Suspensor Length Determines Developmental Progression of the Embryo in Arabidopsis

Abstract

The first structure that differentiates during plant embryogenesis is the extra-embryonic suspensor that positions the embryo in the lumen of the seed. A central role in nutrient transport has been ascribed to the suspensor in species with prominent suspensor structures. Little is known, however, about what impact the size of the rather simple Arabidopsis (Arabidopsis thaliana) suspensor has on embryogenesis. Here, we describe mutations in the predicted exo-polygalacturonase gene NIMNA (NMA) that lead to cell elongation defects in the early embryo and markedly reduced suspensor length. Mutant nma embryos develop slower than wild-type embryos, and we could observe a similar developmental delay in another mutant with shorter suspensors. Interestingly, for both genes, the paternal allele has a stronger influence on the embryonic phenotype. We conclude that the length of the suspensor is crucial for fast developmental progression of the embryo in Arabidopsis.Annual, self-pollinating weeds such as Arabidopsis (Arabidopsis thaliana) benefit from a short life cycle in their natural ephemeral habitats (Snell and Aarssen, 2005). A rapid progression through embryogenesis is a prerequisite for early seed maturation, and it is therefore not surprising that Arabidopsis sets up its body plan already after a very limited number of cell divisions (Aarssen, 2000;Lau et al., 2012).Arabidopsis embryogenesis starts with the fertilized egg cell, the zygote, which elongates about 3-fold before it divides asymmetrically. The smaller apical cell is the founder of the embryo proper that contributes to most of the later seedling, while the larger basal cell develops into a support structure called the suspensor (Jeong et al., 2011a). The suspensor is formed by a series of transverse cell divisions followed by longitudinal cell expansion forming a stalk-like structure. Only the upper-most suspensor cell, the hypophysis, will contribute to parts of the root meristem, while the rest of the suspensor remains extraembryonic and will cease its growth at the heart stage of the embryo (Yeung and Meinke, 1993). The suspensor is thought to be important for pushing the embryo into the lumen of the seed, where the embryo is surrounded by the nourishing endosperm. In addition, a key function in nutrient and hormone transport to the embryo is assigned to the suspensor (Kawashima and Goldberg, 2010).The Arabidopsis suspensor achieves its maximum length with a minimum number of cells by having a rod-shaped structure built by a single cell file. Although several mutants with distorted or shorter suspensors have been described in Arabidopsis, little is known about what impact suspensor length has on embryo development (Schwartz et al., 1994;Vernon and Meinke, 1994;Lukowitz et al., 2004;Breuninger et al., 2008;Bayer et al., 2009;Jeong et al., 2011b).As in all plant cells, the size and shape of suspensor cells is primarily determined by the elasticity of the cell wall. While rigid cellulose microfibrils determine the direction of cell expansion, it is the p...

Direct evidence that suspensor cells have embryogenic potential that is suppressed by the embryo proper during normal embryogenesis

“…Therefore, it is supposed to be critical for the early development of the embryo (1)(2)(3)(4). The suspensor cells have characteristics of transfer cells (e.g., Phaseolus and Stellaria) (5,6) and are known to absorb and transport metabolites from the surrounding material tissue to the embryo proper (Phaseolus and Arabidopsis) (7,8).…”

Is change in ovary carbon status a cause or a consequence of maize ovary abortion in water deficit during flowering?

“…Gene functions were sorted out by following the ontologies proposed in MapMan with the maize genome release Zm_B73_5b_FGS_cds_2012 (http:// mapman.gabipd.org/web/guest/mapmanstore). Two categories were particularly analyzed and presented in Figures 5 and 6, namely genes involved in carbon metabolism (Granot et al, 2013;Yadav et al, 2014) and those involved in expansive growth, either via water transport or via cell wall mechanical properties (Cosgrove, 2005;Wolf et al, 2012;Babu et al, 2013;Xiao et al, 2014).…”

“…5A). This was the case for genes involved in cell wall mechanical properties that drive expansive growth (Cosgrove, 2005;Babu et al, 2013;Xiao et al, 2014), namely four expansins and pectinases (exopolygalacturonase). Conversely, the transcripts of genes involved in carbon metabolism showed small differences in expression between WW and WD1 plants (Fig.…”

NatA is required for suspensor development in Arabidopsis

“…16,17 The suspensor is also important for pushing the embryo into the lumen of the seed, where the embryo is surrounded by the nourishing endosperm. 18 Thus, in Arabidopsis the length and structure of the suspensor are crucial for the fast developmental progression of an embryo. 18 Suspensor cells also have embryogenic potential, which is suppressed by the embryo proper during normal embryogenesis.…”

“…18 Thus, in Arabidopsis the length and structure of the suspensor are crucial for the fast developmental progression of an embryo. 18 Suspensor cells also have embryogenic potential, which is suppressed by the embryo proper during normal embryogenesis. 19 Following embryo removal, auxin gradually accumulates in the top suspensor cell, where cell division occurs to produce a new embryo.…”