Functional Genomics of Seed Development in Cereals

  • Ming Li
  • Sergiy Lopato
  • Nataliya Kovalchuk
  • Peter LangridgeEmail author


Seeds are the product of sexual reproduction in flowering plants. The seeds of cereals are the main source of staple food, animal feed and the raw material of food and fiber-based industries worldwide (Olsen 2001). More recently, cereal seeds have also been used as a source of starch for the production of biofuels, although this use has become controversial (Fischer et al. 2009). New strategies for raising grain production have become a high international priority to help feed a growing world population in a scenario where resources are limiting and climate variability is increasing (Tester and Langridge 2010). Abiotic and biotic stresses such as drought, frost/cold, salt, micronutrient-deficiency, heavy metal toxicity and damage caused by microbes and pests can lead to dramatic yield loss and have a great impact on seed quality


Endosperm Development Aleurone Layer Aleurone Cell Anticlinal Wall Quality Protein Maize 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Aalen R, Opsahl-Ferstad H, Linnestad C, Olsen O-A (1994) Transcripts encoding an oleosin and a dormancy-related protein are present in both the aleurone layer and the embryo of developing barley (Hordeum vulgare L.) seeds. Plant J 5:385–396PubMedCrossRefGoogle Scholar
  2. 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 Agr Food Chem 51:2026–2033CrossRefGoogle Scholar
  3. Aoki N, Scofield GN, Wang XD, Offler CE, Patrick JW, Furbank RT (2006) Pathway of sugar transport in germinating wheat seeds. Plant Physiol 141:1255–1263PubMedCrossRefGoogle Scholar
  4. Aquea F, Poupin MJ, Matus JT, Gebauer M, Medina C, Arce-Johnson P (2008) Synthetic seed production from somatic embryos of Pinus radiata. Biotechnol Lett 30:1847–1852PubMedCrossRefGoogle Scholar
  5. Ashton AR, Polya GM (1978) Cyclic adenosine 3’:5’-monophosphate in axenic rye grass endosperm cell cultures. Plant Physiol 61:718–722PubMedCrossRefGoogle Scholar
  6. Balandin M, Royo J, Gomez E, Muniz LM, Molina A, Hueros G (2005) A protective role for the embryo surrounding region of the maize endosperm, as evidenced by the characterisation of ZmESR-6, a defensin gene specifically expressed in this region. Plant Mol Biol 58:269–282PubMedCrossRefGoogle Scholar
  7. Balasubramanian S, Schneitz K (2000) NOZZLE regulates proximal-distal pattern formation, cell proliferation and early sporogenesis during ovule development in Arabidopsis thaliana. Development 127:4227–4238PubMedGoogle Scholar
  8. Balasubramanian S, Schneitz K (2002) NOZZLE links proximal-distal and adaxial-abaxial pattern formation during ovule development in Arabidopsis thaliana. Development 129:4291–4300PubMedGoogle Scholar
  9. Becraft P (2001) Cell fate specification in the cereal endosperm. Semin Cell Dev Biol 12:387–394PubMedCrossRefGoogle Scholar
  10. Becraft P, Asuncion-Crabb Y (2000) Positional cues specify and maintain aleurone cell fate in maize endosperm development. Development 127:4039–4048PubMedGoogle Scholar
  11. Becraft P, Kang S-H, Suh S-G (2001) The maize CRINKLY4 receptor kinase controls a cell-autonomous differentiation response. Plant Physiol 127:486–496PubMedCrossRefGoogle Scholar
  12. Becraft P, Li K, Dey N, Asuncion-Crabb Y (2002) The maize dek1 gene functions in embryonic pattern formation and cell fate specification. Development 129:5217–5225PubMedGoogle Scholar
  13. Becraft P, Stinard P, McCarty D (1996) CRINKLY4: A TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409PubMedCrossRefGoogle Scholar
  14. Becraft PW, Yi G (2011) Regulation of aleurone development in cereal grains. J Exp Bot 62:1669–1675PubMedCrossRefGoogle Scholar
  15. Bennett MD, Rao MK, Smith JB, Bayliss MW (1973) Cell developmetn in the anther, the ovule, and the young seed of Triticum aestivum L. var. Chinese Spring. Phil Trans Royal S B: Biol Sci 266:49–81Google Scholar
  16. 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 246:219–227PubMedCrossRefGoogle Scholar
  17. Bonello J-F, Sevilla-Lecoq S, Berne A, Risueno M-C, Dumas C, Rogowsky PM (2002) Esr proteins are secreted by the cells of the embryo surrounding region. J Exp Bot 53:1559–1568PubMedCrossRefGoogle Scholar
  18. Bosnes M, Weideman F, Olsen O-A (1992) Endosperm differentiation in barley wild-type and sex mutants. Plant J 2:661–674CrossRefGoogle Scholar
  19. Bradbury D, MacMasters MM, Cull IM (1956) Structure of the mature wheat kernel II. Microscopic structure of pericarp, seed coat, and other coverings of endosperm and germ of hard red winter wheat. Cereal Chem 33:342–360Google Scholar
  20. Brandt SP (2005) Microgenomics: gene expression analysis at the tissue-specific and single-cell levels. J Exp Bot 56:495–505PubMedCrossRefGoogle Scholar
  21. Brink RA, Cooper DC (1947) The endosperm in seed development. Bot Rev 13:423–541CrossRefGoogle Scholar
  22. Brown RC, Lemmon BE, Nguyen H, Olsen O-A (1999) Development of endosperm in Arabidopsis thaliana. Sex Plant Reprod 12:32–42CrossRefGoogle Scholar
  23. Brown RC, Lemmon BE, Olsen O-A (1994) Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell 6:1241–1252PubMedGoogle Scholar
  24. Brown RC, Lemmon BE, Olsen O-A (1996a) Development of the endosperm in rice (Oryza sativa L.): cellularization. J Plant Res 109:301–313CrossRefGoogle Scholar
  25. Brown RC, Lemmon BE, Olsen O-A (1996b) Polarization predicts the pattern of cellularization in cereal endosperm. Protoplasma 192:168–177CrossRefGoogle Scholar
  26. 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 202:414–426PubMedCrossRefGoogle Scholar
  27. Burton RA, Collins HM, Kibble NAJ, Smith JA, Shirley NJ, Jobling SA, Henderson M, Singh RR, Pettolino F, Wilson SM, Bird AR, Topping DL, Bacic A, Fincher GB (2011) Over-expression of specific HvCslF cellulose synthase-like genes in transgenic barley increases the levels of cell wall (1,3;1,4)-β-d-glucans and alters their fine structure. Plant Biotechnol J 9:117–135PubMedCrossRefGoogle Scholar
  28. Chen G, DenBoer L, Shin J (2008) Design of a single plasmid-based modified yeast one-hybrid system for investigation of in vivo protein–protein and protein-DNA interactions. Biotechniques 45:295–304PubMedCrossRefGoogle Scholar
  29. Cheng WH, Taliercio EW, Chourey PS (1996) The miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. Plant Cell 8:971–983PubMedGoogle Scholar
  30. Chung T, Kim CS, Nguyen HN, Meeley RB, Larkins BA (2007) The maize zmsmu2 gene encodes a putative RNA-splicing factor that affects protein synthesis and RNA processing during endosperm development. Plant Physiol 144:821–835PubMedCrossRefGoogle Scholar
  31. Coleman CE, Clore AM, Ranch JP, Higgins R, Lopes MA, Larkins BA (1997) Expression of a mutant alpha-zein creates the floury2 phenotype in transgenic maize. Proc Natl Acad Sci USA 94:7094–7097PubMedCrossRefGoogle Scholar
  32. Costa LM, Gutierrez-Marcos JF, Brutnell TP, Greenland AJ, Dickinson HG (2003) The globby1-1 (glo1-1) mutation disrupts nuclear and cell division in the developing maize seed causing alterations in endosperm cell fate and tissue differentiation. Development 130:5009–5017PubMedCrossRefGoogle Scholar
  33. Costa LM, Gutierrez-Marcos JF, Dickinson HG (2004) More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci 9:507PubMedCrossRefGoogle Scholar
  34. Damerval C, Guilloux ML (1998) Characterization of novel proteins affected by the o2 mutation and expressed during maize endosperm development. Mol Gen Genet 257:354–361PubMedCrossRefGoogle Scholar
  35. Deplancke B, Dupuy D, Vidal M, Walhout AJ (2004) A gateway-compatible yeast one-hybrid system. Genome Res 14:2093–2101PubMedCrossRefGoogle Scholar
  36. Doan DNP, Linnestad C, Olsen O-A (1996) Isolation of molecular markers from the barley endosperm coenocyte and the surrounding nucellus cell layers. Plant Mol Biol 31:877–886PubMedCrossRefGoogle Scholar
  37. Domínguez F, Moreno J, Cejudo FJ (2001) The nucellus degenerates by a process of programmed cell death during the early stages of wheat grain development. Planta 213:352–360PubMedCrossRefGoogle Scholar
  38. Drea S, Leader DJ, Arnold BC, Shaw P, Dolan L, Doonan JH (2005) Systematic spatial analysis of gene expression during wheat caryopsis development. Plant Cell 17:2172–2185PubMedCrossRefGoogle Scholar
  39. Drews GN, Yadegari R (2002) Development and function of the angiospern female gametophyte. Ann Rev Genet 36:99–124PubMedCrossRefGoogle Scholar
  40. Eskelin K, Ritala A, Suntio T, Blumer S, Holkeri H, Wahlström EH, Baez J, Mäkinen K, Maria NA (2009) Production of a recombinant full-length collagen type I alpha-1 and of a 45-kDa collagen type I alpha-1 fragment in barley seeds. Plant Biotechnol J 7:657–672PubMedCrossRefGoogle Scholar
  41. Fincher GB (1989) Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Ann Rev Plant Physiol Plant Mol Biol 40:305–346CrossRefGoogle Scholar
  42. Fischer G, Hizsnyik E, Prieler S, Shah M, Van Velthuizen H (2009) Biofuels and food security: implications of an accelerated biofuels production. Intl Inst Applied Systems Analysis, OFID Pamphlet Series 38Google Scholar
  43. 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 3:421–434PubMedCrossRefGoogle Scholar
  44. Galbraith DW, Birnbaum K (2006) Global studies of cell type-specific gene expression in plants. Annu Rev Plant Biol 57:451–475PubMedCrossRefGoogle Scholar
  45. Gibbon BC, Larkins BA (2005) Molecular genetic approaches to developing quality protein maize. Trends Genet 21:227PubMedCrossRefGoogle Scholar
  46. Gillikin JW, Zhang F, Coleman CE, Bass HW, Larkins BA, Boston RS (1997) A defective signal peptide tethers the floury-2 zein to the endoplasmic reticulum membrane. Plant Physiol 114:345–352PubMedCrossRefGoogle Scholar
  47. Gómez E, Royo J, Guo Y, Thompson R, Hueros G (2002) Establishment of cereal endosperm expression domains: identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1. Plant Cell 14:599–610PubMedCrossRefGoogle Scholar
  48. Gubatz S, Dercksen VJ, Brüss C, Weschke W, Wobus U (2007) Analysis of barley (Hordeum vulgare) grain development using three-dimensional digital models. Plant J 52:779–790PubMedCrossRefGoogle Scholar
  49. Gutiérrez-Marcos JF, Costa LM, Biderre-Petit C, Khbaya B, O’Sullivan DM, Wormald M, Perez P, Dickinson HG (2004) Maternally expressed gene1 is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. Plant Cell 16:1288–1301PubMedCrossRefGoogle Scholar
  50. Habben JE, Kirleis AW, Larkins BA (1993) The origin of lysine-containing proteins in opaque-2 maize endosperm. Plant Mol Biol 23:825–838PubMedCrossRefGoogle Scholar
  51. Haslam TM, Yeung EC (2011) Zygotic embryo culture: an overview plant embryo culture. In: Thorpe TA, Yeung EC (eds). Humana Press, pp 3-15Google Scholar
  52. Hens K, Feuz J-D, Deplancke B (2012) A High-throughput gateway-compatible yeast one-hybrid screen to detect Protein–DNA interactions. In: Deplancke B, Gheldof N (eds) Methods in molecular biology. Gene regulatory networks. Methods and protocols. Humana Press, vol 786, pp 335–355Google Scholar
  53. Himi E, Maekawa M, Miura H, Noda K (2011) Development of PCR markers for Tamyb10 related to R-1 red grain color gene in wheat. Theor Appl Genet 122:1561–1576PubMedCrossRefGoogle Scholar
  54. Holding DR, Hunter BG, Chung T, Gibbon BC, Ford CF, Bharti AK, Messing J, Hamaker BR, Larkins BA (2008) Genetic analysis of opaque2 modifier loci in quality protein maize. Theor Appl Genet 117:157–170PubMedCrossRefGoogle Scholar
  55. Hu S (1982) Embryology of angiosperms. People’s Education Press, BeijingGoogle Scholar
  56. Hueros G, Gomez E, Cheikh N, Edwards J, Weldon M, Salamini F, Thompson RD (1999) Identification of a promoter sequence from the BETL1 gene cluster able to confer transfer-cell-specific expression in transgenic maize. Plant Physiol 121:1143–1152PubMedCrossRefGoogle Scholar
  57. Hueros G, Varotto S, Salamini F, Thompson RD (1995) Molecular characterization of BET1, a gene expressed in the endosperm transfer cells of maize. Plant Cell 7:747–757PubMedGoogle Scholar
  58. Hunter B, Beatty M, Singletary G, Hamaker B, Dilkes B, Larkins B, Jung R (2002) Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell 14:2591–2612PubMedCrossRefGoogle Scholar
  59. Johnson AAT, Kyriacou B, Callahan DL, Carruthers L, Stangoulis J, Lombi E, Tester M (2011) Constitutive overexpression of the OsNAS gene family reveals single-gene strategies for effective iron- and zinc-biofortification of rice endosperm. PLOS ONE 6:e24476PubMedCrossRefGoogle Scholar
  60. 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 154:1842–1854PubMedCrossRefGoogle Scholar
  61. Kawashima T, Goldberg RB (2010) The suspensor: not just suspending the embryo. Trends Plant Sci 15:23–30PubMedCrossRefGoogle Scholar
  62. Kessler S, Seiki S, Sinha N (2002) Xcl1 causes delayed oblique periclinal cell divisions in developing maize leaves, leading to cellular differentiation by lineage instead of position. Development 129:1859–1869PubMedGoogle Scholar
  63. Kim JH, Jung IJ, Kim DY, Fanata WI, Son BH, Yoo JY, Harmoko R, Ko KS, Moon JC, Jang HH, Kim WY, Kim JY, Lim CO, Lee SY, Lee KO (2011) Proteomic identification of an embryo-specific 1Cys-Prx promoter and analysis of its activity in transgenic rice. Biochem Biophys Res Commun 408:78–83PubMedCrossRefGoogle Scholar
  64. Kim Y, Kim S, Park J, Park H, Lim M, Chua N, Park C (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18:3132–3144PubMedCrossRefGoogle Scholar
  65. Klein P, Dietz KJ (2010) Identification of DNA-binding proteins and protein–protein interactions by yeast one-hybrid and yeast two-hybrid screen. Methods Mol Biol 639:171–192PubMedCrossRefGoogle Scholar
  66. Klemsdal S, Hughes W, Lonneborg A, Aalen R, Olsen O (1991) Primary structure of a novel barley gene differentially expressed in immature aleurone layers. Mol Gen Genet 228:9–16PubMedCrossRefGoogle Scholar
  67. Koltunow AM (1993) Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5:1425–1437PubMedGoogle Scholar
  68. Kovalchuk N, Li M, Wittek F, Reid N, Singh R, Shirley N, Ismagul A, Eliby S, Johnson A, Milligan AS, Hrmova M, Langridge P, Lopato S (2010) Defensin promoters as potential tools for engineering disease resistance in cereal grains. Plant Biotechnol J 8:47–64PubMedCrossRefGoogle Scholar
  69. Kovalchuk N, Smith J, Bazanova N, Pyvovarenko T, Singh R, Shirley N, Ismagul A, Johnson A, Milligan AS, Hrmova M, Langridge P, Lopato S (2012a) Characterization of the wheat gene encoding a grain-specific lipid transfer protein TdPR61, and promoter activity in wheat, barley and rice. J Exp Bot 63:2025–2040PubMedCrossRefGoogle Scholar
  70. Kovalchuk N, Smith J, Pallotta M, Singh R, Ismagul A, Eliby S, Bazanova N, Milligan A, Hrmova M, Langridge P, Lopato S (2009) Characterization of the wheat endosperm transfer cell-specific protein TaPR60. Plant Mol Biol 71:81–98PubMedCrossRefGoogle Scholar
  71. Kovalchuk N, Wu W, Eini O, Bazanova N, Pallotta M, Shirley N, Singh R, Ismagul A, Eliby S, Johnson A, Langridge P, Lopato S (2012b) The scutellar vascular bundle–specific promoter of the wheat HD-Zip IV transcription factor shows similar spatial and temporal activity in transgenic wheat, barley and rice. Plant Biotechnol J 10:43–53PubMedCrossRefGoogle Scholar
  72. Kranz E, Lörz H (1994) In vitro fertilisation of maize by single egg and sperm cell protoplast fusion mediated by high calcium and high pH. Zygote 2:125–128PubMedCrossRefGoogle Scholar
  73. Kranz E, Scholten S (2008) In vitro fertilization: analysis of early post-fertilization development using cytological and molecular techniques. Sexual Plant Reprod 21:67–77CrossRefGoogle Scholar
  74. Kranz E, von Wiegen P, Quader H, Lorz H (1998) Endosperm development after fusion of isolated, single maize sperm and central cells in vitro. Plant Cell 10:511–524PubMedGoogle Scholar
  75. Kuwano M, Masumura T, Yoshida KT (2011) A novel endosperm transfer cell-containing region-specific gene and its promoter in rice. Plant Mol Biol 76:47–56PubMedCrossRefGoogle Scholar
  76. 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 52:243–250PubMedCrossRefGoogle Scholar
  77. Leah R, Skriver K, Knudsen S, Ruud-Hansen J, Raikhel NV, Mundy J (1994) Identification of an enhancer/silencer sequence directing the aleurone-specific expression of a barley chitinase gene. Plant J 6:579–589PubMedCrossRefGoogle Scholar
  78. Li M, Singh R, Bazanova N, Milligan AS, Shirley N, Langridge P, Lopato S (2008) Spatial and temporal expression of endosperm transfer cell-specific promoters in transgenic rice and barley. Plant Biotechnol J 6:465–476PubMedCrossRefGoogle Scholar
  79. 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 the mitotic division plane in the aleurone layer of developing endosperm. Planta 218:370–378PubMedCrossRefGoogle Scholar
  80. 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 99:5460–5465PubMedCrossRefGoogle Scholar
  81. 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 118:1169–1180PubMedCrossRefGoogle Scholar
  82. Locatelli F, Manzocchi LA, Viotti A, Genga A (2001) The nitrogen-induced recovery of α-zein gene expression in in vitro cultured opaque2 maize endosperms depends on the genetic background. Physiol Plant 112:414–420PubMedCrossRefGoogle Scholar
  83. Lopato S, Borisjuk L, Milligan A, Shirley N, Bazanova N, Langridge P (2006) Systematic identification of factors involved in post-transcriptional processes in wheat grain. Plant Mol Biol 62:637–653PubMedCrossRefGoogle Scholar
  84. Lopes MA, Larkins BA (1993) Endosperm origin, development, and function. Plant Cell 5:1383–1399PubMedGoogle Scholar
  85. Madrid SM (1991) The barley lipid transfer protein is targeted into the lumen of the endoplasmic reticulum. Plant Physol Biochem 29:695–704Google Scholar
  86. Magnard J-L, Le Deunff E, Domenech J, Rogowsky PM, Testillano PS, Rougier M, Risueño MC, Vergne P, Dumas C (2000) Genes normally expressed in the endosperm are expressed at early stages of microspore embryogenesis in maize. Plant Mol Biol 44:559–574PubMedCrossRefGoogle Scholar
  87. Magnard J-L, Lehouque G, Massonneau A, Frangne N, Heckel T, Gutierrez-Marcos JF, Perez P, Dumas C, Rogowsky PM (2003) ZmEBE genes show a novel, continuous expression pattern in the central cell before fertilization and in specific domains of the resulting endosperm after fertilization. Plant Mol Biol 53:821–836PubMedCrossRefGoogle Scholar
  88. Maitz M, Santandrea G, Zhang Z, Lal S, Hannah LC, Salamini F, Thompson RD (2000) rgf1, a mutation reducing grain filling in maize through effects on basal endosperm and pedicel development. Plant J 23:29–42PubMedCrossRefGoogle Scholar
  89. Mares DJ, Norstog K, Stone BA (1975) Early stages in the development of wheat endosperm. I The change from free nuclear to cellular endosperm. Aust J Bot 23:311–326CrossRefGoogle Scholar
  90. Mares DJ, Stone BA, Jeffery C, Norstog K (1977) Early stages in the development of wheat endosperm. II Ultrastructural observations on cell wall formation. Aust J Bot 25:599–613CrossRefGoogle Scholar
  91. Miller ME, Chourey PS (1992) The Maize Invertase-Deficient miniature-1 seed mutation is associated with aberrant pedicel and endosperm development. Plant Cell 4:297–305PubMedGoogle Scholar
  92. Moco S, Schneider B, Vervoort J (2009) Plant micrometabolomics: the analysis of endogenous metabolites present in a plant cell or tissue. J Proteome Res 8:1694–1703PubMedCrossRefGoogle Scholar
  93. Moriguchi K, Suzuki T, Ito Y, Yamazaki Y, Niwa Y, Kurata N (2005) Functional isolation of novel nuclear proteins showing a variety of subnuclear localizations. Plant Cell 17:389–403PubMedCrossRefGoogle Scholar
  94. Morrison IN, Kuo J, O’Brien TP (1975) Histochemistry and fine structure of developing wheat aleurone cells. Planta 123:105–116CrossRefGoogle Scholar
  95. Morrison IN, O’Brien TP, Kuo J (1978) Initital cellularization and differentiation of the aleurone cells in the ventral region of the developing wheat grain. Planta 140:19–30CrossRefGoogle Scholar
  96. Muñiz LM, Royo J, Gómez E, Barrero C, Bergareche D, Hueros G (2006) The maize transfer cell-specific type-A response regulator ZmTCRR-1 appears to be involved in intercellular signalling. Plant J 48:17–27PubMedCrossRefGoogle Scholar
  97. Muñiz LM, Royo J, Gómez E, Baudot G, Paul W, Hueros G (2010) Atypical response regulators expressed in the maize endosperm transfer cells link canonical two component systems and seed biology. BMC Plant Biol 10:84–100PubMedCrossRefGoogle Scholar
  98. Natesh S, Rau MA (1984) The Embryo. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin, pp 377–434CrossRefGoogle Scholar
  99. Nelson T, Tausta SL, Gandotra N, Liu T (2006) Laser microdissection of plant tissue: what you see is what you get. Annu Rev Plant Biol 57:181–201PubMedCrossRefGoogle Scholar
  100. Nestel P, Bouis HE, Meenakshi JV, Pfeiffer W (2006) Biofortification of staple food crops. J Nutr 136:1064–1067PubMedGoogle Scholar
  101. Ohtsu K, Takahashi H, Schnable PS, Nakazono M (2007) Cell type-specific gene expression profiling in plants by using a combination of laser microdissection and high-throughput technologies. Plant Cell Physiol 48:3–7PubMedCrossRefGoogle Scholar
  102. Olsen LT, Divon HH, Kjetil Fosnes RA, Lid SE, Opsahl-Sorteberg H-G (2008) The defective seed5 (des5) mutant: effects on barley seed development and HvDek1, HvCr4, and HvSal1 gene regulation. J Exp Bot 59:3753–3765PubMedCrossRefGoogle Scholar
  103. Olsen O-A (2001) Endosperm development: cellularization and cell fate specification. Ann Rev Plant Physiol Plant Mol Biol 52:233–267CrossRefGoogle Scholar
  104. Olsen O-A (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16:S214–S227PubMedCrossRefGoogle Scholar
  105. Opsahl-Ferstad H-G, Deunff EL, Dumas C, Rogowsky PM (1997) ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. Plant J 12:235–246PubMedCrossRefGoogle Scholar
  106. Opsahl-Sorteberg H-G, Divon HH, Nielsen PS, Kalla R, Hammond-Kosack M, Shimamoto K, Kohli A (2004) Identification of a 49-bp fragment of the HvLTP2 promoter directing aleurone cell specific expression. Gene 341:49–58PubMedCrossRefGoogle Scholar
  107. Otegui MS, Mastronarde DN, Kang B-H, Bednarek SY, Staehelin LA (2001) Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13:2033–2051PubMedGoogle Scholar
  108. Otegui MS, Staehelin LA (2000) Syncytial-type cell plates: a novel kind of cell plate involved in endosperm cellularization of Arabidopsis. Plant Cell 12:933–947PubMedGoogle Scholar
  109. Pyvovarenko T, Lopato S (2011) Isolation of plant transcription factors using a yeast one-hybrid system. Methods Mol Biol 754:45–66PubMedCrossRefGoogle Scholar
  110. le Qu Q, Takaiwa F (2004) Evaluation of tissue specificity and expression strength of rice seed component gene promoters in transgenic rice. Plant Biotechnol J 2:113–125CrossRefGoogle Scholar
  111. Raghavan V (2003) One hundred years of zygotic embryo culture investigations. In Vitro Cellular and Developmental Biology—Plant 39:437–442 Google Scholar
  112. Raghavan V (2006) Double fertilization: embryo and endosperm development in flowering plants. Springer, BerlinGoogle Scholar
  113. Reece-Hoyes JS, Diallo A, Lajoie B, Kent A, Shrestha S, Kadreppa S, Pesyna C, Dekker J, Myers CL, Walhout AJ (2011) Enhanced yeast one-hybrid assays for high-throughput gene-centered regulatory network mapping. Nat Methods 8:1059–1064PubMedCrossRefGoogle Scholar
  114. Reiser L, Fischer R (1993) The ovule and the embryo sac. Plant Cell 5:1291–1301PubMedGoogle Scholar
  115. Russell S (1993) The egg cell: development and role in fertilization and early embryogenesis. Plant Cell 5:1349–1359PubMedGoogle Scholar
  116. Scanlon MJ, Meyers AM (1998) Phenotypic analysis and molecular cloning of discolored-1 (dsc1), a maize gene required for early kernel development. Plant Mol Biol 37:483–493PubMedCrossRefGoogle Scholar
  117. Schel JHN, Kieft H, Van Lammeren AAM (1984) Interactions between embryo and endosperm during early developmental stages of maize caryopses (Zea mays). Can J Bot 62:483–493CrossRefGoogle Scholar
  118. Schmidt RJ, Burr FA, Burr B (1987) Transposon tagging and molecular analysis of the maize regulatory locus opaque-2. Science 238:960–963PubMedCrossRefGoogle Scholar
  119. 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 25:687–698PubMedCrossRefGoogle Scholar
  120. Sestili F, Janni M, Doherty A, Botticella E, D’Ovidio R, Masci S, Jones HD, Lafiandra D (2010) Increasing the amylose content of durum wheat through silencing of the SBEIIa genes. BMC Plant Biol 10:144–155PubMedCrossRefGoogle Scholar
  121. Shannon J (1982) Maize endosperm cultures. In: Sheridan W (ed) Maize for Biological Research. Plant Molecular Biology Association, Charlottesville, pp 397–400Google Scholar
  122. Shen B, Allen WB, Zheng P, Li C, Glassman K, Ranch J, Nubel D, Tarczynski MC (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol 153:980–987PubMedCrossRefGoogle Scholar
  123. 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 100:6552–6557PubMedCrossRefGoogle Scholar
  124. Skriver K, Leah R, Muller-Uri F, Olsen F, Mundy J (1992) Structure and expression of the barley lipid transfer protein gene Ltp1. Plant Mol Biol 18:585–589PubMedCrossRefGoogle Scholar
  125. Smith LM, Handley J, Li Y, Martin H, Donovan L, Bowles DJ (1992) Temporal and spatial regulation of a novel gene in barley embryos. Plant Mol Biol 20:255PubMedCrossRefGoogle Scholar
  126. Sreenivasulu N, Borisjuk L, Junker BH, Mock HP, Rolletschek H, Seiffert U, Weschke W, Wobus U (2010) Barley grain development toward an integrative view. Int Rev Cell Mol Biol 281:49–89PubMedCrossRefGoogle Scholar
  127. Sreenivasulu N, Usadel B, Winter A, Radchuk V, Scholz U, Stein N, Weschke W, Strickert M, Close TJ, Stitt M, Graner A, Wobus U (2008) Barley grain maturation and germination: metabolic pathway and regulatory network commonalities and differences highlighted by new MapMan/PageMan profiling tools. Plant Physiol 146:1738–1758PubMedCrossRefGoogle Scholar
  128. Stacy RAP, Nordeng TW, Culianez-Macia FA, Aalen RB (1999) The dormancy-related peroxiredoxin anti-oxidant, PER1, is localized to the nucleus of barley embryo and aleurone cells. Plant J 19:1–8PubMedCrossRefGoogle Scholar
  129. Streatfield SJ, Bray J, Love RT, Horn ME, Lane JR, Drees CF, Egelkrout EM, Howard JA (2010) Identification of maize embryo-preferred promoters suitable for high-level heterologous protein production. GM Crops 1:162–172PubMedCrossRefGoogle Scholar
  130. Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822PubMedCrossRefGoogle Scholar
  131. Thiel J, Weier D, Sreenivasulu N, Strickert M, Weichert N, Melzer M, Czauderna T, Wobus U, Weber H, Weschke W (2008) Different hormonal regulation of cellular differentiation and function in nucellar projection and endosperm transfer cells: a microdissection-based transcriptome study of young barley grains. Plant Physiol 148:1436–1452PubMedCrossRefGoogle Scholar
  132. Thiel J, Weier D, Weschke W (2011) Laser-capture microdissection of developing barley seeds and cDNA array analysis of selected tissues. Methods Mol Biol 755:461–475PubMedCrossRefGoogle Scholar
  133. Thobunluepop P, Pawelzik E, Vearasilp S (2009) Possibility of sweet corn synthetic seed production. Pak J Biol Sci 12:1085–1089PubMedCrossRefGoogle Scholar
  134. Tian Q, Olsen L, Sun B, Lid SE, Brown RC, Lemmon BE, Fosnes K, Gruis DF, Opsahl-Sorteberg H-G, Otegui MS, Olsen O-A (2007) Subcellular localization and functional domain studies of Defective Kernerl 1 in maize and Arabidopsis thaliana suggests a model for aleurone cell fate specification involving CRINKLY 4 and Supernumerary Aleurone Layer 1, Plant Cell 19:3127–3145Google Scholar
  135. Tingay S, McElroy D, Kalla R, Fieg S, Wang M, Thornton S, Brettell R (1997) Agrobacterium tumefaciens-mediated barley transformation. Plant J 11:1369–1376CrossRefGoogle Scholar
  136. Tucker MR, Araujo A-CG, Paech NA, Hecht V, Schmidt EDL, Rossell J-B, de Vries SC, Koltunow AMG (2003) Sexual and apomictic reproduction in Hieracium subgenus Pilosella are closely interrelated developmental pathways. Plant Cell 15:1524–1537PubMedCrossRefGoogle Scholar
  137. Van Herpen TW, Riley M, Sparks C, Jones HD, Gritsch C, Dekking EH, Hamer RJ, Bosch D, Salentijn EM, Smulders MJ, Shewry PR, Gilissen LJ (2008) Detailed analysis of the expression of an alpha-gliadin promoter and the deposition of alpha-gliadin protein during wheat grain development. Ann Bot 102:331–342PubMedCrossRefGoogle Scholar
  138. van Went JL, Willemse MTM (1984) Fertilization. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin, pp 273–318CrossRefGoogle Scholar
  139. Vijayaraghavan MR, Prabhakar K (1984) The endosperm. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin, pp 319–338CrossRefGoogle Scholar
  140. Wakasa Y, Hirano K, Urisu A, Matsuda T, Takaiwa F (2011) Generation of transgenic rice lines with reduced contents of multiple potential allergens using a null mutant in combination with an RNA silencing method. Plant Cell Physiol 52:2190–2199PubMedCrossRefGoogle Scholar
  141. 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 189:1281–1295PubMedCrossRefGoogle Scholar
  142. Webb MC, Gunning BES (1991) The microtubular cytoskeleton during development of the zygote, proembryo and free-nuclear endosperm in Arabidopsis thaliana (L.) Heynh. Planta 184:187–195CrossRefGoogle Scholar
  143. Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364PubMedCrossRefGoogle Scholar
  144. Weschke W, Panitz R, Gubatz S, Wang Q, Radchuk R, Weber H, Wobus U (2003) The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J 33:395–411PubMedCrossRefGoogle Scholar
  145. Weterings K, Russell SD (2004) Experimental analysis of the fertilization process. Plant Cell 16(Suppl):S107–S118PubMedGoogle Scholar
  146. White PJ, Broadley MR (2005) Biofortifying crops with essential mineral elements. Trends Plant Sci 10:586–593PubMedCrossRefGoogle Scholar
  147. Wilson SM, Burton RA, Collins HM, Doblin MS, Pettolino FA, Shirley N, Fincher GB, Bacic A (2012) Pattern of deposition of cell wall polysaccharides and transcript abundance of related cell wall synthesis genes during differentiation in barley endosperm. Plant Physiol 159:655–670PubMedCrossRefGoogle Scholar
  148. Ye R, Yao QH, Xu ZH, Xue HW (2004) Development of an efficient method for the isolation of factors involved in gene transcription during rice embryo development. Plant J 38:348–357PubMedCrossRefGoogle Scholar
  149. Yi G, Lauter AM, Scott MP, Becraft PW (2011) The thick aleurone1 mutant defines a negative regulation of maize aleurone cell fate that functions downstream of defective kernel1. Plant Physiol 156:1826–1836PubMedCrossRefGoogle Scholar
  150. Yin LL, Xue HW (2012) The MADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development. Plant Cell 24:1049–1065PubMedCrossRefGoogle Scholar
  151. Zhang C, Baez J, Pappu KM, Glatz CE (2009) Purification and characterization of a transgenic corn grain-derived recombinant collagen type I alpha 1. Biotechnol Prog 25:1660–1668PubMedGoogle Scholar
  152. Zhang J, Martin JM, Beecher B, Lu C, Hannah LC, Wall ML, Altosaar I, Giroux MJ (2010) The ectopic expression of the wheat Puroindoline genes increase germ size and seed oil content in transgenic corn. Plant Mol Biol 74:353–365PubMedCrossRefGoogle Scholar
  153. Zheng Y, Wang Z (2011) Contrast observation and investigation of wheat endosperm transfer cells and nucellar projection transfer cells. Plant Cell Rep 30:1281–1288PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Ming Li
    • 1
  • Sergiy Lopato
    • 1
  • Nataliya Kovalchuk
    • 1
  • Peter Langridge
    • 1
    Email author
  1. 1.Australian Centre for Plant Functional GenomicsUniversity of AdelaideUrrbraeSouth Australia

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