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Differentiation mechanism and function of the cereal aleurone cells and hormone effects on them

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Abstract

The cereal aleurone cells differentiate from the endosperm epidermis with the exception of endosperm transfer cells. Aleurone cells contain proteins, lipids, and minerals, and are important for digesting the endosperm storage products to nurse the embryo under effects of several hormones during the seed germination. The differentiation of aleurone cells is related to location effect and special gene expression. Moreover, the differentiation of aleurone cells is probably affected by the cues from maternal tissues. In the paper, differentiation mechanism and function of aleurone cells and hormone effects on them are reviewed. Some speculations about the differentiation mechanism of aleurone cells are given here.

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Abbreviations

AC:

Aleurone cells

PCD:

Programmed cell death

ROS:

Reactive oxygen species

References

  • Antoine C, Peyron S, Mabille F, Lapierre C, Bouchet B, Abecassis J, Rouau X (2003) Individual contribution of grain outer layers and their cell wall structure to the mechanical properties of wheat bran. J Agric Food Chem 51:2026–2033

    Article  PubMed  CAS  Google Scholar 

  • Barron C, Parker ML, Mills EN, Rouau X, Wilson RH (2005) FTIR imaging of wheat endosperm cell walls in situ reveals compositional and architectural heterogeneity related to grain hardness. Planta 220:667–677

    Article  PubMed  CAS  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, Stinard PS, McCarty DR (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409

    Article  PubMed  CAS  Google Scholar 

  • Becraft PW, Li K, Dey N, Asuncion-Crabb Y (2002) The maize dek1 gene functions in embryonic pattern formation and cell fate specification. Development 129:5217–5225

    PubMed  CAS  Google Scholar 

  • Berger F (1999) Endosperm development. Curr Opin Plant Biol 2:28–32

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Fath A, Jones RL (2001) Regulation of viability and cell death by hormones in cereal aleurone. J Plant Physiol 158:429–438

    Article  CAS  Google Scholar 

  • Bethke PC, Fath A, Spiegel YN, Hwang Y, Jones RL (2002) Abscisic acid, gibberellin and cell viability in cereal aleurone. Euphytica 126:3–11

    Article  CAS  Google Scholar 

  • Bethke PC, Libourel IG, Aoyama N, Chung YY, Still DW, Jones RL (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143:1173–1188

    Article  PubMed  CAS  PubMed Central  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 

  • Charlton WL, Keen CL, Merriman C, Lynch P, Greenland AJ, Dickinson HG (1995) Endosperm development in Zea mays; implication of gametic imprinting and paternal excess in regulation of transfer layer development. Development 121:3089–3097

    CAS  Google Scholar 

  • Costa LM, Yuan J, Rouster J, Paul W, Dickinson H, Gutierrez-Marcos JF (2012) Maternal control of nutrient allocation in plant seeds by genomic imprinting. Curr Biol 22:160–165

    Article  PubMed  CAS  Google Scholar 

  • Eastmond PJ, Jones RL (2005) Hormonal regulation of gluconeogenesis in cereal aleurone is strongly cultivar-dependent and gibberellin action involves SLENDER1 but not GAMYB. Plant J 44:483–493

    Article  PubMed  CAS  Google Scholar 

  • Fath A, Bethke PC, Jones RL (2001) Enzymes that scavenge PCD are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol 126:156–166

    Article  PubMed  CAS  PubMed Central  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 

  • Filardo F, Robertson M, Singh DP, Parish RW, Swain SM (2009) Functional analysis of HvSPY, a negative regulator of GA response, in barley aleurone cells and Arabidopsis. Planta 229:523–537

    Article  PubMed  CAS  Google Scholar 

  • Forestan C, Meda S, Varotto S (2010) ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development. Plant Physiol 152:1373–1390

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Furtado A, Henry RJ (2005) The wheat Em promoter drives reporter gene expression in embryo and aleurone tissue of transgenic barley and rice. Plant Biotechnol J 3:421–434

    Article  PubMed  CAS  Google Scholar 

  • Garcia D, Fitz Gerald JN, Berger F (2005) Maternal control of integument cell elongation and zygotic control of endosperm growth are coordinated to determine seed size in Arabidopsis. Plant Cell 17:52–60

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Geisler-Lee J, Gallie DR (2005) Aleurone cell identity is suppressed following connation in maize kernels. Plant Physiol 139:204–212

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Greenwood JS, Helm M, Gietl C (2005) Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Ricinus seed development. Proc Natl Acad Sci 102:2238–2243

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gruis DF, Guo H, Selinger D, Tian Q, Olsen OA (2006) Surface position, not signaling from surrounding maternal tissues, specifies aleurone epidermal cell fate in maize. Plant Physiol 141:898–909

    Article  PubMed  CAS  Google Scholar 

  • Gubler F, Kalla R, Roberts J, Jacobsen JV (1995) Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pl α-amylase gene promoter. Plant Cell 7:1879–1891

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gubler F, Chandler PM, White RG, Llewellyn DJ, Jacobsen JV (2002) Gibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression. Plant Physiol 129:191–200

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Guo WJ, Ho TH (2008) An abscisic acid-induced protein, HVA22, inhibits gibberellin-mediated programmed cell death in cereal aleurone cells. Plant Physiol 147:1710–1722

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Harris PJ, Chavan RR, Ferguson LR (2005) Production and characterisation of two wheat-bran fractions: an aleurone-rich and a pericarp-rich fraction. Mol Nutr Food Res 49:536–545

    Article  PubMed  Google Scholar 

  • Heine GF, Hernandez JM, Grotewold E (2004) Two cysteines in plant R2R3 MYB domains participate in REDOX-dependent DNA binding. J Biol Chem 279:37878–37885

    Article  PubMed  CAS  Google Scholar 

  • Jacobsen SE, Binkowski KA, Olszewski NE (1996) SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proc Natl Acad Sci USA 93:9292–9296

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jerkovic A, Kriegel AM, Bradner JR, Atwell BJ, Roberts TH, Willows RD (2010) Strategic distribution of protective proteins within bran layers of wheat protects the nutrient-rich endosperm. Plant Physiol 152:1459–1470

    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 

  • Li J, Berger F (2012) Endosperm: food for humankind and fodder for scientific discoveries. New Phytol 195:290–305

    Article  PubMed  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 

  • Lid SE, Al RH, Krekling T, Meeley RB, Ranch J, Opsahl-Ferstad HG, Olsen OA (2004) The maize disorganized aleurone layer 1 and 2 (dil1, dil2) mutants lack control of the mitotic division plane in the aleurone layer of developing endosperm. Planta 218:370–378

    Article  PubMed  CAS  Google Scholar 

  • Lur HS, Setter TL (1993) Role of auxin in maize endosperm development (timing of nuclear DNA endoreduplication, zein expression, and cytokinin). Plant Physiol 103:273–280

    PubMed  CAS  PubMed Central  Google Scholar 

  • Olsen OA (2001) Endosperm development: cellularization and cell fate specification. Annu Rev Plant Physiol Plant Mol Biol 52:233–267

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  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 

  • Philippe S, Saulnier L, Guillon F (2006) Arabinoxylan and (1-3),(1-4)-β-glucan deposition in cell walls during wheat endosperm development. Planta 224:449–461

    Article  PubMed  CAS  Google Scholar 

  • Racagni G, Villasuso AL, Pasquaré S, Giusto N, Machado E (2008) Diacylglycerol pyrophosphate inhibits the alpha-amylase secretion stimulated by gibberellic acid in barley aleurone. Physiol Plant 134:381–393

    Article  PubMed  CAS  Google Scholar 

  • Radchuk V, Weier D, Radchuk R, Weschke W, Weber H (2011) Development of maternal seed tissue in barley is mediated by regulated cell expansion and cell disintegration and coordinated with endosperm growth. J Exp Bot 62:1217–1227

    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 

  • Ritchie S, Gilroy S (1998) Calcium-dependent protein phosphorylation may mediate the gibberellic acid response in barley aleurone. Plant Physiol 116:765–776

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Robert P, Jamme F, Barron C, Bouchet B, Saulnier L, Dumas P, Guillon F (2011) Change in wall composition of transfer and aleurone cells during wheat grain development. Planta 233:393–400

    Article  CAS  Google Scholar 

  • Robertson M (2004) Two transcription factors are negative regulators of gibberellin response in the HvSPY-signaling pathway in barley aleurone. Plant Physiol 136:2747–2761

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rogers SW, Rogers JC (1999) Cloning and characterization of a gibberellin-induced RNase expressed in barley aleurone cells. Plant Physiol 119:1457–1464

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rosa NN, Dufour C, Lullien-Pellerin V, Micard V (2013) Exposure or release of ferulic acid from wheat aleurone: impact on its antioxidant capacity. Food Chem 141:2355–2362

    Article  PubMed  CAS  Google Scholar 

  • Serna A, Maitz M, O’Connell T, Santandrea G, Thevissen K, Tienens K, Hueros G, Faleri C, Cai G, Lottspeich F, Thompson RD (2001) Maize endosperm secretes a novel antifungal protein into adjacent maternal tissue. Plant J 25:687–698

    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 

  • Skadsen RW, Sathish P, Kaeppler HF (2000) Expression of thaumatin-like permatin PR-5 genes switches from the ovary wall to the aleurone in developing barley and oat seeds. Plant Sci 156:11–22

    Article  PubMed  CAS  Google Scholar 

  • Stacy RA, Munthe E, Steinum T, Sharma B, Aalen RB (1996) A peroxiredoxin antioxidant is encoded by a dormancy- related gene, Perl, expressed during late development in the aleurone and embryo of barley grains. Plant Mol Biol 31:1205–1216

    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 

  • Suzuki M, Latshaw S, Sato Y, Settles AM, Koch KE, Hannah LC, Kojima M, Sakakibara H, McCarty DR (2008) The maize viviparous8 locus, encoding a putative ALTERED MERISTEM PROGRAM1-like peptidase, regulates abscisic acid accumulation and coordinates embryo and endosperm development. Plant Physiol 146:1193–1206

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Swanson SJ, Bethke PC, Jones RL (1998) Barley aleurone cells contain two types of vacuoles: characterization of lytic organelles by use of fluorescent probes. Plant Cell 10:685–698

    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 

  • Villasuso AL, Racagni G, Machado E (2008) Phosphatidylinositol kinases as regulators of GA-stimulated alpha-amylase secretion in barley (Hordeum vulgare). Physiol Plant 133:157–166

    Article  PubMed  CAS  Google Scholar 

  • Wang M, Oppedijk BJ, Lu X, Van Duijn B, Schilperoort RA (1996) Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol Biol 32:1125–1134

    Article  PubMed  CAS  Google Scholar 

  • Washio K (2003) Functional dissections between GAMYB and Dof transcription factors suggest a role for protein–protein associations in the gibberellin-mediated expression of the RAmy1A gene in the rice aleurone. Plant Physiol 133:850–863

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Washio K, Morikawa M (2006) Common mechanisms regulating expression of rice aleurone genes that contribute to the primary response for gibberellin. Biochim Biophys Acta 1759:478–490

    Article  PubMed  CAS  Google Scholar 

  • Wisniewski JP, Rogowsky PM (2004) Vacuolar H+-translocating inorganic pyrophosphatase (Vpp1) marks partial aleurone cell fate in cereal endosperm development. Plant Mol Biol 56:325–337

    Article  PubMed  CAS  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 

  • 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 

  • Zee SY, O’brien TP (1970) Studies on the ontogeny of the pigment strand in the caryopses of wheat. Aust J Biol Sci 23:1153–1171

    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.

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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. Differentiation mechanism and function of the cereal aleurone cells and hormone effects on them. Plant Cell Rep 33, 1779–1787 (2014). https://doi.org/10.1007/s00299-014-1654-z

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  • DOI: https://doi.org/10.1007/s00299-014-1654-z

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