Structural and ultrastructural characterization of maize coenocyte and endosperm cellularization

Abstract

Maize coenocytic and cellularizing endosperm development were characterized at optical and transmission electron microscopy levels. Samples were collected daily in 3 consecutive years under different temperature regimes; therefore, the developmental stages were expressed on a growing degree basis. Soon after the primary endosperm nucleus is formed, it starts dividing without cytokinesis, leading to the formation of the coenocyte. The nuclei divide freely on the periphery of the coenocyte and spread from the micropylar region toward the chalazal region. The first anticlinal walls are formed as the nuclei come closer to each other, followed by periclinal wall formation also starting in the micropylar region. As cellularization proceeds, new anticlinal and periclinal walls assume a less organized pattern until the central vacuole is fully occupied by newly formed cells. Overall, our findings suggest that the developmental pattern of maize coenocytic and cellularizing endosperm has many similarities to other species of the Poaceae family.

Maize early endosperm growth and development: From fertilization through cell type differentiation

“…As the free nuclei divided, there was a progression of nuclear localization around the central vacuole from the base to the sides of the endosperm and finally throughout the periphery. The pattern of nuclear migration during formation of the initial layer of nuclei supports previous reports in maize ( Randolph, 1936 ;Monjardino et al, 2007 ), but differs from Arabidopsis. In Arabidopsis , at the 16-nuclei stage, the nuclei are throughout the length of the endosperm, and different growing conditions in these few studies (Randolph: NY fi eld; Schel et al: greenhouse; Phillips and Evans: both fi eld and greenhouse), as well as line differences (Randolph: "Pride of Michigan"; Schel et al: A-188; Phillips and Evans: W23XM14), endosperm sizes vary widely and direct comparison is diffi cult.…”

“…Reviews of cereal endosperm development (e.g., Olsen et al, 1999 ;Olsen, 2001Olsen, , 2004Brown and Lemmon, 2007 ;Sabelli and Larkins, 2009 ;Becraft and Gutierrez-Marcos, 2012 ;Olsen and Becraft, 2013 ) often depict generalized developmental models that are largely based on comprehensive accounts of nuclei proliferation, microtubular networks, and phragmoplast or wall deposition in barley, rice, and wheat, with comparison to analogous observations in Arabidopsis (e.g., Mares et al, 1975Mares et al, , 1977Morrison and O'Brien, 1976 ;Fineran et al, 1982 ;Van Lammeren, 1988 ;Mansfi eld and Briarty, 1990 ;Bosnes et al, 1992 ;Brown et al, 1994Brown et al, , 1996aBrown et al, , b , 1997Brown et al, , 1999Brown et al, , 2003Olsen et al, 1995 ;Sørensen et al, 2002 ). Though these models and descriptions are often extended to all cereals, detailed cytological accounts of the coenocyte and cellularization stages of endosperm development in maize are generally much older and more limited ( Randolph, 1936 ;Kiesselbach, 1949 ;Monjardino et al, 2007 ). Therefore, there is a need for a comprehensive evaluation of maize early endosperm development to highlight possible differences between cereals, as well as emphasize diversity in the nuclear endosperm development pathway with Arabidopsis as a comparative model.…”

“…Previous research described early endosperm size at selected ages in "Pride of Michigan" ( Randolph, 1936 ), a locally adapted yellow dent corn ( Kiesselbach, 1949 ), A-188 ( Schel et al, 1984 ), W23XM14 ( Phillips and Evans, 2011 ), and W64A ( Monjardino et al, 2007 ), but there are vast differences in these genotypes. When compared with B73, fellow founder line Mo17 has been shown to have hundreds of genes with copy differences, and almost 200 genes present in one line and not in the other ( Springer et al, 2009 ).…”

“…Transition to a cellular endosperm occurs via alveolation in both systems, beginning with the formation of anticlinal walls separating peripheral free nuclei of the coenocyte ( Bosnes et al, 1992 ;Brown et al, 1994Brown et al, , 1999Monjardino et al, 2007 ). Interaction of opposing microtubules from adjacent nuclear cytoplasmic domains brings about formation of adventitious phragmoplasts, and cell walls begin to form at the edge of the endosperm and advance inward in association with the phragmoplasts ( Brown et al, 1994 ;Olsen et al, 1995 ).…”

“…Though both cereals and Arabidopsis initiate cellularization near the embryo, there is a more pronounced gradient of alveolar development in Arabidopsis , where the chalazal endosperm cyst remains coenocytic to seed maturation ( Mansfi eld and Briarty, 1990 ;Brown et al, 1999Brown et al, , 2003. Cereal endosperms become fully cellular by continuation of alveolation until the central vacuole is fi lled with cells ( Kiesselbach, 1949 ;Bosnes et al, 1992 ;Brown et al, 1994 ;Becraft, 2001 ;Olsen, 2001 ); however, a more random pattern of cellularization of the inner central vacuole has been noted in maize ( Monjardino et al, 2007 ).…”