@article{kloppe_whetten_kim_powell_lück_douchkov_whetten_hulse‐kemp_balint‐kurti_cowger_2023, title={Two pathogen loci determine <i>Blumeria graminis}, volume={238}, ISSN={0028-646X 1469-8137}, url={http://dx.doi.org/10.1111/nph.18809}, DOI={10.1111/nph.18809}, abstractNote={Blumeria graminis f. sp. tritici (Bgt) is a globally important fungal pathogen of wheat that can rapidly evolve to defeat wheat powdery mildew (Pm) resistance genes. Despite periodic regional deployment of the Pm1a resistance gene in U.S. wheat production, Bgt strains that overcome Pm1a have been notably non-persistent in the U.S., while on other continents they are more widely established. A genome-wide association study (GWAS) was conducted to map sequence variants associated with Pm1a virulence in 216 Bgt isolates from six countries, including the U.S. A virulence variant apparently unique to Bgt isolates from the U.S. was detected in the previously mapped gene AvrPm1a (BgtE-5612) on Bgt chromosome 6; an in-vitro growth assay suggested no fitness reduction associated with this variant. A gene on Bgt chromosome 8, Bgt-51526, was shown to function as a second determinant of Pm1a virulence and despite <30% amino acid identity, BGT-51526 and BGTE-5612 were predicted to share >85% of their secondary structure. A co-expression study in Nicotiana benthamiana showed that BGTE-5612 and BGT-51526 each produce a PM1A-dependent hypersensitive response. More than one member of a B. graminis effector family can be recognized by a single wheat immune receptor, and a two-gene model is necessary to explain virulence to Pm1a.}, number={4}, journal={New Phytologist}, publisher={Wiley}, author={Kloppe, Tim and Whetten, Rebecca B. and Kim, Saet‐Byul and Powell, Oliver R. and Lück, Stefanie and Douchkov, Dimitar and Whetten, Ross W. and Hulse‐Kemp, Amanda M. and Balint‐Kurti, Peter and Cowger, Christina}, year={2023}, month={Mar}, pages={1546–1561} }
 @article{balint-kurti_kim_2022, title={Close encounters in the corn field}, volume={15}, ISSN={1674-2052}, url={http://dx.doi.org/10.1016/J.MOLP.2022.02.008}, DOI={10.1016/j.molp.2022.02.008}, abstractNote={Plants defend themselves against microbial pathogens in several ways. Among the most important of these mechanisms are cytoplasmic nucleotide-binding, leucine-rich repeat (NLR) resistance (R) proteins that are activated by direct or indirect interaction with pathogen-derived effector proteins introduced into the plant cell as part of the pathogenesis process. Effectors that trigger NLR-mediated resistance are known as Avirulence (Avr) proteins. The two major classes of NLR proteins are differentiated by their N-terminal domains being either coiled-coil (CC) or Toll/interleukin-1 receptor (TIR) domains.}, number={5}, journal={Molecular Plant}, publisher={Elsevier BV}, author={Balint-Kurti, Peter and Kim, Saet-Byul}, year={2022}, month={May}, pages={802–804} }
 @article{kim_van den broeck_karre_choi_christensen_wang_jo_cho_balint‐kurti_2021, title={Analysis of the transcriptomic, metabolomic, and gene regulatory responses to
            <i>Puccinia sorghi
            in maize}, volume={22}, ISSN={1464-6722 1364-3703}, url={http://dx.doi.org/10.1111/mpp.13040}, DOI={10.1111/mpp.13040}, abstractNote={Abstract Common rust, caused by Puccinia sorghi, is a widespread and destructive disease of maize. The Rp1‐D gene confers resistance to the P. sorghi IN2 isolate, mediating a hypersensitive cell death response (HR). To identify differentially expressed genes (DEGs) and metabolites associated with the compatible (susceptible) interaction and with Rp1‐D‐mediated resistance in maize, we performed transcriptomics and targeted metabolome analyses of P. sorghi IN2‐infected leaves from the near‐isogenic lines H95 and H95:Rp1‐D, which differed for the presence of Rp1‐D. We observed up‐regulation of genes involved in the defence response and secondary metabolism, including the phenylpropanoid, flavonoid, and terpenoid pathways. Metabolome analyses confirmed that intermediates from several transcriptionally up‐regulated pathways accumulated during the defence response. We identified a common response in H95:Rp1‐D and H95 with an additional H95:Rp1‐D‐specific resistance response observed at early time points at both transcriptional and metabolic levels. To better understand the mechanisms underlying Rp1‐D‐mediated resistance, we inferred gene regulatory networks occurring in response to P. sorghi infection. A number of transcription factors including WRKY53, BHLH124, NKD1, BZIP84, and MYB100 were identified as potentially important signalling hubs in the resistance‐specific response. Overall, this study provides a novel and multifaceted understanding of the maize susceptible and resistance‐specific responses to P. sorghi.}, number={4}, journal={Molecular Plant Pathology}, publisher={Wiley}, author={Kim, Saet‐Byul and Van den Broeck, Lisa and Karre, Shailesh and Choi, Hoseong and Christensen, Shawn A. and Wang, Guan‐Feng and Jo, Yeonhwa and Cho, Won Kyong and Balint‐Kurti, Peter}, year={2021}, month={Feb}, pages={465–479} }
 @article{lee_mang_choi_seo_kim_oh_kim_choi_2021, title={Genome‐wide functional analysis of hot pepper immune receptors reveals an autonomous NLR clade in seed plants}, volume={229}, url={https://doi.org/10.1111/nph.16878}, DOI={10.1111/nph.16878}, abstractNote={Plants possess hundreds of intracellular immune receptors encoding nucleotide-binding domain and leucine-rich repeat (NLR) proteins. Autoactive NLRs, in some cases a specific NLR domain, induce plant cell death in the absence of pathogen infection. In this study, we identified a group of NLRs (G10) carrying autoactive coiled-coil (CC) domains in pepper (Capsicum annuum L. cv. CM334) by genome-wide transient expression analysis. The G10-CC-mediated cell death mimics hypersensitive response (HR) cell death triggered by interaction between NLR and effectors derived from pathogens. Sequence alignment and mutagenesis analyses revealed that the intact α1 helix of G10-CCs is critical for both G10-CC- and R gene-mediated HR cell death. The cell death induced by G10-CCs does not require known helper NLRs, suggesting G10-NLRs are novel singleton NLRs. We also found that G10-CCs localize in the plasma membrane as Arabidopsis singleton NLR ZAR1. Extended studies revealed that autoactive G10-CCs are well conserved in other Solanaceae plants, including tomato, potato, and tobacco, as well as a monocot plant, rice. Furthermore, G10-NLR is an ancient form of NLR that present in all tested seed plants (spermatophytes). Our studies not only uncover the autonomous NLR cluster in plants but also provide powerful resources for dissecting the underlying molecular mechanism of NLR-mediated cell death in plants.}, number={1}, journal={New Phytologist}, publisher={Wiley}, author={Lee, Hye‐Young and Mang, Hyunggon and Choi, Eunhye and Seo, Ye‐Eun and Kim, Myung‐Shin and Oh, Soohyun and Kim, Saet‐Byul and Choi, Doil}, year={2021}, month={Jan}, pages={532–547} }
 @article{karre_kim_kim_khangura_sermons_dilkes_johal_balint-kurti_2021, title={Maize Plants Chimeric for an Autoactive Resistance Gene Display a Cell-Autonomous Hypersensitive Response but Non–Cell Autonomous Defense Signaling}, volume={34}, ISSN={0894-0282 1943-7706}, url={http://dx.doi.org/10.1094/MPMI-04-20-0091-R}, DOI={10.1094/MPMI-04-20-0091-R}, abstractNote={The maize gene Rp1-D21 is a mutant form of the gene Rp1-D that confers resistance to common rust. Rp1-D21 triggers a spontaneous defense response that occurs in the absence of the pathogen and includes a programed cell death called the hypersensitive response (HR). Eleven plants heterozygous for Rp1-D21, in four different genetic backgrounds, were identified that had chimeric leaves with lesioned sectors showing HR abutting green non-lesioned sectors lacking HR. The Rp1-D21 sequence derived from each of the lesioned portions of leaves was unaltered from the expected sequence whereas the Rp1-D21 sequences from nine of the non-lesioned sectors displayed various mutations and we were unable to amplify Rp1-D21 from the other two non-lesioned sectors. In every case, the borders between the sectors were sharp with no transition zone, suggesting that HR and chlorosis associated with Rp1-D21 activity was cell-autonomous. Expression of defense response marker genes was assessed in the lesioned and non-lesioned sectors as well as in near-isogenic plants lacking and carrying Rp1-D21. Defense gene expression was somewhat elevated in non-lesioned sectors abutting sectors carrying Rp1-D21 compared to near-isogenic plants lacking Rp1-D21. This suggests that while the HR itself was cell autonomous, other aspects of the defense response initiated by Rp1-D21 were not.}, number={6}, journal={Molecular Plant-Microbe Interactions®}, publisher={Scientific Societies}, author={Karre, Shailesh and Kim, Saet-Byul and Kim, Bong-Suk and Khangura, Rajdeep S. and Sermons, Shannon M. and Dilkes, Brian and Johal, Guri and Balint-Kurti, Peter}, year={2021}, month={Jun}, pages={606–616} }
 @article{karre_kim_samira_balint‐kurti_2021, title={The maize ZmMIEL1 E3 ligase and ZmMYB83 transcription factor proteins interact and regulate the hypersensitive defence response}, volume={22}, ISSN={1464-6722 1364-3703}, url={http://dx.doi.org/10.1111/mpp.13057}, DOI={10.1111/mpp.13057}, abstractNote={Abstract The plant hypersensitive response (HR), a rapid cell death at the point of pathogenesis, is mediated by nucleotide‐binding site, leucine‐rich repeat (NLR) resistance proteins (R‐proteins) that recognize the presence of specific pathogen‐derived proteins. Rp1‐D21 is an autoactive maize NLR R‐protein that triggers HR spontaneously. We previously mapped loci associated with variation in the strength of HR induced by Rp1‐D21. Here we identify the E3 ligase ZmMIEL1 as the causal gene at a chromosome 10 modifier locus. Transient ZmMIEL1 expression in Nicotiana benthamiana reduced HR induced by Rp1‐D21, while suppression of ZmMIEL1 expression in maize carrying Rp1‐D21 increased HR. ZmMIEL1 also suppressed HR induced by another autoactive NLR, the Arabidopsis R‐protein RPM1D505V, in N. benthamiana. We demonstrated that ZmMIEL1 is a functional E3 ligase and that the effect of ZmMIEL1 was dependent on the proteasome but also that levels of Rp1‐D21 and RPM1D505V were not reduced when coexpressed with ZmMIEL1 in the N. benthamiana system. By comparison to a similar system in Arabidopsis, we identify ZmMYB83 as a potential target of ZmMIEL1. Suppression of ZmMYB83 expression in maize lines carrying Rp1‐D21 suppressed HR. Suppression of ZmMIEL1 expression caused an increase in ZmMYB83 transcript and protein levels in N. benthamiana and maize. Using coimmunoprecipitation and bimolecular fluorescence complementation assays, we demonstrated that ZmMIEL1 and ZmMYB83 physically interacted. Additionally, ZmMYB83 and ZmMIEL1 regulated the expression of a set of maize very long chain fatty acid (VLCFA) biosynthetic genes that may be involved in regulating HR.}, number={6}, journal={Molecular Plant Pathology}, publisher={Wiley}, author={Karre, Shailesh and Kim, Saet‐Byul and Samira, Rozalynne and Balint‐Kurti, Peter}, year={2021}, month={Apr}, pages={694–709} }
 @article{kim_karre_wu_park_meyers_claeys_wisser_jackson_balint‐kurti_2020, title={Multiple insertions of
            <i>COIN
            , a novel maize Foldback transposable element, in the
            <i>Conring
            gene cause a spontaneous progressive cell death phenotype}, volume={104}, ISSN={0960-7412 1365-313X}, url={http://dx.doi.org/10.1111/tpj.14945}, DOI={10.1111/tpj.14945}, abstractNote={Similar progressive leaf lesion phenotypes, named conring for "concentric ring", were identified in 10 independently-derived maize lines. Complementation and mapping experiments indicated that the phenotype had the same genetic basis in each line - a single recessive gene located in a 1.1 Mb region on chromosome 2. Among the 15 predicted genes in this interval, Zm00001d003866 (subsequently renamed Conring or Cnr) had insertions of four related 138 bp transposable element (TE) sequences at precisely the same site in exon 4 in nine of the 10 cnr alleles. The tenth cnr allele had a distinct insertion of 226 bp of in exon 3. Genetic evidence suggested that the 10 cnr alleles were independently-derived, and arose during the derivation of each line. The four TEs, named COINa (for COnring INsertion) through COINd, have not been previously characterized and consist entirely of imperfect 69 bp terminal inverted repeats (TIRs) characteristic of the Foldback class of TEs. They belong to three clades of a family of maize TEs comprising hundreds of sequences in the genome of the B73 maize line. COIN elements preferentially insert at TNA sequences with a preference for C and G nucleotides in the immediately flanking 5' and 3' regions, respectively. They produce a three base target site duplication and do not have homology to other characterized TEs. We propose that Cnr is an unstable gene that is insertionally mutated at high frequency, most commonly due to COIN element insertions at a specific site in the gene.}, number={3}, journal={The Plant Journal}, publisher={Wiley}, author={Kim, Saet‐Byul and Karre, Shailesh and Wu, Qingyu and Park, Minkyu and Meyers, Emily and Claeys, Hannes and Wisser, Randall and Jackson, David and Balint‐Kurti, Peter}, year={2020}, month={Aug}, pages={581–595} }
 @article{murphree_kim_karre_samira_balint‐kurti_2020, title={Use of virus‐induced gene silencing to characterize genes involved in modulating hypersensitive cell death in maize}, volume={21}, ISSN={1464-6722 1364-3703}, url={http://dx.doi.org/10.1111/mpp.12999}, DOI={10.1111/mpp.12999}, abstractNote={Abstract Plant disease resistance proteins (R‐proteins) detect specific pathogen‐derived molecules, triggering a defence response often including a rapid localized cell death at the point of pathogen penetration called the hypersensitive response (HR). The maize Rp1‐D21 gene encodes a protein that triggers a spontaneous HR causing spots on leaves in the absence of any pathogen. Previously, we used fine mapping and functional analysis in a Nicotiana benthamiana transient expression system to identify and characterize a number of genes associated with variation in Rp1‐D21‐induced HR. Here we describe a system for characterizing genes mediating HR, using virus‐induced gene silencing (VIGS) in a maize line carrying Rp1‐D21. We assess the roles of 12 candidate genes. Three of these genes, SGT1, RAR1, and HSP90, are required for HR induced by a number of R‐proteins across several plant–pathogen systems. We confirmed that maize HSP90 was required for full Rp1‐D21‐induced HR. However, suppression of SGT1 expression unexpectedly increased the severity of Rp1‐D21‐induced HR while suppression of RAR1 expression had no measurable effect. We confirmed the effects on HR of two genes we had previously validated in the N. benthamiana system, hydroxycinnamoyltransferase and caffeoyl CoA O‐methyltransferase. We further showed the suppression the expression of two previously uncharacterized, candidate genes, IQ calmodulin binding protein (IQM3) and vacuolar protein sorting protein 37, suppressed Rp1‐D21‐induced HR. This approach is an efficient way to characterize the roles of genes modulating the hypersensitive defence response and other dominant lesion phenotypes in maize.}, number={12}, journal={Molecular Plant Pathology}, publisher={Wiley}, author={Murphree, Colin and Kim, Saet‐Byul and Karre, Shailesh and Samira, Rozalynne and Balint‐Kurti, Peter}, year={2020}, month={Oct}, pages={1662–1676} }
 @article{he_kim_balint-kurti_2019, title={A maize cytochrome b-c1 complex subunit protein ZmQCR7 controls variation in the hypersensitive response}, volume={249}, ISSN={["1432-2048"]}, url={https://doi.org/10.1007/s00425-019-03092-8}, DOI={10.1007/s00425-019-03092-8}, abstractNote={The gene GRMZM2G318346 which encodes a cytochrome b-c1 complex subunit 7 is associated with variation in strength of the hypersensitive response in maize. We previously identified a QTL at 3,545,354 bp (B73 reference genome V2) on maize chromosome 5 associated with variation in the hypersensitive response (HR) conferred by the autoactive R-gene Rp1-D21 (Olukolu et al. in PLoS Genet 10:e1004562 2014). In this study, we show that a gene at this locus, GRMZM2G318346 which encodes a cytochrome b-c1 complex subunit seven (ZmQCR7), an important part of the mitochondrial electron transport chain, can suppress HR mediated by Rp1-D21 in a transient expression assay. ZmQCR7 alleles from two maize lines, W22 and B73 differ for the encoded proteins at just two sites, amino acid 27 (threonine and alanine in B73 and W22, respectively) and amino acid 109 (asparagine and serine), however, the B73 allele is much more effective at suppressing HR. We show that variation at amino acid 27 controlled this variation in HR-suppressing effects. We furthermore demonstrate that the B73 allele of ZmQCR7 can suppress HR induced by RPM1(D505 V), another autoactive R-gene, and that Arabidopsis homologs of ZmQCR7 can also suppress NLR-induced HR. The implications of these findings are discussed.}, number={5}, journal={PLANTA}, publisher={Springer Science and Business Media LLC}, author={He, Yijian and Kim, Saet-Byul and Balint-Kurti, Peter}, year={2019}, month={May}, pages={1477–1485} }
 @article{kim_lee_choi_park_kim_moon_kim_choi_2018, title={The Coiled-Coil and Leucine-Rich Repeat Domain of the Potyvirus Resistance Protein Pvr4 Has a Distinct Role in Signaling and Pathogen Recognition}, volume={31}, url={https://doi.org/10.1094/MPMI-12-17-0313-R}, DOI={10.1094/MPMI-12-17-0313-R}, abstractNote={The pepper Pvr4 protein encoding coiled-coil (CC) nucleotide-binding (NB) leucine-rich repeat (LRR) (NLR) confer hypersensitive response (HR) to potyviruses, including Pepper mottle virus (PepMoV), by recognizing the viral avirulence protein NIb. To figure out the Pvr4-mediated HR mechanism, we analyzed signaling component genes and structure-function relationships of Pvr4, using chimeras and deletion mutants in Nicotiana benthamiana. Molecular chaperone components including HSP90, SGT1, and RAR1 were required, while plant hormones and mitogen-activated protein kinase signaling components had little effect on Pvr4-NIb-mediated HR cell death. Domain swap analyses indicated that the LRR domain of Pvr4 determines recognition of PepMoV-NIb. Our deletion analysis further revealed that the CC domain or CC-NBARC domain alone can trigger autoactive cell death in N. benthamiana. However, the fragments having only an LRR domain could suppress CC-NBARC domain-induced cell death in trans. Further, C-terminal truncation analysis of Pvr4 revealed that a minimum three of five LRR exons showing high similarity was essential for Pvr4 function. The LRR domain may maintain Pvr4 in an inactive state in the absence of NIb. These results provide further insight into the structure and function of NLR protein signaling in plants.}, number={9}, journal={Molecular Plant-Microbe Interactions®}, publisher={Scientific Societies}, author={Kim, Saet-Byul and Lee, Hye-Young and Choi, Eun-Hye and Park, Eunsook and Kim, Ji-Hyun and Moon, Ki-Beom and Kim, Hyun-Soon and Choi, Doil}, year={2018}, month={Sep}, pages={906–913} }