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.
Highlights
Ara h 2 was amplified from 24 species and Ara h 6 from 23 species (Ara h 6 amplification failed in A. tubersosa) using the polymerase chain reaction (PCR) method with primers designed based on a sequence from A. hypogaea (GenBank accession AY007229)
Ara h 2 has undergone a higher proportion of amino acid substitutions compared with Ara h 6 and has accumulated by far a greater number of losses and gains of motifs ranging from 1–24 amino acids (S1 Fig)
The mutational events in Ara h 2 appear to follow phylogenetic trends from the base of the Arachis tree to the terminal branches. These findings raise the questions of the underlying factors that differently affected Ara h 2 and Ara h 6 modes of evolution and whether such molecular alterations are linked to potential accentuation of allergenicity
Summary
Peanuts (Arachis hypogaea L.) are an important global commodity, being among the top 15 crops that feed the world and second only to soybean in terms of legume crop global. Using newly generated nucleotide sequences of Ara h 2 and Ara h 6 from 24 of the approximately 80 Arachis wild species from clades spanning the entire tree, we determined naturally-occurring single nucleotide polymorphism (SNPs) and loss/gain of sequence motifs in the open reading frames (ORF) and their subsequent impact on amino acid composition. We placed these mutational events within a phylogenetic platform using the a phylogenetic tree of Friend et al (2010)[33] to evaluate their modes of evolution, and determined potential selection pressure operating on them. This work provides new allergen protein sequence data for Arachis species and begins to connect this sequence information to protein structure and subsequently to allergenicity within a predicted evolutionary framework
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