Abstract
This chapter summarizes the current understanding of structural aspects of cereal endosperm development with emphasis on the cytoskeleton and its role in morphogenesis. The developmental pathway of nuclear-type endosperm includes unusual cell and microtubule cycles and methods of wall placement. After double fertilization, the primary endosperm nucleus divides repeatedly without cytokinesis resulting in a large syncytium that lines the periphery and surrounds the central vacuole. During interphase this “liquid” endosperm is elegantly organized into functional units termed nuclear cytoplasmic domains (NCDs) by radial microtubule systems (RMSs) emanating from the nuclei. Cellularization is driven by the RMS microtubule cycle in which hoop-like cortical microtubules and preprophase microtubule bands (PPBs) are absent. It comprises alternation of two stages: deposition of anticlinal walls without mitosis leading to formation of alveoli, and periclinal walls following mitosis in the alveoli. Following centripetal cellularization, three principal tissues are differentiated: the central endosperm in which food reserves are stored, a transfer region specialized for uptake of metabolites, and the peripheral aleurone that releases enzymes to mobilize reserves at germination. The PPB microtubule cycle typical of meristematic growth replaces the RMS cycle when cell divisions associated with aleurone expansion and grain enlargement occur in the peripheral layers.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Bacic A, Stone BA (1981) Chemistry and organization of aleurone cell wall components from wheat and barley. Aust J Plant Physiol 8:475–495
Bechtel DB, Pomeranz Y (1980) The rice kernel. In: Pomeranz Y (ed) Advances in cereal science and techology, vol 3. Am Assoc Cereal Chem, St Paul, Minnesota, pp 73–113
Becraft PW, Brown RC, Lemmon BE, Olsen O-A, Opsahl-Ferstad H-G (2001) Endosperm development. In: Bhojwani SS (ed) Current trends in the embryology of angiosperms. Kluwer Academic, Dordrecht, the Netherlands, pp 353–374
Bethke PC, Swanson SJ, Hillmer S, Jones RL (1998) From storage compartment to lytic organelle: The metamorphosis of the aleurone storage vacuole. Ann Bot 82:399–412
Berger F (1999) Endosperm development. Curr Opin Plant Biol 2:28–32
Bonello J-F, Opsahl-Ferstad H-G, Perez P, Dumas C, Rogowsky PM (2000) Esr genes show different levels of expression in the same region of maize endosperm. Gene 246:219–227
Bosnes M, Weideman F, Olsen O-A (1992) Endosperm differentiation in barley wild-type and sex mutants. Plant J 2:661–674
Brown RC, Lemmon BE (1992) Cytoplasmic domain: A model for spatial control of cytokinesis in reproductive cells of plants. EMSA Bull 22:48–53
Brown RC, Lemmon BE (2001) The cytoskeleton and spatial control of cytokinesis in the plant life cycle. Protoplasma 215:35–49
Brown RC, Lemmon BE, Olsen O-A (1994) Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell 6:1241–1252
Brown RC, Lemmon BE, Nguyen H (2002a) Endosperm development. In: O'Neill SD, Roberts AJ (eds) Plant reproduction: annual plant reviews, vol 6. Sheffield Academic, Sheffield, UK, pp 193–220
Brown RC, Lemmon B, Nguyen H (2002b) The microtubule cycle during successive mitotic waves in the syncytial female gametophyte of ginkgo. J Plant Res 115:491–494
Brown RC, Lemmon BE, Nguyen H (2003) Events during the first four rounds of mitosis establish three developmental domains in the syncytial endosperm of Arabidopsis. Protoplasma 222:167–174
Brown RC, Lemmon BE, Nguyen H, Olsen O-A (1999) Development of endosperm in Arabidopsis thaliana. Sex Plant Reprod 12:32–42
Brown RC, Lemmon BE, Olsen O-A (1996a) Development of the endosperm in rice (Oryza sativa L.): cellularization. J Plant Res 109:301–13
Brown RC, Lemmon BE, Olsen O-A (1996b) Polarization predicts the pattern of cellularization in cereal endosperm. Protoplasma 192:168–177
Brown RC, Lemmon BE, Stone BA, Olsen O-A (1997) Cell wall (1–>3)- and (1–>3, 1–>4)-β-glucans during early grain development in rice (Oryza sativa L.). Planta 202:414–426
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
Cheng W-H, Taliercio EW, Chourey PS (1996) The minature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. Plant Cell 8:971–983
Clore AM, Dannenhoffer JM, Larkins BA (1996) EF-1alpha is associated with a cytoskeletal network surrounding protein bodies in maize endosperm cells. Plant Cell 8:2003–2014
Costa L, Gutierrez-Marcos J, Dickinson HG (2004) No longer a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci 9:507–514
Davis RW, Smith JD, Cobb BG (1990) A light and electron microscope investigation of the transfer cell region of maize caryopses. Canad J Bot 68:471–479
Dhonukshe P, Mathur J, Hülskamp M, Gadella Jr TWJ (2005) Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during divison-plane establishment in plant cells. BMC Biology 3:11
Dute RR, Peterson CM (1992) Early endosperm development in ovules of soybean, Glycine max (L.) Merr. (Fabaceae). Ann Bot 69:263–271
Fineran BA, Wild DJC, Ingerfeld M (1982) Initial wall formation in the endosperm of wheat Triticum aestivum: a reevaluation. Canad J Bot 60:1776–1795
Floyd SK, Friedman WE (2000) Evolution of endosperm developmental patterns among basal flowering plants. Int J Plant Sci 161:57–81
Gori P (1987) The fine structure of the developing Euphorbia dulcis endosperm. Ann Bot 60:563–569
Grafi G, Larkins BA (1995) Endoreduplication in maize endosperm: involvement of M phase-promoting factor inhibition and induction of S phase-related kinases. Science 269:1262–1264
Graham LE, Cook ME, Busse JS (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. PNAS 97:4535–4540
Gruis DF, Guo H, Selinger D, Tian Q, Olsen O-A (2006) Surface position, not signaling from surrounding maternal tissues, specify aleurone epidermal cell fate in maize endosperm organ cultures. Plant Physiol 141:898–909
Gunning BES, Pate JS (1969) Transfer cells: plant cells with wall ingrowths, specialized in relation to short distance transport of solutes-their occurrence, structure, and development. Protoplasma 68:107–133
Hargin KD, Morrison WR (1980) The distribution of acyl lipids in the germ, aleurone, starch and nonstarch endosperm of four wheat varieties. J Sci Food Agric 31:877–888
Jacobsen JV, Knox RB, Pyliotis NA (1971) The structure and composition of aleurone grains in the barley aleurone layer. Planta 101:189–209
Jacobsen JV, Pressman E, Pyliotis NA (1976) Gibberellin-induced separation of cells in isolated endosperm of celery seed. Planta 129:113–122
Jones RL (1969) The fine structure of barley aleurone cells. Planta 85:359–375
Juliano BO, Bechtel DB (1985) The rice grain and its gross composition. In: Juliano BO (ed) Rice: chemistry and technology, 2nd edn. Am Assoc Cereal Chem, St Paul, MN, pp 17–57
Kalla R, Shimamoto K, Potter R, Nielsen PS, Linnestad C, Olsen O-A (1994) The promoter of the barley aleurone-specific gene encoding a putative 7 kDalipid transfer protein confers aleurone cell-specific expression in transgenic rice. Plant J 6:849–860
Kermode AR (2005) Role of abscisic acid in seed dormancy. J Plant Growth Regul 24:319–344
Kessler SA, Sinha NR (2000) Characterization of xc1 (extra cell layers), a mutation affecting plane of cell division during maize development. In: Abstracts of Plant Biology 2000, San Diego, CA, 15–19 July 2000. American Society Plant Physiologists, Rockville, MD, p 48
Kiyosue T, Ohad N, Yadegari R, Hannon M, Dinneny J, Wells D, Katz A, Margossian L, Harada J, Goldberg RB, Fischer R (1999) Control of fertilization-independent endosperm development by the MEDEA polycomb gene in Arabidopsis. Proc Natl Acad Sci USA 96:4186–4191
Kyle DJ, Styles ED (1977) Development of aleurone and sub-aleurone layers in maize. Planta 137:185–193
Lid SE, Al RH, Krekling T, Meeley RB, Ranch J, Opsahl-Ferstad H-G, Olsen O-A (2004) The maize disorganized aleurone layer 1 and 2 (dil1, dil2) mutants lack control of mitotic division plane in the aleurone layer of developing endosperm. Planta 218:370–378
Lid SE, Gruis D, Jung R, Lorentzen JA, Ananiev E, Chamberlin M, Niu X, Meeley R, Nichols S, Olsen O-A (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
Linnestad C, Doan DNP, Brown RC, Lemmon BE, Meyer DJ, Jung R, Olsen O-A (1998) Nucellain, a barley homolog of the dicot vacuolar-processing protease, is localized in nucellar cell walls. Plant Physiol 118:1169–1180
Lloyd CW, Venverloo CJ, Goodbody KC, Shaw PJ (1992) Confocal laser microscopy and three-dimensional reconstruction of the nucleus-associated micotubules in the division plane of vacuolated plant cells. J Microsc 166:99–109
Lopes MA, Larkins BA (1993) Endosperm origin, development, and function. Plant Cell 5:1383–1399
Maheshwari P (1950) An introduction to the embryology of angiosperms. McGraw-Hill, New York
Mansfield SG, Briarty LG (1990) Endosperm cellularization in Arabidopsis thaliana (L). Ara Info Serv 27:65–72
Miller ME, Chourey PS (1992) The maize invertase-deficient minature-1 seed mutation is associated with aberrant pedicel and endosperm development. Plant Cell 4:297–305
Morrison IN, Kuo J, O'Brien TP (1975) Histochemistry and fine structure of developing wheat aleurone cells. Planta 123:105–116
Morrison IN, O'Brien TP (1976) Cytokinesis in the developing wheat grain; division with and without a phragmoplast. Planta 130:57–67
Müntz K (1998) Deposition of storage proteins. Plant Mol Biol 38:77–99
Nguyen H, Brown RC, Lemmon BE (2001) Patterns of cytoskeletal organization reflect distinct developmental domains in endosperm of Coronopus didymus (Brassicaceae). Int J Plant Sci 162:1–14
Nonogaki H, Gee OH, Bradford KJ (2000) A germination-specific endo-β-mannanase gene is expressed in the micropylar endosperm cap of tomato seeds. Plant Physiol 123:1235–1245
Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D, Harada JJ, Goldberg RB, Fischer RL (1999) Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 11:407–415
Olsen O-A (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16:S214–S227
Olsen O-A, Brown RC, Lemmon BE (1995) Pattern and process of wall formation in developing endosperm. BioEssays 17:803–812
Opsahl-Ferstad H-G, Le Deunff E, Dumas C, Rogowsky PM (1997) ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. Plant J 12:235–246
Otegui M, Staehelin LA (2000) Syncytial-type cell plates: a novel kind of cell plate involved in endosperm cellularization of Arabidopsis. Plant Cell 12:933–947
Pickett-Heaps JD, Gunning BES, Brown RC, Lemmon BE, Cleary AL (1999) The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell division. Am J Bot 86:153–172
Randolph LF (1936) Developmental morphology of the caryopsis in maize. J Agric Res 53:881–961
Rojo E, Gilmore CS, Somerville CR, Raikel NK (2000) Characterization of mangled, a gene required for normal mitosis and cell growth in Arabidopsis ovules. Am Soc Cell Biol Annual Meeting, San Francisco, Dec 2000, late abstract L51
Schel JHN, Kieft H, van Lammeren AAM (1984) Interactions between embryo and endosperm during early developmental stages of maize caryopses (Zea mays). Canad J Bot 62:2842–2853
Shen B, Li C, Min Z, Meeley RB, Tarczynski MC, Olsen O-A (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
Shibuya N, Iwasaki T (1985) Structural features of rice bran hemicellulose. Phytochem 24:285–289
Singh H (1978) Embryology of gymnosperms. In: Handbuch der Pflanzenanatomie 10. Borntraeger, Berlin, pp 110–287
Sinnot EW, Bloch R (1941) Division in vacuolate plant cells. Am J Bot 28:225–232
Sorensen MB, Chaudhury AM, Robert H, Bancharel E, Berger F (2001) Polycomb group genes control pattern formation in plant seed. Curr Biol 11:277–281
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
Van Lammeren AAM (1988) Structure and function of the microtubular cytoskeleton during endosperm development in wheat: an immunofluorescence study. Protoplasma 146:18–27
Walbot V (1994) Overview of key steps in aleurone development. In: Freeling M, Walbot V (eds) The maize handbook. Springer, Berlin Heidelberg New York, pp 78–80
Wang HL, Offler CE, Patrick JW (1994) Nucellar projection transfer cells in the developing wheat grain. Protoplasma 182:39–52
Wang M, Oppedijk BJ, Caspers MPM, Lamers GEM, Boot MJ, Geerlings DNG, Bakhuizen B, Meijer AH, van Duijn B (1998) Spatial and temporal regulation of DNA fragmentation in the aleurone of germinating barley. J Exp Bot 49:1293–1301
Webb MC, Gunning BES (1991) The microtubular cytoskeleton during development of the zygote, proembryo and free-nuclear endosperm in Arabidopsis thaliana (L.) Heynh. Planta 184:187–195
Williams JH, Friedman WE (2002) Identification of diploid endosperm in an early angiosperm lineage. Nature 415:522–526
Wilson SM, Burton RA, Doblin MS, Stone BA, Newbigin EJ, Fincher GB, Bacic A (2006) Temporal and spatial appearance of wall polysaccharides during cellularization of barley (Hordeum vulgare) endosperm. Planta 224:655–667
Wolf MJ, Cutler HC, Zuber MS, Khoo U (1972) Maize with multilayer aleurone of high protein content. Crop Sci 12:440–442
XuHan X (1995) Seed development in Phaseolus vulgaris L., Populus nigra L., and Ranunculus scleratus L. with special reference to the microtubular cytoskeleton. CIP-Gegevens Koninklijke Bibliotheek, Den Haag, Netherlands
Yang C-Y, Spielman M, Coles JP, Li Y, Ghelani S, Bourdon V, Brown RC, Lemmon BE, Scott RJ, Dickinson HG (2003) TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J 34:229–240
Young TE, Gallie DR, DeMason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development for wild-type and shrunken2 genotypes. Plant Physiol 115:737–751
Author information
Authors and Affiliations
Corresponding author
Editor information
Rights and permissions
Copyright information
© 2007 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Brown, R.C., Lemmon, B.E. (2007). The Developmental Biology of Cereal Endosperm. In: Olsen, OA. (eds) Endosperm. Plant Cell Monographs, vol 8. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_2007_106
Download citation
DOI: https://doi.org/10.1007/7089_2007_106
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-71234-3
Online ISBN: 978-3-540-71235-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)