Abstract
Maize (Zea mays L.) endosperm transfer cells are essential for kernel growth and development so they have a significant impact on grain yield. Although structural and ultrastructural studies have been published, little is known about the development of these cells, and prior to this study, there was a general consensus that they contain only flange ingrowths. We characterized the development of maize endosperm transfer cells by bright field microscopy, transmission electron microscopy, and confocal laser scanning microscopy. The most basal endosperm transfer cells (MBETC) have flange and reticulate ingrowths, whereas inner transfer cells only have flange ingrowths. Reticulate and flange ingrowths are mostly formed in different locations of the MBETC as early as 5 days after pollination, and they are distinguishable from each other at all stages of development. Ingrowth structure and ultrastructure and cellulose microfibril compaction and orientation patterns are discussed during transfer cell development. This study provides important insights into how both types of ingrowths are formed in maize endosperm transfer cells.
Similar content being viewed by others
Abbreviations
- MBETC:
-
Most basal endosperm transfer cells
- CLSM:
-
Confocal laser scanning microscopy
- DAP:
-
Days after pollination
- GDD:
-
Growing degree days
- OPW:
-
Outer periclinal wall
- TEM:
-
Transmission electron microscopy
References
Becraft PW (2001) Cell fate specification in the cereal endosperm. Cell Dev Biol 12:387–394. doi:10.1006/scdb.2001.0268
Becraft PW, Yi G (2011) Regulation of aleurone development in cereal grains. J Exp Bot 62:1669–1675. doi:10.1093/jxb/erq372
Charlton WL, Keen CL, Merriman C, Lynch AJ, Grennland 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 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 8:971–983. doi:10.1105/tpc.8.6.971
Dahiya P, Brewin NJ (2000) Immunogold localization of callose and other cell wall components in pea nodule transfer cells. Protoplasma 214:210–218. doi:10.1007/BF01279065
Davis RW, Smith JD, Cobb BG (1990) A light and electron microscope investigation of the transfer cell region of maize caryopses. Can J Bot 68:471–479. doi:10.1139/B90-063
DeWitt G, Richards J, Mohnen D, Jones AM (1999) Comparative compositional analysis of walls with two different morphologies: archetypical versus transfer-cell-like. Protoplasma 209:238–245. doi:10.1007/BF01453452
Felker FC, Goodwin JC (1988) Sugar uptake by maize endosperm suspension cultures. Plant Physiol 88:1235–1239
Felker FC, Shannon JC (1980) Movement of 14 C-labeled assimilates into kernels of Zea mays L. III. An anatomical examination and microautoradiographic study of assimilate transfer. Plant Physiol 65:864–870. doi:10.1104/pp.65.5.864
Felker FC, Liu K-C, Shannon JC (1990) Sugar uptake and starch biosynthesis by slices of developing maize endosperm. Plant Physiol 94:996–1001. doi:10.1104/pp.94.3.996
Gilmore EC, Rogers JS (1958) Heat units as a method of measuring maturity in corn. Agron J 50:611–615. doi:10.2134/agronj1958.00021962005000100014x
Griffith SM, Jones RJ, Brenner ML (1987) In vitro sugar transport in Zea mays L. kernels; I. Characteristics of sugar absorption and metabolism by developing maize endosperm. Plant Phys 84:467–471. doi:10.1104/pp.84.2.467
Gunning BES, Pate JS (1969) “Transfer cells” plant cells with wall ingrowths in relation to short distance transport of solutes—their occurrence, structure, and development. Protoplasma 68:107–133. doi:10.1007/BF01247900
Gunning BES, Pate JS (1974) Transfer cells. In: Robards AW (ed) Dynamic aspects of plant ultrastructure. McGraw-Hill, London, pp 441–479
Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. California Agricultural Experiment Station. College of Agriculture. Circ. 347, University of California, Berkeley
Kang B-H, Xiong Y, Williams DS, Pozueta-Romero D, Chourey PS (2009) Miniature1-encoded cell wall invertase is essential for assembly and function of wall-in-growth in the maize endosperm transfer cell. Plant Phys 151:1366–1376. doi:10.1104/pp.109.142331
McCurdy DW, Patrick JW, Offler CE (2008) Wall ingrowth formation in transfer cells: novel examples of localized wall deposition in plant cells. Curr Opin Plant Biol 11:653–661. doi:10.1016/j.pbi.2008.08.005
Monjardino P, Machado J, Gil FS, Fernandes R, Salema R (2007) Structural and ultrastructural characterization of maize coenocyte and endosperm cellularization. Can J Bot 85:216–223. doi:10.11.39/B06-156
Offler CE, McCurdy DW, Patrick JW, Talbot MJ (2003) Transfer cells: cells specialized for a special purpose. Annu Rev Plant Biol 54:431.454. doi:10.1146/annurev.arplant.54.031902.134812
Pugh DA, Offler CE, Talbot MJ, Ruan Y-L (2010) Evidence for the role of transfer cells in the evolutionary increase in seed and fiber biomass yield in cotton. Mol Plant 3:1075–1086. doi:10.1093/mp/ssq054
Salema R, Brandão I (1973) The use of PIPES buffer in the fixation of plant cells for electron microscopy. J Submicrosc Cytol 5:79–96
Talbot MJ, Franceschi VR, McCurdy DW, Offler CE (2001) Wall ingrowth architecture in epidermal transfer cells of Vicia faba cotyledons. Protoplasma 215:191–203. doi:10.1007/BF01280314
Talbot MJ, Offler CE, McCurdy DW (2002) Transfer cell architecture: a contribution towards understanding localized wall deposition. Protoplasma 219:197–209. doi:10.1007/s007090200021
Talbot MJ, Wasteneys GO, McCurdy DW, Offler CE (2007a) Deposition patterns of cellulose microfibrils in flange wall ingrowths of transfer cells indicate clear parallels with those of secondary wall thickenings. Funct Plant Biol 34:307–313. doi:10.1071/FP06273
Talbot MJ, Wasteneys GO, Offler CE, McCurdy DW (2007b) Cellulose synthesis is required for deposition of reticulate wall ingrowths in transfer cells. Plant Cell Physiol 48:147–158. doi:10.1093/pcp/pcl046
Thompson RD, Hueros G, Becker H-A, Maitz M (2001) Development and function of seed transfer cells. Plant Sci 160:775–783. doi:10.1016/S0168-9452(01)00345-4
Vaughn KC, Talbot MJ, Offler CE, McCurdy DW (2007) Wall ingrowths in epidermal transfer cells of Vicia faba cotyledons are modified primary walls marked by localized accumulations of arabinogalactan proteins. Plant Cell Physiol 48:159–168. doi:10.1093/pcp/pcl047
Wardini T, Wang X-D, Offler CE, Patrick JW (2007) Induction of wall ingrowths of transfer cells occurs rapidly and depends upon gene expression in cotyledons of developing Vicia faba seeds. Protoplasma 231:15–23. doi:10.1007/s00709-007-0244-0
Young TE, Gallie DR (2000) Programmed cell death during endosperm development. Plant Mol Biol 44:283–301. doi:10.1023/A:1026588408152
Acknowledgments
This research was supported in part by the Instituto de Biotecnologia e Bioengenharia - Centro de Biotecnologia dos Açores, by Grant BIIC M3.1.6/F/038/2009 from Direcção Regional de Ciência e Tecnologia, and by Grant SFRH/BD/8122/2002 from Fundação para a Ciência e Tecnologia. The authors thank Richard M. Twyman and Alan G Smith for critical review of the article and to Fabíola S. Gil for her technical input.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: David McCurdy
Rights and permissions
About this article
Cite this article
Monjardino, P., Rocha, S., Tavares, A.C. et al. Development of flange and reticulate wall ingrowths in maize (Zea mays L.) endosperm transfer cells. Protoplasma 250, 495–503 (2013). https://doi.org/10.1007/s00709-012-0432-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-012-0432-4