Selective egg cell polyspermy bypasses the triploid block

Abstract

Polyploidization, the increase in genome copies, is considered a major driving force for speciation. We have recently provided the first direct in planta evidence for polyspermy induced polyploidization. Capitalizing on a novel sco1-based polyspermy assay, we here show that polyspermy can selectively polyploidize the egg cell, while rendering the genome size of the ploidy-sensitive central cell unaffected. This unprecedented result indicates that polyspermy can bypass the triploid block, which is an established postzygotic polyploidization barrier. In fact, we here show that most polyspermy-derived seeds are insensitive to the triploid block suppressor admetos. The robustness of polyspermy-derived plants is evidenced by the first transcript profiling of triparental plants and our observation that these idiosyncratic organisms segregate tetraploid offspring within a single generation. Polyspermy-derived triparental plants are thus comparable to triploids recovered from interploidy crosses. Our results expand current polyploidization concepts and have important implications for plant breeding.

Polyspermy Block in the Central Cell During Double Fertilization of Arabidopsis thaliana

“…Angiosperms are unique to produce the two adjacent dimorphic female gametes, the egg and central cells (Li and Yang, 2020 ). Polyspermy in the egg cell risks the production of a sterile triploid plant in return for the chance of polyploidization and speciation (Toda et al, 2016 ; Nakel et al, 2017 ; Mao et al, 2020 ). Although the central cell gives rise to the nutritious endosperm after fertilization and does not contribute to the genome of the next generation, polyspermy in the central cell results in a paternal and maternal genome imbalance in the endosperm and disturbs normal seed development (Scott et al, 2008 ; Köhler et al, 2010 ).…”

“…For example, in vitro fertilization studies using isolated egg cells and sperm cells of maize ( Zea mays ) revealed that the fertilized egg cell is unable to fuse with additional sperm cells, possibly by cell wall formation following a calcium ion influx (Faure et al, 1994 ; Kranz et al, 1995 ; Antoine et al, 2000 ). Although triploid plants can be generated in vitro and in planta in several plant species due to polyspermy of the egg cell, they rarely occur under natural conditions (Toda et al, 2016 ; Grossniklaus, 2017 ; Nakel et al, 2017 ; Mao et al, 2020 ). Meanwhile, the polyspermy block mechanism in the central cell has not been studied directly to date.…”

Central Cell in Flowering Plants: Specification, Signaling, and Evolution

“…Study with the polyspermic tetraspore (tes) mutant has suggested that polyspermy block exists in egg, but not in central cell (Scott et al, 2008). Other reports suggest that the egg cell can also fuse with two sperms to form triploid embryo with the central cell fuses with one sperm cell (Grossniklaus, 2017;Mao et al, 2020). Another distinction between the central cell and the egg cell is that plasma membrane fusion with sperm can trigger central cell mitotic division, suggesting signaling link between plasmogamy and activation of the nuclear division (Aw et al, 2010).…”

Data_Sheet_1.docx

“…Angiosperms are unique to produce the two adjacent dimorphic female gametes, the egg and central cells (Li and Yang, 2020). Polyspermy in the egg cell risks the production of a sterile triploid plant in return for the chance of polyploidization and speciation (Toda et al, 2016;Nakel et al, 2017;Mao et al, 2020). Although the central cell gives rise to the nutritious endosperm after fertilization and does not contribute to the genome of the next generation, polyspermy in the central cell results in a paternal and maternal genome imbalance in the endosperm and disturbs normal seed development (Scott et al, 2008;Köhler et al, 2010).…”

“…For example, in vitro fertilization studies using isolated egg cells and sperm cells of maize (Zea mays) revealed that the fertilized egg cell is unable to fuse with additional sperm cells, possibly by cell wall formation following a calcium ion influx (Faure et al, 1994;Kranz et al, 1995;Antoine et al, 2000). Although triploid plants can be generated in vitro and in planta in several plant species due to polyspermy of the egg cell, they rarely occur under natural conditions (Toda et al, 2016;Grossniklaus, 2017;Nakel et al, 2017;Mao et al, 2020). Meanwhile, the polyspermy block mechanism in the central cell has not been studied directly to date.…”