Thomas E. Cleveland

United States Department of Agriculture, Washington, Washington, D.C., United States

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Publications (249)527.1 Total impact

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    ABSTRACT: Aflatoxin contamination of food and livestock feed results in significant annual crop losses internationally. Aspergillus flavus is the major fungus responsible for this loss. Additionally, A. flavus is the second leading cause of aspergillosis in immunocompromised human patients. Here, we report the genome sequence of strain NRRL 3357. FOOTNOTES Address correspondence to William C. Nierman, wnierman{at}jcvi.org. ↵* Present address: Jiujiang Yu, USDA/ARS, Beltsville Agricultural Research Center, Beltsville, Maryland, USA; Natalie D. Fedorova-Abrams, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA. Citation Nierman WC, Yu J, Fedorova-Abrams ND, Losada L, Cleveland TE, Bhatnagar D, Bennett JW, Dean R, Payne GA. 2015. Genome sequence of Aspergillus flavus NRRL 3357, a strain that causes aflatoxin contamination of food and feed. Genome Announc 3(2):e00168-15. doi:10.1128/genomeA.00168-15. Received 8 February 2015. Accepted 4 March 2015. Published 16 April 2015. Copyright © 2015 Nierman et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 3.0 Unported license.
    Full-text · Article · Apr 2015 · Genome Announcements
  • Haibo Yao · Zuzana Hruska · Robert L. Brown · Deepak Bhatnagar · Thomas E. Cleveland
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    ABSTRACT: The focus of this chapter is to ascertain the safety of plants and plant products intended for human and animal consumption by examining them for potential contaminants with the aid of hyperspectral imaging technology. Globally, the demand for fresh plant products is growing due to improved living standards and increased health awareness. This demand also increases the primary concerns of most food producers, food safety and the prevention of food-borne illness. Three major contaminants related to food safety are discussed, including food pathogens, chemical contaminants, and physical contaminants. Generally, the established techniques for food safety inspection are time-consuming and labor intensive. In the new millennium, advances in hyperspectral imaging technology have presented the opportunity for developing rapid and non-invasive methods for novel food safety inspection approaches. Many aspects of using this technology for plant product safety inspection are discussed. Hyperspectral images were acquired in reflectance, transmittance, and/or fluorescence mode. The application of the technology for safety inspection of major commodities such as grains (corn, wheat, barley, soybean), produce (fruits and vegetables), and tree nuts is also discussed in the present chapter. It seems evident that hyperspectral technology could offer a viable detection method to address the contamination issues related to plant products.
    No preview · Chapter · Jan 2015
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    ABSTRACT: Plant β-1,3-glucanases are members of the pathogenesis-related protein 2 (PR-2) family, which is one of the 17 PR protein families and plays important roles in biotic and abiotic stress responses. One of the differentially expressed proteins (spot 842) identified in a recent proteomic comparison between five pairs of closely-related maize (Zea mays L.) lines differing in aflatoxin resistance was further investigated in the present study. Here, the corresponding cDNA was cloned from maize and designated as ZmGns. ZmGns encodes a protein of 338 amino acids containing a potential signal peptide. The expression of ZmGns was detectible in all tissues studied with the highest level in silks. ZmGns was significantly induced by biotic stresses including three bacteria and the fungus Aspergillus flavus. ZmGns was also induced by most abiotic stresses tested and growth hormones including salicylic acid. In vivo, ZmGns showed a significant inhibitory activity against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 and fungal pathogen Botrytis cinerea when it overexpressed in Arabidopsis. Its high level expression in the silk tissue and its induced expression by phytohormone treatment, as well as by bacterial and fungal infections suggest it plays a complex role in maize growth, development and defense.
    No preview · Article · Sep 2014 · Journal of Integrative Plant Biology
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    ABSTRACT: The persistent occurrence of aflatoxins in food and feed remains a problem for producers of commodities subject to colonization with toxigenic molds. Aflatoxins are secondary metabolites of fungi of the Aspergillus spp. associated with deleterious health effects. Because current screening methods for these toxins are lengthy, destructive, and costly, there is a continuous search for a more rapid, noninvasive, and cost-effective technology. The present study utilized a fluorescence excitation–emission matrix (EEM) of aflatoxin as well as two additional secondary metabolites (kojic acid and the bright greenish-yellow fluorescence (BGYF) compound) of Aspergillus flavus measured with a fluorescence spectrophotometer. The results were compared to image data acquired with a fluorescence hyperspectral sensor in order to evaluate the potential of image-based technology for detecting aflatoxin in grain. The excitation–emission matrix of aflatoxin B1 standard produced overlapping peaks in 340–400 nm of excitation range emitting in the blue range at around 450 nm. The spectral signature extracted from the hyperspectral image was also in the blue range, emitting blue fluorescence. Because the results from both systems were comparable, where all fluorescence peaks were in the blue range, the present study validates the feasibility of image-based technology for nondestructive detection of aflatoxin in corn. Additional peaks were revealed in the aflatoxin EEM in the 260-nm excitation range that were not present in the kojic acid and BGYF compound mixture. This new information allows for the separation of the aflatoxin signature from the potentially confounding overlap of other secondary metabolites occurring in the blue and blue-green spectral ranges.
    No preview · Article · Apr 2014 · Food and Bioprocess Technology
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    ABSTRACT: A currently utilized pre-harvest biocontrol method involves field inoculations with non-aflatoxigenic Aspergillus flavus strains, a tactic shown to strategically suppress native aflatoxin-producing strains and effectively decrease aflatoxin contamination in corn. The present in situ study focuses on tracking the invasion and colonization of an aflatoxigenic A. flavus strain (AF70), labeled with green fluorescent protein (GFP), in the presence of a non-aflatoxigenic A. flavus biocontrol strain (AF36), to better understand the competitive interaction between these two strains in seed tissue of corn (Zea mays). Corn kernels that had been co-inoculated with GFP-labeled AF70 and wild-type AF36 were cross-sectioned and observed under UV and blue light to determine the outcome of competition between these strains. After imaging, all kernels were analyzed for aflatoxin levels. There appeared to be a population difference between the co-inoculated AF70-GFP+AF36 and the individual AF70-GFP tests, both visually and with pixel count analysis. The GFP allowed us to observe that AF70-GFP inside the kernels was suppressed up to 82% when co-inoculated with AF36 indicating that AF36 inhibited progression of AF70-GFP. This was in agreement with images taken of whole kernels where AF36 exhibited a more robust external growth compared to AF70-GFP. The suppressed growth of AF70-GFP was reflected in a corresponding (upto 73%) suppression in aflatoxin levels. Our results indicate that the decrease in aflatoxin production correlated with population depression of the aflatoxigenic fungus by the biocontrol strain supporting the theory of competitive exclusion through robust propagation and fast colonization by the non-aflatoxigenic fungus.
    Full-text · Article · Mar 2014 · Frontiers in Microbiology
  • H. Yao · Z. Hruska · R. Kincaid · R.L. Brown · D. Bhatnagar · T.E. Cleveland
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    ABSTRACT: Aflatoxins are toxic secondary metabolites predominantly produced by the fungi Aspergillus flavus and Aspergillus parasiticus. Aflatoxin-contaminated corn is toxic to domestic animals when ingested in feed and is a known carcinogen associated with liver and lung cancer in humans. Consequently, aflatoxin levels in food and feed are regulated by the U.S. Food and Drug Administration (FDA), which allows 20 ppb (parts per billion) limits in food and 100 ppb in feed for interstate commerce. Currently, aflatoxin detection and quantification methods are based on analytical tests, including thin-layer chromatography (TCL) and high-performance liquid chromatography (HPLC). These analytical tests require the destruction of samples and are costly and time consuming. Thus, the ability to detect aflatoxin in a rapid, nondestructive way is crucial to the grain industry, particularly the corn industry. Hyperspectral imaging technology offers a non-invasive approach to screening for food safety inspection and quality control based on spectral signatures. The focus of this study was to classify aflatoxin-contaminated single corn kernels using fluorescence hyperspectral imagery. Field-inoculated corn kernels were used in the study. Contaminated and control kernels under long-wavelength ultraviolet excitation were imaged using a visible near-infrared (VNIR) hyperspectral camera. The imaged kernels were chemically analyzed to provide reference information for image analysis. This article describes a procedure for processing corn kernels located in different images for statistical training and classification. Two classification algorithms (maximum likelihood and binary encoding) were used to classify each corn kernel as "control" or "contaminated" through pixel classification. The binary encoding approach had a slightly better performance, with accuracy equal to 87% or 88% when 20 ppb or 100 ppb, respectively, was used as the classification threshold. In addition, three narrow-band fluorescence indices were developed and tested in this study. It was found that the highest correlation was -0.81 with the normalized difference fluorescence index (NDFI). The two bands used for the NDFI were 437 and 537 nm. The use of key wavelengths for contamination detection would be helpful for developing rapid and non-invasive inspection systems. This study demonstrated the potential of using fluorescence hyperspectral imagery for aflatoxin contamination detection in corn kernels infected with A. flavus.
    No preview · Article · Sep 2013 · Transactions of the ASABE (American Society of Agricultural and Biological Engineers)
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    ABSTRACT: The food industry is always on the lookout for sensing technologies for rapid and nondestructive inspection of food products. Hyperspectral imaging technology integrates both imaging and spectroscopy into unique imaging sensors. Its application for food safety and quality inspection has made significant progress in recent years. Specifically, hyperspectral imaging has shown its potential for surface contamination detection in many food related applications. Most existing hyperspectral imaging systems use pushbroom scanning which is generally used for flat surface inspection. In some applications it is desirable to be able to acquire hyperspectral images on circular objects such as corn ears, apples, and cucumbers. Past research describes inspection systems that examine all surfaces of individual objects. Most of these systems did not employ hyperspectral imaging. These systems typically utilized a roller to rotate an object, such as an apple. During apple rotation, the camera took multiple images in order to cover the complete surface of the apple. The acquired image data lacked the spectral component present in a hyperspectral image. This paper discusses the development of a hyperspectral imaging system for a 3-D surface scan of biological samples. The new instrument is based on a pushbroom hyperspectral line scanner using a rotational stage to turn the sample. The system is suitable for whole surface hyperspectral imaging of circular objects. In addition to its value to the food industry, the system could be useful for other applications involving 3-D surface inspection.
    No preview · Conference Paper · Aug 2013
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    ABSTRACT: In an effort to address the problem of rapid detection of aflatoxin in grain, particularly oilseeds, the current study assessed the spectral differences of aflatoxin production in kernels from a cornfield inoculated with spores from 2 different strains of toxigenic Aspergillus flavus. Aflatoxin production in corn from the same field due to natural infestation was also assessed. A small corn plot in Baton Rouge, La., U.S.A., was used during the 2008-growing season. Two groups of 400 plants were inoculated with 2 different inocula and 1 group of 400 plants was designated as controls. Any contamination detected in the controls was attributed to natural infestation. A subset of each group was imaged with a visible near infra red (VNIR) hyperspectral system under ultra violet (UV) excitation and subsequently analyzed for aflatoxin using affinity column fluorometry. Group differences were statistically analyzed. Results indicate that when all the spectral data across all groups were averaged, any potential differences between groups (treated and untreated) were obscured. However, spectral analysis based on contaminated “hot” pixel classification showed a distinct spectral shift/separation between contaminated and clean ears with fluorescence peaks at 501 and 478 nm, respectively. All inoculated and naturally infected control ears had fluorescence peaks at 501 nm that differed from uninfected corn ears. Results from this study may be useful in evaluating rapid, noninvasive instrumentation and/or methodology for aflatoxin detection in grain. The present study evaluated the possible application of fluorescence hyperspectral imaging methodology for the rapid and noninvasive detection of aflatoxin in postharvest corn during various stages of processing. Specific information from this study may be applicable when developing rapid, noninvasive instrumentation and/or methodology for whole ear inspection as well as shucked kernels.
    No preview · Article · Aug 2013 · Journal of Food Science
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    ABSTRACT: Aflatoxin contamination caused by Aspergillus flavus infection of corn is a significant and chronic threat to corn being used as food or feed. Contamination of crops at levels of 20 ng g(-1) or higher (as regulated by the USFDA) by this toxin and potent carcinogen makes the crop unsalable, resulting in a significant economic burden on the producer. This review focuses on elimination of this contamination in corn which is a major US crop and the basis of many products. Corn is also "nature's example" of a crop containing heritable resistance to aflatoxin contamination, thereby serving as a model for achieving resistance to aflatoxin contamination in other crops as well. This crop is the largest production grain crop worldwide, providing food for billions of people and livestock and critical feedstock for production of biofuels. In 2011, the economic value of the US corn crop was US$76 billion, with US growers producing an estimated 12 billion bushels, more than one-third of the world's supply. Thus, the economics and significance of corn as a food crop and the threat to food safety due to aflatoxin contamination of this major food crop have prompted the many research efforts in many parts of the world to identify resistance in corn to aflatoxin contamination. Plant breeding and varietal selection has been used as a tool to develop varieties resistance to disease. This methodology has been employed in defining a few corn lines that show resistance to A. flavus invasion; however, no commercial lines have been marketed. With the new tools of proteomics and genomics, identification of resistance mechanisms, and rapid resistance marker selection methodologies, there is an increasing possibility of finding significant resistance in corn, and in understanding the mechanism of this resistance.
    No preview · Article · Jul 2013 · Food Additives and Contaminants - Part A Chemistry, Analysis, Control, Exposure and Risk Assessment
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    ABSTRACT: Naturally occurring Aspergillus flavus strains can be either toxigenic or atoxigenic, indicating their ability to produce aflatoxin or not. The objective was to assess, with the use of a hyperspectral sensor, the difference in fluorescence emission between maize kernels inoculated with toxigenic and atoxigenic inoculums of A. flavus. Maize ears were inoculated with AF13, a toxigenic strain of A. flavus, and AF38, an atoxigenic strain of A. flavus, at dough stage of development and harvested 8 weeks after inoculation. After harvest, single kernels were divided into three groups prior to imaging: control, adjacent, and glowing. Both sides of the kernel, germ and endosperm, were imaged separately using a fluorescence hyperspectral imaging system. After imaging each single kernel was processed with affinity column fluorimetry to determine aflatoxin level. Results from discriminant analysis of the imaging data found that the classification accuracies of the three visually designated groups were not promising. The separation of maize kernels based on different fungal inoculums yielded better results. The best results were achieved with the germ side of the maize kernels. The kernels were later grouped into 'contaminated' and 'healthy' with 20 ppb and 100 ppb thresholds. The contaminated kernels all had longer peak wavelength than did the healthy ones. Results from the discriminant analysis classification indicated overall higher classification accuracy for the 100 ppb threshold on the germ side (94.4%). The germ side was also more useful at discriminating healthy from contaminated kernels for the 20 ppb threshold.
    No preview · Article · Jun 2013 · Biosystems Engineering
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    ABSTRACT: Aflatoxin is a mycotoxin produced mainly by Aspergillus flavus (A.flavus) and Aspergillus parasitiucus fungi that grow naturally in corn. Very serious health problems such as liver damage and lung cancer can result from exposure to high toxin levels in grain. Consequently, many countries have established strict guidelines for permissible levels in consumables. Conventional chemical-based analytical methods used to screen for aflatoxin such as thin-layer chromatography (TLC) and high performance liquid chromatography (HPLC) are time consuming, expensive, and require the destruction of samples as well as proper training for data interpretation. Thus, it has been a continuing effort within the research community to find a way to rapidly and non-destructively detect and possibly quantify aflatoxin contamination in corn. One of the more recent developments in this area is the use of spectral technology. Specifically, fluorescence hyperspectral imaging offers a potential rapid, and non-invasive method for contamination detection in corn infected with toxigenic A.flavus spores. The current hyperspectral image system is designed for scanning flat surfaces, which is suitable for imaging single or a group of corn kernels. In the case of a whole corn cob, it is preferred to be able to scan the circumference of the corn ear, appropriate for whole ear inspection. This paper discusses the development of a hyperspectral imaging system for whole corn ear imaging. The new instrument is based on a hyperspectral line scanner using a rotational stage to turn the corn ear.
    No preview · Conference Paper · May 2013
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    Full-text · Dataset · Feb 2013
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    ABSTRACT: Support Vector Machine (SVM) was used in the Genetic Algorithms (GA) process to select and classify a subset of hyperspectral image bands. The method was applied to fluorescence hyperspectral data for the detection of aflatoxin contamination in Aspergillus flavus infected single corn kernels. In the band selection process, the training sample classification accuracy was used as fitness function. Two aflatoxin thresholds, 20 ppb and 100 ppb, were used to divide the single corn kernels into clean and contaminated samples. The validation accuracy was 87.7% for the 20 ppb threshold and 90.5% for the 100 ppb threshold. The results were generated from the GA selected 36 bands and 11 bands, respectively. Compared to the full wavelength classification, the subset of image bands had slightly better or similar performance. A reduced image space could save time both in spectral data acquisition and analysis, which is crucial in the development of rapid and none invasive methods for contamination detection.
    No preview · Conference Paper · Jun 2012
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    ABSTRACT: Naturally occurring Aspergillus flavus strains can be either toxigenic or atoxigenic, indicating their ability to produce aflatoxin or not, under specific conditions. Corn contaminated with toxigenic strains of A. flavus can result in great losses to the agricultural industry and pose threats to public health. Past research showed that fluorescence hyperspectral imaging could be a potential tool for rapid and non-invasive detection of aflatoxin contaminated corn. The objective of the current study was to assess, with the use of a hyperspectral sensor, the difference in fluorescence emission between corn kernels inoculated with toxigenic and atoxigenic inoculums of A. flavus. Corn ears were inoculated with AF13, a toxigenic strain of A. flavus, and AF38, an atoxigenic strain of A. flavus, at dough stage of development and harvested 8 weeks after inoculation. After harvest, single corn kernels were divided into three groups prior to imaging: control, adjacent, and glowing. Both sides of the kernel, germplasm and endosperm, were imaged separately using a fluorescence hyperspectral imaging system. It was found that the classification accuracies of the three manually designated groups were not promising. However, the separation of corn kernels based on different fungal inoculums yielded better results. The best result was achieved with the germplasm side of the corn kernels. Results are expected to enhance the potential of fluorescence hyperspectral imaging for the detection of aflatoxin contaminated corn.
    No preview · Article · May 2012 · Proceedings of SPIE - The International Society for Optical Engineering
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    C. A. Chlan · K. Rajasekaran · J. W. Cary · T. E. Cleveland
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    ABSTRACT: Although most plastid transformation studies have focused on chloroplast expression, plastid transformation can also be used to express genes in plastids of a wide variety of plant tissues by using appropriate plastid promoters. Based on the sequence of the Gossypium hirsutum chloroplast genome, we developed primers and amplified segments of 20 different plastid genes. The PCR products were labeled and used in filter dot blot hybridization studies to characterize their expression levels and patterns in total RNA isolated from light- and dark-grown cotton tissues at different developmental stages. A subset of 6 genes among these was further characterized by real time PCR. Highest expression levels were observed for rrn16 and psbA. Four genes were expressed in all samples at relatively constant levels: accD, atpA, matK and rrn16. Expression in root tissue was generally low. The results of our study can be used to predict which operons and promoters are most likely to be preferentially expressed in the plastids of tissues of interest at levels that would result in the desired phenotype, facilitating the development of plastid transformation vectors.
    Full-text · Article · Mar 2012 · Biologia Plantarum

  • No preview · Chapter · Jan 2012
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    C.A. Chlan · K. Rajasekaran · J. W. Cary · T. E. Cleveland
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    ABSTRACT: Although most plastid transformation studies have focused on chloroplast expression, plastid transformation can also be used to express genes in plastids of a wide variety of plant tissues by using appropriate plastid promoters. Based on the sequence of the Gossypium hirsutum chloroplast genome, we developed primers and amplified segments of 20 different plastid genes. The PCR products were labeled and used in filter dot blot hybridization studies to characterize their expression levels and patterns in total RNA isolated from light- and dark-grown cotton tissues at different developmental stages. A subset of 6 genes among these was further characterized by real time PCR. Highest expression levels were observed for rrn16 and psbA. Four genes were expressed in all samples at relatively constant levels: accD, atpA, matK and rrn16. Expression in root tissue was generally low. The results of our study can be used to predict which operons and promoters are most likely to be preferentially expressed in the plastids of tissues of interest at levels that would result in the desired phenotype, facilitating the development of plastid transformation vectors.
    Full-text · Article · Nov 2011 · Biologia Plantarum
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    ABSTRACT: The genomic study of filamentous fungi has made significant advances in recent years, and the genomes of several species in the genus Aspergillus have been sequenced, including Aspergillus flavus. This ubiquitous mold is present as a saprobe in a wide range of agricultural and natural habits, and can function as an opportunistic animal and plant pathogen. A. flavus produces many secondary metabolites including aflatoxins, aflatrem and cyclopiazonic acid. In this chapter, our main focus is on the current status of the genomics of A. flavus as well as on the potential applications of genomics-based approaches to understanding mycotoxin production and fungal pathogenicity. It is hoped that the results of A. flavus genomics and functional genomics studies will empower researchers to find effective controlling strategies to eliminate mycotoxin contamination and to yield a safer and more abundant food and feed supply.
    No preview · Article · Sep 2011 · Mycology
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    ABSTRACT: To better understand the effect of temperature on mycotoxin biosynthesis, RNA-Seq technology was used to profile the Aspergillus flavus transcriptome under different temperature conditions. This approach allowed us to quantify transcript abundance for over 80% of fungal genes including 1153 genes that were differentially expressed at 30 and 37 °C. Eleven of the 55 secondary metabolite clusters were upregulated at the lower temperature, including aflatoxin biosynthesis genes, which were among the most highly upexpressed genes. On average, transcript abundance for the 30 aflatoxin biosynthesis genes was 3300 times greater at 30 °C as compared with 37 °C. The results are consistent with the view that high temperature negatively affects aflatoxin production by turning down transcription of the two key transcriptional regulators, aflR and aflS. Subtle changes in the expression levels of aflS to aflR appear to control transcription activation of the aflatoxin cluster.
    Full-text · Article · Jun 2011 · FEMS Microbiology Letters
  • Zhi-Yuan Chen · Robert L. Brown · Abebe Menkir · Thomas E. Cleveland
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    ABSTRACT: Aspergillus flavus infection of maize and subsequent contamination with carcinogenic aflatoxins poses serious health concerns, especially in developing countries. Maize lines resistant to A. flavus infection have been identified; however, the development of commercially-useful aflatoxin-resistant maize lines has been hindered due to a lack of breeding markers. To identify maize resistance-associated proteins (RAPs) as potential markers for breeding, 52 BC1S4 lines developed from crosses between five African maize inbreds and five temperate aflatoxin-resistant lines were screened using the kernel screening assay. Five pairs of closely-related lines that had 75–94% genetic similarity within each pair and which varied within each pair in aflatoxin accumulation were selected for proteomic investigation. Kernel embryo and endosperm protein profile differences within the pair and across pairs were compared using two-dimensional polyacrylamide gel electrophoresis. Differentially expressed (≥1.5-fold) RAPs were sequenced through tandem mass spectrometry and were identified as antifungal, stress-related, storage or regulatory proteins. Sequence homology analysis highlighted several proteins in maize that confer resistance to A. flavus infection and/or aflatoxin production. KeywordsTwo-dimensional gel electrophoresis–Corn–Protein profile comparison–Aflatoxin resistance–Antifungal protein–Stress-related protein
    No preview · Article · Jun 2011 · Molecular Breeding

Publication Stats

9k Citations
527.10 Total Impact Points

Institutions

  • 2000-2014
    • United States Department of Agriculture
      • Agricultural Research Service (ARS)
      Washington, Washington, D.C., United States
    • Humboldt-Universität zu Berlin
      Berlín, Berlin, Germany
  • 2000-2013
    • Agricultural Research Service
      ERV, Texas, United States
  • 1989-2013
    • Southern Regional Medical Center
      Georgia, United States
  • 2009
    • Rutgers, The State University of New Jersey
      • School of Environmental and Biological Sciences
      New Brunswick, New Jersey, United States
  • 2007
    • University of Louisville
      • Department of Biology
      Louisville, Kentucky, United States
  • 2006
    • Houston Zoo
      Houston, Texas, United States
  • 1998-2006
    • Louisiana State University Agricultural Center
      Baton Rouge, Louisiana, United States
  • 1995-2006
    • Tulane University
      • • Department of Chemistry
      • • Department of Cell and Molecular Biology
      New Orleans, Louisiana, United States
    • Clemson University
      CEU, South Carolina, United States
  • 2005
    • Government Arts College, Coimbatore
      Koyambattūr, Tamil Nādu, India
  • 2004
    • Kennedy Space Center
      Worcester, Massachusetts, United States
  • 1993-2004
    • North Carolina State University
      • Department of Plant Pathology
      Raleigh, North Carolina, United States
  • 2003
    • Xavier University
      Cincinnati, Ohio, United States
  • 2002
    • Saint Louis University
      • Geriatric Research, Education and Clinical Center
      Saint Louis, MI, United States
  • 1997
    • National Institutes of Health
      Maryland, United States
  • 1987
    • Washington State University
      • Institute of Biological Chemistry
      پولمن، واشینگتن, Washington, United States