Plant Immunity Modulation in Arbuscular Mycorrhizal Symbiosis and Its Impact on Pathogens and Pests.

Arbuscular mycorrhizal (AM) symbiosis is the oldest and most widespread mutualistic association on Earth and involves plants and soil fungi belonging to Glomeromycotina. A complex molecular, cellular, and genetic developmental program enables partner recognition, fungal accommodation in plant tissues, and activation of symbiotic functions such as transfer of phosphorus in exchange for carbohydrates and lipids. AM fungi, as ancient obligate biotrophs, have evolved strategies to circumvent plant defense responses to guarantee an intimate and long-lasting mutualism. They are among those root-associated microorganisms able to boost plants' ability to cope with biotic stresses leading to mycorrhiza-induced resistance (MIR), which can be effective across diverse hosts and against different attackers. Here, we examine the molecular mechanisms underlying the modulation of plant immunity during colonization by AM fungi and at the onset and display of MIR against belowground and aboveground pests and pathogens. Understanding the MIR efficiency spectrum and its regulation is of great importance to optimizing the biotechnological application of these beneficial microbes for sustainable crop protection.

Plant Growth Promoting Rhizobacteria (PGPR) induced protection: A plant immunity perspective.

Plant-environment interactions, particularly biotic stress, are increasingly essential for global food security due to crop losses in the dynamic environment. Therefore, understanding plant responses to biotic stress is vital to mitigate damage. Beneficial microorganisms and their association with plants can reduce the damage associated with plant pathogens. One such group is PGPR (Plant growth-promoting rhizobacteria), which influences plant immunity significantly by interacting with biotic stress factors and plant signalling compounds. This review explores the types, metabolism, and mechanisms of action of PGPR, including their enzyme pathways and the signalling compounds secreted by PGPR that modulate gene and protein expression during plant defence. Furthermore, the review will delve into the crosstalk between PGPR and other plant growth regulators and signalling compounds, elucidating the physiological, biochemical, and molecular insights into PGPR's impact on plants under multiple biotic stresses, including interactions with fungi, bacteria, and viruses. Overall, the review comprehensively adds to our knowledge about PGPR's role in plant immunity and its application for agricultural resilience and food security.

Bacterial homologs of innate eukaryotic antiviral defenses with anti-phage activity highlight shared evolutionary roots of viral defenses.

Prokaryotes have evolved a multitude of defense systems to protect against phage predation. Some of these resemble eukaryotic genes involved in antiviral responses. Here, we set out to systematically project the current knowledge of eukaryotic-like antiviral defense systems onto prokaryotic genomes, using Pseudomonas aeruginosa as a model organism. Searching for phage defense systems related to innate antiviral genes from vertebrates and plants, we uncovered over 450 candidates. We validated six of these phage defense systems, including factors preventing viral attachment, R-loop-acting enzymes, the inflammasome, ubiquitin pathway, and pathogen recognition signaling. Collectively, these defense systems support the concept of deep evolutionary links and shared antiviral mechanisms between prokaryotes and eukaryotes.

Methods for Assessing Plant Immune System Activation by Bacterial Extracellular Vesicles and Other Elicitors.

Bacterial extracellular vesicles (BEVs) are released from the surface of bacterial cells and contain a diverse molecular cargo. Studies conducted primarily with bacterial pathogens of mammals have shown that BEVs are involved in multiple processes such as cell-cell communication, the delivery of RNA, DNA, and proteins to target cells, protection from stresses, manipulation of host immunity, and other functions. Until a decade ago, the roles of BEVs in plant-bacteria interactions were barely investigated. However, recent studies have shown that BEVs of plant pathogens possess similar functions as their mammalian pathogen counterparts, and more research is now devoted to study their roles and interactions with plants. In the following methods chapter, we provide five well-validated assays to examine the interaction of BEVs with the plant immune system. These assays rely on different markers or immune outputs, which indicate the activation of plant immunity (defense marker gene expression, reactive oxygen species burst, seedling inhibition). Furthermore, we offer assays that directly evaluate the priming of the immune system following BEV challenge and the effectiveness of its response to subsequent local or systemic infection. Altogether, these assays provide a thorough examination to the interactions of BEVs and the plant immune system.

Viral Recognition and Evasion in Plants.

Viruses, causal agents of devastating diseases in plants, are obligate intracellular pathogens composed of a nucleic acid genome and a limited number of viral proteins. The diversity of plant viruses, their diminutive molecular nature, and their symplastic localization pose challenges to understanding the interplay between these pathogens and their hosts in the currently accepted framework of plant innate immunity. It is clear, nevertheless, that plants can recognize the presence of a virus and activate antiviral immune responses, although our knowledge of the breadth of invasion signals and the underpinning sensing events is far from complete. Below, I discuss some of the demonstrated or hypothesized mechanisms enabling viral recognition in plants, the step preceding the onset of antiviral immunity, as well as the strategies viruses have evolved to evade or suppress their detection.

Ascorbate, plant hormones and their interactions during plant responses to biotic stress.

Plants can experience a variety of environmental stresses that significantly impact their fitness and survival. Additionally, biotic stress can harm agriculture, leading to reduced crop yields and economic losses worldwide. As a result, plants have developed defense strategies to combat potential invaders. These strategies involve regulating redox homeostasis. Several studies have documented the positive role of plant antioxidants, including Ascorbate (Asc), under biotic stress conditions. Asc is a multifaceted antioxidant that scavenges ROS, acts as a co-factor for different enzymes, regulates gene expression, and facilitates iron transport. However, little attention has been given to Asc and its transport, regulatory effects, interplay with phytohormones, and involvement in defense processes under biotic stress. Asc interacts with other components of the redox system and phytohormones to activate various defense responses that reduce the growth of plant pathogens and promote plant growth and development under biotic stress conditions. Scientific reports indicate that Asc can significantly contribute to plant resistance against biotic stress through mutual interactions with components of the redox and hormonal systems. This review focuses on the role of Asc in enhancing plant resistance against pathogens. Further research is necessary to gain a more comprehensive understanding of the molecular and cellular regulatory processes involved.

Lipids and Lipid-Mediated Signaling in Plant-Pathogen Interactions.

Plant lipids are essential cell constituents with many structural, storage, signaling, and defensive functions. During plant-pathogen interactions, lipids play parts in both the preexisting passive defense mechanisms and the pathogen-induced immune responses at the local and systemic levels. They interact with various components of the plant immune network and can modulate plant defense both positively and negatively. Under biotic stress, lipid signaling is mostly associated with oxygenated natural products derived from unsaturated fatty acids, known as oxylipins; among these, jasmonic acid has been of great interest as a specific mediator of plant defense against necrotrophic pathogens. Although numerous studies have documented the contribution of oxylipins and other lipid-derived species in plant immunity, their specific roles in plant-pathogen interactions and their involvement in the signaling network require further elucidation. This review presents the most relevant and recent studies on lipids and lipid-derived signaling molecules involved in plant-pathogen interactions, with the aim of providing a deeper insight into the mechanisms underpinning lipid-mediated regulation of the plant immune system.

Baking bad: plants in a toasty world with necrotrophs.

Rising global temperatures pose a threat to plant immunity, making them more susceptible to diseases. The impact of temperature on plant immunity against biotrophic and hemi-biotrophic pathogens is well documented, while its effect on necrotrophs remains poorly understood. We venture into the uncharted territory of necrotrophic fungal pathogens in the face of rising temperatures. We discuss the role of the plant hormones salicylic acid (SA) and jasmonic acid (JA) in providing resistance to necrotrophs and delve into the temperature sensitivity of the SA pathway. Additionally, we explore the repercussions of increased temperatures on plant susceptibility to necrotrophs. We put forward a research agenda with an experimental framework aimed at providing a comprehensive understanding of how plants and pathogens adapt to increasing temperatures.

Molecular insights into PGPR fluorescent Pseudomonads complex mediated intercellular and interkingdom signal transduction mechanisms in promoting plant's immunity.

The growth-promoting and immune modulatory properties of different strains of plant growth promoting rhizobacteria (PGPR) fluorescent Pseudomonads complex (PFPC) can be explored to combat food security challenges. These PFPC prime plants through induced systemic resistance, fortify plants to overcome future pathogen-mediated vulnerability by eliciting robust systemic acquired resistance through regulation by nonexpressor of pathogenesis-related genes 1. Moreover, outer membrane vesicles released from Pseudomonas fluorescens also elicit a broad spectrum of immune responses, presenting a rapid viable alternative to whole cells. Thus, PFPC can help the host to maintain an equilibrium between growth and immunity, ultimately leads to increased crop yield.

Pectin-associated immune responses in plant-microbe interactions: A review.

This review explores the role of pectin, a complex polysaccharide found in the plant cell wall, in mediating immune responses during interactions between plants and microbes. The objectives of this study were to investigate the molecular mechanisms underlying pectin-mediated immune responses and to understand how these interactions shape plant-microbe communication. Pectin acts as a signaling molecule, triggering immune responses such as the production of antimicrobial compounds, reinforcement of the cell wall, and activation of defense-related genes. Pectin functions as a target for pathogen-derived enzymes, enabling successful colonization by certain microbial species. The document discusses the complexity of pectin-based immune signaling networks and their modulation by various factors, including pathogen effectors and host proteins. It also emphasizes the importance of understanding the crosstalk between pectin-mediated immunity and other defense pathways to develop strategies for enhancing plant resistance against diseases. The insights gained from this study have implications for the development of innovative approaches to enhance crop protection and disease management in agriculture. Further investigations into the components and mechanisms involved in pectin-mediated immunity will pave the way for future advancements in plant-microbe interaction research.

Decoding the molecular mechanism underlying salicylic acid (SA)-mediated plant immunity: an integrated overview from its biosynthesis to the mode of action.

Salicylic acid (SA) is an important phytohormone, well-known for its regulatory role in shaping plant immune responses. In recent years, significant progress has been made in unravelling the molecular mechanisms underlying SA biosynthesis, perception, and downstream signalling cascades. Through the concerted efforts employing genetic, biochemical, and omics approaches, our understanding of SA-mediated defence responses has undergone remarkable expansion. In general, following SA biosynthesis through Avr effectors of the pathogens, newly synthesized SA undergoes various biochemical changes to achieve its active/inactive forms (e.g. methyl salicylate). The activated SA subsequently triggers signalling pathways associated with the perception of pathogen-derived signals, expression of defence genes, and induction of systemic acquired resistance (SAR) to tailor the intricate regulatory networks that coordinate plant immune responses. Nonetheless, the mechanistic understanding of SA-mediated plant immune regulation is currently limited because of its crosstalk with other signalling networks, which makes understanding this hormone signalling more challenging. This comprehensive review aims to provide an integrated overview of SA-mediated plant immunity, deriving current knowledge from diverse research outcomes. Through the integration of case studies, experimental evidence, and emerging trends, this review offers insights into the regulatory mechanisms governing SA-mediated immunity and signalling. Additionally, this review discusses the potential applications of SA-mediated defence strategies in crop improvement, disease management, and sustainable agricultural practices.

Nanoparticle-mediated defense priming: A review of strategies for enhancing plant resilience against biotic and abiotic stresses.

Nanotechnology has emerged as a promising field with the potential to revolutionize agriculture, particularly in enhancing plant defense mechanisms. Nanoparticles (NPs) are instrumental in plant defense priming, where plants are pre-exposed to controlled levels of stress to heighten their alertness and responsiveness to subsequent stressors. This process improves overall plant performance by enabling quicker and more effective responses to secondary stimuli. This review explores the application of NPs as priming agents, utilizing their unique physicochemical properties to bolster plants' innate defense mechanisms. It discusses key findings in NP-based plant defense priming, including various NP types such as metallic, metal oxide, and carbon-based NPs. The review also investigates the intricate mechanisms by which NPs interact with plants, including uptake, translocation, and their effects on plant physiology, morphology, and molecular processes. Additionally, the review examines how NPs can enhance plant responses to a range of stressors, from pathogen attacks and herbivore infestations to environmental stresses. It also discusses NPs' ability to improve plants' tolerance to abiotic stresses like drought, salinity, and heavy metals. Safety and regulatory aspects of NP use in agriculture are thoroughly addressed, emphasizing responsible and ethical deployment for environmental and human health safety. By harnessing the potential of NPs, this approach shows promise in reducing crop losses, increasing yields, and enhancing global food security while minimizing the environmental impact of traditional agricultural practices. The review concludes by emphasizing the importance of ongoing research to optimize NP formulations, dosages, and delivery methods for practical application in diverse agricultural settings.

Secret Weapon of Insects: The Oral Secretion Cocktail and Its Modulation of Host Immunity.

Plants and insects have co-existed for almost 400 million years and their interactions can be beneficial or harmful, thus reflecting their intricate co-evolutionary dynamics. Many herbivorous arthropods cause tremendous crop loss, impacting the agro-economy worldwide. Plants possess an arsenal of chemical defenses that comprise diverse secondary metabolites that help protect against harmful herbivorous arthropods. In response, the strategies that herbivores use to cope with plant defenses can be behavioral, or molecular and/or biochemical of which salivary secretions are a key determinant. Insect salivary secretions/oral secretions (OSs) play a crucial role in plant immunity as they contain several biologically active elicitors and effector proteins that modulate plants' defense responses. Using this oral secretion cocktail, insects overcome plant natural defenses to allow successful feeding. However, a lack of knowledge of the nature of the signals present in oral secretion cocktails has resulted in reduced mechanistic knowledge of their cellular perception. In this review, we discuss the latest knowledge on herbivore oral secretion derived elicitors and effectors and various mechanisms involved in plant defense modulation. Identification of novel herbivore-released molecules and their plant targets should pave the way for understanding the intricate strategies employed by both herbivorous arthropods and plants in their interactions.

From trade-off to synergy: microbial insights into enhancing plant growth and immunity.

The reduction in crop yield caused by pathogens and pests presents a significant challenge to global food security. Genetic engineering, which aims to bolster plant defence mechanisms, emerges as a cost-effective solution for disease control. However, this approach often incurs a growth penalty, known as the growth-defence trade-off. The precise molecular mechanisms governing this phenomenon are still not completely understood, but they generally fall under two main hypotheses: a "passive" redistribution of metabolic resources, or an "active" regulatory choice to optimize plant fitness. Despite the knowledge gaps, considerable practical endeavours are in the process of disentangling growth from defence. The plant microbiome, encompassing both above- and below-ground components, plays a pivotal role in fostering plant growth and resilience to stresses. There is increasing evidence which indicates that plants maintain intimate associations with diverse, specifically selected microbial communities. Meta-analyses have unveiled well-coordinated, two-way communications between plant shoots and roots, showcasing the capacity of plants to actively manage their microbiota for balancing growth with immunity, especially in response to pathogen incursions. This review centers on successes in making use of specific root-associated microbes to mitigate the growth-defence trade-off, emphasizing pivotal advancements in unravelling the mechanisms behind plant growth and defence. These findings illuminate promising avenues for future research and practical applications.

Redox signaling and oxidative stress in systemic acquired resistance.

Plants fully depend on their immune systems to defend against pathogens. Upon pathogen attack, plants not only activate immune responses at the infection site but also trigger a defense mechanism known as systemic acquired resistance (SAR) in distal systemic tissues to prevent subsequent infections by a broad-spectrum of pathogens. SAR is induced by mobile signals produced at the infection site. Accumulating evidence suggests that reactive oxygen species (ROS) play a central role in SAR signaling. ROS burst at the infection site is one of the earliest cellular responses following pathogen infection and can spread to systemic tissues through membrane-associated NADPH oxidase-dependent relay production of ROS. It is well known that ROS ignite redox signaling and, when in excess, cause oxidative stress, damaging cellular components. In this review, we summarize current knowledge on redox regulation of several SAR signaling components. We discuss the ROS amplification loop in systemic tissues involving multiple SAR mobile signals. Moreover, we highlight the essential role of oxidative stress in generating SAR signals including azelaic acid and extracellular NAD(P) [eNAD(P)]. Finally, we propose that eNAD(P) is a damage-associated molecular pattern serving as a converging point of SAR mobile signals in systemic tissues.

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.

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.

Antiviral defense in plant stem cells.

Undifferentiated plant and animal stem cells are essential for cell, tissue, and organ differentiation, development, and growth. They possess unusual antiviral immunity which differs from that in specialized cells. By comparison to animal stem cells, we discuss how plant stem cells defend against viral invasion and beyond.

Phytopathogens Reprogram Host Alternative mRNA Splicing.

Alternative splicing (AS) is an evolutionarily conserved cellular process in eukaryotes in which multiple messenger RNA (mRNA) transcripts are produced from a single gene. The concept that AS adds to transcriptome complexity and proteome diversity introduces a new perspective for understanding how phytopathogen-induced alterations in host AS cause diseases. Recently, it has been recognized that AS represents an integral component of the plant immune system during parasitic, commensalistic, and symbiotic interactions. Here, I provide an overview of recent progress detailing the reprogramming of plant AS by phytopathogens and the functional implications on disease phenotypes. Additionally, I discuss the vital function of AS of immune receptors in regulating plant immunity and how phytopathogens use effector proteins to target key components of the splicing machinery and exploit alternatively spliced variants of immune regulators to negate defense responses. Finally, the functional association between AS and nonsense-mediated mRNA decay in the context of plant-pathogen interface is recapitulated.