skip to main content


Title: A new mode of NPR1 action via an NB‐ARC–NPR1 fusion protein negatively regulates the defence response in wheat to stem rust pathogen
Summary

NPR1 has been found to be a key transcriptional regulator in some plant defence responses. There are nineNPR1homologues (TaNPR1) in wheat, but little research has been done to understand the function of thoseNPR1‐like genes in the wheat defence response against stem rust (Puccinia graminisf. sp.tritici) pathogens.

We used bioinformatics and reverse genetics approaches to study the expression and function of eachTaNPR1.

We found six members ofTaNPR1located on homoeologous group 3 chromosomes (designated asTaG3NPR1) and three on homoeologous group 7 chromosomes (designated asTaG7NPR1). The group 3 NPR1 proteins regulate transcription of SA‐responsivePRgenes. Downregulation of all theTaNPR1homologues via virus‐induced gene co‐silencing resulted in enhanced resistance to stem rust. More specifically downregulatingTaG7NPR1homeologues orTa7ANPR1expression resulted in stem rust resistance phenotype. By contrast, knocking downTaG3NPR1alone did not show visible phenotypic changes in response to the rust pathogen. Knocking outTa7ANPR1enhanced resistance to stem rust. TheTa7ANPR1locus is alternatively spliced under pathogen inoculated conditions.

We discovered a new mode of NPR1 action in wheat at theTa7ANPR1locus through an NB‐ARC–NPR1 fusion protein negatively regulating the defence to stem rust infection.

 
more » « less
NSF-PAR ID:
10368442
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
New Phytologist
Volume:
228
Issue:
3
ISSN:
0028-646X
Page Range / eLocation ID:
p. 959-972
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Plant subtilases (SBTs) or subtilisin-like proteases comprise a very diverse family of serine peptidases that participates in a broad spectrum of biological functions. Despite increasing evidence for roles of SBTs in plant immunity in recent years, little is known about wheat (Triticum aestivum) SBTs (TaSBTs). Here, we identified 255 TaSBT genes from bread wheat using the latest version 2.0 of the reference genome sequence. The SBT family can be grouped into five clades, from TaSBT1 to TaSBT5, based on a phylogenetic tree constructed with deduced protein sequences. In silico protein-domain analysis revealed the existence of considerable sequence diversification of the TaSBT family which, together with the local clustered gene distribution, suggests that TaSBT genes have undergone extensive functional diversification. Among those TaSBT genes whose expression was altered by biotic factors, TaSBT1.7 was found to be induced in wheat leaves by chitin and flg22 elicitors, as well as six examined pathogens, implying a role for TaSBT1.7 in plant defense. Transient overexpression of TaSBT1.7 in Nicotiana benthamiana leaves resulted in necrotic cell death. Moreover, knocking down TaSBT1.7 in wheat using barley stripe mosaic virus-induced gene silencing compromised the hypersensitive response and resistance against Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. Taken together, this study defined the full complement of wheat SBT genes and provided evidence for a positive role of one particular member, TaSBT1.7, in the incompatible interaction between wheat and a stripe rust pathogen. 
    more » « less
  2. Summary

    Epigenetic modifications have emerged as an important mechanism underlying plant defence against pathogens. We examined the role of JMJ14, a Jumonji (JMJ) domain‐containing H3K4 demethylase,in local and systemic plant immune responses in Arabidopsis.

    The function of JMJ14 in local or systemic defence response was investigated by pathogen growth assays and by analysing expression and H3K4me3 enrichments of key defence genes using qPCR and ChIP‐qPCR. Salicylic acid (SA) and pipecolic acid (Pip) levels were quantified and function of JMJ14 in SA‐ and Pip‐mediated defences was analysed in Col‐0 andjmj14plants.

    jmj14mutants were compromised in both local and systemic defences. JMJ14 positively regulates pathogen‐induced H3K4me3 enrichment and expression of defence genes involved in SA‐ and Pip‐mediated defence pathways. Consequently, loss of JMJ14 results in attenuated defence gene expression and reduced Pip accumulation during establishment of systemic acquired resistance (SAR). Exogenous Pip partially restored SAR injmj14plants, suggesting that JMJ14 regulated Pip biosynthesis and other downstream factors regulate SAR injmj14plants.

    JMJ14 positively modulates defence gene expressions and Pip levels in Arabidopsis.

     
    more » « less
  3. Abstract

    Stem rust is an important disease of wheat that can be controlled using resistance genes. The geneSuSr-D1identified in cultivar ‘Canthatch’ suppresses stem rust resistance.SuSr-D1mutants are resistant to several races of stem rust that are virulent on wild-type plants. Here we identifySuSr-D1by sequencing flow-sorted chromosomes, mutagenesis, and map-based cloning. The gene encodes Med15, a subunit of the Mediator Complex, a conserved protein complex in eukaryotes that regulates expression of protein-coding genes. Nonsense mutations in Med15b.D result in expression of stem rust resistance. Time-course RNAseq analysis show a significant reduction or complete loss of differential gene expression at 24 h post inoculation inmed15b.Dmutants, suggesting that transcriptional reprogramming at this time point is not required for immunity to stem rust. Suppression is a common phenomenon and this study provides novel insight into suppression of rust resistance in wheat.

     
    more » « less
  4. Summary

    Actin filament assembly in plants is a dynamic process, requiring the activity of more than 75 actin‐binding proteins. Central to the regulation of filament assembly and stability is the activity of a conserved family of actin‐depolymerizing factors (ADFs), whose primarily function is to regulate the severing and depolymerization of actin filaments. In recent years, the activity ofADFproteins has been linked to a variety of cellular processes, including those associated with response to stress. Herein, a wheatADFgene,TaADF4,was identified and characterized.TaADF4encodes a 139‐amino‐acid protein containing five F‐actin‐binding sites and two G‐actin‐binding sites, and interacts with wheat (Triticum aestivum) Actin1 (TaACT1),in planta. Following treatment of wheat, separately, with jasmonic acid, abscisic acid or with the avirulent race,CYR23, of the stripe rust pathogenPuccinia striiformisf. sp.tritici, we observed a rapid induction in accumulation ofTaADF4mRNA. Interestingly, accumulation ofTaADF4mRNAwas diminished in response to inoculation with a virulent race,CYR31. Silencing ofTaADF4resulted in enhanced susceptibility toCYR23, demonstrating a role forTaADF4in defense signaling. Using a pharmacological‐based approach, coupled with an analysis of host response to pathogen infection, we observed that treatment of plants with the actin‐modifying agent latrunculin B enhanced resistance toCYR23, including increased production of reactive oxygen species and enhancement of localized hypersensitive cell death. Taken together, these data support the hypothesis thatTaADF4 positively modulates plant immunity in wheat via the modulation of actin cytoskeletal organization.

     
    more » « less
  5. Summary

    Local adaptation is an important process in plant evolution, which can be impacted by differential pathogen pressures along environmental gradients. However, the degree to which pathogen resistance loci vary in effect across space and time is incompletely described.

    To understand how the genetic architecture of resistance varies across time and geographic space, we quantified rust (Pucciniaspp.) severity in switchgrass (Panicum virgatum) plantings at eight locations across the central USA for 3 yr and conducted quantitative trait locus (QTL) mapping for rust progression.

    We mapped several variable QTLs, but two large‐effect QTLs which we have namedPrr1andPrr2were consistently associated with rust severity in multiple sites and years, particularly in northern sites. By contrast, there were numerous small‐effect QTLs at southern sites, indicating a genotype‐by‐environment interaction in rust resistance loci. Interestingly,Prr1andPrr2had a strong epistatic interaction, which also varied in the strength and direction of effect across space.

    Our results suggest that abiotic factors covarying with latitude interact with the genetic loci underlying plant resistance to control rust infection severity. Furthermore, our results indicate that segregating genetic variation in epistatically interacting loci may play a key role in determining response to infection across geographic space.

     
    more » « less