Publications by authors named "Peter J Balint-Kurti"

31 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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1073/pnas.2021965118DOI 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.
View Article and Find Full Text PDF

Download full-text PDF

Source
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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1111/tpj.15047DOI Listing
January 2021

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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.tplants.2020.02.008DOI Listing
July 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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1111/tpj.14787DOI Listing
August 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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/s41598-019-54802-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6893015PMC
December 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.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.3390/toxins11020086DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6410224PMC
February 2019

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 ().
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.21769/BioProtoc.2745DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8203974PMC
March 2018

The Genetics of Leaf Flecking in Maize and Its Relationship to Plant Defense and Disease Resistance.

Plant Physiol 2016 11 26;172(3):1787-1803. Epub 2016 Sep 26.

Department of Plant Pathology, North Carolina State University, Raleigh, North Carolina 27695-7616 (B.A.O., P.J.B.-K.);

Physiological leaf spotting, or flecking, is a mild-lesion phenotype observed on the leaves of several commonly used maize (Zea mays) inbred lines and has been anecdotally linked to enhanced broad-spectrum disease resistance. Flecking was assessed in the maize nested association mapping (NAM) population, comprising 4,998 recombinant inbred lines from 25 biparental families, and in an association population, comprising 279 diverse maize inbreds. Joint family linkage analysis was conducted with 7,386 markers in the NAM population. Genome-wide association tests were performed with 26.5 million single-nucleotide polymorphisms (SNPs) in the NAM population and with 246,497 SNPs in the association population, resulting in the identification of 18 and three loci associated with variation in flecking, respectively. Many of the candidate genes colocalizing with associated SNPs are similar to genes that function in plant defense response via cell wall modification, salicylic acid- and jasmonic acid-dependent pathways, redox homeostasis, stress response, and vesicle trafficking/remodeling. Significant positive correlations were found between increased flecking, stronger defense response, increased disease resistance, and increased pest resistance. A nonlinear relationship with total kernel weight also was observed whereby lines with relatively high levels of flecking had, on average, lower total kernel weight. We present evidence suggesting that mild flecking could be used as a selection criterion for breeding programs trying to incorporate broad-spectrum disease resistance.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1104/pp.15.01870DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100796PMC
November 2016

Maize Homologs of CCoAOMT and HCT, Two Key Enzymes in Lignin Biosynthesis, Form Complexes with the NLR Rp1 Protein to Modulate the Defense Response.

Plant Physiol 2016 07 10;171(3):2166-77. Epub 2016 May 10.

Department of Plant Pathology, North Carolina State University, Raleigh, North Carolina 27695 (G.-F.W., P.J.B.-K.)Key Laboratory of Plant Cell Engineering and Germplasm Innovation, Ministry of Education, School of Life Sciences, Shandong University, Jinan, Shandong 250100, P.R. China (G.-F.W.); U.S. Department of Agriculture-Agricultural Research Service, Plant Science Research Unit, Raleigh, North Carolina 27695 (P.J.B.-K.).

Disease resistance (R) genes encode nucleotide binding Leu-rich-repeat (NLR) proteins that confer resistance to specific pathogens. Upon pathogen recognition they trigger a defense response that usually includes a so-called hypersensitive response (HR), a rapid localized cell death at the site of pathogen infection. Intragenic recombination between two maize (Zea mays) NLRs, Rp1-D and Rp1-dp2, resulted in the formation of a hybrid NLR, Rp1-D21, which confers an autoactive HR in the absence of pathogen infection. From a previous quantitative trait loci and genome-wide association study, we identified genes encoding two key enzymes in lignin biosynthesis, hydroxycinnamoyltransferase (HCT) and caffeoyl CoA O-methyltransferase (CCoAOMT), adjacent to the nucleotide polymorphisms that were highly associated with variation in the severity of Rp1-D21-induced HR We have previously shown that the two maize HCT homologs suppress the HR conferred by Rp1-D21 in a heterologous system, very likely through physical interaction. Here, we show, similarly, that CCoAOMT2 suppresses the HR induced by either the full-length or by the N-terminal coiled-coil domain of Rp1-D21 also likely via physical interaction and that the metabolic activity of CCoAOMT2 is unlikely to be necessary for its role in suppressing HR. We also demonstrate that CCoAOMT2, HCTs, and Rp1 proteins can form in the same complexes. A model is derived to explain the roles of CCoAOMT and HCT in Rp1-mediated defense resistance.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1104/pp.16.00224DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4936554PMC
July 2016

A Genome-Wide Association Study for Partial Resistance to Maize Common Rust.

Phytopathology 2016 Jul 9;106(7):745-51. Epub 2016 May 9.

First author: Department of Plant Pathology and Department of Horticulture, North Carolina State University, Raleigh 27695; second and fourth authors: Department of Agronomy, University of Wisconsin-Madison, Madison 53706; third author: Department of Plant & Soil Sciences, University of Delaware, Newark 19716; and fifth author: Department of Plant Pathology, North Carolina State University, and United States Department of Agriculture-Agricultural Research Service Plant Science Research Unit, Raleigh, NC 27695.

Quantitative resistance to maize common rust (causal agent Puccinia sorghi) was assessed in an association mapping population of 274 diverse inbred lines. Resistance to common rust was found to be moderately correlated with resistance to three other diseases and with the severity of the hypersensitive defense response previously assessed in the same population. Using a mixed linear model accounting for the confounding effects of population structure and flowering time, genome-wide association tests were performed based at 246,497 single-nucleotide polymorphism loci. Three loci associated with maize common rust resistance were identified. Candidate genes at each locus had predicted roles, mainly in cell wall modification. Other candidate genes included a resistance gene and a gene with a predicted role in regulating accumulation of reactive oxygen species.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1094/PHYTO-11-15-0305-RDOI Listing
July 2016

Maize Homologs of Hydroxycinnamoyltransferase, a Key Enzyme in Lignin Biosynthesis, Bind the Nucleotide Binding Leucine-Rich Repeat Rp1 Proteins to Modulate the Defense Response.

Plant Physiol 2015 Nov 15;169(3):2230-43. Epub 2015 Sep 15.

Departments of Plant Pathology (G.-F.W., Y.H., B.A.O., P.J.B.-K.),Plant and Microbial Biology (R.S., X.L.), andBiological Sciences (D.N.), North Carolina State University, Raleigh, North Carolina 27695;Plants for Human Health Institute, North Carolina State University, Kannapolis, North Carolina 28081 (R.S., X.L.); andPlant Science Research Unit, United States Department of Agriculture-Agricultural Research Service, Raleigh, North Carolina 27695 (P.J.B.-K.)

In plants, most disease resistance genes encode nucleotide binding Leu-rich repeat (NLR) proteins that trigger a rapid localized cell death called a hypersensitive response (HR) upon pathogen recognition. The maize (Zea mays) NLR protein Rp1-D21 derives from an intragenic recombination between two NLRs, Rp1-D and Rp1-dp2, and confers an autoactive HR in the absence of pathogen infection. From a previous quantitative trait loci and genome-wide association study, we identified a single-nucleotide polymorphism locus highly associated with variation in the severity of Rp1-D21-induced HR. Two maize genes encoding hydroxycinnamoyltransferase (HCT; a key enzyme involved in lignin biosynthesis) homologs, termed HCT1806 and HCT4918, were adjacent to this single-nucleotide polymorphism. Here, we show that both HCT1806 and HCT4918 physically interact with and suppress the HR conferred by Rp1-D21 but not other autoactive NLRs when transiently coexpressed in Nicotiana benthamiana. Other maize HCT homologs are unable to confer the same level of suppression on Rp1-D21-induced HR. The metabolic activity of HCT1806 and HCT4918 is unlikely to be necessary for their role in suppressing HR. We show that the lignin pathway is activated by Rp1-D21 at both the transcriptional and metabolic levels. We derive a model to explain the roles of HCT1806 and HCT4918 in Rp1-mediated disease resistance.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1104/pp.15.00703DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4634058PMC
November 2015

Cytoplasmic and Nuclear Localizations Are Important for the Hypersensitive Response Conferred by Maize Autoactive Rp1-D21 Protein.

Mol Plant Microbe Interact 2015 Sep 25;28(9):1023-31. Epub 2015 Aug 25.

1 Dept. of Plant Pathology, North Carolina State University, Raleigh, NC 27695, U.S.A.;

Disease resistance (R) genes have been isolated from many plant species. Most encode nucleotide binding leucine-rich repeat (NLR) proteins that trigger a rapid localized programmed cell death called the hypersensitive response (HR) upon pathogen recognition. Despite their structural similarities, different NLR are distributed in a range of subcellular locations, and analogous domains play diverse functional roles. The autoactive maize NLR gene Rp1-D21 derives from an intragenic recombination between two NLR genes, Rp1-D and Rp1-dp2, and confers a HR independent of the presence of a pathogen. Rp1-D21 and its N-terminal coiled coil (CC) domain (CCD21) confer autoactive HR when transiently expressed in Nicotiana benthamiana. Rp1-D21 was predominantly localized in cytoplasm with a small amount in the nucleus, while CCD21 was localized in both nucleus and cytoplasm. Targeting of Rp1-D21 or CCD21 predominantly to either the nucleus or the cytoplasm abolished HR-inducing activity. Coexpression of Rp1-D21 or CCD21 constructs confined, respectively, to the nucleus and cytoplasm did not rescue full activity, suggesting nucleocytoplasmic movement was important for HR induction. This work emphasizes the diverse structural and subcellular localization requirements for activity found among plant NLR R genes.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1094/MPMI-01-15-0014-RDOI Listing
September 2015

QTL mapping using high-throughput sequencing.

Methods Mol Biol 2015 ;1284:257-85

Department of Crop Science, North Carolina State University, Raleigh, NC, 27695-7620, USA.

Quantitative trait locus (QTL) mapping in plants dates to the 1980s (Stuber et al. Crop Sci 27: 639-648, 1987; Paterson et al. Nature 335: 721-726, 1988), but earlier studies were often hindered by the expense and time required to identify large numbers of polymorphic genetic markers that differentiated the parental genotypes and then to genotype them on large segregating mapping populations. High-throughput sequencing has provided an efficient means to discover single nucleotide polymorphisms (SNPs) that can then be assayed rapidly on large populations with array-based techniques (Gupta et al. Heredity 101: 5-18, 2008). Alternatively, high-throughput sequencing methods such as restriction site-associated DNA sequencing (RAD-Seq) (Davey et al. Nat Rev Genet 12: 499-510, 2011; Baird et al. PloS ONE 3: e3376, 2008) and genotyping-by-sequencing (GBS) (Elshire et al. PLoS One 6: 2011; Glaubitz et al. PLoS One 9: e90346, 2014) can be used to identify and genotype polymorphic markers directly. Linkage disequilibrium (LD) between markers and causal variants is needed to detect QTL. The earliest QTL mapping methods used backcross and F2 generations of crosses between inbred lines, which have high levels of linkage disequilibrium (dependent entirely on the recombination frequency between chromosomal positions), to ensure that QTL would have sufficiently high linkage disequilibrium with one or more markers on sparse genetic linkage maps. The downside of this approach is that resolution of QTL positions is poor. The sequencing technology revolution, by facilitating genotyping of vastly more markers than was previously feasible, has allowed researchers to map QTL in situations of lower linkage disequilibrium, and consequently, at higher resolution. We provide a review of methods to identify QTL with higher precision than was previously possible. We discuss modifications of the traditional biparental mapping population that provide higher resolution of QTL positions, QTL fine-mapping procedures, and genome-wide association studies, all of which are greatly facilitated by high-throughput sequencing methods. Each of these procedures has many variants, and consequently many details to consider; we focus our chapter on the consequences of practical decisions that researchers make when designing QTL mapping studies and when analyzing the resulting data. The ultimate goal of many of these studies is to resolve a QTL to its causal sequence variation.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1007/978-1-4939-2444-8_13DOI Listing
November 2015

Molecular and functional analyses of a maize autoactive NB-LRR protein identify precise structural requirements for activity.

PLoS Pathog 2015 Feb 26;11(2):e1004674. Epub 2015 Feb 26.

Department of Plant Pathology, North Carolina State University, Raleigh, North Carolina, United States of America; USDA-ARS Plant Science Research Unit, Raleigh, North Carolina, United States of America.

Plant disease resistance is often mediated by nucleotide binding-leucine rich repeat (NLR) proteins which remain auto-inhibited until recognition of specific pathogen-derived molecules causes their activation, triggering a rapid, localized cell death called a hypersensitive response (HR). Three domains are recognized in one of the major classes of NLR proteins: a coiled-coil (CC), a nucleotide binding (NB-ARC) and a leucine rich repeat (LRR) domains. The maize NLR gene Rp1-D21 derives from an intergenic recombination event between two NLR genes, Rp1-D and Rp1-dp2 and confers an autoactive HR. We report systematic structural and functional analyses of Rp1 proteins in maize and N. benthamiana to characterize the molecular mechanism of NLR activation/auto-inhibition. We derive a model comprising the following three main features: Rp1 proteins appear to self-associate to become competent for activity. The CC domain is signaling-competent and is sufficient to induce HR. This can be suppressed by the NB-ARC domain through direct interaction. In autoactive proteins, the interaction of the LRR domain with the NB-ARC domain causes de-repression and thus disrupts the inhibition of HR. Further, we identify specific amino acids and combinations thereof that are important for the auto-inhibition/activity of Rp1 proteins. We also provide evidence for the function of MHD2, a previously uncharacterized, though widely conserved NLR motif. This work reports several novel insights into the precise structural requirement for NLR function and informs efforts towards utilizing these proteins for engineering disease resistance.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1371/journal.ppat.1004674DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4342346PMC
February 2015

New insight into a complex plant-fungal pathogen interaction.

Nat Genet 2015 Feb;47(2):101-3

Plant Science Research Unit, US Department of Agriculture-Agricultural Research Service (USDA-ARS) and the Department of Crop Science, North Carolina State University, Raleigh, North Carolina, USA.

The coevolution of plants and microbes has shaped plant mechanisms that detect and repel pathogens. A newly identified plant gene confers partial resistance to a fungal pathogen not by preventing initial infection but by limiting its spread through the plant.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/ng.3203DOI Listing
February 2015

Limits on the reproducibility of marker associations with southern leaf blight resistance in the maize nested association mapping population.

BMC Genomics 2014 Dec 5;15:1068. Epub 2014 Dec 5.

Department of Crop Science, North Carolina State University, Raleigh, NC 27695, USA.

Background: A previous study reported a comprehensive quantitative trait locus (QTL) and genome wide association study (GWAS) of southern leaf blight (SLB) resistance in the maize Nested Association Mapping (NAM) panel. Since that time, the genomic resources available for such analyses have improved substantially. An updated NAM genetic linkage map has a nearly six-fold greater marker density than the previous map and the combined SNPs and read-depth variants (RDVs) from maize HapMaps 1 and 2 provided 28.5 M genomic variants for association analysis, 17 fold more than HapMap 1. In addition, phenotypic values of the NAM RILs were re-estimated to account for environment-specific flowering time covariates and a small proportion of lines were dropped due to genotypic data quality problems. Comparisons of original and updated QTL and GWAS results confound the effects of linkage map density, GWAS marker density, population sample size, and phenotype estimates. Therefore, we evaluated the effects of changing each of these parameters individually and in combination to determine their relative impact on marker-trait associations in original and updated analyses.

Results: Of the four parameters varied, map density caused the largest changes in QTL and GWAS results. The updated QTL model had better cross-validation prediction accuracy than the previous model. Whereas joint linkage QTL positions were relatively stable to input changes, the residual values derived from those QTL models (used as inputs to GWAS) were more sensitive, resulting in substantial differences between GWAS results. The updated NAM GWAS identified several candidate genes consistent with previous QTL fine-mapping results.

Conclusions: The highly polygenic nature of resistance to SLB complicates the identification of causal genes. Joint linkage QTL are relatively stable to perturbations of data inputs, but their resolution is generally on the order of tens or more Mbp. GWAS associations have higher resolution, but lower power due to stringent thresholds designed to minimize false positive associations, resulting in variability of detection across studies. The updated higher density linkage map improves QTL estimation and, along with a much denser SNP HapMap, greatly increases the likelihood of detecting SNPs in linkage with causal variants. We recommend use of the updated genetic resources and results but emphasize the limited repeatability of small-effect associations.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1186/1471-2164-15-1068DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4300987PMC
December 2014

Southern leaf blight disease severity is correlated with decreased maize leaf epiphytic bacterial species richness and the phyllosphere bacterial diversity decline is enhanced by nitrogen fertilization.

Front Plant Sci 2014 15;5:403. Epub 2014 Aug 15.

Department of Biology and Marine Biology, University of North Carolina Wilmington Wilmington, NC, USA.

Plant leaves are inhabited by a diverse group of microorganisms that are important contributors to optimal growth. Biotic and abiotic effects on plant growth are usually studied in controlled settings examining response to variation in single factors and in field settings with large numbers of variables. Multi-factor experiments with combinations of stresses bridge this gap, increasing our understanding of the genotype-environment-phenotype functional map for the host plant and the affiliated epiphytic community. The maize inbred B73 was exposed to single and combination abiotic and the biotic stress treatments: low nitrogen fertilizer and high levels of infection with southern leaf blight (causal agent Cochliobolus heterostrophus). Microbial epiphyte samples were collected at the vegetative early-season phase and species composition was determined using 16S ribosomal intergenic spacer analysis. Plant traits and level of southern leaf blight disease were measured late-season. Bacterial diversity was different among stress treatment groups (P < 0.001). Lower species richness-alpha diversity-was correlated with increased severity of southern leaf blight disease when disease pressure was high. Nitrogen fertilization intensified the decline in bacterial alpha diversity. While no single bacterial ribotype was consistently associated with disease severity, small sets of ribotypes were good predictors of disease levels. Difference in leaf bacterial-epiphyte diversity early in the season were correlated with plant disease severity, supporting further tests of microbial epiphyte-disease correlations for use in predicting disease progression.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.3389/fpls.2014.00403DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4133650PMC
September 2014

A genome-wide association study of the maize hypersensitive defense response identifies genes that cluster in related pathways.

PLoS Genet 2014 Aug 28;10(8):e1004562. Epub 2014 Aug 28.

Department of Botany and Plant Pathology, Purdue University, Lilly Hall, West Lafayette, Indiana, United States of America.

Much remains unknown of molecular events controlling the plant hypersensitive defense response (HR), a rapid localized cell death that limits pathogen spread and is mediated by resistance (R-) genes. Genetic control of the HR is hard to quantify due to its microscopic and rapid nature. Natural modifiers of the ectopic HR phenotype induced by an aberrant auto-active R-gene (Rp1-D21), were mapped in a population of 3,381 recombinant inbred lines from the maize nested association mapping population. Joint linkage analysis was conducted to identify 32 additive but no epistatic quantitative trait loci (QTL) using a linkage map based on more than 7000 single nucleotide polymorphisms (SNPs). Genome-wide association (GWA) analysis of 26.5 million SNPs was conducted after adjusting for background QTL. GWA identified associated SNPs that colocalized with 44 candidate genes. Thirty-six of these genes colocalized within 23 of the 32 QTL identified by joint linkage analysis. The candidate genes included genes predicted to be in involved programmed cell death, defense response, ubiquitination, redox homeostasis, autophagy, calcium signalling, lignin biosynthesis and cell wall modification. Twelve of the candidate genes showed significant differential expression between isogenic lines differing for the presence of Rp1-D21. Low but significant correlations between HR-related traits and several previously-measured disease resistance traits suggested that the genetic control of these traits was substantially, though not entirely, independent. This study provides the first system-wide analysis of natural variation that modulates the HR response in plants.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1371/journal.pgen.1004562DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4148229PMC
August 2014

Multivariate mixed linear model analysis of longitudinal data: an information-rich statistical technique for analyzing plant disease resistance.

Phytopathology 2012 Nov;102(11):1016-25

Department of Plant and Soil Sciences, University of Delaware, Newark 19716, USA.

ABSTRACT The mixed linear model (MLM) is an advanced statistical technique applicable to many fields of science. The multivariate MLM can be used to model longitudinal data, such as repeated ratings of disease resistance taken across time. In this study, using an example data set from a multi-environment trial of northern leaf blight disease on 290 maize lines with diverse levels of resistance, multivariate MLM analysis was performed and its utility was examined. In the population and environments tested, genotypic effects were highly correlated across disease ratings and followed an autoregressive pattern of correlation decay. Because longitudinal data are often converted to the univariate measure of area under the disease progress curve (AUDPC), comparisons between univariate MLM analysis of AUDPC and multivariate MLM analysis of longitudinal data were made. Univariate analysis had the advantage of simplicity and reduced computational demand, whereas multivariate analysis enabled a comprehensive perspective on disease development, providing the opportunity for unique insights into disease resistance. To aid in the application of multivariate MLM analysis of longitudinal data on disease resistance, annotated program syntax for model fitting is provided for the software ASReml.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1094/PHYTO-10-11-0268DOI Listing
November 2012

Analysis of quantitative disease resistance to southern leaf blight and of multiple disease resistance in maize, using near-isogenic lines.

Theor Appl Genet 2012 Feb 14;124(3):433-45. Epub 2011 Oct 14.

Department of Plant Pathology, North Carolina State University, Raleigh, NC 27695-7616, USA.

Maize inbred lines NC292 and NC330 were derived by repeated backcrossing of an elite source of southern leaf blight (SLB) resistance (NC250P) to the SLB-susceptible line B73, with selection for SLB resistance among and within backcross families at each generation. Consequently, while B73 is very SLB susceptible, its sister lines NC292 and NC330 are both SLB resistant. Previously, we identified the 12 introgressions from NC250P that differentiate NC292 and NC330 from B73. The goals of this study were to determine the effects of each introgression on resistance to SLB and to two other foliar fungal diseases of maize, northern leaf blight and gray leaf spot. This was achieved by generating and testing a set of near isogenic lines carry single or combinations of just two or three introgressions in a B73 background. Introgressions 3B, 6A, and 9B (bins 3.03-3.04, 6.01, and 9.02-9.03) all conferred significant levels of SLB resistance in the field. Introgression 6A was the only introgression that had a significant effect on juvenile plant resistance to SLB. Introgressions 6A and 9B conferred resistance to multiple diseases.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1007/s00122-011-1718-1DOI Listing
February 2012

Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene.

Proc Natl Acad Sci U S A 2011 May 13;108(18):7339-44. Epub 2011 Apr 13.

Department of Plant and Soil Sciences, University of Delaware, Newark, DE 19716-1304, USA.

Plants are attacked by pathogens representing diverse taxonomic groups, such that genes providing multiple disease resistance (MDR) are expected to be under positive selection pressure. To address the hypothesis that naturally occurring allelic variation conditions MDR, we extended the framework of structured association mapping to allow for the analysis of correlated complex traits and the identification of pleiotropic genes. The multivariate analytical approach used here is directly applicable to any species and set of traits exhibiting correlation. From our analysis of a diverse panel of maize inbred lines, we discovered high positive genetic correlations between resistances to three globally threatening fungal diseases. The maize panel studied exhibits rapidly decaying linkage disequilibrium that generally occurs within 1 or 2 kb, which is less than the average length of a maize gene. The positive correlations therefore suggested that functional allelic variation at specific genes for MDR exists in maize. Using a multivariate test statistic, a glutathione S-transferase (GST) gene was found to be associated with modest levels of resistance to all three diseases. Resequencing analysis pinpointed the association to a histidine (basic amino acid) for aspartic acid (acidic amino acid) substitution in the encoded protein domain that defines GST substrate specificity and biochemical activity. The known functions of GSTs suggested that variability in detoxification pathways underlie natural variation in maize MDR.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1073/pnas.1011739108DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3088610PMC
May 2011

Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population.

Nat Genet 2011 Feb 9;43(2):163-8. Epub 2011 Jan 9.

Department of Crop Science, North Carolina State University, Raleigh, North Carolina, USA.

Nested association mapping (NAM) offers power to resolve complex, quantitative traits to their causal loci. The maize NAM population, consisting of 5,000 recombinant inbred lines (RILs) from 25 families representing the global diversity of maize, was evaluated for resistance to southern leaf blight (SLB) disease. Joint-linkage analysis identified 32 quantitative trait loci (QTLs) with predominantly small, additive effects on SLB resistance. Genome-wide association tests of maize HapMap SNPs were conducted by imputing founder SNP genotypes onto the NAM RILs. SNPs both within and outside of QTL intervals were associated with variation for SLB resistance. Many of these SNPs were within or near sequences homologous to genes previously shown to be involved in plant disease resistance. Limited linkage disequilibrium was observed around some SNPs associated with SLB resistance, indicating that the maize NAM population enables high-resolution mapping of some genome regions.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1038/ng.747DOI Listing
February 2011

Identification of a maize locus that modulates the hypersensitive defense response, using mutant-assisted gene identification and characterization.

Genetics 2010 Mar 22;184(3):813-25. Epub 2010 Feb 22.

Department of Botany and Plant Pathology, Purdue University, West Lafayette, Indiana 47907-2054, USA.

Potentially useful naturally occurring genetic variation is often difficult to identify as the effects of individual genes are subtle and difficult to observe. In this study, a novel genetic technique called Mutant-Assisted Gene Identification and Characterization is used to identify naturally occurring loci modulating the hypersensitive defense response (HR) in maize. Mutant-Assisted Gene Identification and Characterization facilitates the identification of naturally occurring alleles underlying phenotypic variation from diverse germplasm, using a mutant phenotype as a "reporter." In this study the reporter phenotype was caused by a partially dominant autoactive disease resistance gene, Rp1-D21, which caused HR lesions to form spontaneously all over the plant. Here it is demonstrated that the Rp1-D21 phenotype is profoundly affected by genetic background. By crossing the Rp1-D21 gene into the IBM mapping population, it was possible to map and identify Hrml1 on chromosome 10, a locus responsible for modulating the HR phenotype conferred by Rp1-D21. Other loci with smaller effects were identified on chromosomes 1 and 9. These results demonstrate that Mutant-Assisted Gene Identification and Characterization is a viable approach for identifying naturally occurring useful genetic variation.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1534/genetics.109.111880DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2845348PMC
March 2010

Genetic control of photoperiod sensitivity in maize revealed by joint multiple population analysis.

Genetics 2010 Mar 14;184(3):799-812. Epub 2009 Dec 14.

Department of Crop Science, North Carolina State University, Raleigh, North Carolina 27695, USA.

Variation in maize for response to photoperiod is related to geographical adaptation in the species. Maize possesses homologs of many genes identified as regulators of flowering time in other species, but their relation to the natural variation for photoperiod response in maize is unknown. Candidate gene sequences were mapped in four populations created by crossing two temperate inbred lines to two photoperiod-sensitive tropical inbreds. Whole-genome scans were conducted by high-density genotyping of the populations, which were phenotyped over 3 years in both short- and long-day environments. Joint multiple population analysis identified genomic regions controlling photoperiod responses in flowering time, plant height, and total leaf number. Four key genome regions controlling photoperiod response across populations were identified, referred to as ZmPR1-4. Functional allelic differences within these regions among phenotypically similar founders suggest distinct evolutionary trajectories for photoperiod adaptation in maize. These regions encompass candidate genes CCA/LHY, CONZ1, CRY2, ELF4, GHD7, VGT1, HY1/SE5, TOC1/PRR7/PPD-1, PIF3, ZCN8, and ZCN19.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1534/genetics.109.110304DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2845347PMC
March 2010

Mapping resistance quantitative trait Loci for three foliar diseases in a maize recombinant inbred line population-evidence for multiple disease resistance?

Phytopathology 2010 Jan;100(1):72-9

Department of Plant Pathology, North Carolona State University, Raleigh, NC 27695, USA.

Southern leaf blight (SLB), gray leaf spot (GLS), and northern leaf blight (NLB) are all important foliar diseases impacting maize production. The objectives of this study were to identify quantitative trait loci (QTL) for resistance to these diseases in a maize recombinant inbred line (RIL) population derived from a cross between maize lines Ki14 and B73, and to evaluate the evidence for the presence genes or loci conferring multiple disease resistance (MDR). Each disease was scored in multiple separate trials. Highly significant correlations between the resistances and the three diseases were found. The highest correlation was identified between SLB and GLS resistance (r = 0.62). Correlations between resistance to each of the diseases and time to flowering were also highly significant. Nine, eight, and six QTL were identified for SLB, GLS, and NLB resistance, respectively. QTL for all three diseases colocalized in bin 1.06, while QTL colocalizing for two of the three diseases were identified in bins 1.08 to 1.09, 2.02/2.03, 3.04/3.05, 8.05, and 10.05. QTL for time to flowering were also identified at four of these six loci (bins 1.06, 3.04/3.05, 8.05, and 10.05). No disease resistance QTL was identified at the largest-effect QTL for flowering time in bin 10.03.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1094/PHYTO-100-1-0072DOI Listing
January 2010

Use of selection with recurrent backcrossing and QTL mapping to identify loci contributing to southern leaf blight resistance in a highly resistant maize line.

Theor Appl Genet 2009 Mar 8;118(5):911-25. Epub 2009 Jan 8.

Department of Plant Pathology, North Carolina State University, Raleigh, NC 27695-7616, USA.

B73 is a historically important maize line with excellent yield potential but high susceptibility to the foliar disease southern leaf blight (SLB). NC292 and NC330 are B73 near-isogenic lines (NILs) that are highly resistant to SLB. They were derived by repeated backcrossing of an elite source of SLB resistance (NC250P) to B73, with selection for SLB resistance among and within backcross families. The goal of this paper was to characterize the loci responsible for the increased SLB resistance of NC292 and NC330 and to determine how many of the SLB disease resistance quantitative trait loci (dQTL) were selected for in the development of NC292 and NC330. Genomic regions that differentiated NC292 and NC330 from B73 and which may contribute to NC292 and NC330s enhanced SLB resistance were identified. Ten NC250P-derived introgressions were identified in both the NC292 and NC330 genomes of which eight were shared between genomes. dQTL were mapped in two F(2:3) populations derived from lines very closely related to the original parents of NC292 and NC330--(B73rhm1 x NC250A and NC250A x B73). Nine SLB dQTL were mapped in the combined populations using combined SLB disease data over all locations (SLB AllLocs). Of these, four dQTL precisely colocalized with NC250P introgressions in bins 2.05-2.06, 3.03, 6.01, and 9.02 and three were identified near NC250P introgressions in bins 1.09, 5.05-5.06, and 10.03. Therefore the breeding program used to develop NC292 and NC330 was highly effective in selecting for multiple SLB resistance alleles.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1007/s00122-008-0949-2DOI Listing
March 2009

Shades of gray: the world of quantitative disease resistance.

Trends Plant Sci 2009 Jan 4;14(1):21-9. Epub 2008 Dec 4.

Department of Plant Breeding & Genetics, Cornell University, Ithaca, NY 14853, USA.

A thorough understanding of quantitative disease resistance (QDR) would contribute to the design and deployment of durably resistant crop cultivars. However, the molecular mechanisms that control QDR remain poorly understood, largely due to the incomplete and inconsistent nature of the resistance phenotype, which is usually conditioned by many loci of small effect. Here, we discuss recent advances in research on QDR. Based on inferences from analyses of the defense response and from the few isolated QDR genes, we suggest several plausible hypotheses for a range of mechanisms underlying QDR. We propose that a new generation of genetic resources, complemented by careful phenotypic analysis, will produce a deeper understanding of plant defense and more effective utilization of natural resistance alleles.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1016/j.tplants.2008.10.006DOI Listing
January 2009

The genetic architecture of disease resistance in maize: a synthesis of published studies.

Phytopathology 2006 Feb;96(2):120-9

ABSTRACT Fifty publications on the mapping of maize disease resistance loci were synthesized. These papers reported the locations of 437 quantitative trait loci (QTL) for disease (dQTL), 17 resistance genes (R-genes), and 25 R-gene analogs. A set of rules was devised to enable the placement of these loci on a single consensus map, permitting analysis of the distribution of resistance loci identified across a variety of maize germplasm for a number of different diseases. The confidence intervals of the dQTL were distributed over all 10 chromosomes and covered 89% of the genetic map to which the data were anchored. Visual inspection indicated the presence of clusters of dQTL for multiple diseases. Clustering of dQTL was supported by statistical tests that took into account genome-wide variations in gene density. Several novel clusters of resistance loci were identified. Evidence was also found for the association of dQTL with maturity-related QTL. It was evident from the distinct dQTL distributions for the different diseases that certain breeding schemes may be more suitable for certain diseases. This review provides an up-to-date synthesis of reports on the locations of resistance loci in maize.
View Article and Find Full Text PDF

Download full-text PDF

Source
http://dx.doi.org/10.1094/PHYTO-96-0120DOI Listing
February 2006
-->