From molecule to cell:the expanding frontiers of plant immunity

In recent years,the field of plant immunity has witnessed remarkable breakthroughs.During the co-evolution between plants and pathogens,plants have developed a wealth of intricate defense mechanisms to safeguard their survival.Newly identified immune receptors have added unexpected complexity to the surface and intracellular sensor networks,enriching our understanding of the ongoing plant–pathogen interplay.Deciphering the molecular mechanisms of resistosome shapes our understanding of these mysterious molecules in plant immunity.Moreover,technological innovations are expanding the horizon of the plant–pathogen battlefield into spatial and temporal scales.While the development provides new opportunities for untangling the complex realm of plant immunity,challenges remain in uncovering plant immunity across spatiotemporal dimensions from both molecular and cellular levels.

New insight into Ca^(2+)-permeable channel in plant immunity

Calcium ions(Ca^(2+)) are crucial intracellular second messengers in eukaryotic cells. Upon pathogen perception, plants generate a transient and rapid increase in cytoplasmic Ca^(2+)levels, which is subsequently decoded by Ca^(2+)sensors and effectors to activate downstream immune responses. The elevation of cytosolic Ca^(2+)is commonly attributed to Ca^(2+)influx mediated by plasma membranelocalized Ca^(2+)–permeable channels. However, the contribution of Ca^(2+)release triggered by intracellular Ca^(2+)-permeable channels in shaping Ca^(2+)signaling associated with plant immunity remains poorly understood. This review discusses recent advances in understanding the mechanism underlying the shaping of Ca^(2+)signatures upon the activation of immune receptors, with particular emphasis on the identification of intracellular immune receptors as non-canonical Ca^(2+)-permeable channels. We also discuss the involvement of Ca^(2+)release from the endoplasmic reticulum in generating Ca^(2+)signaling during plant immunity.

Molecular actions of NLR immune receptors in plants and animals

NLRs constitute intracellular immune receptors in both plants and animals. Direct or indirect ligand recognition results in formation of oligomeric NLR complexes to mediate immune signaling. Over the past 20 years, rapid progress has been made in our understanding of NLR signaling. Structural and biochemical studies provide insight into molecular basis of autoinhibition,ligand recognition, and resistosome/inflammasome formation of several NLRs. In this review, we summarize these studies focusing on the structural aspect of NLRs. We also discuss the analogies and differences between plant and animal NLRs in their mechanisms of action and how the available knowledge may shed light on the signaling mechanisms of other NLRs.

Bacterial Effectors Induce Oligomerization of Immune Receptor ZAR1 In Vivo

Plants utilize nucleotide-binding,leucine-rich repeat receptors(NLRs)to detect pathogen effectors,leading to effector-triggered immunity.The NLR ZAR1 indirectly recognizes the Xanthomonas campestris pv.campestris effector AvrAC and Pseudomonas syringae effector HopZIa by associating with closely related receptor-like cytoplasmic kinase subfamily XII-2(RLCK XII-2)members RKS1 and ZED1,respectively.ZAR1,RKS1,and the AvrAC-modified decoy PBL2ump form a pentameric resistosome in vitro,and the ability of resistosome formation is required for AvrAC-triggered cell death and disease resistance.However,it remains unknown whether the effectors induce ZAR1 oligomerization in the plant cell.In this study,we show that both AvrAC and HopZ1 a can induce oligomerization of ZAR1 in Arabidopsis protoplasts.Residues mediating ZAR1-ZED1 interaction are indispensable for HopZIa-induced ZAR1 oligomerization in vivo and disease resistance.In addition,ZAR1 residues required for the assembly of ZAR1 resistosome in vitro are also essential for HopZIa-induced ZAR1 oligomerization in vivo and disease resistance.Our study provides evidence that pathogen effectors induce ZAR1 resistosome formation in the plant cell and that the resistosome formation triggers disease resistance.

Structure, biochemical function, and signaling mechanism of plant NLRs

To counter pathogen invasion,plants have evolved a large number of immune receptors,including membrane-resident pattern recognition receptors(PRRs)and intracellular nucleotide-binding and leucine-rich repeat receptors(NLRs).Our knowledge about PRR and NLR signaling mechanisms has expanded significantly over the past few years.Plant NLRs form multi-protein complexes called resistosomes in response to pathogen effectors,and the signaling mediated by NLR resistosomes converges on Ca2+-permeable channels.Ca2+-permeable channels important for PRR signaling have also been identified.These findings highlight a crucial role of Ca2+in triggering plant immune signaling.In this review,we first discuss the structural and biochemical mechanisms of non-canonical NLR Ca2+channels and then summarize our knowledge about immune-related Ca2+-permeable channels and their roles in PRR and NLR signaling.We also discuss the potential role of Ca2+in the intricate interaction between PRR and NLR signaling.

Plant NLRs: The Whistleblowers of Plant Immunity

The study of plant diseases is almost as old as agriculture itself. Advancements in molecular biology havegiven us much more insight into the plant immune system and how it detects the many pathogens plantsmay encounter. Members of the primary family of plant resistance (R) proteins, NLRs, contain three distinctdomains, and appear to use several different mechanisms to recognize pathogen effectors and trigger immunity. Understanding the molecular process of NLR recognition and activation has been greatly aided byadvancements in structural studies, with ZAR1 recently becoming the first full-length NLR to be visualized.Genetic and biochemical analysis identified many critical components for NLR activation and homeostasiscontrol. The increased study of helper NLRs has also provided insights into the downstream signaling pathways of NLRs. This review summarizes the progress in the last decades on plant NLR research, focusing onthe mechanistic understanding that has been achieved.

Rpivnt1 provides resistance through the mediation of a light responsive guardee in potato

The disease triangle describes the interrelationship among pathogen,host,and environment towards disease prevalence in the field.The mechanistic role of environment on NLR-mediated resistance was not known until now.Recently,a comprehensive work revealed that light controls late blight disease reaction in potato caused by the lrish famine pathogen.A specific R gene Rpivnt1 in potato showed dichotomous behavior in disease reaction due to the light-responsive alternate promoter selection of another host gene glycerate 3 kinase(GLYK)during its transcription.The full-length GLYK protein traps the pathogen effector AVRvnt1 into a recognition event which is later sensed by Rpivnt1 in the presence of light.In dark,the truncated GLYK protein devoid of its chloroplastic transit peptide could not able to recognize AVRvnt1 and thus resistance get compromised.A possible model for this event is proposed here for ease in understanding.

Structures of plant resistosome reveal how NLR immune receptors are activated

Nucleotide-binding domain and leucine-rich repeat(NLR)proteins make up the largest immune receptor family in plants.Although many studies have put effort into revealing the working mechanism of NLRs,the activation details of plant NLRs still remain obscure.Recently,two remarkable works resolved the structures of a plant NLR protein,the Arabidopsis thaliana HOPZ-ACTIVATED RESISTANCE1(ZAR1),both in resting and activation states.The activated ZAR1 with its partner proteins form a wheel-like pentamer called resistosome that is thought to be able to trigger cell death by perturbing plasma membrane integrity.These findings greatly further our understanding of plant immune system.