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Abstract Plants contain many nucleotide-binding leucine-rich repeat (NLR) proteins that are postulated to function as intracellular immune receptors but do not yet have an identified function during plant-pathogen interactions. SUPPRESSOR OF NPR1-1, CONSTITUTIVE 1 (SNC1) one such NLR protein of the Toll-interleukin 1 receptor (TIR) type despite its well characterized gain-of-function activity and its involvement in autoimmunity in Arabidopsis (Arabidopsis thaliana). Here, we investigated the role of SNC1 in natural plant-pathogen interactions and genetically tested the importance of the enzymatic activities of its TIR domain for its function. The SNC1 loss-of-function mutants were more susceptible to avirulent bacterial pathogen strains of Pseudomonas syringae containing specific effectors, especially under constant light growth condition. The mutants also had reduced defense gene expression induction and hypersensitive responses upon infection by avirulent pathogens under constant light growth condition. In addition, genetic and biochemical studies supported that the TIR enzymatic activity of SNC1 is required for its gain-of-function activity. In sum, our study uncovers a role of SNC1 as an amplifier of plant defense responses during natural plant-pathogen interactions and indicates its use of enzymatic activity and intermolecular interactions for triggering autoimmune responses. 

Chemical defense systems involving tryptophan-derived secondary metabolites (TDSMs) and salicylic acid (SA) are induced by general nonself signals and pathogen signals, respectively, in Arabidopsis thaliana. Whether and how these chemical defense systems are connected and balanced is largely unknown. In this study, we identified the AVRRPT2-INDUCED GENE2A (AIG2A) and AIG2B genes as gatekeepers that prevent activation of SA defense systems by TDSMs. These genes also were identified as important contributors to natural variation in disease resistance among A. thaliana natural accessions. The loss of AIG2A and AIG2B function leads to upregulation of both SA and TDSM defense systems. Suppressor screens and genetic analysis revealed that a functional TDSM system is required for the upregulation of the SA pathway in the absence of AIG2A and AIG2B, but not vice versa. Furthermore, the AIG2A and AIG2B genes are co-induced with TDSM biosynthesis genes by general pathogen elicitors and nonself signals, thereby functioning as a feedback control of the TDSM defense system, as well as limiting activation of the SA defense system by TDSMs. Thus, this study uncovers an AIG2A- and AIG2B-mediated mechanism that fine-tunes and balances SA and TDSM chemical defense systems in response to nonpathogenic and pathogenic microbes.

 

Plant intracellular immune receptor NLR (nucleotide-binding leucine-rich repeat) proteins sense the presence of pathogens and trigger strong and robust immune responses. NLR genes are known to be tightly controlled at the protein level, but little is known about their dynamics at the transcript level. In this study, we presented a meta-analysis of transcript dynamics of all 207 NLR genes in the Col-0 accession of Arabidopsis thaliana under various biotic and abiotic stresses based on 88 publicly available RNA sequencing datasets from 27 independent studies. We find that about two thirds of the NLR genes are generally induced by pathogens, immune elicitors, or salicylic acid (SA), suggesting that transcriptional induction of NLR genes might be an important mechanism in plant immunity regulation. By contrast, NLR genes induced by biotic stresses are often repressed by abscisic acid, high temperature and drought, suggesting that transcriptional regulation of NLR genes might be important for interaction between abiotic and biotic stress responses. In addition, pathogen-induced expression of some NLR genes are dependent on SA induction. Interestingly, a small group of NLR genes are repressed under certain biotic stress treatments, suggesting an unconventional function of this group of NLRs. This meta-analysis thus reveals the transcript dynamics of NLR genes under biotic and abiotic stress conditions and suggests a contribution of NLR transcript regulation to plant immunity as well as interactions between abiotic and biotic stress responses. 

The expression of an intracellular immune receptor geneSNC1(SUPPRESSOR OF npr1,CONSTITUTIVE 1) is regulated by multiple chromatin‐associated proteins for tuning immunity and growth in Arabidopsis. Whether and how these regulators coordinate to regulateSNC1expression under varying environmental conditions is not clear.

Here, we identified two activation and one repression regulatory modules based on genetic and molecular characterizations of five chromatin‐associated regulators ofSNC1.

Modifier ofsnc1(MOS1) constitutes the first module and is required for the interdependent functions of ARABIDOPSIS TRITHORAX‐RELATED 7 (ATXR7) and HISTONE MONOUBIQUITINATION 1 (HUB1) to deposit H3K4me3 and H2Bub1 at theSNC1locus. CHROMATIN REMODELING 5 (CHR5) constitutes a second module and works independently of ATXR7 and HUB1 in the MOS1 module. HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 15 (HOS15) constitutes a third module responsible for removing H3K9ac to repressSNC1expression under nonpathogenic conditions. The upregulation ofSNC1resulting from removing the HOS15 repression module is partially dependent on the function of the CHR5 module and the MOS1 module.

Together, this study reveals both the distinct and interdependent regulatory mechanisms at the chromatin level forSNC1expression regulation and highlights the intricacy of regulatory mechanisms of NLR expression under different environment.

 

Primary metabolism provides energy for growth and development as well as secondary metabolites for diverse environmental responses. Here we describe an unexpected consequence of disruption of a glycolytic enzyme enolase named LOW EXPRESSION OF OSMOTICALLY RESPONSIVE GENE 2 (LOS2) in causing constitutive defense responses or autoimmunity in Arabidopsis thaliana. The autoimmunity in the los2 mutant is accompanied by a higher expression of about one-quarter of intracellular immune receptor nucleotide-binding leucine-rich repeat (NLR) genes in the genome and is partially dependent on one of these NLR genes. The LOS2 gene was hypothesized to produce an alternatively translated protein c-Myc Binding Protein (MBP-1) that functions as a transcriptional repressor. Complementation tests show that LOS2 executes its function in growth and immunity regulation through the canonical enolase activity but not the production of MBP-1. In addition, the autoimmunity in the los2 mutants leads to a higher accumulation of sugars and organic acids and a depletion of glycolytic metabolites. These findings indicate that LOS2 does not exert its function in immune responses through an alternatively translated protein MBP-1. Rather, they show that a perturbation of glycolysis from the reduction of the enolase activity results in activation of NLR-involved immune responses which further influences primary metabolism and plant growth, highlighting the complex interaction between primary metabolism and plant immunity.

 

TheSAUR26subfamily genes play an important role in conferring variations of thermo‐responsiveness of growth architecture among natural accessions ofArabidopsis thaliana. The expression variations are critical for their activity variations, but how expression variations are generated is unknown.

We identified genetic loci for gene expression variations through expression genome‐wide association study (eGWAS) and investigated their mechanisms through molecular analyses.

We found thatciselements are the major determinants for expression variations ofSAUR26,SAUR27, andSAUR28. Polymorphisms in the promoter region likely impact PIF4 regulation while those at the 3′UTR affect mRNA stability to generate variations inSAUR26expression levels. These polymorphisms also differentially affect the mRNA stability ofSAUR26at two temperatures.

This study reveals two mechanisms involvingciselements in generating gene expression diversity, which is likely important for local adaptations in Arabidopsis natural accessions.

 

Plant immune responses need to be tightly controlled for growth–defense balance. The mechanism underlying this tight control is not fully understood. Here we identify epigenetic regulation of nucleotide‐binding leucine rich repeat or Nod‐Like Receptor (NLR) genes as an important mechanism for immune responses.

Through a sensitized genetic screen and molecular studies, we identified and characterized HOS15 and its associated protein HDA9 as negative regulators of immunity and NLR gene expression.

The loss‐of‐function ofHOS15orHDA9confers enhanced resistance to pathogen infection accompanied with increased expression of one‐third of the 207 NLR genes inArabidopsis thaliana. HOS15 and HDA9 are physically associated with some of these NLR genes and repress their expression likely through reducing the acetylation of H3K9 at these loci. In addition, these NLR genes are repressed by HOS15 under both pathogenic and nonpathogenic conditions but by HDA9 only under infection condition.

Together, this study uncovers a previously uncharacterized histone deacetylase complex in plant immunity and highlights the importance of epigenetic regulation of NLR genes in modulating growth–defense balance.

 

How diversity in growth thermo‐responsiveness is generated for local adaptation is a long‐standing biological question. We investigated molecular genetic basis of natural variations in thermo‐responsiveness of plant architecture inArabidopsis thaliana.

We measured the extent of rosette architecture at 22°C and 28°C in a set of 69 natural accessions and determined their thermo‐responsiveness of plant architecture. A genome‐wide association study was performed to identify major loci for variations in thermo‐responsiveness.

TheSAUR26subfamily, a new subfamily ofSAURgenes, was identified as a major locus for the thermo‐responsive architecture variations. The expression ofSAUR26/27/28is modulated by temperature andPIF4. Extensive natural polymorphisms in these genes affect theirRNAexpression levels and protein activities and influence the thermo‐responsiveness of plant architecture. In addition, theSAUR26subfamily genes exhibit a high variation frequency and their variations are associated with the local temperature climate.

This study reveals that theSAUR26subfamily is a key variation for thermo‐responsive architecture and suggests a preference for generating diversity for local adaptation through signaling connectors.

 

Emerging evidence indicates a close connection between cell‐cycle progression and the plant immune responses. In Arabidopsis,MODIFIER OFsnc1‐1(MOS1) modulates a number of processes including endoreduplication and plant disease resistance, but the molecular mechanism underlying this modulation was not fully understood. Here, we provide biochemical and genetic evidence thatTEOSINTE BRANCHED1,CYCLOIDEA,PCF1 (TCP) transcription factorsTCP15 and its homologues are mediators ofMOS1 function in the immune response and are likely to be also involved in cell‐cycle control.MOS1 andTCPproteins have a direct physical interaction. They both bind to the promoter of the immune receptor geneSUPRESSOR OFnpr1‐1,CONSTITUTIVE1(SNC1) and modulate its expression and consequently immune responses.MOS1 andTCP15 both affect the expression of cell‐cycle genesD‐typeCYCLIN3;1(CYCD3;1), which may mediate theMOS1 function in cell‐cycle modulation. In addition,CYCD3;1overexpression upregulates immune responses, andSNC1expression. This study investigated and revealed a role forMOS1 in transcriptional regulation throughTCP15 and its homologues. This finding suggests the coordination of cell‐cycle progression and plant immune responses at multiple levels.