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

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 s...

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Main Authors: 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
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-07-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3000564
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author 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
author_facet 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
author_sort Kirill S Antonets
collection DOAJ
description 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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spelling doaj.art-f8927a4807e746d39343a88533d84ce82022-12-21T21:24:29ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852020-07-01187e300056410.1371/journal.pbio.3000564Accumulation of storage proteins in plant seeds is mediated by amyloid formation.Kirill S AntonetsMikhail V BelousovAnna I SulatskayaMaria E BelousovaAnastasiia O KosolapovaMaksim I SulatskyElena A AndreevaPavel A ZykinYury V MalovichkoOksana Y ShtarkAnna N LykholayKirill V VolkovIrina M KuznetsovaKonstantin K TuroverovElena Y KochetkovaAlexander G BobylevKonstantin S UsachevOleg N DemidovIgor A TikhonovichAnton A NizhnikovAmyloids 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.https://doi.org/10.1371/journal.pbio.3000564
spellingShingle 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
Accumulation of storage proteins in plant seeds is mediated by amyloid formation.
PLoS Biology
title Accumulation of storage proteins in plant seeds is mediated by amyloid formation.
title_full Accumulation of storage proteins in plant seeds is mediated by amyloid formation.
title_fullStr Accumulation of storage proteins in plant seeds is mediated by amyloid formation.
title_full_unstemmed Accumulation of storage proteins in plant seeds is mediated by amyloid formation.
title_short Accumulation of storage proteins in plant seeds is mediated by amyloid formation.
title_sort accumulation of storage proteins in plant seeds is mediated by amyloid formation
url https://doi.org/10.1371/journal.pbio.3000564
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