Publications by authors named "Peter Balint-Kurti"

64 Publications

Microbe-dependent heterosis in maize.

Proc Natl Acad Sci U S A 2021 Jul;118(30)

Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695;

Hybrids account for nearly all commercially planted varieties of maize and many other crop plants because crosses between inbred lines of these species produce first-generation [F] offspring that greatly outperform their parents. The mechanisms underlying this phenomenon, called heterosis or hybrid vigor, are not well understood despite over a century of intensive research. The leading hypotheses-which focus on quantitative genetic mechanisms (dominance, overdominance, and epistasis) and molecular mechanisms (gene dosage and transcriptional regulation)-have been able to explain some but not all of the observed patterns of heterosis. Abiotic stressors are known to impact the expression of heterosis; however, the potential role of microbes in heterosis has largely been ignored. Here, we show that heterosis of root biomass and other traits in maize is strongly dependent on the belowground microbial environment. We found that, in some cases, inbred lines perform as well by these criteria as their F offspring under sterile conditions but that heterosis can be restored by inoculation with a simple community of seven bacterial strains. We observed the same pattern for seedlings inoculated with autoclaved versus live soil slurries in a growth chamber and for plants grown in steamed or fumigated versus untreated soil in the field. In a different field site, however, soil steaming increased rather than decreased heterosis, indicating that the direction of the effect depends on community composition, environment, or both. Together, our results demonstrate an ecological phenomenon whereby soil microbes differentially impact the early growth of inbred and hybrid maize.
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http://dx.doi.org/10.1073/pnas.2021965118DOI Listing
July 2021

The maize ZmMIEL1 E3 ligase and ZmMYB83 transcription factor proteins interact and regulate the hypersensitive defence response.

Mol Plant Pathol 2021 Jun 6;22(6):694-709. Epub 2021 Apr 6.

Department of Entomology and Plant Pathology, NC State University, Raleigh, North Carolina, USA.

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.
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http://dx.doi.org/10.1111/mpp.13057DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8126188PMC
June 2021

Analysis of the transcriptomic, metabolomic, and gene regulatory responses to Puccinia sorghi in maize.

Mol Plant Pathol 2021 04 28;22(4):465-479. Epub 2021 Feb 28.

Department of Entomology and Plant Pathology, NC State University, Raleigh, North Carolina, USA.

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.
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http://dx.doi.org/10.1111/mpp.13040DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7938627PMC
April 2021

Maize Plants Chimeric for an Autoactive Resistance Gene Display a Cell-Autonomous Hypersensitive Response but Non-Cell Autonomous Defense Signaling.

Mol Plant Microbe Interact 2021 Jul 21:MPMI04200091R. Epub 2021 Jul 21.

Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC 27695-7613, U.S.A.

The maize gene is a mutant form of the gene that confers resistance to common rust. 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 in four different genetic backgrounds, were identified that had chimeric leaves with lesioned sectors showing HR abutting green nonlesioned sectors lacking HR. The sequence derived from each of the lesioned portions of leaves was unaltered from the expected sequence whereas the sequences from nine of the nonlesioned sectors displayed various mutations, and we were unable to amplify from the other two nonlesioned sectors. In every case, the borders between the sectors were sharp, with no transition zone, suggesting that HR and chlorosis associated with activity was cell autonomous. Expression of defense response marker genes was assessed in the lesioned and nonlesioned sectors as well as in near-isogenic plants lacking and carrying . Defense gene expression was somewhat elevated in nonlesioned sectors abutting sectors carrying compared with near-isogenic plants lacking . This suggests that, whereas the HR itself was cell autonomous, other aspects of the defense response initiated by were not. [Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
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http://dx.doi.org/10.1094/MPMI-04-20-0091-RDOI Listing
July 2021

Genome-wide association analysis of the strength of the MAMP-elicited defense response and resistance to target leaf spot in sorghum.

Sci Rep 2020 11 30;10(1):20817. Epub 2020 Nov 30.

Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27695-7613, USA.

Plants have the capacity to respond to conserved molecular features known as microbe-associated molecular patterns (MAMPs). The goal of this work was to assess variation in the MAMP response in sorghum, to map loci associated with this variation, and to investigate possible connections with variation in quantitative disease resistance. Using an assay that measures the production of reactive oxygen species, we assessed variation in the MAMP response in a sorghum association mapping population known as the sorghum conversion population (SCP). We identified consistent variation for the response to chitin and flg22-an epitope of flagellin. We identified two SNP loci associated with variation in the flg22 response and one with the chitin response. We also assessed resistance to Target Leaf Spot (TLS) disease caused by the necrotrophic fungus Bipolaris cookei in the SCP. We identified one strong association on chromosome 5 near a previously characterized disease resistance gene. A moderately significant correlation was observed between stronger flg22 response and lower TLS resistance. Possible reasons for this are discussed.
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http://dx.doi.org/10.1038/s41598-020-77684-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7704633PMC
November 2020

Maize metacaspases modulate the defense response mediated by the NLR protein Rp1-D21 likely by affecting its subcellular localization.

Plant J 2021 01 20;105(1):151-166. Epub 2020 Nov 20.

The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong, 266237, PR China.

Plants usually employ resistance (R) genes to defend against the infection of pathogens, and most R genes encode intracellular nucleotide-binding, leucine-rich repeat (NLR) proteins. The recognition between R proteins and their cognate pathogens often triggers a rapid localized cell death at the pathogen infection sites, termed the hypersensitive response (HR). Metacaspases (MCs) belong to a cysteine protease family, structurally related to metazoan caspases. MCs play crucial roles in plant immunity. However, the underlying molecular mechanism and the link between MCs and NLR-mediated HR are not clear. In this study, we systematically investigated the MC gene family in maize and identified 11 ZmMCs belonging to two types. Further functional analysis showed that the type I ZmMC1 and ZmMC2, but not the type II ZmMC9, suppress the HR-inducing activity of the autoactive NLR protein Rp1-D21 and of its N-terminal coiled-coil (CC ) signaling domain when transiently expressed in Nicotiana benthamiana. ZmMC1 and ZmMC2 physically associate with CC in vivo. We further showed that ZmMC1 and ZmMC2, but not ZmMC9, are predominantly localized in a punctate distribution in both N. benthamiana and maize (Zea mays) protoplasts. Furthermore, the co-expression of ZmMC1 and ZmMC2 with Rp1-D21 and CC causes their re-distribution from being uniformly distributed in the nucleocytoplasm to a punctate distribution co-localizing with ZmMC1 and ZmMC2. We reveal a novel role of plant MCs in modulating the NLR-mediated defense response and derive a model to explain it.
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http://dx.doi.org/10.1111/tpj.15047DOI Listing
January 2021

What are the Top 10 Unanswered Questions in Molecular Plant-Microbe Interactions?

Mol Plant Microbe Interact 2020 Dec 26;33(12):1354-1365. Epub 2020 Oct 26.

Centro de Investigaciones en Química Biológica de Córdoba, CIQUIBIC, CONICET, Departamento de Química Biológica Ranwel Caputto, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Córdoba X5000HUA, Argentina.

This article is part of the Top 10 Unanswered Questions in MPMI invited review series.The past few decades have seen major discoveries in the field of molecular plant-microbe interactions. As the result of technological and intellectual advances, we are now able to answer questions at a level of mechanistic detail that we could not have imagined possible 20 years ago. The Editorial Board felt it was time to take stock and reassess. What big questions remain unanswered? We knew that to identify the fundamental, overarching questions that drive our research, we needed to do this as a community. To reach a diverse audience of people with different backgrounds and perspectives, working in different areas of plant-microbe interactions, we queried the more than 1,400 participants at the 2019 International Congress on Molecular Plant-Microbe Interactions meeting in Glasgow. This group effort resulted in a list of ten, broad-reaching, fundamental questions that influence and inform our research. Here, we introduce these Top 10 unanswered questions, giving context and a brief description of the issues. Each of these questions will be the subject of a detailed review in the coming months. We hope that this process of reflecting on what is known and unknown and identifying the themes that underlie our research will provide a framework to use going forward, giving newcomers a sense of the mystery of the big questions and inspiring new avenues and novel insights.[Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.
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http://dx.doi.org/10.1094/MPMI-08-20-0229-CRDOI Listing
December 2020

Use of virus-induced gene silencing to characterize genes involved in modulating hypersensitive cell death in maize.

Mol Plant Pathol 2020 12 10;21(12):1662-1676. Epub 2020 Oct 10.

Department of Entomology and Plant Pathology, NC State University, Raleigh, North Carolina, USA.

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.
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http://dx.doi.org/10.1111/mpp.12999DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7694674PMC
December 2020

A CRISPR/dCas9 toolkit for functional analysis of maize genes.

Plant Methods 2020 2;16:133. Epub 2020 Oct 2.

Department of Plant Pathology, The Ohio State University, 483B Kottman Hall, 2021 Coffey Road, Columbus, OH 43210 USA.

Background: The Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)/Cas9 system has become a powerful tool for functional genomics in plants. The RNA-guided nuclease can be used to not only generate precise genomic mutations, but also to manipulate gene expression when present as a deactivated protein (dCas9).

Results: In this study, we describe a vector toolkit for analyzing dCas9-mediated activation (CRISPRa) or inactivation (CRISPRi) of gene expression in maize protoplasts. An improved maize protoplast isolation and transfection method is presented, as well as a description of dCas9 vectors to enhance or repress maize gene expression.

Conclusions: We anticipate that this maize protoplast toolkit will streamline the analysis of gRNA candidates and facilitate genetic studies of important trait genes in this transformation-recalcitrant plant.
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http://dx.doi.org/10.1186/s13007-020-00675-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7532566PMC
October 2020

Multiple insertions of COIN, a novel maize Foldback transposable element, in the Conring gene cause a spontaneous progressive cell death phenotype.

Plant J 2020 11 26;104(3):581-595. Epub 2020 Aug 26.

Department of Entomology and Plant Pathology, NC State University, Raleigh, NC, USA.

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 10th 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 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 mutated insertionally at high frequency, most commonly due to COIN element insertions at a specific site in the gene.
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http://dx.doi.org/10.1111/tpj.14945DOI Listing
November 2020

Fine-Tuning Immunity: Players and Regulators for Plant NLRs.

Trends Plant Sci 2020 07 17;25(7):695-713. Epub 2020 Mar 17.

The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, PR China. Electronic address:

Plants have evolved a sophisticated innate immune system to defend against pathogen infection, and intracellular nucleotide-binding, leucine-rich repeat (NLR or NB-LRR) immune receptors are one of the main components of this system. NLR activity is fine-tuned by intra- and intermolecular interactions. We survey what is known about the conservation and diversity of NLR-interacting proteins, and divide them into seven major categories. We discuss the molecular mechanisms by which NLR activities are regulated and how understanding this regulation has potential to facilitate the engineering of NLRs for crop improvement.
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http://dx.doi.org/10.1016/j.tplants.2020.02.008DOI Listing
July 2020

Heterosis of leaf and rhizosphere microbiomes in field-grown maize.

New Phytol 2020 11 12;228(3):1055-1069. Epub 2020 Jul 12.

Plant Science Research Unit, Agricultural Research Service, United States Department of Agriculture, Raleigh, NC, 27695, USA.

Macroorganisms' genotypes shape their phenotypes, which in turn shape the habitat available to potential microbial symbionts. This influence of host genotype on microbiome composition has been demonstrated in many systems; however, most previous studies have either compared unrelated genotypes or delved into molecular mechanisms. As a result, it is currently unclear whether the heritability of host-associated microbiomes follows similar patterns to the heritability of other complex traits. We take a new approach to this question by comparing the microbiomes of diverse maize inbred lines and their F hybrid offspring, which we quantified in both rhizosphere and leaves of field-grown plants using 16S-v4 and ITS1 amplicon sequencing. We show that inbred lines and hybrids differ consistently in the composition of bacterial and fungal rhizosphere communities, as well as leaf-associated fungal communities. A wide range of microbiome features display heterosis within individual crosses, consistent with patterns for nonmicrobial maize phenotypes. For leaf microbiomes, these results were supported by the observation that broad-sense heritability in hybrids was substantially higher than narrow-sense heritability. Our results support our hypothesis that at least some heterotic host traits affect microbiome composition in maize.
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http://dx.doi.org/10.1111/nph.16730DOI Listing
November 2020

Genotypic and phenotypic characterization of a large, diverse population of maize near-isogenic lines.

Plant J 2020 08 26;103(3):1246-1255. Epub 2020 May 26.

Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27695, USA.

Genome-wide association (GWA) studies can identify quantitative trait loci (QTL) putatively underlying traits of interest, and nested association mapping (NAM) can further assess allelic series. Near-isogenic lines (NILs) can be used to characterize, dissect and validate QTL, but the development of NILs is costly. Previous studies have utilized limited numbers of NILs and introgression donors. We characterized a panel of 1270 maize NILs derived from crosses between 18 diverse inbred lines and the recurrent inbred parent B73, referred to as the nested NILs (nNILs). The nNILs were phenotyped for flowering time, height and resistance to three foliar diseases, and genotyped with genotyping-by-sequencing. Across traits, broad-sense heritability (0.4-0.8) was relatively high. The 896 genotyped nNILs contain 2638 introgressions, which span the entire genome with substantial overlap within and among allele donors. GWA with the whole panel identified 29 QTL for height and disease resistance with allelic variation across donors. To date, this is the largest and most diverse publicly available panel of maize NILs to be phenotypically and genotypically characterized. The nNILs are a valuable resource for the maize community, providing an extensive collection of introgressions from the founders of the maize NAM population in a B73 background combined with data on six agronomically important traits and from genotyping-by-sequencing. We demonstrate that the nNILs can be used for QTL mapping and allelic testing. The majority of nNILs had four or fewer introgressions, and could readily be used for future fine mapping studies.
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http://dx.doi.org/10.1111/tpj.14787DOI Listing
August 2020

Genetic and Physiological Characterization of a Calcium Deficiency Phenotype in Maize.

G3 (Bethesda) 2020 06 1;10(6):1963-1970. Epub 2020 Jun 1.

Dept. of Entomology and Plant Pathology, NC State University, Raleigh NC 27695

Calcium (Ca) is an essential plant nutrient, required for signaling, cell wall fortification and growth and development. Calcium deficiency (Ca-deficiency) in maize causes leaf tip rot and a so-called "bull-whipping" or "buggy-whipping" phenotype. Seedlings of the maize line B73 displayed these Ca-deficiency-like symptoms when grown in the greenhouse with excess fertilizer during the winter months, while seedlings of the Mo17 maize line did not display these symptoms under the same conditions. These differential phenotypes could be recapitulated in 'mini-hydroponic' systems in the laboratory in which high ammonium, but not nitrate, levels induced the symptoms in B73 but not Mo17 seedlings. Consistent with this phenotype being caused by Ca-deficiency, addition of Ca completely relieved the symptoms. These data suggest that ammonium reduces the seedling's ability to absorb calcium, which causes the Ca-deficiency phenotype, and that this trait varies among genotypes. A recombinant inbred line (RIL) population derived from a B73 x Mo17 cross was used to map quantitative trait loci (QTL) associated with the Ca-deficiency phenotype. QTL associated with variation in susceptibility to Ca-deficiency were detected on chromosomes 1, 2, 3, 6 which explained between 3.30-9.94% of the observed variation. Several genes predicted to bind or be activated by calcium map to these QTL on chromosome 1, 2, 6. These results describe for the first time the genetics of Ca-deficiency symptoms in maize and in plants in general.
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http://dx.doi.org/10.1534/g3.120.401069DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7263677PMC
June 2020

Identification of QTL for Target Leaf Spot resistance in Sorghum bicolor and investigation of relationships between disease resistance and variation in the MAMP response.

Sci Rep 2019 12 4;9(1):18285. Epub 2019 Dec 4.

Dept of Entomology and Plant Pathology, NC State University, Raleigh, NC, 27695, USA.

Target leaf spot (TLS) of sorghum, a foliar disease caused by the necrotrophic fungus Bipolaris cookei (also known as Bipolaris sorghicola), can affect grain yield in sorghum by causing premature drying of leaves and defoliation. Two sorghum recombinant inbred line (RIL) populations, BTx623/BTx642 and BTx623/SC155-14E, were assessed for TLS resistance in replicated trials. Using least square mean trait data, four TLS resistance QTL were identified, two in each population. Of these, three were previously unidentified while a major QTL on chromosome 5 in the BTx623/BTx642 RIL population corresponded to the previously identified TLS resistance gene ds1. A set of sorghum lines were assessed for production of reactive oxygen species induced by treatment with the microbe-associated molecular pattern (MAMP) flg22 (a derivative of flagellin). Flg22-induced ROS production varied between lines in a consistent fashion. One QTL associated with variation in the flg22 response was detected in the RIL populations. No evidence was found to link variation in the MAMP response to variation in TLS resistance.
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http://dx.doi.org/10.1038/s41598-019-54802-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6893015PMC
December 2019

as a Phytopathogenic Model to Study the Immune System of .

Mol Plant Microbe Interact 2020 Feb 27;33(2):235-246. Epub 2019 Dec 27.

Divisions of Plant Science and Biochemistry, C.S. Bond Life Science Center, University of Missouri, Columbia, MO 65211, U.S.A.

is the causal agent of red stripe disease (RSD) and mottle stripe disease of sorghum and sugarcane, respectively. In all, 63 genotypes of were inoculated with , with 59 showing RSD symptoms. Quantitative trait loci (QTL) analysis in a recombinant inbred line (RIL) population identified several QTL associated with variation in resistance to RSD. RNA sequencing analysis identified a number of genes whose transcript levels were differentially regulated during infection. Among those genes that responded to inoculation were many involved in plant-pathogen interactions such as leucine-rich repeat receptors, mitogen-activated protein kinase 1, calcium-binding proteins, transcriptional factors (ethylene-responsive element binding factor), and callose synthase. Pretreatment of sorghum leaves with the pathogen-associated molecular pattern (PAMP) molecules flg22 and chitooctaose provided protection against subsequent challenge with the pathogen, suggesting that PAMP-triggered immunity plays an important role in the sorghum immunity response. These data present baseline information for the use of the genetically tractable sorghum pathosystem for the study of innate immunity and disease resistance in this important grain and bioenergy crop. Information gained from the use of this system is likely to be informative for other monocots, including those more intractable for experimental study (e.g., sugarcane).
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http://dx.doi.org/10.1094/MPMI-06-19-0154-RDOI Listing
February 2020

Dominant, Heritable Resistance to Stewart's Wilt in Maize Is Associated with an Enhanced Vascular Defense Response to Infection with .

Mol Plant Microbe Interact 2019 Dec 28;32(12):1581-1597. Epub 2019 Oct 28.

Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA 92093, U.S.A.

Vascular wilt bacteria such as , the causal agent of Stewart's bacterial wilt of maize (SW), are destructive pathogens that are difficult to control. These bacteria colonize the xylem, where they form biofilms that block sap flow leading to characteristic wilting symptoms. Heritable forms of SW resistance exist and are used in maize breeding programs but the underlying genes and mechanisms are mostly unknown. Here, we show that seedlings of maize inbred lines with mutations are highly resistant to SW. However, current evidence suggests that other genes introgressed along with are responsible for resistance. Genomic analyses of lines were used to identify candidate resistance genes. In-depth comparison of interaction with susceptible and resistant maize lines revealed an enhanced vascular defense response in lines characterized by accumulation of electron-dense materials in xylem conduits visible by electron microscopy. We propose that this vascular defense response restricts spread through the vasculature, reducing both systemic bacterial colonization of the xylem network and consequent wilting. Though apparently unrelated to the resistance phenotype of lines, we also demonstrate that the effector WtsE is essential for xylem dissemination, show evidence for a nutritional immunity response to that alters xylem sap composition, and present the first analysis of maize transcriptional responses to infection.
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http://dx.doi.org/10.1094/MPMI-05-19-0129-RDOI Listing
December 2019

Analysis of leaf microbiome composition of near-isogenic maize lines differing in broad-spectrum disease resistance.

New Phytol 2020 03 26;225(5):2152-2165. Epub 2019 Nov 26.

Plant Science Research Unit, Agricultural Research Service, United States Department of Agriculture, Raleigh, NC, 27695, USA.

Plant genotype strongly affects disease resistance, and also influences the composition of the leaf microbiome. However, these processes have not been studied and linked in the microevolutionary context of breeding for improved disease resistance. We hypothesised that broad-spectrum disease resistance alleles also affect colonisation by nonpathogenic symbionts. Quantitative trait loci (QTL) conferring resistance to multiple fungal pathogens were introgressed into a disease-susceptible maize inbred line. Bacterial and fungal leaf microbiomes of the resulting near-isogenic lines were compared with the microbiome of the disease-susceptible parent line at two time points in multiple fields. Introgression of QTL from disease-resistant lines strongly shifted the relative abundance of diverse fungal and bacterial taxa in both 3-wk-old and 7-wk-old plants. Nevertheless, the effects on overall community structure and diversity were minor and varied among fields and years. Contrary to our expectations, host genotype effects were not any stronger in fields with high disease pressure than in uninfected fields, and microbiome succession over time was similar in heavily infected and uninfected plants. These results show that introgressed QTL can greatly improve broad-spectrum disease resistance while having only limited and inconsistent pleiotropic effects on the leaf microbiome in maize.
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http://dx.doi.org/10.1111/nph.16284DOI Listing
March 2020

A maize polygalacturonase functions as a suppressor of programmed cell death in plants.

BMC Plant Biol 2019 Jul 15;19(1):310. Epub 2019 Jul 15.

Dept. of Entomology and Plant Pathology, NC State University, Raleigh, NC, 27695-7616, USA.

Background: The hypersensitive defense response (HR) in plants is a fast, localized necrotic response around the point of pathogen ingress. HR is usually triggered by a pathogen recognition event mediated by a nucleotide-binding site, leucine-rich repeat (NLR) protein. The autoactive maize NLR gene Rp1-D21 confers a spontaneous HR response in the absence of pathogen recognition. Previous work identified a set of loci associated with variation in the strength of Rp1-D21-induced HR. A polygalacturonase gene homolog, here termed ZmPGH1, was identified as a possible causal gene at one of these loci on chromosome 7.

Results: Expression of ZmPGH1 inhibited the HR-inducing activity of both Rp1-D21 and that of another autoactive NLR, RPM1(D505V), in a Nicotiana benthamiana transient expression assay system. Overexpression of ZmPGH1 in a transposon insertion line of maize was associated with suppression of chemically-induced programmed cell death and with suppression of HR induced by Rp1-D21 in maize plants grown in the field.

Conclusions: ZmPGH1 functions as a suppressor of programmed cell death induced by at least two autoactive NLR proteins and by two chemical inducers. These findings deepen our understanding of the control of the HR in plants.
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http://dx.doi.org/10.1186/s12870-019-1897-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6628502PMC
July 2019

The plant hypersensitive response: concepts, control and consequences.

Mol Plant Pathol 2019 08 15;20(8):1163-1178. Epub 2019 Jul 15.

Plant Science Research Unit, USDA-ARS, Raleigh, NC, USA.

The hypersensitive defence response is found in all higher plants and is characterized by a rapid cell death at the point of pathogen ingress. It is usually associated with pathogen resistance, though, in specific situations, it may have other consequences such as pathogen susceptibility, growth retardation and, over evolutionary timescales, speciation. Due to the potentially severe costs of inappropriate activation, plants employ multiple mechanisms to suppress inappropriate activation of HR and to constrain it after activation. The ubiquity of this response among higher plants despite its costs suggests that it is an extremely effective component of the plant immune system.
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http://dx.doi.org/10.1111/mpp.12821DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6640183PMC
August 2019

Validation and Characterization of Maize Multiple Disease Resistance QTL.

G3 (Bethesda) 2019 09 4;9(9):2905-2912. Epub 2019 Sep 4.

Plant Science Research Unit, USDA-ARS, Raleigh NC 27695-7616

Southern Leaf Blight, Northern Leaf Blight, and Gray Leaf Spot, caused by ascomycete fungi, are among the most important foliar diseases of maize worldwide. Previously, disease resistance quantitative trait loci (QTL) for all three diseases were identified in a connected set of chromosome segment substitution line (CSSL) populations designed for the identification of disease resistance QTL. Some QTL for different diseases co-localized, indicating the presence of multiple disease resistance (MDR) QTL. The goal of this study was to perform an independent test of several of the MDR QTL identified to confirm their existence and derive a more precise estimate of allele additive and dominance effects. Twelve F family populations were produced, in which selected QTL were segregating in an otherwise uniform genetic background. The populations were assessed for each of the three diseases in replicated trials and genotyped with markers previously associated with disease resistance. Pairwise phenotypic correlations across all the populations for resistance to the three diseases ranged from 0.2 to 0.3 and were all significant at the alpha level of 0.01. Of the 44 QTL tested, 16 were validated (identified at the same genomic location for the same disease or diseases) and several novel QTL/disease associations were found. Two MDR QTL were associated with resistance to all three diseases. This study identifies several potentially important MDR QTL and demonstrates the importance of independently evaluating QTL effects following their initial identification.
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http://dx.doi.org/10.1534/g3.119.400195DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6723135PMC
September 2019

Diverse Components of Resistance to Infection and Fumonisin Contamination in Four Maize Recombinant Inbred Families.

Toxins (Basel) 2019 02 1;11(2). Epub 2019 Feb 1.

School of Integrative Plant Science, Cornell University, Ithaca, NY 14853, USA.

The fungus can infect maize ears, causing Fusarium ear rot (FER) and contaminating the grain with fumonisins (FUM), which are harmful to humans and animals. Breeding for resistance to FER and FUM and post-harvest sorting of grain are two strategies for reducing FUM in the food system. Kernel and cob tissues have been previously associated with differential FER and FUM. Four recombinant inbred line families from the maize nested associated mapping population were grown and inoculated with across four environments, and we evaluated the kernels for external and internal infection severity as well as FUM contamination. We also employed publicly available phenotypes on innate ear morphology to explore genetic relationships between ear architecture and resistance to FER and FUM. The four families revealed wide variation in external symptomatology at the phenotypic level. Kernel bulk density under inoculation was an accurate indicator of FUM levels. Genotypes with lower kernel density-under both inoculated and uninoculated conditions-and larger cobs were more susceptible to infection and FUM contamination. Quantitative trait locus (QTL) intervals could be classified as putatively resistance-specific and putatively shared for ear and resistance traits. Both types of QTL mapped in this study had substantial overlap with previously reported loci for resistance to FER and FUM. Ear morphology may be a component of resistance to infection and FUM accumulation.
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http://dx.doi.org/10.3390/toxins11020086DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6410224PMC
February 2019

A maize cytochrome b-c1 complex subunit protein ZmQCR7 controls variation in the hypersensitive response.

Planta 2019 May 29;249(5):1477-1485. Epub 2019 Jan 29.

Department of Entomology and Plant Pathology, NC State University, Raleigh, NC, 27695-7616, USA.

Main Conclusion: 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.
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http://dx.doi.org/10.1007/s00425-019-03092-8DOI Listing
May 2019

Using Maize Chromosome Segment Substitution Line Populations for the Identification of Loci Associated with Multiple Disease Resistance.

G3 (Bethesda) 2019 01 9;9(1):189-201. Epub 2019 Jan 9.

Dept. of Entomology and Plant Pathology, North Carolina State University, Box 7616 Raleigh, NC 27695

Southern Leaf Blight (SLB), Northern Leaf Blight (NLB), and Gray Leaf Spot (GLS) caused by , , and respectively, are among the most important diseases of corn worldwide. Previously, moderately high and significantly positive genetic correlations between resistance levels to each of these diseases were identified in a panel of 253 diverse maize inbred lines. The goal of this study was to identify loci underlying disease resistance in some of the most multiple disease resistant (MDR) lines by the creation of chromosome segment substitution line (CSSL) populations in multiple disease susceptible (MDS) backgrounds. Four MDR lines (NC304, NC344, Ki3, NC262) were used as donor parents and two MDS lines (Oh7B, H100) were used as recurrent parents to produce eight BCF CSSL populations comprising 1,611 lines in total. Each population was genotyped and assessed for each disease in replicated trials in two environments. Moderate to high heritabilities on an entry mean basis were observed (0.32 to 0.83). Several lines in each population were significantly more resistant than the MDS parental lines for each disease. Multiple quantitative trait loci (QTL) for disease resistance were detected for each disease in most of the populations. Seventeen QTL were associated with variation in resistance to more than one disease (SLB/NLB: 2; SLB/GLS: 7; NLB/GLS: 2 and 6 to all three diseases). For most populations and most disease combinations, significant correlations were observed between disease scores and also between marker effects for each disease. The number of lines that were resistant to more than one disease was significantly higher than would be expected by chance. Using the results from individual QTL analyses, a composite statistic based on Mahalanobis distance () was used to identify joint marker associations with multiple diseases. Across all populations and diseases, 246 markers had significant values. However further analysis revealed that most of these associations were due to strong QTL effects on a single disease. Together, these findings reinforce our previous conclusions that loci associated with resistance to different diseases are clustered in the genome more often than would be expected by chance. Nevertheless true MDR loci which have significant effects on more than one disease are still much rarer than loci with single disease effects.
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http://dx.doi.org/10.1534/g3.118.200866DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6325898PMC
January 2019

Identification of a locus in maize controlling response to a host-selective toxin derived from Cochliobolus heterostrophus, causal agent of southern leaf blight.

Theor Appl Genet 2018 Dec 6;131(12):2601-2612. Epub 2018 Sep 6.

Department of Entomology and Plant Pathology, NC State University, Raleigh, NC, 27695-7616, USA.

Key Message: A host-selective, proteinaceous maize toxin was identified from the culture filtrate of the maize pathogen Cochliobolus heterostrophus. A dominant gene for toxin susceptibility was identified on maize chromosome 4. A toxic activity was identified from the culture filtrate (CF) of the fungus Cochliobolus heterostrophus, causal agent of the maize disease southern leaf blight (SLB) with differential toxicity on maize lines. Two independent mapping populations; a 113-line recombinant inbred line population and a 258-line association population, were used to map loci associated with sensitivity to the CF at the seedling stage. A major QTL on chromosome 4 was identified at the same locus using both populations. Mapping in the association population defined a 400 kb region that contained the sensitivity locus. By comparing CF-sensitivity of the parents of the RIL population with that of the F progeny, we determined that the sensitivity allele was dominant. No relationship was observed between CF-sensitivity in seedlings and SLB susceptibility in mature plants; however, a significant correlation (- 0.58) was observed between SLB susceptibility and CF-sensitivity in seedlings. The activity of the CF was light-dependent and was sensitive to pronase, indicating that the toxin was proteinaceous.
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http://dx.doi.org/10.1007/s00122-018-3175-6DOI Listing
December 2018

Large Scale Field Inoculation and Scoring of Maize Southern LeafBlight and Other Maize Foliar Fungal Diseases.

Bio Protoc 2018 Mar 5;8(5):e2745. Epub 2018 Mar 5.

Plant Science Research Unit USDA-ARS, Raleigh NC, USA and Dept. of Entomology and Plant Pathology, NC State University, Raleigh NC, USA.

Field-grown maize is inoculated with , causal agent of southern leaf blight disease, by dropping sorghum grains infested with the fungus into the whorl of each maize plant at an early stage of growth. The initial lesions produce secondary inoculum that is dispersed by wind and rain, causing multiple cycles of infection that assures a high uniform disease pressure over the entire field by the time of disease scoring, which occurs after anthesis. This method, with slight modifications, can also be used to study the maize fungal diseases northern leaf blight (caused by ) and gray leaf spot ().
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http://dx.doi.org/10.21769/BioProtoc.2745DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8203974PMC
March 2018

Navigating complexity to breed disease-resistant crops.

Nat Rev Genet 2018 Jan 7;19(1):21-33. Epub 2017 Nov 7.

United States Department of Agriculture Agricultural Research Service (USDA-ARS), Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, North Carolina 27695-7616, USA.

Plant diseases are responsible for substantial crop losses each year and pose a threat to global food security and agricultural sustainability. Improving crop resistance to pathogens through breeding is an environmentally sound method for managing disease and minimizing these losses. However, it is challenging to breed varieties with resistance that is effective, stable and broad-spectrum. Recent advances in genetic and genomic technologies have contributed to a better understanding of the complexity of host-pathogen interactions and have identified some of the genes and mechanisms that underlie resistance. This new knowledge is benefiting crop improvement through better-informed breeding strategies that utilize diverse forms of resistance at different scales, from the genome of a single plant to the plant varieties deployed across a region.
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http://dx.doi.org/10.1038/nrg.2017.82DOI Listing
January 2018

A gene encoding maize caffeoyl-CoA O-methyltransferase confers quantitative resistance to multiple pathogens.

Nat Genet 2017 Sep 24;49(9):1364-1372. Epub 2017 Jul 24.

Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, North Carolina, USA.

Alleles that confer multiple disease resistance (MDR) are valuable in crop improvement, although the molecular mechanisms underlying their functions remain largely unknown. A quantitative trait locus, qMdr, associated with resistance to three important foliar maize diseases-southern leaf blight, gray leaf spot and northern leaf blight-has been identified on maize chromosome 9. Through fine-mapping, association analysis, expression analysis, insertional mutagenesis and transgenic validation, we demonstrate that ZmCCoAOMT2, which encodes a caffeoyl-CoA O-methyltransferase associated with the phenylpropanoid pathway and lignin production, is the gene within qMdr conferring quantitative resistance to both southern leaf blight and gray leaf spot. We suggest that resistance might be caused by allelic variation at the level of both gene expression and amino acid sequence, thus resulting in differences in levels of lignin and other metabolites of the phenylpropanoid pathway and regulation of programmed cell death.
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http://dx.doi.org/10.1038/ng.3919DOI Listing
September 2017

Fine mapping of a quantitative resistance gene for gray leaf spot of maize (Zea mays L.) derived from teosinte (Z. mays ssp. parviglumis).

Theor Appl Genet 2017 Jun 24;130(6):1285-1295. Epub 2017 Mar 24.

Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27695, USA.

Key Message: In this study we mapped the QTL Qgls8 for gray leaf spot (GLS) resistance in maize to a ~130 kb region on chromosome 8 including five predicted genes. In previous work, using near isogenic line (NIL) populations in which segments of the teosinte (Zea mays ssp. parviglumis) genome had been introgressed into the background of the maize line B73, we had identified a QTL on chromosome 8, here called Qgls8, for gray leaf spot (GLS) resistance. We identified alternate teosinte alleles at this QTL, one conferring increased GLS resistance and one increased susceptibility relative to the B73 allele. Using segregating populations derived from NIL parents carrying these contrasting alleles, we were able to delimit the QTL region to a ~130 kb (based on the B73 genome) which encompassed five predicted genes.
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http://dx.doi.org/10.1007/s00122-017-2888-2DOI Listing
June 2017

Genetic dissection of the maize (Zea mays L.) MAMP response.

Theor Appl Genet 2017 Jun 13;130(6):1155-1168. Epub 2017 Mar 13.

Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27695, USA.

Key Message: Loci associated with variation in maize responses to two microbe-associated molecular patterns (MAMPs) were identified. MAMP responses were correlated. No relationship between MAMP responses and quantitative disease resistance was identified. Microbe-associated molecular patterns (MAMPs) are highly conserved molecules commonly found in microbes which can be recognized by plant pattern recognition receptors. Recognition triggers a suite of responses including production of reactive oxygen species (ROS) and nitric oxide (NO) and expression changes of defense-related genes. In this study, we used two well-studied MAMPs (flg22 and chitooctaose) to challenge different maize lines to determine whether there was variation in the level of responses to these MAMPs, to dissect the genetic basis underlying that variation and to understand the relationship between MAMP response and quantitative disease resistance (QDR). Naturally occurring quantitative variation in ROS, NO production, and defense genes expression levels triggered by MAMPs was observed. A major quantitative traits locus (QTL) associated with variation in the ROS production response to both flg22 and chitooctaose was identified on chromosome 2 in a recombinant inbred line (RIL) population derived from the maize inbred lines B73 and CML228. Minor QTL associated with variation in the flg22 ROS response was identified on chromosomes 1 and 4. Comparison of these results with data previously obtained for variation in QDR and the defense response in the same RIL population did not provide any evidence for a common genetic basis controlling variation in these traits.
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http://dx.doi.org/10.1007/s00122-017-2876-6DOI Listing
June 2017
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