Phytophthora is a long-established, well-known, and globally important genus of plant pathogens. Phylogenetic evidence has shown that the biologically distinct, obligate biotrophic downy mildews evolved from Phytophthora at least twice. Because, cladistically, this renders Phytophthora "paraphyletic," it has been proposed that Phytophthora evolutionary clades be split into multiple genera (Crous et al. 2021; Runge et al. 2011; Thines 2023, 2024). In this letter, we review arguments for the retention of the generic name Phytophthora with a broad circumscription made by Brasier et al. (2022) and by many delegates at an open workshop organized by The American Phytopathological Society. We present our well-considered responses to the genus splitting proposals, both in general terms and in terms of the specific proposals for new genera, alongside new information regarding the biological properties and mode of origin of the Phytophthora clades. We consider that the proposals are mostly non-rigorous and not supported by the scientific evidence. Further, given (i) the apparent lack of any distinguishing biological characteristics (synapomorphies) between the Phytophthora clades; (ii) the fundamental monophyly of Phytophthora in the original Haeckelian sense (Haeckel 1877); (iii) the fact that paraphyly is not a justification for taxonomic splitting; and (iv) the considerable likely damage to effective scientific communication and disease management from an unnecessary breakup of the genus, we report that workshop delegates voted unanimously in favor of preserving the current generic concept and for seeking endorsement of this view by a working group of the International Commission on the Taxonomy of Fungi. [Formula: see text] Copyright © 2025 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Downy mildew (DMs) dieases are caused by destructive obligate pathogens with limited control options, posing a significant threat to global agriculture. RNA interference (RNAi) has emerged as a promising, environmentally sustainable strategy for disease management. In this study, we evaluated the efficacy of dsRNA-mediated RNAi in suppressing key biological functions in DM pathogens of Arabidopsis thaliana , pea and lettuce DM pathogens, Hyaloperonospora arabidopsidis ( Hpa ), Peronospora viciae f. sp. pisi ( Pvp ) and Bremia lactucae ( Bl ), respectively. We specifically targeted the cellulose synthase 3 ( CesA3) and the beta tubulin (BTUB) genes. Silencing CesA3 impaired spore germination and infection across multiple species, while BTUB silencing reinforced the potential of dsRNA-mediated inhibition. Reduction in gene expression levels correlated well with the sporulation assays confirming the effectiveness of dsRNA-mediated gene silencing. We used dsRNAs that were chemically synthesized, in vitro transcribed (IVT) or produced in E. coli . We found that the length and concentration of these dsRNAs significantly affected uptake efficiency, spore germination, and sporulation, with higher concentrations enhancing inhibitory effects. Confocal microscopy using Cy-5-labelled short-synthesized dsRNA (SS-dsRNA) provided direct evidence of spore uptake, confirming the potential of SS-dsRNA for pathogen control. However, species-specific sequence variations influenced dsRNA efficacy, underscoring the importance of target sequence design. Multiplexed RNAi impacted silencing synergisticly, further reducing germination and sporulation in Hpa . Additionally, we demonstrated that SS-dsRNA-mediated gene silencing is sustained over time, with a significant reduction in gene expression level at 4, 7, 10 and 11dpi. This indicates the durability and efficacy of this approach. Taken together, these findings demonstrate the potential of dsRNA-mediated gene silencing as a precision tool for managing DM pathogens. ### Competing Interest Statement The authors have declared no competing interest.

Downy mildew (DM) diseases are caused by destructive obligate pathogens with limited control options, posing a significant threat to global agriculture. RNA interference (RNAi) has emerged as a promising, environmentally sustainable strategy for disease management. We evaluated the efficacy of dsRNA-mediated RNAi in suppressing key biological functions in DM pathogens of Arabidopsis thaliana, pea and lettuce: Hyaloperonospora arabidopsidis (Hpa), Peronospora viciae f. sp. pisi (Pvp) and Bremia lactucae (Bl), respectively. Conserved genes, cellulose synthase 3 (CesA3) and beta-tubulin (BTUB), were targeted. Silencing these genes significantly impaired spore germination and infection across species and reduced gene expression correlated with suppressed sporulation, confirming silencing efficacy. We tested dsRNAs from chemical synthesis, in vitro transcription, and Escherichia coli expression. Uptake and silencing efficiency varied with dsRNA length and concentration. In Hpa, short dsRNAs (21-25 bp) produced a variable spore germination rate, with 25 bp dsRNA causing a 247.10% increase, whereas longer dsRNAs (≥ 30 bp) completely inhibited germination. Similarly, in Pvp, dsRNAs of 21-25 bp resulted in a 73.05%-77.46% germination rate, while 30-75 bp dsRNAs abolished germination. Confocal microscopy using Cy-5-labelled short-synthesised dsRNA (SS-dsRNA) confirmed uptake by spores. Sequence specificity influenced efficacy, highlighting the need for precise target design. Multiplexed RNAi impacted silencing synergistically, further reducing germination and sporulation in Hpa. Importantly, SS-dsRNA-mediated silencing was durable, with reduced gene expression sustained at 4, 7, 10 and 11 days post-inoculation. Taken together, our findings demonstrate the potential of dsRNA-mediated gene silencing as a precise, sustainable tool for managing DM pathogens in multiple crop species.

Organisms across all kingdoms have an internal circadian clock running in 24h cycles. This clock affects a variety of processes, including innate immunity in plants. However, the role of pathogen circadian clocks had not been extensively explored. We previously showed that light can influence infection of the oomycete Hyaloperonospora arabidopsidis ( Hpa , downy mildew disease) on its natural host Arabidopsis thaliana . Here, we identified Hpa orthologs of known circadian clock genes (CCGs) Drosophila TIMELESS (TIM) and Arabidopsis Sensitive to Red Light Reduced 1 (AtSRR1) genes. Expression of both HpaTIM and HpaSRR1 showed a circadian rhythm when Hpa was exposed to constant light. Contrastingly, these two genes were negatively regulated by constant dark exposure. Furthermore, the expression patterns of HpaTIM and HpaSRR1 correlate with those of AtCCA1 and AtLHY , indicating a synchronisation of biological clock genes between the host and the pathogen. In addition, screening mutants of Arabidopsis Clock Regulated Genes ( AtCRGs ) with three virulent Hpa isolates revealed that mutations in AtCRGs influenced HpaTIM and HpaSRR1 expression and Hpa development, indicating a functional link between the plant biological clock and virulence. Moreover, sporulation of Hpa was reduced by targeting HpaTIM and HpaSRR1 with short synthesized small interfering RNAs, indicating that the pathogen clock is also relevant to virulence. We propose that plant and pathogen clocks are synchronized during infection and that proper regulation of both clocks are genetically necessary for pathogen virulence.### Competing Interest StatementThe authors have declared no competing interest.

Single-cell genomics, combined with advanced AI models, hold transformative potential for understanding complex biological processes in plants. This article reviews deep-learning approaches in single-cell genomics, focusing on foundation models, a type of large-scale, pretrained, multi-purpose generative AI models. We explore how these models, such as Generative Pre-trained Transformers (GPT), Bidirectional Encoder Representations from Transformers (BERT), and other Transformer-based architectures, are applied to extract meaningful biological insights from diverse single-cell datasets. These models address challenges in plant single-cell genomics, including improved cell-type annotation, gene network modeling, and multi-omics integration. Moreover, we assess the use of Generative Adversarial Networks (GANs) and diffusion models, focusing on their capacity to generate high-fidelity synthetic single-cell data, mitigate dropout events, and handle data sparsity and imbalance. Together, these AI-driven approaches hold immense potential to enhance research in plant genomics, facilitating discoveries in crop resilience, productivity, and stress adaptation.

The landscape of scientific publishing is experiencing a transformative shift toward open access, a paradigm that mandates the availability of research outputs such as data, code, materials, and publications. Open access provides increased reproducibility and allows for reuse of these resources. This article provides guidance for best publishing practices of scientific research, data, and associated resources, including code, in The American Phytopathological Society journals. Key areas such as diagnostic assays, experimental design, data sharing, and code deposition are explored in detail. This guidance aligns with that observed by other leading journals. We hope the information assembled in this paper will raise awareness of best practices and enable greater appraisal of the true effects of biological phenomena in plant pathology.

Downy mildews are obligate oomycete pathogens that attack a wide range of plants and can cause significant economic impacts on commercial crops and ornamental plants. Traditionally, downy mildew disease control relied on an integrated strategies, that incorporate cultural practices, deployment of resistant cultivars, crop rotation, application of contact and systemic pesticides, and biopesticides. Recent advances in genomics provided data that significantly advanced understanding of downy mildew evolution, taxonomy and classification. In addition, downy mildew genomics also revealed that these obligate oomycetes have reduced numbers of virulence factor genes in comparison to hemibiotrophic and necrotrophic oomycetes. However, downy mildews do deploy significant arrays of virulence proteins, including so-called RXLR proteins that promote virulence or are recognized as avirulence factors. Pathogenomics are being applied to downy mildew population studies to determine the genetic diversity within the downy mildew populations and manage disease by selection of appropriate varieties and management strategies. Genome editing technologies have been used to manipulate host disease susceptibility genes in different plants including grapevine and sweet basil and thereby provide new soucres of resistance genes against downy mildews. Previously, it has proved difficult to transform and manipulate downy mildews because of their obligate lifestyle. However, recent exploitation of RNA interference machinery through Host-Induced Gene Silencing (HIGS) and Spray-Induced Gene Silencing (SIGS) indicate that functional genomics in downy mildews is now possible. Altogether, these breakthrough technologies and attendant fundamental understanding will advance our ability to mitigate downy mildew diseases.

Translating ribosome affinity purification (TRAP) utilizes transgenic plants expressing a ribosomal protein fused to a tag for affinity co-purification of ribosomes and the mRNAs that they are translating. This population of actively translated mRNAs (translatome) can be interrogated by quantitative PCR or RNA sequencing. Condition- or cell-specific promoters can be utilized to isolate the translatome of specific cell types, at different growth stages and/or in response to environmental variables. While advantageous for revealing differential expression, this approach may not provide sufficient sensitivity when activity of the condition/cell-specific promoter is weak, when ribosome turnover is low in the cells of interest, or when the targeted cells are ephemeral. In these situations, expressing tagged ribosomes under the control of these specific promoters may not yield sufficient polysomes for downstream analysis. Here, we describe a new TRAP system that employs two transgenes: One is constitutively expressed and encodes a ribosomal protein fused to one fragment of a split green fluorescent protein (GFP); the second is controlled by a stimulus-specific promoter and encodes the second GFP fragment fused to an affinity purification tag. In cells where both transgenes are active, the purification tag is attached to ribosomes by bi-molecular folding and assembly of the split GFP fragments. This approach provides increased sensitivity and better temporal resolution because it labels pre-existing ribosomes and does not depend on rapid ribosome turnover. We describe the optimization and key parameters of this system, and then apply it to a plant-pathogen interaction in which spatial and temporal resolution are difficult to achieve with current technologies.

Plant diseases cause significant decreases in yield and quality of crops and consequently pose a very substantial threat to food security. In the continuous search for environmentally friendly crop protection, exploitation of RNA interferance machinery is showing promising results. It is well established that small RNAs (sRNAs) including microRNA (miRNA) and small interfering RNA (siRNA) are involved in the regulation of gene expression via both transcriptional and post-transcriptional RNA silencing. sRNAs from host plants can enter into pathogen cells during invasion and silence pathogen genes. This process has been exploited through Host-Induced Gene Silencing (HIGS), in which plant transgenes that produce sRNAs are engineered to silence pest and pathogen genes. Similarly, exogenously applied sRNAs can enter pest and pathogen cells, either directly or via the hosts, and silence target genes. This process has been exploited in Spray-Induced Gene Silencing (SIGS). Here, we focus on the role of sRNAs and review how they have recently been used against various plant pathogens through HIGS or SIGS-based methods and discuss advantages and drawbacks of these approaches.

Fungal and oomycete pathogens secrete complex arrays of proteins and small RNAs to interface with plant-host targets and manipulate plant regulatory networks to the microbes’ advantage. Research on these important virulence factors has been accelerated by improved genome sequences, refined bioinformatic prediction tools, and exploitation of efficient platforms for understanding effector gene expression and function. Recent studies have validated the expectation that oomycetes and fungi target many of the same sectors in immune signaling networks, but the specific host plant targets and modes of action are diverse. Effector research has also contributed to deeper understanding of the mechanisms of effector-triggered immunity.

Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth–promoting bacteria and fungi in the rhizosphere prime the whole plant body for ...Read More

The biochemical versatility of sulfur (S) lends itself to myriad roles in plant-pathogen interactions. This review evaluates the current understanding of mechanisms by which pathogens acquire S from their plant hosts and highlights new evidence that plants can limit S availability during the immune responses. We discuss the discovery of host disease-susceptibility genes related to S that can be genetically manipulated to create new crop resistance. Finally, we summarize future research challenges and propose a research agenda that leverages systems biology approaches for a holistic understanding of this important element's diverse roles in plant disease resistance and susceptibility.

In addition to their role in the biosynthesis of important molecules such as proteins and specialized metabolites, amino acids are known to function as signaling molecules through various pathways to report nitrogen status and trigger appropriate metabolic and cellular responses. Moreover, changes in amino acid levels through altered amino acid transporter activities trigger plant immune responses. Specifically, loss of function of major amino acid transporter, over-expression of cationic amino acid transporter, or over-expression of the positive regulators of membrane amino acid export all lead to dwarfed phenotypes and upregulated salicylic acid (SA)-induced stress marker genes. However, whether increasing amino acid exporter protein levels lead to similar stress phenotypes has not been investigated so far. Recently, a family of transporters, namely USUALLY MULTIPLE ACIDS MOVE IN AND OUT TRANSPORTERS (UMAMITs), were identified as amino acid exporters. The goal of this study was to investigate the effects of increased amino acid export on plant development, growth, and reproduction to further examine the link between amino acid transport and stress responses. The results presented here show strong evidence that an increased expression of UMAMIT transporters induces stress phenotypes and pathogen resistance, likely due to the establishment of a constitutive stress response via a SA-dependent pathway.

Iron metabolism and the plant immune system are both critical for plant vigor in natural ecosystems and for reliable agricultural productivity. Mechanistic studies of plant iron home-ostasis and plant immunity have traditionally been carried out in isolation from each other; however, our growing understanding of both processes has uncovered significant connections. For example, iron plays a critical role in the generation of reactive oxygen intermediates during immunity and has been recently implicated as a critical factor for immune-initiated cell death via ferroptosis. Moreover, plant iron stress triggers immune activation, suggesting that sensing of iron depletion is a mechanism by which plants recognize a pathogen threat. The iron deficiency response engages hormone signaling sectors that are also utilized for plant immune signaling, providing a probable explanation for iron-immunity cross-talk. Finally, interference with iron acquisition by pathogens might be a critical component of the immune response. Efforts to address the global burden of iron deficiency–related anemia have focused on classical breeding and transgenic approaches to develop crops biofortified for iron content. However, our improved mechanistic understanding of plant iron metabolism suggests that such alterations could promote or impede plant immunity, depending on the nature of the alteration and the virulence strategy of the pathogen. Effects of iron biofortification on disease resistance should be evaluated while developing plants for iron biofortification. Iron metabolism and the plant immune system are both critical for plant vigor in natural ecosystems and for reliable agricultural productivity. Mechanistic studies of plant iron home-ostasis and plant immunity have traditionally been carried out in isolation from each other; however, our growing understanding of both processes has uncovered significant connections. For example, iron plays a critical role in the generation of reactive oxygen intermediates during immunity and has been recently implicated as a critical factor for immune-initiated cell death via ferroptosis. Moreover, plant iron stress triggers immune activation, suggesting that sensing of iron depletion is a mechanism by which plants recognize a pathogen threat. The iron deficiency response engages hormone signaling sectors that are also utilized for plant immune signaling, providing a probable explanation for iron-immunity cross-talk. Finally, interference with iron acquisition by pathogens might be a critical component of the immune response. Efforts to address the global burden of iron deficiency–related anemia have focused on classical breeding and transgenic approaches to develop crops biofortified for iron content. However, our improved mechanistic understanding of plant iron metabolism suggests that such alterations could promote or impede plant immunity, depending on the nature of the alteration and the virulence strategy of the pathogen. Effects of iron biofortification on disease resistance should be evaluated while developing plants for iron biofortification. Iron (Fe) is an essential micronutrient for all living organisms, including plants and their associated microbes (1Camprubi E. Jordan S.F. Vasiliadou R. Lane N. Iron catalysis at the origin of life.IUBMB Life. 2017; 69 (28470848): 373-38110.1002/iub.1632Crossref PubMed Scopus (39) Google Scholar). Iron readily donates and accepts electrons, as it can exist in multiple oxidation states, particularly its ferric (Fe3+) and ferrous forms (Fe2+). Therefore, iron cofactors such as heme and Fe-sulfur clusters function in all primary metabolic processes, including respiration, DNA synthesis and repair, and cell proliferation and differentiation (1Camprubi E. Jordan S.F. Vasiliadou R. Lane N. Iron catalysis at the origin of life.IUBMB Life. 2017; 69 (28470848): 373-38110.1002/iub.1632Crossref PubMed Scopus (39) Google Scholar). In plants, iron is also essential for chlorophyll and hormone synthesis and photosynthesis. Despite iron's essentiality, iron overload can cause damage in any organism. This is because iron's potent electron chemistry also makes it dangerous when it is in physiological excess. Iron acts as a catalyst with hydrogen peroxide through the Fenton reaction (Table 1), producing more dangerous reactive oxygen species (ROS), including the highly reactive hydroxide ion (2Winterbourn C.C. Toxicity of iron and hydrogen peroxide: the Fenton reaction.Toxicol. Lett. 1995; 82-83 (8597169): 969-97410.1016/0378-4274(95)03532-XCrossref PubMed Scopus (675) Google Scholar). These potent oxidizers damage lipids, proteins, and nucleic acids (3Becana M. Moran J. Iturbe-Ormaetxe I. Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection.Plant Soil. 1998; 201: 137-14710.1023/A:1004375732137Crossref Scopus (203) Google Scholar, 4Pinto S.D S. Souza A.E.D. Oliva M.A. Pereira E.G. Oxidative damage and photosynthetic impairment in tropical rice cultivars upon exposure to excess iron.Sci. Agric. 2016; 73: 217-22610.1590/0103-9016-2015-0288Crossref Scopus (24) Google Scholar). When the damage becomes too severe, the cell cannot be saved and undergoes programmed cell death (5Tsai T.-M. Huang H.-J. Effects of iron excess on cell viability and mitogen-activated protein kinase activation in rice roots.Physiol. Plant. 2006; 127: 583-59210.1111/j.1399-3054.2006.00696.xCrossref Scopus (18) Google Scholar). Thus, balance of iron levels is imperative for all organisms. Accordingly, plants tightly regulate iron uptake, localization, transport, and storage. Exciting recent progress has been achieved in understanding how plants acquire and transport biologically active iron from the soil and respond to iron-deficient environments (6Samira R. Stallmann A. Massenburg L.N. Long T.A. Ironing out the issues: integrated approaches to understanding iron homeostasis in plants.Plant Sci. 2013; 210 (23849132): 250-25910.1016/j.plantsci.2013.06.004Crossref PubMed Scopus (0) Google Scholar, 7Kobayashi T. Nozoye T. Nishizawa N.K. Iron transport and its regulation in plants.Free Radic. Biol. Med. 2019; 133 (30385345): 11-2010.1016/j.freeradbiomed.2018.10.439Crossref PubMed Scopus (43) Google Scholar).Table 1GlossaryFenton reaction—A catalytic process by which free iron converts hydrogen peroxide to the biologically dangerous hydroxide radical.Pathogen-associated molecular pattern (PAMP)—Conserved epitopes of plant-pathogenic microbes that are recognized by plants to initiate an immune response.Pattern-triggered immunity (PTI)—A plant immune response triggered by receptor-mediated perception of PAMPs, typified by production of ROS, cell wall reinforcement, and transcriptional reprogramming.Pathogen effector—Proteinaceous virulence factor secreted by plant pathogens into host tissues or cells to disrupt immune functioning and accommodate pathogen growth and reproduction.Effector-triggered immunity (ETI)—A potent plant immune response triggered by perception of intracellular pathogen effectors or their activity; typified by programmed cell death called hypersensitive response (HR) to limit pathogen spread.Biotrophic pathogen—A plant pathogen that subsists on living host tissue during its entire life cycle.Necrotrophic pathogen—A plant pathogen that secretes virulence factors to kill host tissues and facilitate its feeding or reproduction.Hemibiotrophic pathogen—A plant pathogen that employs a biotrophic lifestyle at the start of infection but transitions to a necrotroph to complete its life cycle.Strategy I iron uptake—Mechanism for plant iron acquisition that relies on rhizosphere acidification and iron reduction, followed by direct import of ferrous iron; utilized by all non-Poaceae (nongrass) plants.Strategy II iron uptake—Mechanism for plant iron acquisition employed by the Poaceae (grasses); involves secretion of iron-binding phytosiderophores into the rhizosphere followed by uptake of the iron-siderophore complex.Nutritional immunity—A process, first described in mammals, by which a host organism restricts availability of nutrients following infection to starve a pathogen.Ferroptosis—Programmed cell death marked by accumulation of iron and loss of antioxidant protections, culminating in a runaway Fenton reaction and lipid peroxidation.Biofortification—Breeding or genetic engineering efforts designed to improve the nutritional content of edible plant tissues. Open table in a new tab Along with the challenge of maintaining nutrient homeostasis, plants also must cope with a wide variety of pathogens and pests. Plants have evolved robust mechanisms for perception of detrimental microbes, which in turn trigger physiological responses to impede infection (8Cook D.E. Mesarich C.H. Thomma B.P. Understanding plant immunity as a surveillance system to detect invasion.Annu. Rev. Phytopathol. 2015; 53 (26047564): 541-56310.1146/annurev-phyto-080614-120114Crossref PubMed Scopus (217) Google Scholar). Recent progress on iron homeostasis has been paralleled by progress in the molecular plant-microbe interaction field on understanding plant pathogen surveillance proteins, immune system signaling, and suppression of immunity by pathogen virulence proteins. These foci have provided huge payoffs in understanding how plants and microbes interact at the molecular level (9Michelmore R. Coaker G. Bart R. Beattie G. Bent A. Bruce T. Cameron D. Dangl J. Dinesh-Kumar S. Edwards R. Eves-van den Akker S. Gassmann W. Greenberg J.T. Hanley-Bowdoin L. Harrison R.J. et al.Foundational and translational research opportunities to improve plant health.Mol. Plant Microbe Interact. 2017; 30 (28398839): 515-51610.1094/MPMI-01-17-0010-CRCrossref PubMed Scopus (12) Google Scholar). The impact of iron on plant-pathogen interactions has been acknowledged for a considerable span of time but has received limited attention; indeed, iron homeostasis and plant immunity are typically studied in isolation from each other. One goal of this review is to highlight recent studies that connect iron and plant-pathogen interactions. We also discuss the implications of iron-immunity cross-talk on efforts to breed iron-fortified crops. We begin with primers on the regulatory networks that mediate plant immunity and plant iron homeostasis. Plant immune responses are activated when the plant detects signals that are diagnostic of pathogen invasion. For example, plants recognize a variety of pathogen-associated molecular patterns (PAMPs), initiating pattern-triggered immunity (PTI; Fig. 1C) (10Katagiri F. Tsuda K. Understanding the plant immune system.Mol. Plant Microbe Interact. 2010; 23 (20653410): 1531-153610.1094/MPMI-04-10-0099Crossref PubMed Scopus (136) Google Scholar). PAMPs are epitopes such as bacterial flagellin or fungal and oomycete cell wall components. Such epitopes are often evolutionarily conserved, allowing for detection of groups of pathogens (e.g. multiple species) that share the epitope (11Boller T. He S.Y. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens.Science. 2009; 324 (19423812): 742-74410.1126/science.1171647Crossref PubMed Scopus (582) Google Scholar). PAMPs can be detected in the apoplast by cell-surface receptors (12Gust A.A. Felix G. Receptor like proteins associate with sobir1-type of adaptors to form bimolecular receptor kinases.Curr. Opin. Plant Biol. 2014; 21 (25064074): 104-11110.1016/j.pbi.2014.07.007Crossref PubMed Scopus (0) Google Scholar). Such recognition initiates cytoplasmic protein kinase cascades, Ca2+ influx, and rapid production of ROS (13Macho A.P. Zipfel C. Plant PRRs and the activation of innate immune signaling.Mol. Cell. 2014; 54 (24766890): 263-27210.1016/j.molcel.2014.03.028Abstract Full Text Full Text PDF PubMed Scopus (438) Google Scholar). As discussed below, iron plays a key role in ROS generation. ROS and hormone signals interact with each other to stimulate diverse molecular and cellular responses that strengthen plant cells against pathogen attack (14Karapetyan S. Dong X. Redox and the circadian clock in plant immunity: a balancing act.Free Radic. Biol. Med. 2018; 119 (29274381): 56-6110.1016/j.freeradbiomed.2017.12.024Crossref PubMed Scopus (24) Google Scholar). PAMP perception leads to reprogramming of thousands of genes, including genes for antimicrobial proteins (e.g. iron-sequestering defensins discussed below) and secondary metabolites with antimicrobial activity (13Macho A.P. Zipfel C. Plant PRRs and the activation of innate immune signaling.Mol. Cell. 2014; 54 (24766890): 263-27210.1016/j.molcel.2014.03.028Abstract Full Text Full Text PDF PubMed Scopus (438) Google Scholar). At the cellular level, pathogens often require access to individual cells or host vasculature; thus, the plant produces callose to reinforce cell walls against hydrolases and pathogen secretion systems (15Luna E. Pastor V. Robert J. Flors V. Mauch-Mani B. Ton J. Callose deposition: a multifaceted plant defense response.Mol. Plant Microbe Interact. 2011; 24 (20955078): 183-19310.1094/MPMI-07-10-0149Crossref PubMed Scopus (374) Google Scholar). All microbial pathogens produce PAMPs and are therefore vulnerable to PTI. Accordingly, pathogen success depends on evasion of detection and/or suppression of PTI signaling (16Nobori T. Mine A. Tsuda K. Molecular networks in plant-pathogen holobiont.FEBS Lett. 2018; 592 (29714033): 1937-195310.1002/1873-3468.13071Crossref PubMed Scopus (10) Google Scholar). Many pathogens disguise themselves by secreting proteins to bind PAMPs, thereby obscuring recognition, leading to PTI (17Sánchez-Vallet A. Saleem-Batcha R. Kombrink A. Hansen G. Valkenburg D.-J. Thomma B.P. Mesters J.R. Fungal effector ECP6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization.eLife. 2013; 2 (23840930): e0079010.7554/eLife.00790Crossref PubMed Scopus (141) Google Scholar). In a second strategy to interfere with activation of host immunity, pathogens secrete virulence proteins called effectors to inhibit critical regulatory components of host immune signaling (18Toruño T.Y. Stergiopoulos I. Coaker G. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners.Annu. Rev. Phytopathol. 2016; 54 (27359369): 419-44110.1146/annurev-phyto-080615-100204Crossref PubMed Google Scholar). Effectors from bacteria, fungi, and oomycetes have been shown to target similar hubs in the host immune signaling network (19Mukhtar M.S. Carvunis A.R. Dreze M. Epple P. Steinbrenner J. Moore J. Tasan M. Galli M. Hao T. Nishimura M.T. Pevzner S.J. Donovan S.E. Ghamsari L. Santhanam B. Romero V. et al.Independently evolved virulence effectors converge onto hubs in a plant immune system network.Science. 2011; 333 (21798943): 596-60110.1126/science.1203659Crossref PubMed Scopus (511) Google Scholar). The action of these effectors results in an attenuated immune response called effector-triggered susceptibility (20Chisholm S.T. Coaker G. Day B. Staskawicz B.J. Host-microbe interactions: shaping the evolution of the plant immune response.Cell. 2006; 124 (16497589): 803-81410.1016/j.cell.2006.02.008Abstract Full Text Full Text PDF PubMed Scopus (1797) Google Scholar). To counter the threat of effector-triggered susceptibility, plants have evolved resistance proteins (R proteins) to detect pathogen effectors and initiate effector-triggered immunity (ETI; Fig. 1D) (21Kourelis J. van der Hoorn R.A.L. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function.Plant Cell. 2018; 30 (29382771): 285-29910.1105/tpc.17.00579Crossref PubMed Scopus (173) Google Scholar). Some R proteins bind directly to the cognate effector, similar to direct binding of PAMP ligands by pattern recognition receptors. However, it is more common for R proteins to indirectly detect effectors by “guarding” immune hubs that effectors target (21Kourelis J. van der Hoorn R.A.L. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function.Plant Cell. 2018; 30 (29382771): 285-29910.1105/tpc.17.00579Crossref PubMed Scopus (173) Google Scholar). By perceiving the virulence activities of effectors (e.g. proteolytic degradation of an immune signaling protein) rather than the effectors themselves, a single R protein can protect the plant from multiple pathogens that have converged to target the same protein complex (22Van Der Biezen E.A. Jones J.D. Plant disease-resistance proteins and the gene-for-gene concept.Trends Biochem. Sci. 1998; 23 (9868361): 454-45610.1016/S0968-0004(98)01311-5Abstract Full Text Full Text PDF PubMed Scopus (561) Google Scholar). ETI and PTI activate many of the same signaling pathways and defense responses. However, ETI is typically faster, its signaling is more resistant to pathogen interference, and the downstream responses are stronger than in PTI (10Katagiri F. Tsuda K. Understanding the plant immune system.Mol. Plant Microbe Interact. 2010; 23 (20653410): 1531-153610.1094/MPMI-04-10-0099Crossref PubMed Scopus (136) Google Scholar). Moreover, ETI is often distinguished from PTI by activation of programmed cell death at the site of infection, referred to as the hypersensitive response (HR). A recent study describes a novel role for iron in activation of ETI and will be discussed below (23Dangol S. Chen Y. Hwang B.K. Jwa N.-S. Iron-and reactive oxygen species-dependent ferroptotic cell death in rice-Magnaporthe oryzae interactions.Plant Cell. 2019; 31 (30563847): 189-20910.1105/tpc.18.00535Crossref PubMed Scopus (0) Google Scholar). Plant pathogens typically follow one of three lifestyles: biotrophic, hemibiotrophic, or necrotrophic (Fig. 1C). Biotrophic pathogens can only extract nutrients from living host cells (24McDowell J.M. Genomes of obligate plant pathogens reveal adaptations for obligate parasitism.Proc. Natl. Acad. Sci. U. S. A. 2011; 108 (21576481): 8921-892210.1073/pnas.1105802108Crossref PubMed Scopus (0) Google Scholar). Such pathogens are able to suppress host immunity, extract nutrients, and complete their life cycle without killing host cells. Contrastingly, necrotrophic pathogens kill host cells with toxins and complete their life cycle by feeding from dead or dying plant tissue (25Mengiste T. Plant immunity to necrotrophs.Annu. Rev. Phytopathol. 2012; 50 (22726121): 267-29410.1146/annurev-phyto-081211-172955Crossref PubMed Scopus (285) Google Scholar). Hemibiotrophic pathogens begin the infection cycle with an extended period of biotrophy before triggering a necrotrophic program. Plants deploy different immune responses against pathogens with these contrasting lifestyles, and plant hormones play key roles in coordinating the immune responses that are most efficient against pathogens with these contrasting lifestyles (26Spoel S.H. Dong X. 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Moreover, the response of rice and other monocots to iron deficiency differs from that of maize by utilizing aspects of both Strategy I and II for iron uptake (49Wairich A. de Oliveira B.H.N. Arend E.B. Duarte G.L. Ponte L.R. Sperotto

Plant NLR-type receptors serve as sensitive triggers of host immunity. Their expression has to be well-balanced, due to their interference with various cellular processes and dose-dependency of their defense-inducing activity. A genetic "arms race" with fast-evolving pathogenic microbes requires plants to constantly innovate their NLR repertoires. We previously showed that insertion of the COPIA-R7 retrotransposon into RPP7 co-opted the epigenetic transposon silencing signal H3K9me2 to a new function promoting expression of this Arabidopsis thaliana NLR gene. Recruitment of the histone binding protein EDM2 to COPIA-R7-associated H3K9me2 is required for optimal expression of RPP7. By profiling of genome-wide effects of EDM2, we now uncovered additional examples illustrating effects of transposons on NLR gene expression, strongly suggesting that these mobile elements can play critical roles in the rapid evolution of plant NLR genes by providing the "raw material" for gene expression mechanisms. We further found EDM2 to have a global role in NLR expression control. Besides serving as a positive regulator of RPP7 and a small number of other NLR genes, EDM2 acts as a suppressor of a multitude of additional NLR genes. We speculate that the dual functionality of EDM2 in NLR expression control arose from the need to compensate for fitness penalties caused by high expression of some NLR genes by suppression of others. Moreover, we are providing new insights into functional relationships of EDM2 with its interaction partner, the RNA binding protein EDM3/AIPP1, and its target gene IBM1, encoding an H3K9-demethylase.

Iron metabolism and the plant immune system are both critical for plant vigor in natural ecosystems and for reliable agricultural productivity. Mechanistic studies of plant iron home-ostasis and plant immunity have traditionally been carried out in isolation from each other; however, our growing understanding of both processes has uncovered significant connections. For example, iron plays a critical role in the generation of reactive oxygen intermediates during immunity and has been recently implicated as a critical factor for immune-initiated cell death via ferroptosis. Moreover, plant iron stress triggers immune activation, suggesting that sensing of iron depletion is a mechanism by which plants recognize a pathogen threat. The iron deficiency response engages hormone signaling sectors that are also utilized for plant immune signaling, providing a probable explanation for iron-immunity cross-talk. Finally, interference with iron acquisition by pathogens might be a critical component of the immune response. Efforts to address the global burden of iron deficiency-related anemia have focused on classical breeding and transgenic approaches to develop crops biofortified for iron content. However, our improved mechanistic understanding of plant iron metabolism suggests that such alterations could promote or impede plant immunity, depending on the nature of the alteration and the virulence strategy of the pathogen. Effects of iron biofortification on disease resistance should be evaluated while developing plants for iron biofortification.

Disease development in plants requires a susceptible host, a virulent pathogen, and a favourable environment. Oomycete pathogens cause many important diseases and have evolved sophisticated molecular mechanisms to manipulate their hosts. Day length has been shown to impact plant-oomycete interactions but a need exists for a tractable reference system to understand the mechanistic interplay between light regulation, oomycete pathogen virulence, and plant host immunity. Here we present data demonstrating that light is a critical factor in the interaction between Arabidopsis thaliana and its naturally occurring downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa). We investigated the role of light on spore germination, mycelium development, sporulation and oospore formation of Hpa, along with defence responses in the host. We observed abundant Hpa sporulation on compatible Arabidopsis under day lengths ranging from 10 to 14 hours. Contrastingly, exposure to constant light or constant dark suppressed sporulation. Exposure to constant dark suppressed spore germination, mycelial development and oospore formation. Interestingly, exposure to constant light stimulated spore germination, mycelial development and oospore formation. A biomarker of plant immune system activation was induced under both constant light and constant dark. Altogether, these findings demonstrate that Hpa has the molecular mechanisms to perceive and respond to light and that both the host and pathogen responses are influenced by the light regime. Therefore, this pathosystem can be used for investigations to understand the molecular mechanisms through which oomycete pathogens like Hpa perceive and integrate light signals, and how light influences pathogen virulence and host immunity during their interactions.

Understanding the mechanisms through which pathogens alter plant cell networks is essential for understanding plant-pathogen interactions and will inform efforts to reduce crop diseases. Oomycetes secrete diverse effector proteins into plant cells. The mechanisms through which these effectors promote virulence are largely unknown. We show that the HaRxL10 effector protein from the Arabidopsis thaliana pathogen Hyaloperonospora arabidopsidis (Hpa) targets a transcriptional repressor (JAZ3) involved in jasmonic acid (JA) signalling. This manipulation activates a regulatory cascade that inhibits salicylic acid (SA) signalling, which normally restricts Hpa infection. This virulence mechanism is functionally equivalent to but mechanistically distinct from activation of the antagonistic JA-SA hormone crosstalk by the bacterial JA-mimicking toxin coronatine and by bacterial Type III effectors. These results reveal a key role for JAZ3 in plant immunity and emphasize that JA-SA crosstalk is an Achilles heel in the plant immune system, vulnerable to manipulation by diverse microbes.