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.

Myosin Binding Protein-C Forms Amyloid-Like Aggregates In Vitro

“…Diffuse rings on the diffraction pattern have been explained and described [ 48 ] in studies of non-oriented and weakly oriented amyloid samples. Similar diffuse ring reflections have been shown for amyloid aggregates of many proteins [ 10 , 40 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 ].…”

Perspectives on the genetic improvement of health- and nutrition-related traits in pea

“…These amino acids have been identified as limiting in pea and increasing their concentrations has been identified as a primary target for the nutritional improvement of pea and other pulse crops ( Robinson et al, 2019 ). Vicilin has also been shown to form amyloids in pea cotyledon cells ( Antonets et al, 2020 ); amyloids are protein aggregates with unique physicochemical properties. Amyloids are resistant to the action of proteases and vicilin amyloids show resistance to gastrointestinal digestion ( Antonets et al, 2020 ).…”

“…Vicilin has also been shown to form amyloids in pea cotyledon cells ( Antonets et al, 2020 ); amyloids are protein aggregates with unique physicochemical properties. Amyloids are resistant to the action of proteases and vicilin amyloids show resistance to gastrointestinal digestion ( Antonets et al, 2020 ). The same term has been used to describe protein depositions that can cause health problems in humans and other organisms ( Kyle, 2001 ).…”

Mechanistic Insights into the Role of Molecular Chaperones in Protein Misfolding Diseases: From Molecular Recognition to Amyloid Disassembly

“…Nonetheless, functional amyloids have been found to play key roles in several systems, including: (i) Scaffolding systems, such as curli in microbial biofilm, providing a scaffold to protect bacteria and promote adherence to host cells [128]. (ii) Storage systems, such as Pmel17, which allows for the sequestration and condensation of melanin in the lumen of melanosomes [129]; vicilin, a 7S globulin in garden pea Pisum sativum L. seeds, which plays a crucial role in seed longevity [130]; peptide hormones for storage and release of certain hormones in the pituitary secretory granules [8]; Xvelo in Xenopus or Bucky Ball in zebrafish, which form a non-membranous compartment termed the Balbiani body to store germline-specific maternal mRNAs [131]. (iii) Signal transduction systems, such as the RIPK1-RIPK3 heterodimer, which controls necrotic signaling in mammals [132], or the fungal prion [HET-s], which regulates heterokaryon incompatibility between genetically similar fungi acting as a trigger for cell death activation [133].…”