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Molecular evolution of genes encoding allergen proteins in the peanuts genus Arachis: Structural and functional implications.

ABSTRACT: Food allergies are severe immune responses to plant and animal products mediated by immunoglobulin E (IgE). Peanuts (Arachis hypogaea L.) are among the top 15 crops that feed the world. However, peanuts is among the "big eight food allergens", and allergies induced by peanuts are a significant public health problem and a life-threatening concern. Targeted mutation studies in peanuts demonstrate that single residue alterations in these allergen proteins could result in substantial reduction in allergenicity. Knowledge of peanut allergen proteins is confined to the allotetraploid crop and its two progenitors. We explored frequencies and positions of natural mutations in the hyperallergenic homologues Ara h 2 and Ara h 6 in newly generated sequences for 24 Arachis wild species and the crop species, assessed potential mutational impact on allergenicity using immunoblots and structural modeling, and evaluated whether these mutations follow evolutionary trends. We uncovered a wealth of natural mutations, both substitutions and gaps, including the elimination of immunodominant epitopes in some species. These molecular alterations appear to be associated with substantial reductions in allergenicity. The study demonstrated that Ara h 2 and Ara h 6 follow contrasting modes of natural selection and opposing mutational patterns, particularly in epitope regions. Phylogenetic analysis revealed a progressive trend towards immunodominant epitope evolution in Ara h 2. The findings provide valuable insight into the interactions among mutations, protein structure and immune system response, thus presenting a valuable platform for future manipulation of allergens to minimize, treat or eliminate allergenicity. The study strongly encourages exploration of genepools of economically important plants in allergenicity research.

SUBMITTER: Hilu KW

PROVIDER: S-EPMC6824556 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Molecular evolution of genes encoding allergen proteins in the peanuts genus Arachis: Structural and functional implications.

Hilu Khidir W KW Friend Sheena A SA Vallanadu Viruthika V Brown Anne M AM Hollingsworth Louis R LR Bevan David R DR

PloS one 20191101 11

Food allergies are severe immune responses to plant and animal products mediated by immunoglobulin E (IgE). Peanuts (Arachis hypogaea L.) are among the top 15 crops that feed the world. However, peanuts is among the "big eight food allergens", and allergies induced by peanuts are a significant public health problem and a life-threatening concern. Targeted mutation studies in peanuts demonstrate that single residue alterations in these allergen proteins could result in substantial reduction in al ...[more]

PMID: 31675366

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Project description:BACKGROUND:Phosphatidyl ethanolamine-binding proteins (PEBPs) are involved in the regulation of plant architecture and flowering time. The functions of PEBP genes have been studied in many plant species. However, little is known about the characteristics and expression profiles of PEBP genes in wild peanut species, Arachis duranensis and Arachis ipaensis, the diploid ancestors of cultivated peanuts. RESULTS:In this study, genome-wide identification methods were used to identify and characterize a total of 32 peanut PEBP genes, 16 from each of the two wild peanut species, A. duranensis and A. ipaensis. These PEBP genes were classified into 3 groups (TERMINAL FLOWER1-like, FLOWERING LOCUS T-like, and MOTHER OF FT AND TFL1-like) based on their phylogenetic relationships. The gene structures, motifs, and chromosomal locations for each of these PEBPs were analyzed. In addition, 4 interchromosomal duplications and 1 tandem duplication were identified in A. duranensis, and 2 interchromosomal paralogs and 1 tandem paralog were identified in A. ipaensis. Ninety-five different cis-acting elements were identified in the PEBP gene promoter regions and most genes had different numbers and types of cis-elements. As a result, the transcription patterns of these PEBP genes varied in different tissues and under long day and short day conditions during different growth phases, indicating the functional diversities of PEBPs in different tissues and their potential functions in plant photoperiod dependent developmental pathways. Moreover, our analysis revealed that AraduF950M/AraduWY2NX in A. duranensis, and Araip344D4/Araip4V81G in A. ipaensis are good candidates for regulating plant architecture, and that Aradu80YRY, AraduYY72S, and AraduEHZ9Y in A. duranensis and AraipVEP8T in A. ipaensis may be key factors regulating flowering time. CONCLUSION:Sixteen PEBP genes were identified and characterized from each of the two diploid wild peanut genomes, A. duranensis and A. ipaensis. Genetic characterization and spatio-temporal expression analysis support their importance in plant growth and development. These findings further our understanding of PEBP gene functions in plant species.

Project description:BACKGROUND:The cultivated peanut (Arachis hypogaea) is one of the most important oilseed crops worldwide, however, its improvement is restricted by its narrow genetic base. The highly variable wild peanut species, especially within Sect. Arachis, may serve as a rich genetic source of favorable alleles to peanut improvement; Sect. Arachis is the biggest taxonomic section within genus Arachis and its members also include the cultivated peanut. In order to make good use of these wild resources, the genetic bases and the relationships of the Arachis species need first to be better understood. RESULTS:Here, in this study, we have sequenced and/or assembled twelve Arachis complete chloroplast (cp) genomes (eleven from Sect. Arachis). These cp genome sequences enriched the published Arachis cp genome data. From the twelve acquired cp genomes, substantial genetic variation (1368 SNDs, 311 indels) has been identified, which, together with 69 SSR loci that have been identified from the same data set, will provide powerful tools for future explorations. Phylogenetic analyses in our study have grouped the Sect. Arachis species into two major lineages (I & II), this result together with reports from many earlier studies show that lineage II is dominated by AA genome species that are mostly perennial, while lineage I includes species that have more diverse genome types and are mostly annual/biennial. Moreover, the cultivated peanuts and A. monticola that are the only tetraploid (AABB) species within Arachis are nested within the AA genome species-dominated lineage, this result together with the maternal inheritance of chloroplast indicate a maternal origin of the two tetraploid species from an AA genome species. CONCLUSION:In summary, we have acquired sequences of twelve complete Arachis cp genomes, which have not only helped us better understand how the cultivated peanut and its close wild relatives are related, but also provided us with rich genetic resources that may hold great potentials for future peanut breeding.

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Molecular evolution of genes encoding allergen proteins in the peanuts genus Arachis: Structural and functional implications.

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Molecular evolution of genes encoding allergen proteins in the peanuts genus Arachis: Structural and functional implications.

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