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

Wang, Guifeng; Wang, Gang; Wang, Jiajia; Du, Yulong; Yao, Dongsheng; Shuai, Bilian; Han, Liang; Tang, Yiming; Song, Rentao

doi:10.1093/jxb/erw396

Cited by 28 publications

(23 citation statements)

References 61 publications

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“…In addition to their general roles in intracellular motility and cell growth, certain MyoBs are involved in more specialized processes. Thus, a pollen-specific MyoB has been implicated in pollen tube growth in tobacco (36), whereas maize MyoBs have been found in association with protein bodies specific to maize endosperm (37,38).…”

Section: Discussionmentioning

confidence: 99%

Myosin-driven transport network in plants

Kurth

Peremyslov

Turner

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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We investigate the myosin XI-driven transport network in Arabidopsis using protein-protein interaction, subcellular localization, gene knockout, and bioinformatics analyses. The two major groups of nodes in this network are myosins XI and their membrane-anchored receptors (MyoB) that, together, drive endomembrane trafficking and cytoplasmic streaming in the plant cells. The network shows high node connectivity and is dominated by generalists, with a smaller fraction of more specialized myosins and receptors. We show that interaction with myosins and association with motile vesicles are common properties of the MyoB family receptors. We identify previously uncharacterized myosin-binding proteins, putative myosin adaptors that belong to two unrelated families, with four members each (MadA and MadB). Surprisingly, MadA1 localizes to the nucleus and is rapidly transported to the cytoplasm, suggesting the existence of myosin XI-driven nucleocytoplasmic trafficking. In contrast, MadA2 and MadA3, as well as MadB1, partition between the cytosolic pools of motile endomembrane vesicles that colocalize with myosin XI-K and diffuse material that does not. Gene knockout analysis shows that MadB1-4 contribute to polarized root hair growth, phenocopying myosins, whereas MadA1-4 are redundant for this process. Phylogenetic analysis reveals congruent evolutionary histories of the myosin XI, MyoB, MadA, and MadB families. All these gene families emerged in green algae and show concurrent expansions via serial duplication in flowering plants. Thus, the myosin XI transport network increased in complexity and robustness concomitantly with the land colonization by flowering plants and, by inference, could have been a major contributor to this process.myosins | receptors | adaptors | cytoplasmic streaming | nuclear transport F or half of a century, it had been assumed that rapid organelle trafficking and cytoplasmic streaming in plant cells rely on myosin motors (1) and, in particular, class XI myosins that are homologous to fungal and animal class V myosins (2). Over the past decade, a massive amount of information on specific functions of myosins and mechanisms of myosin XI-dependent processes in plants has been obtained (3-5). The first genetic evidence of myosin function in cell expansion involved the demonstration of a dramatic reduction of the polarized root hair growth upon inactivation of the myosin XI-K and XI-2 genes (6, 7). Subsequently, it has been shown that myosindependent trafficking is required for the growth of multiple cell types, as well as normal plant growth and development (4,(8)(9)(10). Among the 13 paralogous myosins XI encoded in the Arabidopsis thaliana genome, the highly expressed myosins XI-K, XI-1, and XI-2 have been shown to provide the most pronounced, functionally redundant contributions to each of these processes. In contrast, another highly expressed paralog, myosin XI-I, plays only limited roles in cell and plant growth but has a specialized function in nuclear repositioning through binding nuclear e...

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Section: Discussionmentioning

confidence: 99%

Myosin-driven transport network in plants

Kurth

Peremyslov

Turner

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…It has been proposed that the molecular chaperone BiP (binding protein) facilitates prolamin folding and assembly into PBs in the endosperm cells of maize and rice (Li et al , ; Zhang and Boston, ). Because BiP2 (GRMZM2G114793) and BiP3 (GRMZM2G415007) homologs were enriched in maize PB proteomes (Wang et al , ), we analysed their expression in Etglo3 transgenic and non‐transgenic control plants. The expression of BiP2 was up‐regulated more than twofold in the developing endosperms of Etglo3 transgenic plants (Figure S7).…”

Section: Resultsmentioning

confidence: 99%

Towards coeliac‐safe bread

Zhang

Deng

Zhang

et al. 2019

Plant Biotechnology Journal

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Summary Gluten‐free foods cannot substitute for products made from wheat flour. When wheat products are digested, the remaining peptides can trigger an autoimmune disease in 1% of the North American and European population, called coeliac disease. Because wheat proteins are encoded by a large gene family, it has been impossible to use conventional breeding to select wheat varieties that are coeliac‐safe. However, one can test the properties of protein variants by expressing single genes in coeliac‐safe cereals like maize. One source of protein that can be considered as coeliac‐safe and has bread‐making properties is teff (Eragrostis tef), a grain consumed in Ethiopia. Here, we show that teff α‐globulin3 (Etglo3) forms storage vacuoles in maize that are morphologically similar to those of wheat. Using transmission electron microscopy, immunogold labelling shows that Etglo3 is almost exclusively deposited in the storage vacuole as electron‐dense aggregates. Of maize seed storage proteins, 27‐kDa γ‐zein is co‐deposited with Etglo3. Etglo3 polymerizes via intermolecular disulphide bonds in maize, similar to wheat HMW glutenins under non‐reducing conditions. Crossing maize Etglo3 transgenic lines with α‐, β‐ and γ‐zein RNA interference (RNAi) lines reveals that Etglo3 accumulation is only dramatically reduced in γ‐zein RNAi background. This suggests that Etglo3 and 27‐kDa γ‐zein together cause storage vacuole formation and behave similar to the interactions of glutenins and gliadins in wheat. Therefore, expression of teff α‐globulins in maize presents a major step in the development of a coeliac‐safe grain with bread‐making properties.

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“…Neighboring inside the BL is an endosperm tissue called BETL, and outside is a pericarp IEP. The proteome of whole maize seeds, embryos, and endosperm has been intensively investigated in recent decades [23,25,[38][39][40][41][42][43][44]. Due to the difficulty of separating tissues from kernels, the proteome for some targeted seed parts has seldom been the focus, except for BETL, whose functions have been implied to mediate embryo-endosperm interactions and play a role in plant defense by this method [45][46][47][48] To date, no attempt has been focused on BL, and very little is known about its developmental processes, as well as the physiological and molecular roles of this tissue in kernel development.…”

Section: Discussionmentioning

confidence: 99%

“…Proteomics studies in maize whole kernel development have been intensively conducted at different scales of genotype, growth stage, and treatment [17][18][19][20][21][22][23]. Proteomics has also been performed in specific kernel tissue of BETL and cellular component of protein body to investigate their special function and developmental process [24,25]. However, no attempt has been made to attach to BL tissue.…”

Section: Introductionmentioning

confidence: 99%

Label-Free Comparative Proteomic Analysis Combined with Laser-Capture Microdissection Suggests Important Roles of Stress Responses in the Black Layer of Maize Kernels

Chen

Huang

et al. 2020

IJMS

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The black layer (BL) is traditionally used as an indicator for kernel harvesting in maize, as it turns visibly dark when the kernel reaches physiological maturity. However, the molecular roles of BL in kernel development have not been fully elucidated. In this work, microscopy images showed that BL began to appear at a growth stage earlier than 10 days after pollination (DAP), and its color gradually deepened to become dark as the development period progressed. Scanning electron microscopy observations revealed that BL is a tissue structure composed of several layers of cells that are gradually squeezed and compressed during kernel development. Laser-capture microdissection (LCM) was used to sample BL and its neighboring inner tissue, basal endosperm transfer layer (BETL), and outer tissue, inner epidermis (IEP), from 20 DAP of kernels. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry profiling (MALDI-TOF MS profiling) detected 41, 104, and 120 proteins from LCM-sampled BL, BETL, and IEP, respectively. Gene ontology (GO) analysis indicated that the 41 BL proteins were primarily involved in the response to stress and stimuli. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis found that the BL proteins were enriched in several defense pathways, such as the ascorbate and aldarate metabolic pathways. Among the 41 BL proteins, six were BL-specific proteins that were only detected from BL. Annotations of five BL-specific proteins were related to stress responses. During kernel development, transcriptional expression of most BL proteins showed an increase, followed by a decrease, and reached a maximum zero to 20 DAP. These results suggest a role for BL in stress responses for protecting filial tissue against threats from maternal sides, which helps to elucidate the biological functions of BL.

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

Abstract: HighlightProteomic analysis of developing maize protein bodies (PBs) reveals an unexpected diversity and complexity of PB proteins, and provides a roadmap for the transport and translation of mRNAs of zein genes, and the assembly of PBs.

Cited by 28 publications

References 61 publications

Myosin-driven transport network in plants

Myosin-driven transport network in plants

Towards coeliac‐safe bread

Label-Free Comparative Proteomic Analysis Combined with Laser-Capture Microdissection Suggests Important Roles of Stress Responses in the Black Layer of Maize Kernels

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