to promote positive feedback. Finally, we discuss research priorities for integrating the plant microbiome into efforts to expand Earth's forests.

Plant pathology has developed a wide range of concepts and tools for improving plant disease management, including models for understanding and responding to new risks from climate change. Most of these tools can be improved using new advances in artificial intelligence (AI), such as machine learning to integrate massive data sets in predictive models. There is the potential to develop automated analyses of risk that alert decision-makers, from farm managers to national plant protection organizations, to the likely need for action and provide decision support for targeting responses. We review machine-learning applications in plant pathology and synthesize ideas for the next steps to make the most of these tools in digital agriculture. Global projects, such as the proposed global surveillance system for plant disease, will be strengthened by the integration of the wide range of new data, including data from tools like remote sensors, that are used to evaluate the risk ofplant disease. There is exciting potential for the use of AI to strengthen global capacity building as well, from image analysis for disease diagnostics and associated management recommendations on farmers’ phones to future training methodologies for plant pathologists that are customized in real-time for management needs in response to the current risks. International cooperation in integrating data and models will help develop the most effective responses to new challenges from climate change.

Resistance to the soybean cyst nematode (SCN) is a topic incorporating multiple mechanisms and multiple types of science. It is also a topic of substantial agricultural importance, as SCN is estimated to cause more yield damage than any other pathogen of soybean, one of the world's main food crops. Both soybean and SCN have experienced jumps in experimental tractability in the past decade, and significant advances have been made. The rhg1-b locus, deployed on millions of farm acres, has been durable and will remain important, but local SCN populations are gradually evolving to overcome rhg1-b. Multiple other SCN resistance quantitative trait loci (QTL) of proven value are now in play with soybean breeders. QTL causal gene discovery and mechanistic insights into SCN resistance are contributing to both basic and applied disciplines. Additional understanding of SCN and other cyst nematodes will also grow in importance and lead to novel disease control strategies.