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

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Accumulation of storage proteins in plant seeds is mediated by amyloid formation. / Антонец, Кирилл Сергеевич ; Белоусов, Михаил Владимирович; Сулацкая, Анна; Белоусова, Мария; Косолапова, Анастасия Олеговна; Сулацкий, Максим; Андреева, Елена Александровна ; Зыкин, Павел Александрович ; Маловичко, Юрий Викторович; Штарк, Оксана Юрьевна; Лыхолай, Анна Николаевна; Волков, Кирилл Владимирович; Кузнецова, Ирина; Туроверов, Константин; Кочеткова, Елена Юрьевна; Бобылёв, Александр; Усачёв, Константин; Демидов, Олег; Тихонович, Игорь Анатольевич ; Нижников, Антон Александрович.

In: PLoS Biology, Vol. 18, No. 7, e3000564, 23.07.2020.

Research output: Contribution to journal › Article › peer-review

Harvard

Антонец, КС , Белоусов, МВ, Сулацкая, А, Белоусова, М, Косолапова, АО, Сулацкий, М, Андреева, ЕА , Зыкин, ПА , Маловичко, ЮВ, Штарк, ОЮ, Лыхолай, АН, Волков, КВ, Кузнецова, И, Туроверов, К, Кочеткова, ЕЮ, Бобылёв, А, Усачёв, К, Демидов, О, Тихонович, ИА & Нижников, АА 2020, 'Accumulation of storage proteins in plant seeds is mediated by amyloid formation', PLoS Biology, vol. 18, no. 7, e3000564. https://doi.org/10.1371/journal.pbio.3000564

BibTeX

@article{4d64c0ea82e1472090de7562799a6c82,

title = "Accumulation of storage proteins in plant seeds is mediated by amyloid formation",

abstract = "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.",

keywords = "Amyloid/metabolism, Detergents/pharmacology, Escherichia coli/metabolism, Ions, Pancreatin/metabolism, Peas/drug effects, Pepsin A/metabolism, Protein Aggregates, Protein Domains, Recombinant Proteins/chemistry, Saccharomyces cerevisiae/metabolism, Seed Storage Proteins/chemistry, Seeds/metabolism, VICILIN, FUNCTIONAL AMYLOIDS, IDENTIFICATION, PEA, PEPTIDE, THIOFLAVIN T, CIRCULAR-DICHROISM SPECTRA, FIBRILS, BINDING, YEAST PRION",

author = "Антонец, {Кирилл Сергеевич} and Белоусов, {Михаил Владимирович} and Анна Сулацкая and Мария Белоусова and Косолапова, {Анастасия Олеговна} and Максим Сулацкий and Андреева, {Елена Александровна} and Зыкин, {Павел Александрович} and Маловичко, {Юрий Викторович} and Штарк, {Оксана Юрьевна} and Лыхолай, {Анна Николаевна} and Волков, {Кирилл Владимирович} and Ирина Кузнецова and Константин Туроверов and Кочеткова, {Елена Юрьевна} and Александр Бобылёв and Константин Усачёв and Олег Демидов and Тихонович, {Игорь Анатольевич} and Нижников, {Антон Александрович}",

note = "Publisher Copyright: Copyright: {\textcopyright} 2020 Antonets et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.",

year = "2020",

month = jul,

day = "23",

doi = "10.1371/journal.pbio.3000564",

language = "English",

volume = "18",

journal = "PLoS Biology",

issn = "1544-9173",

publisher = "Public Library of Science",

number = "7",

}

RIS

TY - JOUR

T1 - Accumulation of storage proteins in plant seeds is mediated by amyloid formation

AU - Антонец, Кирилл Сергеевич

AU - Белоусов, Михаил Владимирович

AU - Сулацкая, Анна

AU - Белоусова, Мария

AU - Косолапова, Анастасия Олеговна

AU - Сулацкий, Максим

AU - Андреева, Елена Александровна

AU - Зыкин, Павел Александрович

AU - Маловичко, Юрий Викторович

AU - Штарк, Оксана Юрьевна

AU - Лыхолай, Анна Николаевна

AU - Волков, Кирилл Владимирович

AU - Кузнецова, Ирина

AU - Туроверов, Константин

AU - Кочеткова, Елена Юрьевна

AU - Бобылёв, Александр

AU - Усачёв, Константин

AU - Демидов, Олег

AU - Тихонович, Игорь Анатольевич

AU - Нижников, Антон Александрович

N1 - Publisher Copyright: Copyright: © 2020 Antonets et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2020/7/23

Y1 - 2020/7/23

N2 - 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.

AB - 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.

KW - Amyloid/metabolism

KW - Detergents/pharmacology

KW - Escherichia coli/metabolism

KW - Ions

KW - Pancreatin/metabolism

KW - Peas/drug effects

KW - Pepsin A/metabolism

KW - Protein Aggregates

KW - Protein Domains

KW - Recombinant Proteins/chemistry

KW - Saccharomyces cerevisiae/metabolism

KW - Seed Storage Proteins/chemistry

KW - Seeds/metabolism

KW - VICILIN

KW - FUNCTIONAL AMYLOIDS

KW - IDENTIFICATION

KW - PEA

KW - PEPTIDE

KW - THIOFLAVIN T

KW - CIRCULAR-DICHROISM SPECTRA

KW - FIBRILS

KW - BINDING

KW - YEAST PRION

UR - http://www.scopus.com/inward/record.url?scp=85088510561&partnerID=8YFLogxK

UR - https://www.mendeley.com/catalogue/40795f6b-cff4-3837-9855-8958f6b45b5d/

U2 - 10.1371/journal.pbio.3000564

DO - 10.1371/journal.pbio.3000564

M3 - Article

C2 - 32701952

VL - 18

JO - PLoS Biology

JF - PLoS Biology

SN - 1544-9173

IS - 7

M1 - e3000564

ER -

ID: 60836091