Evolution of jasmonate and salicylate signal crosstalk

The evolution of land plants approximately 470 million years ago created a new adaptive zone for natural enemies (attackers) of plants. In response to attack, plants evolved highly effective, inducible defense systems. Two plant hormones modulating inducible defenses are salicylic acid (SA) and jasmonic acid (JA). Current thinking is that SA induces resistance against biotrophic pathogens and some phloem feeding insects and JA induces resistance against necrotrophic pathogens, some phloem feeding insects and chewing herbivores. Signaling crosstalk between SA and JA commonly manifests as a reciprocal antagonism and may be adaptive, but this remains speculative. We examine evidence for and against adaptive explanations for antagonistic crosstalk, trace its phylogenetic origins and provide a hypothesis-testing framework for future research on the adaptive significance of SA-JA crosstalk.     

New insights into the regulation of plant immunity by amino acid metabolic pathways

Besides defence pathways regulated by classical stress hormones, distinct amino acid metabolic pathways constitute integral parts of the plant immune system. Mutations in several genes involved in Asp‐derived amino acid biosynthetic pathways can have profound impact on plant resistance to specific pathogen types. For instance, amino acid imbalances associated with homoserine or threonine accumulation elevate plant immunity to oomycete pathogens but not to pathogenic fungi or bacteria. The catabolism of Lys produces the immune signal pipecolic acid (Pip), a cyclic, non‐protein amino acid. Pip amplifies plant defence responses and acts as a critical regulator of plant systemic acquired resistance, defence priming and local resistance to bacterial pathogens. Asp‐derived pyridine nucleotides influence both pre‐ and post‐invasion immunity, and the catabolism of branched chain amino acids appears to affect plant resistance to distinct pathogen classes by modulating crosstalk of salicylic acid‐ and jasmonic acid‐regulated defence pathways. It also emerges that, besides polyamine oxidation and NADPH oxidase, Pro metabolism is involved in the oxidative burst and the hypersensitive response associated with avirulent pathogen recognition. Moreover, the acylation of amino acids can control plant resistance to pathogens and pests by the formation of protective plant metabolites or by the modulation of plant hormone activity.     

Recognition and response in plant-pathogen interactions

Most plants are resistant to the majority of pathogens. Susceptibility is the exception to the more common state of resistance, i.e., being refractory to infection. However, plant pathogens cause serious economic losses by reducing crop yield and quality. Although such organisms are relatively simple genetic entities, in plants, the mechanisms underlying the generation of disease symptoms and resistance responses are complex and, often, unknown. The study of genes associated with plant-pathogen resistance addresses fundamental questions about the molecular, biochemical, cellular, and physiological means of these interactions. Over the past 10 years, the cloning and analysis of numerous plant resistance genes has led researchers to formulate unifying theories about resistance and susceptibility, and the co-evolution of plant pathogens and their hosts. In this review, we discuss the identification of response genes that have been characterized at the molecular level, as well as their putative links to various signaling pathways. We also summarize the knowledge regarding crosstalk among signaling pathways and plant resistance genes.     

Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity

Recent studies have revealed an important role for hormones in plant immunity. We are now beginning to understand the contribution of crosstalk among different hormone signaling networks to the outcome of plant-pathogen interactions. Cytokinins are plant hormones that regulate development and responses to the environment. Cytokinin signaling involves a phosphorelay circuitry similar to two-component systems used by bacteria and fungi to perceive and react to various environmental stimuli. In this study, we asked whether cytokinin and components of cytokinin signaling contribute to plant immunity. We demonstrate that cytokinin levels in Arabidopsis are important in determining the amplitude of immune responses, ultimately influencing the outcome of plant-pathogen interactions. We show that high concentrations of cytokinin lead to increased defense responses to a virulent oomycete pathogen, through a process that is dependent on salicylic acid (SA) accumulation and activation of defense gene expression. Surprisingly, treatment with lower concentrations of cytokinin results in increased susceptibility. These functions for cytokinin in plant immunity require a host phosphorelay system and are mediated in part by type-A response regulators, which act as negative regulators of basal and pathogen-induced SA-dependent gene expression. Our results support a model in which cytokinin up-regulates plant immunity via an elevation of SA-dependent defense responses and in which SA in turn feedback-inhibits cytokinin signaling. The crosstalk between cytokinin and SA signaling networks may help plants fine-tune defense responses against pathogens.     

Signal transduction cascades regulating pseudohyphal differentiation of Saccharomyces cerevisiae

In response to nitrogen limitation, diploid cells of the yeast Saccharomyces cerevisiae undergo a dimorphic transition to filamentous pseudohyphal growth. At least two signaling pathways regulate filamentation. One involves components of the MAP kinase cascade that also regulates mating of haploid cells. The second involves a nutrient-sensing G-protein-coupled receptor that signals via an unusual G(alpha) protein, cAMP and protein kinase A. Recent studies reveal crosstalk between these pathways during pseudohyphal growth. Related MAP kinase and cAMP pathways regulate filamentation and virulence of human and plant fungal pathogens, and represent novel targets for antifungal drug design.     

Cytokinin action in response to abiotic and biotic stresses in plants

The phytohormone cytokinin was originally discovered as a regulator of cell division. Later, it was described to be involved in regulating numerous processes in plant growth and development including meristem activity, tissue patterning, and organ size. More recently, diverse functions for cytokinin in the response to abiotic and biotic stresses have been reported. Cytokinin is required for the defence against high light stress and to protect plants from a novel type of abiotic stress caused by an altered photoperiod. Additionally, cytokinin has a role in the response to temperature, drought, osmotic, salt, and nutrient stress. Similarly, the full response to certain plant pathogens and herbivores requires a functional cytokinin signalling pathway. Conversely, different types of stress impact cytokinin homeostasis. The diverse functions of cytokinin in responses to stress and crosstalk with other hormones are described. Its emerging roles as a priming agent and as a regulator of growth‐defence trade‐offs are discussed.     

Ethylene in mutualistic symbioses

Ethylene (ET) is a gaseous phytohormone that participates in various plant physiological processes and essentially contributes to plant immunity. ET conducts its functions by regulating the expression of ET-responsive genes or in crosstalk with other hormones. Several recent studies have shown the significance of ET in the establishment and development of plant-microbe interactions. Therefore, it is not surprising that pathogens and mutualistic symbionts target ET synthesis or signaling to colonize plants. This review introduces the significance of ET metabolism in plant-microbe interactions, with an emphasis on its role in mutualistic symbioses.     

Role of pathogen's effectors in understanding host-pathogen interaction

Pathogens can pose challenges to plant growth and development at various stages of their life cycle. Two interconnected defense strategies prevent the growth of pathogens in plants, i.e., molecular patterns triggered immunity (PTI) and pathogenic effector-triggered immunity (ETI) that often provides resistance when PTI no longer functions as a result of pathogenic effectors. Plants may trigger an ETI defense response by directly or indirectly detecting pathogen effectors via their resistance proteins. A typical resistance protein is a nucleotide-binding receptor with leucine-rich sequences (NLRs) that undergo structural changes as they recognize their effectors and form associations with other NLRs. As a result of dimerization or oligomerization, downstream components activate “helper” NLRs, resulting in a response to ETI. It was thought that ETI is highly dependent on PTI. However, recent studies have found that ETI and PTI have symbiotic crosstalk, and both work together to create a robust system of plant defense. In this article, we have summarized the recent advances in understanding the plant's early immune response, its components, and how they cooperate in innate defense mechanisms. Moreover, we have provided the current perspective on engineering strategies for crop protection based on up-to-date knowledge.     

Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants?

The identification of several lesion mimic mutants (LMM) that misregulate cell death constitutes a powerful tool to unravel programmed cell death (PCD) pathways in plants, particularly the hypersensitive response (HR), a form of PCD associated with resistance to pathogens. Recently, the characterization of novel LMM has enabled genes that might regulate cell death programmes to be identified as well as the dissection of defense signaling pathways and of crosstalk between multiple pathways in ways that might not be possible by studying the responses of wild-type plants to pathogens.     

Immobile ligands enhance FcγR-TLR2/1 crosstalk by promoting interface overlap of receptor clusters

Innate immune cells detect pathogens through simultaneous stimulation of multiple receptors, but how cells use the receptor crosstalk to elicit context-appropriate responses is unclear. Here, we reveal that the inflammatory response of macrophages from FcγR-TLR2/1 crosstalk inversely depends on the ligand mobility within a model pathogen membrane. The mechanism is that FcγR and TLR2/1 form separate nanoclusters that interact at their interfaces during crosstalk. Less mobile ligands induce stronger interactions and more overlap between the receptor nanoclusters, leading to enhanced signaling. Different from the prevailing view that immune receptors colocalize to synergize their signaling, our results show that FcγR-TLR2/1 crosstalk occurs through interface interactions between non-colocalizing receptor nanoclusters, which are modulated by ligand mobility. This suggests a mechanism by which innate immune cells could use physical properties of ligands to fine-tune host responses.     

Auxin as compère in plant hormone crosstalk

The architecture of many hormone perceptions and signalling pathways has been recently well established, together with an awareness that plant hormone responses are the product of networks of interactions involving multiple hormones. As growth is quantitative, so are hormone responses, which underlie a systems approach to development and response. Auxin is arguably one of the best characterised hormones in plant development, and despite many excellent reviews on auxin perception, polar transport, and signal transduction, too little attention has been given to auxin crosstalk. This review, therefore, gives a précis of recent developments in hormone crosstalk involving auxin. For decades, the literature has described the involvement of multiple hormones in particular processes, although the mechanistic bases underlying points of crosstalk have been harder to pinpoint. Crosstalk falls into different categories, such as direct, indirect, or co-regulation. One conclusion for auxin crosstalk is that crosstalk operates extensively via the metabolism of other hormones, however, microarray approaches are increasingly identifying co-regulated genes and nodes of crosstalk at shared signalling components. Auxin crosstalk is often local, and is spatially and temporally regulated to provide adaptive value to environmental conditions and fine-tuning of responses.     

Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction

Recent advances along numerous research avenues show that plant interactions with biotrophic and necrotrophic pathogens use similar pathways with opposing effects. The hypersensitive response is associated with increased biotroph resistance but decreased necrotroph resistance. In plant/herbivore interactions, opposing effects of defenses against specialist versus generalist herbivores are controlled by plant secondary metabolites, where a metabolite that provides resistance to generalist herbivores may stimulate specialist herbivores. This multi-trophic interaction is presented as an ecological cost of plant resistance, but similar concepts are rarely applied to plant interactions with different classes of pathogens. In this review, we begin to describe how necrotrophic pathogens may place an ecological cost upon plant resistance to biotrophic pathogens. We separate these potential ecological costs into three concepts: (1) the local cost of the hypersensitive response, (2) organismal cost of having machinery for a hypersensitive response and (3) antagonism between salicylate and jasmonate signaling. We describe the literature supporting these concepts and some predictions that they generate.     

Microbial manipulation of receptor crosstalk in innate immunity

In the arms race of host-microbe co-evolution, successful microbial pathogens have evolved ingenious ways to evade host immune responses. In this Review, we focus on 'crosstalk manipulation' - the microbial strategies that instigate, subvert or disrupt the molecular signalling crosstalk between receptors of the innate immune system. This proactive interference undermines host defences and contributes to microbial adaptive fitness and persistent infections. Understanding how pathogens exploit host receptor crosstalk mechanisms and infiltrate the host signalling network is essential for developing interventions to redirect the host response and achieve protective immunity.     

The role and regulation of programmed cell death in plant-pathogen interactions

It is commonly known that animal pathogens often target and suppress programmed cell death (pcd) pathway components to manipulate their hosts. In contrast, plant pathogens often trigger pcd. In cases in which plant pcd accompanies disease resistance, an event called the hypersensitive response, the plant surveillance system has learned to detect pathogen-secreted molecules in order to mount a defence response. In plants without genetic disease resistance, these secreted molecules serve as virulence factors that act through largely unknown mechanisms. Recent studies suggest that plant bacterial pathogens also secrete antiapoptotic proteins to promote their virulence. In contrast, a number of fungal pathogens secrete pcd-promoting molecules that are critical virulence factors. Here, we review recent progress in determining the role and regulation of plant pcd responses that accompany both resistance and susceptible interactions. We also review progress in discerning the mechanisms by which plant pcd occurs during these different interactions.     

Implications of endophyte-plant crosstalk in light of quorum responses for plant biotechnology

Quorum sensing, the cell-to-cell communication system mediated by autoinducers, is responsible for regulation of virulence factors, infections, invasion, colonization, biofilm formation, and antibiotic resistance within bacterial populations. Concomitantly, quorum quenching is a process that involves attenuation of virulence factors by inhibiting or degrading quorum signaling autoinducers. Survival of endophytic microorganisms, commonly known as endophytes, in planta is a continuous mêlée with invading pathogens and pests. In order to survive in their microhabitats inside plants, endophytes have co-evolved to not only utilize an arsenal of biologically active defense compounds but also impede communication between invading pathogens. Such antivirulence strategies prevent pathogens from communicating with or recognizing each other and thus, colonizing plants. The quenching phenomena often involves microbial crosstalk within single or mixed population(s) vis-à-vis gene expression, and production/modulation of quenching enzymes coupled to various antagonistic and synergistic interactions. This concept is particularly interesting because it can be biotechnologically translated in the future to quorum inhibiting antivirulence therapies without triggering resistance in bacteria, which is currently a major problem worldwide that cannot be tackled only with antimicrobial therapies. In this mini-review, we highlight the quorum quenching capacity of endophytes with respect to attenuation of virulence factors and aiding in plant defense response. Further, benefits and potential challenges of using such systems in biotechnology are discussed.     

Crosstalk between intracellular and extracellular salicylic acid signaling events leading to long-distance spread of signals

It is well recognized that salicylic acid (SA) acts as a natural signaling molecule involved in both local and systemic plant defense responses upon attacks by pathogens. Recently, cellular SA receptors and a number of SA-related phloem-mobile signals were identified. Here, we compare the old and up-to-date concepts of plant defense signaling events involving SA. Finally, the crosstalk between intracellular and extracellular SA signaling events leading to long-distance spread of signals was outlined by focusing on the modes of both the short- and long-distance signaling events involving the actions of SA. For the above purpose, two distinct conceptual models for local SA perception and signaling mechanisms in the intracellular and extracellular paths (referred to as models i and ii, respectively) were proposed. In addition to two local SA perception models, we propose that the long-distance SA action could be attributed to three different modes, namely, (iii) local increase in SA followed by transport of SA and SA intermediates, (iv) systemic propagation of SA-derived signals with both chemical and electrical natures without direct movement of SA, and (v) integrated crosstalk allowing alternately repeated secondary signal propagation and biosynthesis of SA and/or conversion of inert SA intermediates to free SA finally contributing to the systemic spread of SA-derived signals. We review here that the long-distance SA signaling events (models iii–v), inevitably involve the mechanisms described in the local signaling models (models i and ii) as the key pieces of the crosstalk.