Advances in Botanical Research 28: 231-261 (1998)
Gametes, Fertilization and Early Embryogenesis in Flowering Plants
Christian Dumas, Fredéric Berger, Jean-Emmanuel Faure, Elizabeth Matthys-Rochon

A FERTILIZATION OF THE CENTRAL CELL AND DEVELOPMENT OF THE ENDOSPERM

Double fertilization is characterized by the formation of two embryos: the embryo-proper which is diploid, and the fusion product of the central cell with one male gamete which is triploid. This secondary triploid zygote develops into the endosperm (Fig. 2) (for reviews see Maheshwari, 1950; Vijayaraghavan and Prabhakar, 1984; Lopes and Larkins, 1993). In some species (e.g. cereals) the endosperm persists in seeds and stores reserves which will be mobilized during germination. In other plants, such as legumes and Brassicaceae, reserves accumulate in cotyledons and endosperm development is limited. In relation to its role in the seed, the endosperm is classically considered as a reserve tissue. However, recent results point to the fact that the endosperm is a unique organism which develops parallel to the embryo-proper and probably has a parasitic/symbiotic relationship with it (Friedman, 1992). Although the two developmental pathways are apparently very dissimilar, both zygotes share identical haplotypes since both male gametes and female gametes (the oosphere and the central cell) each derive from a common mitosis. The study of endosperm development in relation to the development of the embryo proper should thus unravel key mechanisms involved in plant morphogenesis. Various approaches towards this goal have been undertaken.

A search for archaic forms of double fertilization in non-flowering seed plants has provided thought-provoking data on the evolutionary origin of endosperm and its significance (Friedman, 1990, 1992). In parallel, knowledge of the mechanism of double fertilization has benefited from improvements in in vitro procedures (Faure et al., 1994; Mòl et al., 1995; Kranz and Dresselhaus, 1996). A renewal of interest in endosperm development has been initiated with two extensive cytological studies on potential experimental models, namely barley (Bosnes et al., 1992; Brown et al., 1994) and Arabidopsis (Mansfield and Briarty, 1990a,b). Although several mutants for endosperm development have been described (Neufer and Sheridan, 1980; Bosnes et al., 1992), our understanding of mechanisms involved in differentiating the development of both embryos issuing from double fertilization remains restricted to hypotheses. Potential relationships involved in developmental regulation remain to be uncovered. These fields of study will be reviewed in the following section.

1 Introduction

Double fertilization is a major characteristic of flowering plants (angiosperms). This complex process involves intensive cross-talk between the male gametophyte (pollen and pollen tube, respectively) with the female tissues of the pistil (e.g., stigma, style, and ovule) and the female gametophyte (embryo sac), respectively (Dresselhaus & Franklin-Tong, 2013). Development and function of male and female gametophytes are described in chapters “The evolution and patterning of male gametophyte development” by Hackenberg and Twell (this issue) and “Development and function of the flowering plant female gametophyte” by Serbes et al. (this issue). Fertilization begins with the adhesion of pollen grains at the stigma of the pistil, continues with pollen tube germination and growth toward and inside ovules, culminating in sperm cell release. This is also called the progamic phase of fertilization. Fertilization is completed by the syngamic phase after successful fusion of one sperm cell with the egg cell and the second sperm cell with the central cell, respectively.

The pollen tube is an invention of seed plants and it plays a major role in signaling during fertilization. Its main task is to deliver two sperm cells to accomplish double fertilization. Whether sperm cells themselves contribute to pollen tube growth and guidance has been a debate since many years. Mutant pollen tubes lacking sperm cells that were able to grow toward ovules were recently used to show that sperm cells are indeed dispensable for fertilization (Glöckle et al., 2018; Zhang, Huang, et al., 2017). Thus, it is the vegetative pollen tube cell that interacts and exchanges signals with the female tissues of the pistil and the embryo sac, respectively. Signaling mechanisms during fertilization therefore caused most attention during the past years to understand the various components of fertilization in angiosperms. 10 years ago, only one signaling ligand and two cell surface receptors with known functions in the final steps of double fertilization of angiosperms were known (Márton & Dresselhaus, 2008). Since then, the research community has made tremendous progress to identify molecules secreted by the pollen tube as well as the surrounding tissues, and identified a number of receptors/co-receptors as well as downstream signaling components involved in both, the progamic and syngamic phases. This research progress was regularly accompanied by reviews highlighting the progress made (e.g., Bleckmann, Alter, & Dresselhaus, 2014; Dresselhaus & Franklin-Tong, 2013; Dresselhaus, Sprunck, & Wessel, 2016; Hamamura, Nagahara, & Higashiyama, 2012; Li, Meng, & Yang, 2018; Mizuta & Higashiyama, 2018). A key finding was that some of the signaling mechanisms are specific to plant species/families, while other components are highly conserved and even occur in unicellular organisms with sexually differentiated gametes. Another important finding was that many of the components identified in the context of fertilization were previously known to play roles in defense responses and cell death, confirming previous hypothesis that reproductive signaling mechanisms may have partially evolved from ancient defense signaling mechanisms (see details below).

Hetero-Fertilization / Endosperm Failure