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Plant-parasitic nematodes (PPNs), such as root-knot nematodes (RKNs) and cyst nematodes (CNs), are among the most devastating pests in agriculture. RKNs and CNs induce redifferentiation of root cells into feeding cells, which provide water and nutrients to these nematodes. Plants trigger immune responses to PPN infection by recognizing PPN invasion through several different but complementary systems. Plants recognize pathogen-associated molecular patterns (PAMPs) sderived from PPNs by cell surface–localized pattern recognition receptors (PRRs), leading to pattern-triggered immunity (PTI). Plants can also recognize tissue and cellular damage caused by invasion or migration of PPNs through PRR-based recognition of damage-associated molecular patterns (DAMPs). Resistant plants have the added ability to recognize PPN effectors via intracellular nucleotide-binding domain leucine-rich repeat (NLR)-type immune receptors, leading to NLR-triggered immunity. Some PRRs may also recognize apoplastic PPN effectors and induce PTI. Plant immune responses against PPNs include the secretion of anti-nematode enzymes, the production of anti-nematode compounds, cell wall reinforcement, production of reactive oxygen species and nitric oxide, and hypersensitive response–mediated cell death. In this review, we summarize the recognition mechanisms for PPN infection and what is known about PPN-induced immune responses in plants.

Cell-surface receptors play pivotal roles in many biological processes, including immunity, development, and reproduction, across diverse organisms. How cell-surface receptors evolve to become specialised in different biological processes remains elusive. To shed light on the immune-specificity of cell-surface receptors, we analyzed more than 200,000 genes encoding cell-surface receptors from 350 genomes and traced the evolutionary origin of immune-specific leucine-rich repeat receptor-like proteins (LRR-RLPs) in plants. Surprisingly, we discovered that the motifs crucial for co-receptor interaction in LRR-RLPs are closely related to those of the LRR-receptor-like kinase (RLK) subgroup Xb, which perceives phytohormones and primarily governs growth and development. Functional characterisation further reveals that LRR-RLPs initiate immune responses through their juxtamembrane and transmembrane regions, while LRR-RLK-Xb members regulate development through their cytosolic kinase domains. Our data suggest that the cell-surface receptors involved in immunity and development share a common origin. After diversification, their ectodomains, juxtamembrane, transmembrane, and cytosolic regions have either diversified or stabilised to recognise diverse ligands and activate differential downstream responses. Our work reveals a mechanism by which plants evolve to perceive diverse signals to activate the appropriate responses in a rapidly changing environment. Plant cell-surface receptors perceive both self- and nonself-molecules to regulate biological processes. Here the authors show that a subclass of phytohormone and immune receptors share a common origin, which have diverged to perceive distinct ligands and activate differential downstream responses.

Parasitic plants in the family Orobanchaceae, such as Striga, Orobanche and Phelipanche, often cause significant damage to agricultural crops. The Orobanchaceae family comprises more than 2000 species in about 100 genera, providing an excellent system for studying the molecular basis of parasitism and its evolution. Notably, the establishment of model Orobanchaceae parasites, such as Triphysaria versicolor and Phtheirospermum japonicum, that can infect the model host Arabidopsis, has greatly facilitated transgenic analyses of genes important for parasitism. In addition, recent genomic and transcriptomic analyses of several Orobanchaceae parasites have revealed fascinating molecular insights into the evolution of parasitism and strategies for adaptation in this family. This review highlights recent progress in understanding how Orobanchaceae parasites attack their hosts and how the hosts mount a defense against the threats.

Pathogen attack sequentially confers pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) after sensing of pathogen patterns and effectors by plant immune receptors, respectively. Reactive oxygen species (ROS) play pivotal roles in PTI and ETI as signaling molecules. Nicotiana benthamiana RBOHB, an NADPH oxidase, is responsible for both the transient PTI ROS burst and the robust ETI ROS burst. Here, we show that RBOHB transactivation mediated by MAPK contributes to R3a/AVR3a-triggered ETI (AVR3a-ETI) ROS burst. RBOHB is markedly induced during the ETI and INF1-triggered PTI (INF1-PTI), but not flg22-tiggered PTI (flg22-PTI).We found that the RBOHB promoter contains a functionalW-box in the R3a/AVR3a and INF1 signalresponsive cis-element. Ectopic expression of four phospho-mimicking mutants of WRKY transcription factors, which are MAPK substrates, induced RBOHB, and yeast one-hybrid analysis indicated that these mutants bind to the cis-element. Chromatin immunoprecipitation assays indicated direct binding of the WRKY to the cis-element in plants. Silencing of multiple WRKY genes compromised the upregulation of RBOHB, resulting in impairment of AVR3a-ETI and INF1-PTI ROS bursts, but not the flg22-PTI ROS burst. These results suggest that the MAPK-WRKY pathway is required for AVR3a-ETI and INF1-PTI ROS bursts by activation of RBOHB.

Enzyme biosensors are useful tools that can monitor rapid changes in metabolite levels in real-time. However, current approaches are largely constrained to metabolites within a limited chemical space. With the rising development of artificial metalloenzymes (ArM), a unique opportunity exists to design biosensors from the ground-up for metabolites that are difficult to detect using current technologies. Here we present the design and development of the ArM ethylene probe ( AEP ), where an albumin scaffold is used to solubilize and protect a quenched ruthenium catalyst. In the presence of the phytohormone ethylene, cross metathesis can occur to produce fluorescence. The probe can be used to detect both exogenous- and endogenous-induced changes to ethylene biosynthesis in fruits and leaves. Overall, this work represents an example of an ArM biosensor, designed specifically for the spatial and temporal detection of a biological metabolite previously not accessible using enzyme biosensors. Existing methods to detect ethylene in plant tissue typically require gas chromatography or use ethylene-dependent gene expression as a proxy. Here Vong et al . show that an artificial metalloenzyme-based ethylene probe can be used to detect ethylene in plants with improved spatiotemporal resolution.

The phytohormone auxin plays critical roles in the regulation of plant growth and development. Indole-3-acetic acid (IAA) has been recognized as the major auxin for more than 70 y. Although several pathways have been proposed, how auxin is synthesized in plants is still unclear. Previous genetic and enzymatic studies demonstrated that both TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA) and YUCCA (YUC) flavin monooxygenase-like proteins are required for biosynthesis of IAA during plant development, but these enzymes were placed in two independent pathways. In this article, we demonstrate that the TAA family produces indole-3-pyruvic acid (IPA) and the YUC family functions in the conversion of IPA to IAA in Arabidopsis (Arabidopsis thaliana) by a quantification method of IPA using liquid chromatography–electrospray ionization–tandem MS. We further show that YUC protein expressed in Escherichia coli directly converts IPA to IAA. Indole-3-acetaldehyde is probably not a precursor of IAA in the IPA pathway. Our results indicate that YUC proteins catalyze a rate-limiting step of the IPA pathway, which is the main IAA biosynthesis pathway in ARABIDOPSIS:

Hemibiotrophic fungal plant pathogens represent a group of agronomically significant disease‐causing agents that grow first on living tissue and then cause host death in later, necrotrophic growth. Among these, Colletotrichum spp. are devastating pathogens of many crops. Identifying expanded classes of genes in the genomes of phytopathogenic Colletotrichum, especially those associated with specific stages of hemibiotrophy, can provide insights on how these pathogens infect a large number of hosts. The genomes of Colletotrichum orbiculare, which infects cucurbits and Nicotiana benthamiana, and C. gloeosporioides, which infects a wide range of crops, were sequenced and analyzed, focusing on features with potential roles in pathogenicity. Regulation of C. orbiculare gene expression was investigated during infection of N. benthamiana using a custom microarray. Genes expanded in both genomes compared to other fungi included sequences encoding small, secreted proteins (SSPs), secondary metabolite synthesis genes, proteases and carbohydrate‐degrading enzymes. Many SSP and secondary metabolite synthesis genes were upregulated during initial stages of host colonization, whereas the necrotrophic stage of growth is characterized by upregulation of sequences encoding degradative enzymes. Hemibiotrophy in C. orbiculare is characterized by distinct stage‐specific gene expression profiles of expanded classes of potential pathogenicity genes.

Obligate parasitic plants in the Orobanchaceae germinate after sensing plant hormones, strigolactones, exuded from host roots. In Arabidopsis thaliana, the α/β-hydrolase D14 acts as a strigolactone receptor that controls shoot branching, whereas its ancestral paralog, KAI2, mediates karrikin-specific germination responses. We observed that KAI2, but not D14, is present at higher copy numbers in parasitic species than in nonparasitic relatives. KAI2 paralogs in parasites are distributed into three phylogenetic clades. The fastest-evolving clade, KAI2d, contains the majority of KAI2 paralogs. Homology models predict that the ligand-binding pockets of KAI2d resemble D14. KAI2d transgenes confer strigolactone-specific germination responses to Arabidopsis thaliana. Thus, the KAI2 paralogs D14 and KAI2d underwent convergent evolution of strigolactone recognition, respectively enabling developmental responses to strigolactones in angiosperms and host detection in parasites.

Transposable elements (TEs) are accumulated in both intergenic and intragenic regions in plant genomes. Intragenic TEs often act as regulatory elements of associated genes and are also co-transcribed with genes, generating chimeric TE-gene transcripts. Despite the potential impact on mRNA regulation and gene function, the prevalence and transcriptional regulation of TE-gene transcripts are poorly understood. By long-read direct RNA sequencing and a dedicated bioinformatics pipeline, ParasiTE, we investigated the transcription and RNA processing of TE-gene transcripts in Arabidopsis thaliana . We identified a global production of TE-gene transcripts in thousands of A. thaliana gene loci, with TE sequences often being associated with alternative transcription start sites or transcription termination sites. The epigenetic state of intragenic TEs affects RNAPII elongation and usage of alternative poly(A) signals within TE sequences, regulating alternative TE-gene isoform production. Co-transcription and inclusion of TE-derived sequences into gene transcripts impact regulation of RNA stability and environmental responses of some loci. Our study provides insights into TE-gene interactions that contributes to mRNA regulation, transcriptome diversity, and environmental responses in plants. Transposons can be co-transcribed with genes in plant genomes. Here, the authors show the global production of chimeric transposon-gene transcripts and their epigenetic regulation in Arabidopsis thaliana .

Key messagePlant U-box E3 ligases PUB20 and PUB21 are flg22-triggered signaling components and negatively regulate immune responses.Plant U-box proteins (PUBs) constitute a class of E3 ligases that are associated with various stress responses. Among the class IV PUBs featuring C-terminal Armadillo (ARM) repeats, PUB20 and PUB21 are closely related homologs. Here, we show that both PUB20 and PUB21 negatively regulate innate immunity in plants. Loss of PUB20 and PUB21 function leads to enhanced resistance to surface inoculation with the virulent bacterium Pseudomonas syringae pv. tomato DC3000 (Pst DC3000). However, the resistance levels remain unaffected after infiltration inoculation, suggesting that PUB20 and PUB21 primarily function during the early defense stages. The enhanced resistance to Pst DC3000 in PUB mutant plants (pub20-1, pub21-1, and pub20-1/pub21-1) correlates with extensive flg22-triggered reactive oxygen production, strong MPK3 activation, and enhanced transcriptional activation of early immune response genes. Additionally, PUB mutant plants (except pub21-1) exhibit constitutive stomatal closure after Pst DC3000 inoculation, implying the significant role of PUB20 in stomatal immunity. Comparative analyses of flg22 responses between PUB mutants and wild-type plants reveals that the robust activation of the pattern-induced immune responses may enhance resistance against Pst DC3000. Notably, the hypersensitivity responses triggered by RPM1/avrRpm1 and RPS2/avrRpt2 are independent of PUB20 and PUB21. These results suggest that PUB20 and PUB21 knockout mutations affect bacterial invasion, likely during the early stages, acting as negative regulators of plant immunity.