Accumulation of storage proteins in plant seeds is mediated by amyloid formation

by Kirill S. Antonets, Mikhail V. Belousov, Anna I. Sulatskaya, Maria E. Belousova, Anastasiia O. Kosolapova, Maksim I. Sulatsky, Elena A. Andreeva, Pavel A. Zykin, Yury V. Malovichko, Oksana Y. Shtark, Anna N. Lykholay, Kirill V. Volkov, Irina M. Kuznetsova, Konstantin K. Turoverov, Elena Y. Kochetkova, Alexander G. Bobylev, Konstantin S. Usachev, Oleg. N. Demidov, Igor A. Tikhonovich, Anton A. Nizhnikov

Amyloids are protein aggregates with a highly ordered spatial structure giving them unique physicochemical properties. Different amyloids not only participate in the development of numerous incurable diseases but control vital functions in archaea, bacteria and eukarya. Plants are a poorly studied systematic group in the field of amyloid biology. Amyloid properties have not yet been demonstrated for plant proteins under native conditions in vivo. Here we show that seeds of garden pea Pisum sativum L. contain amyloid-like aggregates of storage proteins, the most abundant one, 7S globulin Vicilin, forms bona fide amyloids in vivo and in vitro. Full-length Vicilin contains 2 evolutionary conserved β-barrel domains, Cupin-1.1 and Cupin-1.2, that self-assemble in vitro into amyloid fibrils with similar physicochemical properties. However, Cupin-1.2 fibrils unlike Cupin-1.1 can seed Vicilin fibrillation. In vivo, Vicilin forms amyloids in the cotyledon cells that bind amyloid-specific dyes and possess resistance to detergents and proteases. The Vicilin amyloid accumulation increases during seed maturation and wanes at germination. Amyloids of Vicilin resist digestion by gastrointestinal enzymes, persist in canned peas, and exhibit toxicity for yeast and mammalian cells. Our finding for the first time reveals involvement of amyloid formation in the accumulation of storage proteins in plant seeds.

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