Where do Protein Bodies of Cereal Seeds Come From?

Abstract

Protein bodies of cereal seeds consist of ordered, largely insoluble heteropolymers formed by prolamin storage proteins within the endoplasmic reticulum (ER) of developing endosperm cells. Often these structures are permanently unable to traffic along the secretory pathway, thus representing a unique example for the use of the ER as a protein storage compartment. In recent years, marked progress has been made in understanding what is needed to make a protein body and in formulating hypotheses on how protein body formation might have evolved as an efficient mechanism to store large amounts of protein during seed development, as opposed to the much more common system of seed storage protein accumulation in vacuoles. The major key evolutionary events that have generated prolamins appear to have been insertions or deletions that have disrupted the conformation of the eight-cysteine motif, a protein folding motif common to many proteins with different functions and locations along the secretory pathway, and, alternatively, the fusion between the eight-cysteine motif and domains containing additional cysteine residues.

Maize 16-kD γ-zein forms very unusual disulfide-bonded polymers in the endoplasmic reticulum: implications for prolamin evolution

“…Mutations and insertions in the ancient seed storage proteins of the 2S albumin class were the first events in the origination of prolamins ( Xu and Messing, 2009 ; Gu et al , 2010 ; Pedrazzini et al , 2016 ). This led to the assembly in PBs and a change in the subcellular compartment used for permanent accumulation from the vacuole to the ER, particularly in rice and panicoid cereals such as maize, sorghum, and millet ( Lending and Larkins, 1989 ; Shewry and Halford, 2002 ; Saito et al , 2012 ).…”

“…Prolamins are present only in the seeds of grasses, where they are usually the main proteins, and thus constitute the major global source of food protein ( Shewry and Halford, 2002 ). Their most striking and unique cell biology feature is their accumulation within the lumen of the endoplasmic reticulum (ER) as very large heteropolymers, termed protein bodies (PBs; Shewry and Halford, 2002 ; Pedrazzini et al , 2016 ). Most proteins that enter the ER are destined to be secreted or sorted to distal locations of the endomembrane system, whereas ER residents, which are mainly folding helpers, have specific amino acid signals that allow their retention/retrieval in the ER ( Gomez-Navarro and Miller, 2016 ).…”

“…1 ) consists of the transient signal peptide for translocation into the ER (co-translationally removed), followed by a region containing eight or seven (depending on the maize variety) repeats of the hexapeptide PPPVHL and seven Cys residues involved in inter-chain bonds that make the protein insoluble in non-reducing conditions, and finally a second region homologous to 2S albumins, which are vacuolar storage proteins present in various amounts in all land plants ( Vitale et al , 1982 ; Prat et al , 1985 ; Mainieri et al , 2014 ). 2S albumins belong to a larger class characterized by the eight-cysteine motif, consisting of four intra-chain disulfide bonds between three helical domains ( Pedrazzini et al , 2016 ; Fig. 1 ).…”

HOP3 a new regulator of the ER stress response in Arabidopsis with possible implications in plant development and response to biotic and abiotic stresses

“…In line with this evidence, it is tempting to speculate that HOP3 could have a major impact on other developmental processes with special demand in protein folding or secretion, as it is the case of seed maturation 23 (Fig. 1).…”

Transgenic technologies in cassava for nutritional improvement and viral disease resistance: a key strategy for food security in Africa

“…The unique characteristic of prolamins is the cysteine-rich region, which forms disulfide bridges and sequentially creates a large insoluble protein granule. The advantage of protein bodies is that they require only the ER protein folding machinery, reducing cellular energy during protein trafficking [44] . Zein is a maize prolamin that has been extensively studied; with 27 kDa, g-zein is the main subunit essential to initiate the formation of protein bodies [45] .…”