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Comprehensive proteomic analysis of developing protein bodies in maize (Zea mays) endosperm provides novel insights into its biogenesis

Prolamins, the major cereal seed storage proteins, are sequestered and accumulated in the lumen of the endoplasmic reticulum (ER), and are directly assembled into protein bodies (PBs). The content and composition of prolamins are the key determinants for protein quality and texture-related traits of...

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Autores principales: Wang, Guifeng, Wang, Gang, Wang, Jiajia, Du, Yulong, Yao, Dongsheng, Shuai, Bilian, Han, Liang, Tang, Yuanping, Song, Rentao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5181578/
https://www.ncbi.nlm.nih.gov/pubmed/27789589
http://dx.doi.org/10.1093/jxb/erw396
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author Wang, Guifeng
Wang, Gang
Wang, Jiajia
Du, Yulong
Yao, Dongsheng
Shuai, Bilian
Han, Liang
Tang, Yuanping
Song, Rentao
author_facet Wang, Guifeng
Wang, Gang
Wang, Jiajia
Du, Yulong
Yao, Dongsheng
Shuai, Bilian
Han, Liang
Tang, Yuanping
Song, Rentao
author_sort Wang, Guifeng
collection PubMed
description Prolamins, the major cereal seed storage proteins, are sequestered and accumulated in the lumen of the endoplasmic reticulum (ER), and are directly assembled into protein bodies (PBs). The content and composition of prolamins are the key determinants for protein quality and texture-related traits of the grain. Concomitantly, the PB-inducing fusion system provides an efficient target to produce therapeutic and industrial products in plants. However, the proteome of the native PB and the detailed mechanisms underlying its formation still need to be determined. We developed a method to isolate highly purified and intact PBs from developing maize endosperm and conducted proteomic analysis of intact PBs of zein, a class of prolamine protein found in maize. We thus identified 1756 proteins, which fall into five major categories: metabolic pathways, response to stimulus, transport, development, and growth, as well as regulation. By comparing the proteomes of crude and enriched extractions of PBs, we found substantial evidence for the following conclusions: (i) ribosomes, ER membranes, and the cytoskeleton are tightly associated with zein PBs, which form the peripheral border; (ii) zein RNAs are probably transported and localized to the PB–ER subdomain; and (iii) ER chaperones are essential for zein folding, quality control, and assembly into PBs. We futher confirmed that OPAQUE1 (O1) cannot directly interact with FLOURY1 (FL1) in yeast, suggesting that the interaction between myosins XI and DUF593-containing proteins is isoform-specific. This study provides a proteomic roadmap for dissecting zein PB biogenesis and reveals an unexpected diversity and complexity of proteins in PBs.
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spelling pubmed-51815782016-12-27 Comprehensive proteomic analysis of developing protein bodies in maize (Zea mays) endosperm provides novel insights into its biogenesis Wang, Guifeng Wang, Gang Wang, Jiajia Du, Yulong Yao, Dongsheng Shuai, Bilian Han, Liang Tang, Yuanping Song, Rentao J Exp Bot Research Paper Prolamins, the major cereal seed storage proteins, are sequestered and accumulated in the lumen of the endoplasmic reticulum (ER), and are directly assembled into protein bodies (PBs). The content and composition of prolamins are the key determinants for protein quality and texture-related traits of the grain. Concomitantly, the PB-inducing fusion system provides an efficient target to produce therapeutic and industrial products in plants. However, the proteome of the native PB and the detailed mechanisms underlying its formation still need to be determined. We developed a method to isolate highly purified and intact PBs from developing maize endosperm and conducted proteomic analysis of intact PBs of zein, a class of prolamine protein found in maize. We thus identified 1756 proteins, which fall into five major categories: metabolic pathways, response to stimulus, transport, development, and growth, as well as regulation. By comparing the proteomes of crude and enriched extractions of PBs, we found substantial evidence for the following conclusions: (i) ribosomes, ER membranes, and the cytoskeleton are tightly associated with zein PBs, which form the peripheral border; (ii) zein RNAs are probably transported and localized to the PB–ER subdomain; and (iii) ER chaperones are essential for zein folding, quality control, and assembly into PBs. We futher confirmed that OPAQUE1 (O1) cannot directly interact with FLOURY1 (FL1) in yeast, suggesting that the interaction between myosins XI and DUF593-containing proteins is isoform-specific. This study provides a proteomic roadmap for dissecting zein PB biogenesis and reveals an unexpected diversity and complexity of proteins in PBs. Oxford University Press 2016-12 2016-10-27 /pmc/articles/PMC5181578/ /pubmed/27789589 http://dx.doi.org/10.1093/jxb/erw396 Text en © The Author 2016. Published by Oxford University Press on behalf of the Society for Experimental Biology. http://creativecommons.org/licenses/by/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Paper
Wang, Guifeng
Wang, Gang
Wang, Jiajia
Du, Yulong
Yao, Dongsheng
Shuai, Bilian
Han, Liang
Tang, Yuanping
Song, Rentao
Comprehensive proteomic analysis of developing protein bodies in maize (Zea mays) endosperm provides novel insights into its biogenesis
title Comprehensive proteomic analysis of developing protein bodies in maize (Zea mays) endosperm provides novel insights into its biogenesis
title_full Comprehensive proteomic analysis of developing protein bodies in maize (Zea mays) endosperm provides novel insights into its biogenesis
title_fullStr Comprehensive proteomic analysis of developing protein bodies in maize (Zea mays) endosperm provides novel insights into its biogenesis
title_full_unstemmed Comprehensive proteomic analysis of developing protein bodies in maize (Zea mays) endosperm provides novel insights into its biogenesis
title_short Comprehensive proteomic analysis of developing protein bodies in maize (Zea mays) endosperm provides novel insights into its biogenesis
title_sort comprehensive proteomic analysis of developing protein bodies in maize (zea mays) endosperm provides novel insights into its biogenesis
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5181578/
https://www.ncbi.nlm.nih.gov/pubmed/27789589
http://dx.doi.org/10.1093/jxb/erw396
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