Twin Plants from Supernumerary Egg Cells in Arabidopsis

Abstract

Sexual reproduction of flowering plants is distinguished by double fertilization—the two sperm cells delivered by a pollen tube fuse with the two gametic cells of the female gametophyte, the egg and the central cell—inside the ovule to give rise to the embryo and the nutritive endosperm, respectively. The pollen tube is attracted by nongametic synergid cells, and how these two cells of the female gametophyte are specified is currently unclear. Here, we show that ALTERED MERISTEM PROGRAM 1 (AMP1), encoding a protein associated with the endoplasmic reticulum, is required for synergid cell fate during Arabidopsis female gametophyte development. Loss of AMP1 function leads to supernumerary egg cells at the expense of synergids, enabling the generation of dizygotic twins. However, if twin embryos are formed, endosperm formation is prevented, eventually resulting in ovule abortion. The latter can be overcome by the delivery of supernumerary sperm cells in tetraspore (tes) pollen, enabling the formation of twin plants. Thus, both primary and supernumerary egg cells are fully functional in amp1 mutant plants. Sporophytic AMP1 expression is sufficient to prevent cell-fate change of synergids, indicating that one or more AMP1-dependent mobile signals from outside the female gametophyte can contribute to its patterning, in addition to the previously reported lateral inhibition between gametophytic cells. Our results provide insight into the mechanism of synergid fate specification and emphasize the importance of specifying only one egg cell within the female gametophyte to ensure central-cell fertilization by the second sperm cell.

The small molecule hyperphyllin enhances leaf formation rate and mimics shoot meristem integrity defects associated with AMP1 deficiency

“…It could also be used to further dissect the diverse roles of AMP1 in plant development by manipulating AMP1 activity in a spatially and temporally controlled manner. Moreover, it will be interesting to test to what extent HP is able to modulate other AMP1-dependent processes including egg cell fate determination, somatic embryogenesis, or ABA-mediated abiotic stress resistance (Mordhorst et al, 1998;Shi H et al, 2013;Kong et al, 2015). In case HP does not act on AMP1 directly, it may serve as a useful agent in search for additional components of the AMP1-regulatory pathway.…”

“…Additional phenotypes of amp1 in seemingly unrelated processes were described including constitutive photomorphogenesis, ecotype-dependent alterations in germination and flowering time (Chaudhury et al, 1993;Lee, 2009;Griffiths et al, 2011), synergid to egg cell conversion in the embryo sac (Kong et al, 2015), suspensor proliferation in the presence of an intact embryo (Vidaurre et al, 2007), increased capacity for somatic embryogenesis (Mordhorst et al, 1998), and elevated abiotic stress resistance (Shi H et al, 2013;Yao et al, 2014).…”

Patterning the Female Gametophyte of Flowering Plants

“…However, they differ markedly with respect to nuclear position: While synergid nuclei characteristically localize toward the proximal cell pole, the egg cell nucleus occupies the distal portion of the cell. In all mutants described thus far exhibiting a reprogramming of synergids into egg cells (Groß-Hardt et al, 2007;Pagnussat et al, 2007;Moll et al, 2008;Kirioukhova et al, 2011;Kong et al, 2015), the identity switch is strictly correlated with a shift in nuclear position. Nuclear position can thus serve as an important diagnostic feature and supports the notion that egg cell ablation induces an identity shift in synergids.…”

“…Another mutant that can be reconciled with a shift or misinterpretation of the micropylar-chalazal axis is altered meristem program1 (amp1), which differentiates fully functional egg cells at the expense of synergid cells (Kong et al, 2015). Notably, the defect can be complemented by sporophytic AMP1 expression, suggesting the presence of a mobile factor generated in the maternal ovule tissue, which represses egg cell identity in synergids (Kong et al, 2015).…”

“…Notably, the defect can be complemented by sporophytic AMP1 expression, suggesting the presence of a mobile factor generated in the maternal ovule tissue, which represses egg cell identity in synergids (Kong et al, 2015). wyrd mutants are defective in a putative Arabidopsis ortholog of the inner centromere protein (INCENP) and also exhibit a reprogramming of one or two synergids into egg cells and defects in central cell differentiation .…”