Characterization of Celiac Disease-Related Epitopes and Gluten Fractions, and Identification of Associated Loci in Durum Wheat

Francesca Taranto,Fatma Boukid,Justyna Milc,Stefano Sforza,Enrico Francia,Giovanna Visioli,Luca Laviano,Mariolina Gullì,Pasquale De Vita,Franz-W Badeck,Marcello Catellani,Nelson Marmiroli,Sara Graziano,Nicola Pecchioni,Ivano Pecorella,Nunzio D’Agostino,Barbara Prandi,Anna Paola Minervini,Domenico Ronga

doi:10.3390/agronomy10091231

Abstract

While durum wheat is a major food source in Mediterranean countries, storage (i.e., gluten) proteins are however responsible for celiac disease (CD), a serious autoimmune disease that occurs in genetically predisposed subjects. Different gluten epitopes—defined as “immunogenic” (IP) and “toxic” (TP) peptides—are involved in the pathology and their content in wheat grain depends on environmental and genetic factors. Detection of IP and TP is not trivial, and no work has been conducted so far to identify the genomic regions associated with their accumulation in wheat. In the present study, a genome-wide association study was performed on a durum wheat collection to identify marker–trait associations (MTAs) between 5730 high quality SNPs and the accumulation of CD-related peptides and gluten protein composition measured in two consecutive cropping seasons (2015/2016 and 2016/2017). High-molecular-weight glutenin subunits (HMW-GS) were more stable between the two years, and differences in total gluten proteins were mainly due to low-molecular-weight glutenin subunits (LMW-GS) and accumulation of gliadins. In the first instance, association tests were conducted on yellow pigment content (YP), a highly inheritable trait with a well-known genetic basis, and several significant MTAs were found corresponding to loci already known for being related to YP. These findings showed that MTAs found for the rest of the measured traits were reliable. In total, 28 significant MTAs were found for gluten composition, while 14 were found to be associated with IP and TP. Noteworthy, neither significant (−log10p > 4.7) nor suggestive (−log10p > 3.3) MTAs for the accumulation of CD-triggering epitopes were found on Gli-A1/Glu-A3 and Gli-B1/Glu-B3 loci, thus suggesting regulatory rather than structural gene effect. A PBF transcription factor on chromosome 5B, known to be involved in the regulation of the expression of CD-related peptides, was identified among the positional candidate genes in the LD-decay range around significant SNPs. Results obtained in the present study provide useful insights and resources for the long-term objective of selecting low-toxic durum wheat varieties while maintaining satisfactory gluten quality.

Highlights

Durum wheat (Triticum turgidum subsp. durum Desf.) world production is only 5–8% of the total wheat production, it is an economically important crop and the species is primarily associated with pasta and semolina production
A Water Stress Index (WSI) per day value equal to 0.31 was estimated for the 35 days following sowing with an accumulated WSI = 10.89 in coincidence with the early plant development phases, that is crucial for crop establishment in Mediterranean environments
The insights and resources generated here provide useful information to (i) assess the relationship between grain protein content, gluten composition, and celiac disease (CD)-related peptides; (ii) identify candidate genes related to the accumulation of toxic and immunogenic CD-related epitopes, and (iii) develop useful molecular markers to select durum wheat varieties with reduced influence on the immunologic mechanisms of digestive disorders

Summary

Introduction

Durum wheat (Triticum turgidum subsp. durum Desf.) world production is only 5–8% of the total wheat production, it is an economically important crop and the species is primarily associated with pasta and semolina production. Durum Desf.) world production is only 5–8% of the total wheat production, it is an economically important crop and the species is primarily associated with pasta and semolina production. For this reason, durum wheat has been subjected to intense breeding activities. Pasta quality is estimated from its color, cooking attributes, and sensory properties [2,3]. The cooking quality of pasta mostly depends on its protein content and on the quality of gluten proteins [4,5]. I.e., glutenins (Glu) and gliadins (Gli), encoded by multiple genes at complex loci on durum wheat chromosomes 1 and 6, are responsible for the strength and extensibility of the dough, respectively [6]

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Discussion

Conclusion