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Protein accumulation in aleurone cells, sub-aleurone cells and the center starch endosperm of cereals

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Abstract

There are mainly three endosperm storage tissues in the cereal endosperm: aleurone cells, sub-aleurone cells and the center starch endosperm. The protein accumulation is very different in the three endosperm storage tissues. The aleurone cells accumulate protein in aleurone granules. The sub-aleurone cells and the center starch endosperm accumulate protein in endoplasmic reticulum-derived protein bodies and vacuolar protein bodies. Proteins are deposited in different patterns within different endosperm storage tissues probably because of the special storage properties of these tissues. There are several special genes and other molecular factors to mediate the protein accumulation in these tissues. Different proteins have distinct functions in the protein body formation and the protein interactions determine protein body assembly. There are both cooperation and competition relationships between protein, starch and lipid in the cereal endosperm. This paper reviews the latest investigations on protein accumulation in aleurone cells, sub-aleurone cells and the center starch endosperm. Useful information will be supplied for future investigations on the cereal endosperm development.

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Abbreviations

AC:

Aleurone cells

AG:

Aleurone granule

BiP:

Luminal-binding protein

CL:

Constitution lipid

CP:

Constitution protein

CSE:

Center starch endosperm

DCC:

Dilute salt solution

Em:

Embryo

ERPB:

Endoplasmic reticulum-derived protein body

ESP:

Endosperm storage protein

ESR:

Embryo surrounding region

ETC:

Endosperm transfer cells

LB:

Lipid body

PB:

Protein body

PDI:

Protein disulfide isomerase

RPBF:

Prolamin-box binding factor

SAC:

Sub-aleurone cells

SE:

Starch endosperm

SG:

Starch granule

SGM:

Starch granule membrane

SL:

Storage lipid

SP:

Storage protein

SSE:

Starch synthesis enzyme

VPB:

Vacuolar protein body

References

  • Arcalis E, Marcel S, Altmann F, Kolarich D, Drakakaki G, Fischer R, Christou P, Stoger E (2004) Unexpected deposition patterns of recombinant proteins in post-endoplasmic reticulum compartments of wheat endosperm. Plant Physiol 136:3457–3466

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Arcalis E, Stadlmann J, Marcel S, Drakakaki G, Winter V, Rodriguez J, Fischer R, Altmann F, Stoger E (2010) The changing fate of a secretory glycoprotein in developing maize endosperm. Plant Physiol 153:693–702

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Becraft PW (2001) Cell fate specification in the cereal endosperm. Semin Cell Dev Biol 12:387–394

    Article  PubMed  CAS  Google Scholar 

  • Becraft PW, Asuncion-Crabb Y (2000) Positional cues specify and maintain aleurone cell fate in maize endosperm development. Development 127:4039–4048

    PubMed  CAS  Google Scholar 

  • Becraft PW, Gutierrez-Marcos J (2012) Endosperm development: dynamic processes and cellular innovations underlying sibling altruism. Wiley Interdiscip Rev Dev Biol 1:579–593

    Article  PubMed  CAS  Google Scholar 

  • Becraft PW, Yi G (2011) Regulation of aleurone development in cereal grains. J Exp Bot 62:1669–1675

    Article  PubMed  CAS  Google Scholar 

  • Becraft PW, Stinard PS, McCarty DR (1996) CRINKLY4: a TNFRlike receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409

    Article  PubMed  CAS  Google Scholar 

  • Brouns F, Hemery Y, Price R, Anson NM (2012) Wheat aleurone: separation, composition, health aspects, and potential food use. Crit Rev Food Sci Nutr 52:553–568

    Article  PubMed  CAS  Google Scholar 

  • Clore AM, Dannenhoffer JM, Larkins BA (1996) EF-1[alpha] is associated with a cytoskeletal network surrounding protein bodies in maize endosperm cells. Plant Cell 8:2003–2014

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dombrink-Kurtzman MA, Bietz JA (1993) Zein composition in hard and soft endosperm of maize. Cereal Chem 70:105–108

    CAS  Google Scholar 

  • Fath A, Bethke P, Beligni V, Jones R (2002) Active oxygen and cell death in cereal aleurone cells. J Exp Bot 53:1273–1282

    Article  PubMed  CAS  Google Scholar 

  • Frizzi A, Caldo RA, Morrell JA, Wang M, Lutfiyya LL, Brown WE, Malvar TM, Huang S (2010) Compositional and transcriptional analyses of reduced zein kernels derived from the opaque2 mutation and RNAi suppression. Plant Mol Biol 73:569–585

    Article  PubMed  CAS  Google Scholar 

  • Fukuda M, Wen L, Satoh-Cruz M, Kawagoe Y, Nagamura Y, Okita TW, Washida H, Sugino A, Ishino S, Ishino Y, Ogawa M, Sunada M, Ueda T, Kumamaru T (2013) A guanine nucleotide exchange factor for Rab5 proteins is essential for intracellular transport of the proglutelin from the Golgi apparatus to the protein storage vacuole in rice endosperm. Plant Physiol 162:663–674

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gibbon BC, Larkins BA (2005) Molecular genetics approaches to developing quality protein maize. Trends Genet 21:227–233

    Article  PubMed  CAS  Google Scholar 

  • Griesemer M, Young C, Robinson A, Petzold L (2012) Spatial localisation of chaperone distribution in the endoplasmic reticulum of yeast. IET Syst Biol 6:54–63

    Article  PubMed  CAS  Google Scholar 

  • Guo X, Yuan L, Chen H, Sato SJ, Clemente TE, Holding DR (2013) Nonredundant function of zeins and their correct stoichiometric ratio drive protein body formation in maize endosperm. Plant Physiol 162:1359–1369

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ishibashi Y, Tawaratsumida T, Kondo K, Kasa S, Sakamoto M, Aoki N, Zheng SH, Yuasa T, Iwaya-Inoue M (2012) Reactive oxygen species are involved in gibberellin/abscisic acid signaling in barley aleurone cells. Plant Physiol 158:1705–1714

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • James MG, Denyerz K, Myers AM (2003) Starch synthesis in the cereal endosperm. Curr Opin Plant Biol 6:215–222

    Article  PubMed  CAS  Google Scholar 

  • Kawagoe Y, Suzuki K, Tasaki M, Yasuda H, Akagi K, Katoh E, Nishizawa NK, Ogawa M, Takaiwa F (2005) The critical role of disulfide bond formation in protein sorting in the endosperm of rice. Plant Cell 17:1141–1153

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kawakatsu T, Yamamoto MP, Hirose S, Yano M, Takaiwa F (2008) Characterization of a new rice glutelin gene GluD-1 expressed in the starchy endosperm. J Exp Bot 59:4233–4245

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kawakatsu T, Yamamoto MP, Touno SM, Yasuda H, Takaiwa F (2009) Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. Plant J 59:908–920

    Article  PubMed  CAS  Google Scholar 

  • Kawakatsu T, Hirose S, Yasuda H, Takaiwa F (2010) Reducing rice seed storage protein accumulation leads to changes in nutrient quality and storage organelle formation. Plant Physiol 154:1842–1854

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kim CS, Woo Ym YM, Clore AM, Burnett RJ, Carneiro NP, Larkins BA (2002) Zein protein interactions, rather than the asymmetric distribution of zein mRNAs on endoplasmic reticulum membranes, influence protein body formation in maize endosperm. Plant Cell 14:655–672

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lamacchia C, Shewry PR, Di Fonzo N, Forsyth JL, Harris N, Lazzeri PA, Napier JA, Halford NG, Barcelo P (2001) Endosperm-specific activity of a storage protein gene promoter in transgenic wheat seed. J Exp Bot 52:243–250

    Article  PubMed  CAS  Google Scholar 

  • Lending CR (1996) A novel tubular array associated with protein bodies in the rough endoplasmic reticulum of opaque-2 maize. Protoplasma 195:68–77

    Article  CAS  Google Scholar 

  • Lending CR, Larkins BA (1989) Changes in the zein composition of protein bodies during maize endosperm development. Plant Cell 1:1011–1023

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Levanony H, Rubin R, Altschuler Y, Galili G (1992) Evidence for a novel route of wheat storage proteins to vacuoles. J Cell Biol 119:1117–1128

    Article  PubMed  CAS  Google Scholar 

  • Li X, Wu Y, Zhang DZ, Gillikin JW, Boston RS, Franceschi VR, Okita TW (1993) Rice prolamine protein body biogenesis: a BiP-mediated process. Science 262:1054–1056

    Article  PubMed  CAS  Google Scholar 

  • Lid SE, Gruis D, Jung R, Lorentzen JA, Ananiev E, Chamberlin M, Niu X, Meeley R, Nichols S, Olsen OA (2002) The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proc Natl Acad Sci USA 99:5460–5465

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Liu F, Ren Y, Wang Y, Peng C, Zhou K, Lv J, Guo X, Zhang X, Zhong M, Zhao S, Jiang L, Wang H, Bao Y, Wan J (2013) OsVPS9A functions cooperatively with OsRAB5A to regulate post-Golgi dense vesicle-mediated storage protein trafficking to the protein storage vacuole in rice endosperm cells. Mol Plant 6:1918–1932

    Article  PubMed  CAS  Google Scholar 

  • Loussert C, Popineau Y, Mangavel C (2008) Protein bodies ontogeny and localization of prolamin components in the developing endosperm of wheat caryopses. J Cereal Sci 47:445–456

    Article  CAS  Google Scholar 

  • Marion D, Dubreil L, Douliez JP (2003) Functionality of lipids and lipid-protein interactions in cereal-derived food products. OLC-Ol Corps Gras Li 10:47–56

    Article  CAS  Google Scholar 

  • Marzábal P, Gas E, Fontanet P, Vicente-Carbajosa J, Torrent M, Ludevid MD (2008) The maize Dof protein PBF activates transcription of γ-zein during maize seed development. Plant Mol Biol 67:441–454

    Article  PubMed  Google Scholar 

  • Møgelsvang S, Simpson DJ (1998) Changes in the levels of seven proteins involved in polypeptide folding and transport during endosperm development of two barley genotypes differing in storage protein localization. Plant Mol Biol 36:541–552

    Article  PubMed  Google Scholar 

  • Muench DG, Chuong SDX, Franceschi VR, Okita TW (2000) Developing prolamine protein bodies are associated with the cortical cytoskeleton in rice endosperm cells. Planta 211:227–238

    Article  PubMed  CAS  Google Scholar 

  • Norre F, Peyrot C, Garcia C, Rancé I, Drevet J, Theisen M, Gruber V (2002) Powerful effect of an atypical bifactorial endosperm box from wheat HMWG-Dx5 promoter in maize endosperm. Plant Mol Biol 50:699–712

    Article  PubMed  CAS  Google Scholar 

  • Offler CE, McCurdy DW, Patrick JW, Talbot MJ (2003) Transfer cells: cells specialized for a special purpose. Annu Rev Plant Biol 54:431–454

    Article  PubMed  CAS  Google Scholar 

  • Olsen OA (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16 (Suppl):S214–S227

    Article  Google Scholar 

  • Olsen OA, Lemmon B, Brown RC (1998) A model for aleurone development. Trends Plant Sci 3:168–169

    Article  Google Scholar 

  • Olsen OA, Linnestad C, Nichols SE (1999) Developmental biology of the cereal endosperm. Trends Plant Sci 4:253–257

    Article  PubMed  Google Scholar 

  • Randall JJ, Sutton DW, Hanson SF, Kemp JD (2005) BiP and zein binding domains within the delta zein protein. Planta 221:656–666

    Article  PubMed  CAS  Google Scholar 

  • Ren Y, Wang Y, Liu F, Zhou K, Ding Y, Zhou F, Wang Y, Liu K, Gan L, Ma W, Han X, Zhang X, Guo X, Wu F, Cheng Z, Wang J, Lei C, Lin Q, Jiang L, Wu C, Bao Y, Wang H, Wan J (2014) GLUTELIN PRECURSOR ACCUMULATION3 encodes a regulator of post-Golgi vesicular traffic essential for vacuolar protein sorting in rice endosperm. Plant Cell 26:410–425

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Reyes FC, Chung T, Holding D, Jung R, Vierstra R, Otegui MS (2011) Delivery of prolamins to the protein storage vacuole in maize aleurone cells. Plant Cell 23:769–784

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rolletschek H, Koch K, Wobus U, Borisjuk L (2005) Positional cues for the starch/lipid balance in maize kernels and resource partitioning to the embryo. Plant J 42:69–83

    Article  PubMed  CAS  Google Scholar 

  • Rubin R, Levanony H, Galili G (1992) Evidence for the presence of two different types of protein bodies in wheat endosperm. Plant Physiol 99:718–724

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Saito Y, Kashida K, Takata K et al (2009) A green fluorescent protein fused to rice prolamin forms protein body-like structures in transgenic rice. J Exp Bot 60:615–627

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Satoh-Cruz M, Crofts AJ, Takemoto-Kuno Y, Sugino A, Washida H, Crofts N, Okita TW, Ogawa M, Satoh H, Kumamaru T (2010) Protein disulfide isomerase like 1-1 participates in the maturation of proglutelin within the endoplasmic reticulum in rice endosperm. Plant Cell Physiol 51:1581–1593

    Article  PubMed  CAS  Google Scholar 

  • Shen B, Li C, Min Z, Meeley RB, Tarczynski MC, Olsen OA (2003) sal1 determines the number of aleurone cell layers in maize endosperm and encodes a class E vacuolar sorting protein. Proc Natl Acad Sci USA 100:6552–6557

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Shewry PR, Halford NG (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot 53:947–958

    Article  PubMed  CAS  Google Scholar 

  • Subbarao KV, Datta R, Sharma R (1998) Amylases synthesis in scutellum and aleurone layer of maize seeds. Phytochemistry 49:657–666

    Article  PubMed  CAS  Google Scholar 

  • Svihus B, Uhlen AK, Harstad OM (2005) Effect of starch granule structure associated components and processing on nutritive value of cereal starch. Anim Feed Sci Tech 122:303–320

    Article  CAS  Google Scholar 

  • Takahashi H, Saito Y, Kitagawa T, Morita S, Masumura T, Tanaka K (2005) A novel vesicle derived directly from endoplasmic reticulum is involved in the transport of vacuolar storage proteins in rice endosperm. Plant Cell Physiol 46:245–249

    Article  PubMed  CAS  Google Scholar 

  • Takemoto Y, Coughlan SJ, Okita TW, Satoh H, Ogawa M, Kumamaru T (2002) The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiol 128:1212–1222

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tian Q, Olsen L, Sun B, Lid SE, Brown RC, Lemmon BE, Fosnes K, Gruis DF, Opsahl-Sorteberg HG, Otegui MS, Olsen OA (2007) Subcellular localization and functional domain studies of DEFECTIVE KERNEL1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. Plant Cell 19:3127–3145

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tosi P (2012) Trafficking and deposition of prolamins in wheat. J Cereal Sci 56:81–90

    Article  CAS  Google Scholar 

  • Tosi P, Parker M, Carzaniga R, Martin B, Gritsch CS, Shewry PR (2009) Trafficking of storage proteins in developing grain of wheat. J Exp Bot 60:979–991

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang C, Washida H, Crofts AJ, Hamada S, Katsube-Tanaka T, Kim D, Choi SB, Modi M, Singh S, Okita TW (2008) The cytoplasmic-localized, cytoskeletal-associated RNA binding protein OsTudor-SN: evidence for an essential role in storage protein RNA transport and localization. Plant J 55:443–454

    Article  PubMed  CAS  Google Scholar 

  • Wang G, Sun X, Wang G, Wang F, Gao Q, Sun X, Tang Y, Chang C, Lai J, Zhu L, Xu Z, Song R (2011) Opaque7 encodes an acyl-activating enzyme-like protein that affects storage protein synthesis in maize endosperm. Genetics 189:1281–1295

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang G, Wang F, Wang G, Wang F, Zhang X, Zhong M, Zhang J, Lin D, Tang Y, Xu Z, Song R (2012) Opaque1 encodes a myosin XI motor protein that is required for endoplasmic reticulum motility and protein body formation in maize endosperm. Plant Cell 24:3447–3462

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Washida H, Sugino A, Doroshenk KA et al (2012) RNA targeting to a specific ER sub-domain is required for efficient transport and packaging of alphaglobulins to the protein storage vacuole in developing rice endosperm. Plant J 70:471–479

    Article  PubMed  CAS  Google Scholar 

  • Wu Y, Holdingb DR, Messinga J (2010) γ-Zeins are essential for endosperm modification in quality protein maize. Proc Natl Acad Sci USA 107:12810–12815

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Xiong F, Yu X-R, Zhou L, Wang Z, Wang F, Xiong A-S (2013) Structural development of aleurone and its function in common wheat. Mol Biol Rep 40:6785–6792

    Article  PubMed  CAS  Google Scholar 

  • Yamagata H, Sugimoto T, Tanaka K, Kasai Z (1982) Biosynthesis of storage proteins in developing rice seeds. Plant Physiol 70:1094–1100

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yamamoto MP, Onodera Y, Touno SM, Takaiwa F (2006) Synergism between RPBF Dof and RISBZ1 bZIP activators in the regulation of rice seed expression genes. Plant Physiol 141:1694–1707

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yasuda H, Hirose S, Kawakatsu T, Wakasa Y, Takaiwa F (2009) Overexpression of BiP has inhibitory effects on the accumulation of seed storage proteins in endosperm cells of rice. Plant Cell Physiol 50:1532–1543

    Article  PubMed  CAS  Google Scholar 

  • Zhang W, Sangtong V, Peterson J, Scott MP, Messing J (2013) Divergent properties of prolamins in wheat and maize. Planta 237:1465–1473

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work is supported by the National Natural Science Foundation of China Grant (no. 31270228, 31071341) to Prof. Yunjie Gu and Prof. Zhong Wang.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. College of Agriculture, Yangzhou University, Yangzhou, 225009, Jiangsu, China

    Yankun Zheng

  2. College of Bioscience and Biotechnology, Yangzhou University, Yangzhou, 225009, Jiangsu, China

    Zhong Wang

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  1. Yankun Zheng
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  2. Zhong Wang
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Correspondence to Zhong Wang.

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Communicated by Neal Stewart.

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Zheng, Y., Wang, Z. Protein accumulation in aleurone cells, sub-aleurone cells and the center starch endosperm of cereals. Plant Cell Rep 33, 1607–1615 (2014). https://doi.org/10.1007/s00299-014-1651-2

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