Papers by Martin I Chilvers
ISME Communications, Feb 23, 2022
Fungicides reduce fungal pathogen populations and are essential to food security. Understanding t... more Fungicides reduce fungal pathogen populations and are essential to food security. Understanding the impacts of fungicides on crop microbiomes is vital to minimizing unintended consequences while maintaining their use for plant protection. However, fungicide disturbance of plant microbiomes has received limited attention, and has not been examined in different agricultural management systems. We used amplicon sequencing of fungi and prokaryotes in maize and soybean microbiomes before and after foliar fungicide application in leaves and roots from plots under long-term no-till and conventional tillage management. We examined fungicide disturbance and resilience, which revealed consistent non-target effects and greater resiliency under no-till management. Fungicides lowered pathogen abundance in maize and soybean and decreased the abundance of Tremellomycetes yeasts, especially Bulleribasidiaceae, including core microbiome members. Fungicide application reduced network complexity in the soybean phyllosphere, which revealed altered co-occurrence patterns between yeast species of Bulleribasidiaceae, and Sphingomonas and Hymenobacter in fungicide treated plots. Results indicate that foliar fungicides lower pathogen and non-target fungal abundance and may impact prokaryotes indirectly. Treatment effects were confined to the phyllosphere and did not impact belowground microbial communities. Overall, these results demonstrate the resilience of no-till management to fungicide disturbance, a potential novel ecosystem service provided by no-till agriculture.
We performed multiyear and multi-location evaluations of seed treatments, in-furrow, and foliar p... more We performed multiyear and multi-location evaluations of seed treatments, in-furrow, and foliar products for management of sudden death syndrome (SDS) of soybean. • Among the seed treatments we evaluated in our trials, only fluopyram seed treatment reduced SDS severity compared to a commercial base seed treatment. • We found a 35 percent reduction in symptoms of SDS and a yield increase of 4.4 bushels per acre (7.6 percent) with fluopyram seed treatment relative to a commercial base seed treatment that consisted of fungicide, insecticide, and biological nematicide products. • When SDS symptoms were severe (>10 FDX in the base seed treatment), fluopyram protected grain yield more than 80 percent of the time compared to the commercial base seed treatment. The probability of seeing a yield advantage from seed treatment in the absence of SDS symptoms was very low. • Effective use of fluopyram seed treatment can complement resistant varieties for management of SDS.
Theoretical and Applied Genetics, Sep 10, 2022
Pythium root rot is an important seedling disease of soybean [Glycine max (L.) Merr.], a crop gro... more Pythium root rot is an important seedling disease of soybean [Glycine max (L.) Merr.], a crop grown worldwide for protein and oil content. Pythium irregulare and P. sylvaticum are two of the most prevalent and aggressive Pythium species in soybean producing regions in the North Central U.S. A few studies have been conducted to identify soybean resistance against the two pathogens. In this study, a mapping population (derived from E13390 x E13901) with 228 F4:5 recombinant inbred lines were screened against P. irregulare isolate MISO 11 -6 and P. sylvaticum isolate C-MISO2-2-30 for QDRL mapping. Correlation analysis indicated signi cant positive correlations between soybean responses to the two pathogens, and a pleiotropic QDRL (qPirr16.1) was identi ed. Further investigation found that the qPirr16.1 imparts dominant resistance against P. irregulare, but recessive resistance against P. sylvaticum. In addition, two QDRL, qPsyl15.1, and qPsyl18.1 were identi ed for partial resistance to P. sylvaticum. Further analysis revealed epistatic interactions between qPirr16.1 and qPsyl15.1 for RRW and DRX, whereas qPsyl18.1 contributed resistance to RSE. Marker assisted resistance spectrum analysis using F6:7 progeny lines veri ed the resistance of qPirr16.1 against four additional P. irregulare isolates. Intriguingly, although the epistatic interaction of qPirr16.1 and qPsyl15.1 can be con rmed using two additional isolates of P. sylvaticum, the interaction appears to be suppressed for the other two P. sylvaticum isolates. An 'epistatic gene-for-gene' model was proposed to explain the isolate-speci c epistatic interactions. The integration of the QDRL into elite soybean lines has been initiated containing all the desirable alleles. Pleiotropic and epistatic quantitative disease resistance loci (QDRL) were identi ed for soybean partial resistance to different isolates of Pythium irregulare and Pythium sylvaticum.
Plant Disease, Aug 1, 2021
Soybean production in the upper midwestern United States is affected by Sclerotinia stem rot (SSR... more Soybean production in the upper midwestern United States is affected by Sclerotinia stem rot (SSR) caused by the fungal pathogen Sclerotinia sclerotiorum. Genetic resistance is an important management strategy for this disease; however, assessing genetic resistance to S. sclerotiorum is challenging because a standardized method of examining resistance across genotypes is lacking. Using a panel of nine diverse S. sclerotiorum isolates, four soybean lines were assessed for reproducible responses to S. sclerotiorum infection. Significant differences in SSR severity were found across isolates (P < 0.01) and soybean lines (P < 0.01), including one susceptible, two moderately resistant, and one highly resistant line. These four validated lines were used to screen 11 other soybean genotypes to evaluate their resistance levels, and significant differences were found across genotypes (P < 0.01). Among these 11 genotypes, five commercial and public cultivars displayed high resistance and were assessed during field studies across the upper midwestern United States growing region to determine their response to SSR and yield. These five cultivars resulted in low disease levels (P < 0.01) in the field that were consistent with greenhouse experiment results. The yields were significantly different in fields with disease present (P < 0.01) and disease absent (P < 0.01), and the order of cultivar performance was consistent between environments where disease was present or absent, suggesting that resistance prevented yield loss to disease. This study suggests that the use of a soybean check panel can accurately assess SSR resistance in soybean germplasm and aid in breeding and commercial soybean development.
Plant Health Progress, 2016
Early season brown spot caused by Septoria glycines was compared in Illinois, Indiana, Iowa, Mich... more Early season brown spot caused by Septoria glycines was compared in Illinois, Indiana, Iowa, Michigan, and Ontario, Canada, soybean fields planted with differing commercial seed treatments. Seed treatments that included fluopyram significantly reduced brown spot (P < 0.001). A greenhouse mist chamber experiment revealed that fluopyram seed treatment reduced the Area Under Disease Progress Curve of brown spot over a 6-week period (P < 0.001). Brown spot severity was unaffected by plant age at inoculation for the control treatment without fluopyram (P = 0.911); however, severity increased with plant age at inoculation for the fluopyram treatment (P = 0.009). The sensitivity of two S. glycines isolates to fluopyram was assessed by determining the effective concentration required to reduce its colony diameter growth in culture by 50% (EC 50 ). Both isolates had an EC 50 of 0.41 μg/ml of fluopyram. These results demonstrate that fluopyram seed treatment is effecttive at controlling early season brown spot in soybean.
Journal of Integrated Pest Management, 2020
Tar spot on corn, caused by the fungus (Phyllachora maydis Maubl. [Phyllachorales: Phyllachoracea... more Tar spot on corn, caused by the fungus (Phyllachora maydis Maubl. [Phyllachorales: Phyllachoraceae]), is an emerging disease in the United States. In 2018 and 2019, significant but localized epidemics of tar spot occurred across the major corn producing region of the Midwest. After being first detected in 2015, tar spot was detected in 135 and 139 counties where the disease was not previously detected in 2018 and 2019, respectively, and is now established across 310 counties across the United Sates. Foliage with signs (stromata) of P. maydis and symptoms of tar spot were collected from 128 fields in 2018 and 191 fields in 2019, across seven states. Samples were assessed for severity of fungal stromata (percent leaf area covered with stromata) on foliage and the incidence of fisheye lesions (proportion of lesions with fisheye symptoms) associated with fungal stromata. Stromatal severity on samples in 2018 ranged from 0.5 to 67% and incidence of fisheye lesions ranged from 0 to 12%, whereas in 2019, stromatal severity ranged from 0.1 to 35% and incidence of fisheye lesions ranged from 0 to 80%, with 95% of samples presenting less than 6% incidence of fisheye lesions. Tar spot has spread substantially from where it was first reported in the United States. Collaborative efforts to monitor the spread and educate clientele on management are essential as this disease spreads into new areas.
Plant Disease, Jul 1, 2019
Sudden death syndrome (SDS), caused by Fusarium virguliforme, is an important soilborne disease o... more Sudden death syndrome (SDS), caused by Fusarium virguliforme, is an important soilborne disease of soybean. Risk of SDS increases when cool and wet conditions occur soon after planting. Recently, multiple seed treatment and foliar products have been registered and advertised for management of SDS but not all have been tested side by side in the same field experiment at multiple field locations. In 2015 and 2016, seed treatment fungicides fluopyram and thiabendazole; seed treatment biochemical pesticides citric acid and saponins extract of Chenopodium quinoa; foliar fungicides fluoxastrobin + flutriafol; and an herbicide, lactofen, were evaluated in Illinois,
Frontiers in Microbiology, Jun 3, 2020
Soybean (Glycine max) is an important leguminous crop that is grown throughout the United States ... more Soybean (Glycine max) is an important leguminous crop that is grown throughout the United States and around the world. In 2016, soybean was valued at $41 billion USD in the United States alone. Increasingly, soybean farmers are adopting alternative management strategies to improve the sustainability and profitability of their crop. Various benefits have been demonstrated for alternative management systems, but their effects on soybean-associated microbial communities are not well-understood. In order to better understand the impact of crop management systems on the soybean-associated microbiome, we employed DNA amplicon sequencing of the Internal Transcribed Spacer (ITS) region and 16S rRNA genes to analyze fungal and prokaryotic communities associated with soil, roots, stems, and leaves. Soybean plants were sampled from replicated fields under long-term conventional, no-till, and organic management systems at three time points throughout the growing season. Results indicated that sample origin was the main driver of beta diversity in soybean-associated microbial communities, but management regime and plant growth stage were also significant factors. Similarly, differences in alpha diversity are driven by compartment and sample origin. Overall, the organic management system had lower fungal and bacterial Shannon diversity. In prokaryotic communities, aboveground tissues were dominated by Sphingomonas and Methylobacterium while belowground samples were dominated by Bradyrhizobium and Sphingomonas. Aboveground fungal communities were dominated by Davidiella across all management systems, while belowground samples were dominated by Fusarium and Mortierella. Specific taxa including potential plant beneficials such as Mortierella were indicator species of the conventional and organic management systems. No-till management increased the abundance of groups known to contain plant beneficial organisms such as Bradyrhizobium and Glomeromycotina. Network analyses show different highly connected hub taxa were present in each management system. Overall, this research demonstrates how specific long-term cropping management systems alter microbial communities and how those communities change throughout the growth of soybean.
Modern Integrated Management Practices for Controlling White Mold of Soybean
Impact of foliar fungicide timing and fungicide class on corn yield response in the United States and Ontario, Canada
Crop Protection, Feb 1, 2021
The filamentous plant pathogenic fungus Fusarium graminearum and Fusarium asiaticum are members o... more The filamentous plant pathogenic fungus Fusarium graminearum and Fusarium asiaticum are members of the F. graminearum species complex (FGSC) and are the two main pathogens causing Fusarium head blight (FHB) of winter wheat in China (
Crop Science, May 18, 2017
S eed-applied fungicides and insecticides have become a common component in modern soybean produc... more S eed-applied fungicides and insecticides have become a common component in modern soybean production systems for protection against various seedling diseases and insects. reported that only 8 and 30% of soybean seed in the United States was treated in 1996 and 2008, respectively. Since 2008, seed treatment use has more than doubled to >75% in 2015 according to seed industry personnel. The drastic surge in soybean seed treatment use over the past 15 yr is most likely a result of four underlying factors. First, farmers within the Midwest are planting earlier into cooler and wetter soil, which slows seedling emergence and gives the seed greater exposure to earlyseason root rooting pathogens and insects . Second, soybean seed costs have nearly doubled in the past decade to ~US$50 unit -1 (140,000 seeds) and now represent 36% of the total annual variable operating expenses worth protecting
A β‐lactamase gene of <i>Fusarium oxysporum</i> alters the rhizosphere microbiota of soybean
Plant Journal, May 18, 2021
SummaryThe rhizosphere is a multitrophic environment, and for soilborne pathogens such as Fusariu... more SummaryThe rhizosphere is a multitrophic environment, and for soilborne pathogens such as Fusarium oxysporum, microbial competition in the rhizosphere is inevitable before reaching and infecting roots. This study established a tritrophic interaction among the plant growth‐promoting rhizobacterium Burkholderia ambifaria, F. oxysporum and Glycine max (soybean) to study the effects of F. oxysporum genes on shaping the soybean microbiota. Although B. ambifaria inhibited mycelial growth and increased bacterial propagation in the presence of F. oxysporum, F. oxysporum still managed to infect soybean in the presence of B. ambifaria. RNA‐Seq identified a putative F. oxysporum secretory β‐lactamase‐coding gene, FOXG_18438 (abbreviated as Fo18438), that is upregulated during soybean infection in the presence of B. ambifaria. The ∆Fo18438 mutants displayed reduced mycelial growth towards B. ambifaria, and the complementation of full Fo18438 and the Fo18438 β‐lactamase domain restored mycelial growth. Using the F. oxysporum wild type, ∆Fo18438 mutants and complemented strains with full Fo18438, Fo18438 β‐lactamase domain or Fo18438 RTA1‐like domain for soil inoculation, 16S rRNA amplicon sequencing revealed that the abundance of a Burkholderia operational taxonomic unit (OTU) was increased in the rhizosphere microbiota infested by the strains with Fo18438 β‐lactamase domain. Non‐metric multidimensional scaling and PICRUSt2 functional analysis revealed differential abundance for the bacterial β‐lactam‐related functions when contrasting the genotypes of F. oxysporum. These results indicated that the Fo18438 β‐lactamase domain provides F. oxysporum with the advantage of growing into the soybean rhizosphere, where β‐lactam antibiosis is involved in microbial competition. Accordingly, this study highlights the capability of an F. oxysporum gene for altering the soybean rhizosphere and taproot microbiota.
Plant Health Progress, 2020
Plant Disease, Jun 1, 2018
A meta-analytic approach was used to summarize data on the effects of fluopyram-amended seed trea... more A meta-analytic approach was used to summarize data on the effects of fluopyram-amended seed treatment on sudden death syndrome (SDS) and yield of soybean (Glycine max L.) in over 200 field trials conducted in 12 U.S. states and Ontario, Canada from 2013 to 2015. In those trials, two treatments-the commercial base (CB), and CB plus fluopyram (CBF)-were tested, and all disease and yield data were combined to conduct a random-effects and mixed-effects meta-analysis (test of moderators) to estimate percent control and yield response relative to CB. Overall, a 35% reduction in foliar disease and 295 kg/ha (7.6%) increase in yield were estimated for CBF relative to CB. Sowing date and geographic region affected both estimates. The variation in yield response was explained partially by disease severity (19%), geographic region (8%), and sowing date (10%) but not by the resistance level of the cultivar. The probability of not offsetting the cost of fluopyram was estimated on a range of grain prices and treatment cost combinations. There was a high probability (>80%) of yield gains when disease level was high in any cost-price combinations tested but very low when the foliar symptoms of the disease were absent.
BMC Genomics, Sep 23, 2014
Background: Sudden death syndrome (SDS) is a serious threat to soybean production that can be man... more Background: Sudden death syndrome (SDS) is a serious threat to soybean production that can be managed with host plant resistance. To dissect the genetic architecture of quantitative resistance to the disease in soybean, two independent association panels of elite soybean cultivars, consisting of 392 and 300 unique accessions, respectively, were evaluated for SDS resistance in multiple environments and years. The two association panels were genotyped with 52,041 and 5,361 single nucleotide polymorphisms (SNPs), respectively. Genome-wide association mapping was carried out using a mixed linear model that accounted for population structure and cryptic relatedness. Result: A total of 20 loci underlying SDS resistance were identified in the two independent studies, including 7 loci localized in previously mapped QTL intervals and 13 novel loci. One strong peak of association on chromosome 18, associated with all disease assessment criteria across the two panels, spanned a physical region of 1.2 Mb around a previously cloned SDS resistance gene (GmRLK18-1) in locus Rfs2. An additional variant independently associated with SDS resistance was also found in this genomic region. Other peaks were within, or close to, sequences annotated as homologous to genes previously shown to be involved in plant disease resistance. The identified loci explained an average of 54.5% of the phenotypic variance measured by different disease assessment criteria. Conclusions: This study identified multiple novel loci and refined the map locations of known loci related to SDS resistance. These insights into the genetic basis of SDS resistance can now be used to further enhance durable resistance to SDS in soybean. Additionally, the associations identified here provide a basis for further efforts to pinpoint causal variants and to clarify how the implicated genes affect SDS resistance in soybean.
Fungicide sensitivity of <i>Sclerotinia sclerotiorum</i> from U.S. soybean and dry bean, compared to different regions and climates
Plant Disease, Jan 23, 2023
bioRxiv (Cold Spring Harbor Laboratory), Sep 21, 2021
Fungicides reduce fungal pathogen populations and are essential to food security. Fungicide distu... more Fungicides reduce fungal pathogen populations and are essential to food security. Fungicide disturbance of plant microbiomes has received limited attention. Understanding the impacts of fungicides on crop microbiomes in different cropping systems is vital to minimizing unintended consequences while maintaining their use for plant protection. • We used amplicon sequencing of fungi and prokaryotes in maize and soybean microbiomes before and after foliar fungicide application in leaves and roots from plots under long-term no-till and conventional tillage managements. We examine fungicide disturbance and microbiome resilience across these treatments. • Foliar fungicides directly affected phyllosphere fungal communities, but not root fungal communities or prokaryote communities. Impacts on fungal phyllosphere composition and resiliency were management-dependent and lasted more than thirty days. Fungicides lowered pathogen abundance in maize and soybean and decreased the abundance of Tremellomycetes yeasts, especially the Bulleribacidiaceae, including core microbiome members. • Fungicide application reduced network complexity in the soybean phyllosphere. Bulleribacidiaceae often co-occurred with Sphingomonas and Hymenobacter in control plots, but co-occurrences were altered in fungicide plots. Results indicate that foliar fungicides lower pathogen and non-target fungal abundance and may impact prokaryotes indirectly. Notill management was more resilient following fungicide disturbance and recovery.
Plant Disease, Dec 1, 2020
Fusarium root rot (FRR) is a global limiter of dry bean (Phaseolus vulgaris L.) production. In co... more Fusarium root rot (FRR) is a global limiter of dry bean (Phaseolus vulgaris L.) production. In common bean and other legumes, resistance to FRR is related to both root development and root architecture, providing a breeding strategy for FRR resistance. Here, we describe the relationships between root traits and FRR disease symptoms. Using "shovelomics" techniques, a subset of recombinant inbred lines was phenotyped for root architecture traits and disease symptoms across three Michigan fields, including one field with artificially increased Fusarium brasiliense disease pressure. At the early growth stages, stem diameter, basal root number, and distribution of hypocotyl-borne adventitious roots were all significantly related to FRR disease scores. These results demonstrate that root architecture is a component of resistance to FRR in the field at early growth stages (first expanded trifoliate) complementing previous studies that evaluated root traits at later developmental stages (flowering, pod fill, etc.). Correlation matrices of root traits indicate that resistant and susceptible lines have statistically different root systems and show that basal root number is a key feature in resistant root systems while adventitious root distribution is an important feature in susceptible root systems. Based on the results of this study, selection for increased basal root number, increased adventitious root number, and even distribution of adventitious roots in early growth stages (first expanded trifoliate) would positively impact resistance to FRR.
PART III: Fungicide Stewardship
The American Phytopathological Society eBooks, Aug 2, 2017