Modulation of plant immunity and biotic interactions under phosphate deficiency.

Phosphorus (P) is an essential macronutrient for plant life and growth. P is primarily acquired in the form of inorganic phosphate (Pi) from soil. To cope with Pi deficiency, plants have evolved an elaborate system to improve Pi acquisition and utilization through an array of developmental and physiological changes, termed Pi starvation response (PSR). Plants also assemble and manage mutualistic microbes to enhance Pi uptake, through integrating PSR and immunity signaling. A trade-off between plant growth and defense favors the notion that plants lower a cellular state of immunity to accommodate host-beneficial microbes for nutrition and growth at the cost of infection risk. However, the existing data indicate that plants selectively activate defense responses against pathogens, but do not or less against non-pathogens, even under nutrient deficiency. In this review, we highlight recent advances in the principles and mechanisms with which plants balance immunity and growth-related processes to optimize their adaptation to Pi deficiency.

Molecular complexity of quantitative immunity in plants: from QTL mapping to functional and systems biology.

In nature, plants defend themselves against pathogen attack by activating an arsenal of defense mechanisms. During the last decades, work mainly focused on the understanding of qualitative disease resistance mediated by a few genes conferring an almost complete resistance, while quantitative disease resistance (QDR) remains poorly understood despite the fact that it represents the predominant and more durable form of resistance in natural populations and crops. Here, we review our past and present work on the dissection of the complex mechanisms underlying QDR in Arabidopsis thaliana. The strategies, main steps and challenges of our studies related to one atypical QDR gene, RKS1 (Resistance related KinaSe 1), are presented. First, from genetic analyses by QTL (Quantitative Trait Locus) mapping and GWAs (Genome Wide Association studies), the identification, cloning and functional analysis of this gene have been used as a starting point for the exploration of the multiple and coordinated pathways acting together to mount the QDR response dependent on RKS1. Identification of RKS1 protein interactors and complexes was a first step, systems biology and reconstruction of protein networks were then used to decipher the molecular roadmap to the immune responses controlled by RKS1. Finally, exploration of the potential impact of key components of the RKS1-dependent gene network on leaf microbiota offers interesting and challenging perspectives to decipher how the plant immune systems interact with the microbial communities' systems.

Dans la nature, les plantes se défendent contre les attaques pathogènes en activant tout un arsenal de mécanismes de défense. Au cours des décennies passées, la recherche s'est principalement focalisée sur la compréhension de la résistance qualitative médiée par quelques gènes majeurs conférant une résistance quasi complète, alors que la résistance quantitative (QDR) demeure peu comprise bien qu'elle représente la forme de résistance prédominante et la plus durable dans les populations naturelles ou les cultures. Nous donnons ici une revue de nos travaux passés et présents sur la dissection des mécanismes complexes qui sous-tendent la QDR chez Arabidopsis thaliana. Les stratégies, étapes clés et défis de nos études concernant un gène QDR atypique, RKS1 (Resistance related KinaSe 1), sont rapportés. En premier lieu, à partir d'analyses génétiques par cartographie de QTL et GWA, l'identification, le clonage et l'analyse fonctionnelle de ce gène ont été utilisés comme point de départ à l'exploration des voies multiples et coordonnées agissant ensemble pour le développement de la réponse QDR dépendante de RKS1. L'identification des interacteurs et complexes protéiques impliquant RKS1 a été une première étape, la biologie des systèmes et la reconstruction de réseaux d'interactions protéines-protéines ont ensuite été mises en œuvre pour décoder les voies moléculaires conduisant aux réponses immunitaires contrôlées par RKS1. Finalement, l'exploration de l'impact potentiel de composantes clés du réseau de gènes dépendant de RKS1 sur le microbiote, offre des perspectives intéressantes et ambitieuses pour comprendre comment le système immunitaire de la plante interagit avec le système des communautés microbiennes.

Unveiling Methods to Stimulate Plant Resistance against Pathogens.

Plant diseases caused by pathogens pose significant threats to agricultural productivity and food security worldwide. The traditional approach of relying on chemical pesticides for disease management has proven to be unsustainable, emphasizing the urgent need for sustainable and environmentally friendly alternatives. One promising strategy is to enhance plant resistance against pathogens through various methods. This review aims to unveil and explore effective methods for stimulating plant resistance, transforming vulnerable plants into vigilant defenders against pathogens. We discuss both conventional and innovative approaches, including genetic engineering, induced systemic resistance (ISR), priming, and the use of natural compounds. Furthermore, we analyze the underlying mechanisms involved in these methods, highlighting their potential advantages and limitations. Through an understanding of these methods, scientists and agronomists can develop novel strategies to combat plant diseases effectively while minimizing the environmental impact. Ultimately, this research offers valuable insights into harnessing the plant's innate defense mechanisms and paves the way for sustainable disease management practices in agriculture.

The plant immune system: From discovery to deployment.

Plant diseases cause famines, drive human migration, and present challenges to agricultural sustainability as pathogen ranges shift under climate change. Plant breeders discovered Mendelian genetic loci conferring disease resistance to specific pathogen isolates over 100 years ago. Subsequent breeding for disease resistance underpins modern agriculture and, along with the emergence and focus on model plants for genetics and genomics research, has provided rich resources for molecular biological exploration over the last 50 years. These studies led to the identification of extracellular and intracellular receptors that convert recognition of extracellular microbe-encoded molecular patterns or intracellular pathogen-delivered virulence effectors into defense activation. These receptor systems, and downstream responses, define plant immune systems that have evolved since the migration of plants to land ∼500 million years ago. Our current understanding of plant immune systems provides the platform for development of rational resistance enhancement to control the many diseases that continue to plague crop production.

Structural homology of mite profilins to plant profilins is not indicative of allergic cross-reactivity.

Structural and allergenic characterization of mite profilins has not been previously pursued to a similar extent as plant profilins. Here, we describe structures of profilins originating from Tyrophagus putrescentiae (registered allergen Tyr p 36.0101) and Dermatophagoides pteronyssinus (here termed Der p profilin), which are the first structures of profilins from Arachnida. Additionally, the thermal stabilities of mite and plant profilins are compared, suggesting that the high number of cysteine residues in mite profilins may play a role in their increased stability. We also examine the cross-reactivity of plant and mite profilins as well as investigate the relevance of these profilins in mite inhalant allergy. Despite their high structural similarity to other profilins, mite profilins have low sequence identity with plant and human profilins. Subsequently, these mite profilins most likely do not display cross-reactivity with plant profilins. At the same time the profilins have highly conserved poly(l-proline) and actin binding sites.

Cytoskeleton remodeling: a central player in plant-fungus interactions.

The eukaryotic cytoskeleton is a complex scaffold consisting of actin filaments, intermediate filaments, and microtubules. Although fungi and plants lack intermediate filaments, their dynamic structural network of actin filaments and microtubules regulates cell shape, division, polarity, and vesicular trafficking. However, the specialized functions of the cytoskeleton during plant-fungus interactions remain elusive. Recent reports demonstrate that the plant cytoskeleton responds to signal cues and pathogen invasion through remodeling, thereby coordinating immune receptor trafficking, membrane microdomain formation, aggregation of organelles, and transport of defense compounds. Emerging evidence also suggests that cytoskeleton remodeling further regulates host immunity by triggering salicylic acid signaling, reactive oxygen species generation, and pathogenesis-related gene expression. During host invasion, fungi undergo systematic cytoskeleton remodeling, which is crucial for successful host penetration and colonization. Furthermore, phytohormones act as an essential regulator of plant cytoskeleton dynamics and are frequently targeted by fungal effectors to disrupt the host's growth-defense balance. This review discusses recent advances in the understanding of cytoskeleton dynamics during plant-fungus interactions and provides novel insights into the relationship between phytohormones and cytoskeleton remodeling upon pathogen attack. We also highlight the importance of fungal cytoskeleton rearrangements during host colonization and suggest directions for future investigations in this field.

Plant cell wall-mediated disease resistance: Current understanding and future perspectives.

Beyond their function as structural barriers, plant cell walls are essential elements for the adaptation of plants to environmental conditions. Cell walls are dynamic structures whose composition and integrity can be altered in response to environmental challenges and developmental cues. These wall changes are perceived by plant sensors/receptors to trigger adaptative responses during development and upon stress perception. Plant cell wall damage caused by pathogen infection, wounding, or other stresses leads to the release of wall molecules, such as carbohydrates (glycans), that function as damage-associated molecular patterns (DAMPs). DAMPs are perceived by the extracellular ectodomains (ECDs) of pattern recognition receptors (PRRs) to activate pattern-triggered immunity (PTI) and disease resistance. Similarly, glycans released from the walls and extracellular layers of microorganisms interacting with plants are recognized as microbe-associated molecular patterns (MAMPs) by specific ECD-PRRs triggering PTI responses. The number of oligosaccharides DAMPs/MAMPs identified that are perceived by plants has increased in recent years. However, the structural mechanisms underlying glycan recognition by plant PRRs remain limited. Currently, this knowledge is mainly focused on receptors of the LysM-PRR family, which are involved in the perception of various molecules, such as chitooligosaccharides from fungi and lipo-chitooligosaccharides (i.e., Nod/MYC factors from bacteria and mycorrhiza, respectively) that trigger differential physiological responses. Nevertheless, additional families of plant PRRs have recently been implicated in oligosaccharide/polysaccharide recognition. These include receptor kinases (RKs) with leucine-rich repeat and Malectin domains in their ECDs (LRR-MAL RKs), Catharanthus roseus RECEPTOR-LIKE KINASE 1-LIKE group (CrRLK1L) with Malectin-like domains in their ECDs, as well as wall-associated kinases, lectin-RKs, and LRR-extensins. The characterization of structural basis of glycans recognition by these new plant receptors will shed light on their similarities with those of mammalians involved in glycan perception. The gained knowledge holds the potential to facilitate the development of sustainable, glycan-based crop protection solutions.

Logistics of defense: The contribution of endomembranes to plant innate immunity.

Phytopathogens cause plant diseases that threaten food security. Unlike mammals, plants lack an adaptive immune system and rely on their innate immune system to recognize and respond to pathogens. Plant response to a pathogen attack requires precise coordination of intracellular traffic and signaling. Spatial and/or temporal defects in coordinating signals and cargo can lead to detrimental effects on cell development. The role of intracellular traffic comes into a critical focus when the cell sustains biotic stress. In this review, we discuss the current understanding of the post-immune activation logistics of plant defense. Specifically, we focus on packaging and shipping of defense-related cargo, rerouting of intracellular traffic, the players enabling defense-related traffic, and pathogen-mediated subversion of these pathways. We highlight the roles of the cytoskeleton, cytoskeleton-organelle bridging proteins, and secretory vesicles in maintaining pathways of exocytic defense, acting as sentinels during pathogen attack, and the necessary elements for building the cell wall as a barrier to pathogens. We also identify points of convergence between mammalian and plant trafficking pathways during defense and highlight plant unique responses to illustrate evolutionary adaptations that plants have undergone to resist biotic stress.

Reviewing impacts of biotic and abiotic stresses on the regulation of phosphate homeostasis in plants.

Adapting to varying phosphate levels in the environment is vital for plant growth. The PHR1 phosphate starvation response transcription factor family, along with SPX inhibitors, plays a pivotal role in plant phosphate responses. However, this regulatory hub intricately links with diverse biotic and abiotic signaling pathways, as outlined in this review. Understanding these intricate networks is crucial, not only on a fundamental level but also for practical applications, such as enhancing sustainable agriculture and optimizing fertilizer efficiency. This comprehensive review explores the multifaceted connections between phosphate homeostasis and environmental stressors, including various biotic factors, such as symbiotic mycorrhizal associations and beneficial root-colonizing fungi. The complex coordination between phosphate starvation responses and the immune system are explored, and the relationship between phosphate and nitrate regulation in agriculture are discussed. Overall, this review highlights the complex interactions governing phosphate homeostasis in plants, emphasizing its importance for sustainable agriculture and nutrient management to contribute to environmental conservation.

Chitin-induced disease resistance in plants: A review.

Chitin is composed of N-acetylglucosamine units. Chitin a polysaccharide found in the cell walls of fungi and exoskeletons of insects and crustaceans, can elicit a potent defense response in plants. Through the activation of defense genes, stimulation of defensive compound production, and reinforcement of physical barriers, chitin enhances the plant's ability to defend against pathogens. Chitin-based treatments have shown efficacy against various plant diseases caused by fungal, bacterial, viral, and nematode pathogens, and have been integrated into sustainable agricultural practices. Furthermore, chitin treatments have demonstrated additional benefits, such as promoting plant growth and improving tolerance to abiotic stresses. Further research is necessary to optimize treatment parameters, explore chitin derivatives, and conduct long-term field studies. Continued efforts in these areas will contribute to the development of innovative and sustainable strategies for disease management in agriculture, ultimately leading to improved crop productivity and reduced reliance on chemical pesticides.

Long-Term Consequences of PTI Activation and Its Manipulation by Root-Associated Microbiota.

In nature, plants are constantly colonized by a massive diversity of microbes engaged in mutualistic, pathogenic or commensal relationships with the host. Molecular patterns present in these microbes activate pattern-triggered immunity (PTI), which detects microbes in the apoplast or at the tissue surface. Whether and how PTI distinguishes among soil-borne pathogens, opportunistic pathogens, and commensal microbes within the soil microbiota remains unclear. PTI is a multimodal series of molecular events initiated by pattern perception, such as Ca2+ influx, reactive oxygen burst, and extensive transcriptional and metabolic reprogramming. These short-term responses may manifest within minutes to hours, while the long-term consequences of chronic PTI activation persist for days to weeks. Chronic activation of PTI is detrimental to plant growth, so plants need to coordinate growth and defense depending on the surrounding biotic and abiotic environments. Recent studies have demonstrated that root-associated commensal microbes can activate or suppress immune responses to variable extents, clearly pointing to the role of PTI in root-microbiota interactions. However, the molecular mechanisms by which root commensals interfere with root immunity and root immunity modulates microbial behavior remain largely elusive. Here, with a focus on the difference between short-term and long-term PTI responses, we summarize what is known about microbial interference with host PTI, especially in the context of root microbiota. We emphasize some missing pieces that remain to be characterized to promote the ultimate understanding of the role of plant immunity in root-microbiota interactions.

Salicylic acid in plant immunity and beyond.

As the most widely used herbal medicine in human history and a major defence hormone in plants against a broad spectrum of pathogens and abiotic stresses, salicylic acid (SA) has attracted major research interest. With applications of modern technologies over the past 30 years, studies of the effects of SA on plant growth, development, and defence have revealed many new research frontiers and continue to deliver surprises. In this review, we provide an update on recent advances in our understanding of SA metabolism, perception, and signal transduction mechanisms in plant immunity. An overarching theme emerges that SA executes its many functions through intricate regulation at multiple steps: SA biosynthesis is regulated both locally and systemically, while its perception occurs through multiple cellular targets, including metabolic enzymes, redox regulators, transcription cofactors, and, most recently, an RNA-binding protein. Moreover, SA orchestrates a complex series of post-translational modifications of downstream signaling components and promotes the formation of biomolecular condensates that function as cellular signalling hubs. SA also impacts wider cellular functions through crosstalk with other plant hormones. Looking into the future, we propose new areas for exploration of SA functions, which will undoubtedly uncover more surprises for many years to come.

Pathogen perception and signaling in plant immunity.

Plant diseases are a constant and serious threat to agriculture and ecological biodiversity. Plants possess a sophisticated innate immunity system capable of detecting and responding to pathogen infection to prevent disease. Our understanding of this system has grown enormously over the past century. Early genetic descriptions of plant disease resistance and pathogen virulence were embodied in the gene-for-gene hypothesis, while physiological studies identified pathogen-derived elicitors that could trigger defense responses in plant cells and tissues. Molecular studies of these phenomena have now coalesced into an integrated model of plant immunity involving cell surface and intracellular detection of specific pathogen-derived molecules and proteins culminating in the induction of various cellular responses. Extracellular and intracellular receptors engage distinct signaling processes but converge on many similar outputs with substantial evidence now for integration of these pathways into interdependent networks controlling disease outcomes. Many of the molecular details of pathogen recognition and signaling processes are now known, providing opportunities for bioengineering to enhance plant protection from disease. Here we provide an overview of the current understanding of the main principles of plant immunity, with an emphasis on the key scientific milestones leading to these insights.

Extracellular niche establishment by plant pathogens.

The plant extracellular space, referred to as the apoplast, is inhabited by a variety of microorganisms. Reflecting the crucial nature of this compartment, both plants and microorganisms seek to control, exploit and respond to its composition. Upon sensing the apoplastic environment, pathogens activate virulence programmes, including the delivery of effectors with well-established roles in suppressing plant immunity. We posit that another key and foundational role of effectors is niche establishment - specifically, the manipulation of plant physiological processes to enrich the apoplast in water and nutritive metabolites. Facets of plant immunity counteract niche establishment by restricting water, nutrients and signals for virulence activation. The complex competition to control and, in the case of pathogens, exploit the apoplast provides remarkable insights into the nature of virulence, host susceptibility, host defence and, ultimately, the origin of phytopathogenesis. This novel framework focuses on the ecology of a microbial niche and highlights areas of future research on plant-microorganism interactions.

Antibody-based defense may protect plants from disease.

A "creative" strategy to keep crops healthy borrows key pathogen detectors from the animal immune system.

The emerging frontier of plant immunity's core hubs.

The ever-growing world population, increasingly frequent extreme weather events and conditions, emergence of novel devastating crop pathogens and the social strive for quality food products represent a huge challenge for current and future agricultural production systems. To address these challenges and find realistic solutions, it is becoming more important by the day to understand the complex interactions between plants and the environment, mainly the associated organisms, but in particular pathogens. In the past several years, research in the fields of plant pathology and plant-microbe interactions has enabled tremendous progress in understanding how certain receptor-based plant innate immune systems function to successfully prevent infections and diseases. In this review, we highlight and discuss some of these new ground-breaking discoveries and point out strategies of how pathogens counteract the function of important core convergence hubs of the plant immune system. For practical reasons, we specifically place emphasis on potential applications that can be detracted by such discoveries and what challenges the future of agriculture has to face, but also how these challenges could be tackled.

Deploying Viruses against Phytobacteria: Potential Use of Phage Cocktails as a Multifaceted Approach to Combat Resistant Bacterial Plant Pathogens.

Plants in nature are under the persistent intimidation of severe microbial diseases, threatening a sustainable food production system. Plant-bacterial pathogens are a major concern in the contemporary era, resulting in reduced plant growth and productivity. Plant antibiotics and chemical-based bactericides have been extensively used to evade plant bacterial diseases. To counteract this pressure, bacteria have evolved an array of resistance mechanisms, including innate and adaptive immune systems. The emergence of resistant bacteria and detrimental consequences of antimicrobial compounds on the environment and human health, accentuates the development of an alternative disease evacuation strategy. The phage cocktail therapy is a multidimensional approach effectively employed for the biocontrol of diverse resistant bacterial infections without affecting the fauna and flora. Phages engage a diverse set of counter defense strategies to undermine wide-ranging anti-phage defense mechanisms of bacterial pathogens. Microbial ecology, evolution, and dynamics of the interactions between phage and plant-bacterial pathogens lead to the engineering of robust phage cocktail therapeutics for the mitigation of devastating phytobacterial diseases. In this review, we highlight the concrete and fundamental determinants in the development and application of phage cocktails and their underlying mechanism, combating resistant plant-bacterial pathogens. Additionally, we provide recent advances in the use of phage cocktail therapy against phytobacteria for the biocontrol of devastating plant diseases.

Distribution of flagellin CD2-1, flg22, and flgII-28 recognition systems in plant species and regulation of plant immune responses through these recognition systems.

The first layer of active plant immunity relies upon the recognition of pathogen-associated molecular patterns (PAMPs), and the induction of PTI. Flagellin is the major protein component of the bacterial flagellum. Flagellin-derived peptide fragments such as CD2-1, flg22, and flgII-28 function as PAMPs in most higher plants. To determine the distribution of CD2-1, flg22, and flgII-28 recognition systems within plant species, the inducibility of PTI by CD2-1, flg22, and flgII-28 in 8 plant species, including monocotyledonous and dicotyledonous plants, was investigated. CD2-1 caused PTI responses in Oryza sativa, Brachypodium distachyon, and Asparagus persicus; flg22 caused PTI responses in Phyllostachys nigra, A. persicus, Arabidopsis thaliana, Nicotiana tabacum, Solanum lycopersicum, and Lotus japonicus; and flgII-28 caused PTI responses only in S. lycopersicum. Furthermore, quantitative analysis of FLS2 receptor revealed that the responsiveness of flg22 in plants was dependent on the expression level of the receptor.

Network organization of the plant immune system: from pathogen perception to robust defense induction.

The plant immune system has been explored essentially through the study of qualitative resistance, a simple form of immunity, and from a reductionist point of view. The recent identification of genes conferring quantitative disease resistance revealed a large array of functions, suggesting more complex mechanisms. In addition, thanks to the advent of high-throughput analyses and system approaches, our view of the immune system has become more integrative, revealing that plant immunity should rather be seen as a distributed and highly connected molecular network including diverse functions to optimize expression of plant defenses to pathogens. Here, we review the recent progress made to understand the network complexity of regulatory pathways leading to plant immunity, from pathogen perception, through signaling pathways and finally to immune responses. We also analyze the topological organization of these networks and their emergent properties, crucial to predict novel immune functions and test them experimentally. Finally, we report how these networks might be regulated by environmental clues. Although system approaches remain extremely scarce in this area of research, a growing body of evidence indicates that the plant response to combined biotic and abiotic stresses cannot be inferred from responses to individual stresses. A view of possible research avenues in this nascent biology domain is finally proposed.