Pattern formation in miniature: the female gametophyte of flowering plants

Abstract

SummaryPlant reproduction involves gamete production by a haploid generation, the gametophyte. For flowering plants, a defining characteristic in the evolution from the 'naked-seed' plants, or gymnosperms, is a reduced female gametophyte, comprising just seven cells of four different types -a microcosm of pattern formation and gamete specification about which only little is known. However, several genes involved in the differentiation, fertilization and post-fertilization functions of the female gametophyte have been identified and, recently, the morphogenic activity of the plant hormone auxin has been found to mediate patterning and egg cell specification. This article reviews recent progress in understanding the pattern formation, maternal effects and evolution of this essential unit of plant reproduction. Key words: Embryo sac, Gametophyte, Flowering plant, Reproduction, Gametes IntroductionThe life cycle of land plants involves an alternation of generations between a haploid gametophyte (see Glossary, Box 1) and a diploid sporophyte (see Glossary, Box 1). Whereas animal gametes are formed directly after meiosis, plant gametes are produced only after growth of the multicellular haploid gametophyte. The morphological complexity of the haploid generation ranges from the macroscopic moss gametophytes, which dwarf the sporophyte, to the three-celled male gametophyte (pollen) and seven-celled female gametophyte (embryo sac) that are characteristic of most flowering plants (Maheshwari, 1950). The latter evolved through an extreme reduction from the female gametophytes of the gymnosperms (see Glossary, Box 1), which frequently contain over a thousand cells, and is considered a key innovation in the evolution of flowering plants (reviewed by Friedman and Williams, 2003). These 'stripped down to essentials' female gametophytes confer two major defining characteristics of the flowering plants. First, they are small enough to be packaged within an ovary. Second, they generate two gametes that undergo double-fertilization to produce the nutritive tissue called endosperm concordantly with the embryo, which allows more efficient resource allocation to fertilized seeds (reviewed by Raghavan, 2003). The reduced female gametophyte of flowering plants enabled much more rapid seed setting (i.e. the production of seeds during reproductive growth) than is possible in gymnosperms, allowing for habitat adaptations that require short reproductive cycles and facilitating the expansion of flowering plants into diverse ecological niches.Despite the crucial importance of the female gametophyte of flowering plants, much remains to be learnt about its development and overall biology, partly because it is a highly inaccessible structure. The past few years, however, have seen some exciting progress in the field. Here, we focus primarily on the female gametophyte of the model plant Arabidopsis, which has been studied more extensively than that of other plants, and review recent advances in the understanding of the patterning, the maternal e...

Plant germline formation: common concepts and developmental flexibility in sexual and asexual reproduction

“…The exact position of nuclei within the syncytium may thus be an important factor for cell specification during cellularization (Sundaresan and Alandete-Saez, 2010;Sprunck and Gross-Hardt, 2011). It is also evident that variations in this developmental pattern exist: while megasporogenesis typically leads to a single surviving one-nucleate FMS (monosporic megasporogenesis), failures in cell plate formation after meiosis I or after both meiotic divisions can lead to two-or four-nucleate FMSs, developmental patterns referred to as bisporic or tetrasporic megasporogenesis, respectively (Maheshwari, 1950;Willemse and Went, 1984;Haig, 1990;Huang and Russell, 1992;Drews and Koltunow, 2011).…”

“…How cell fate acquisition is regulated and when cell fate is determined during this process is still largely unclear. It has been proposed that positional information might be involved in the determination of cell fate (Grossniklaus and Schneitz, 1998;Sundaresan and Alandete-Saez, 2010;Sprunck and Gross-Hardt, 2011;Lituiev and Grossniklaus, 2014). During the syncytial phase, nuclei migrate and occupy predefined positions in the female gametophyte.…”

Theoretical and experimental evidence indicates that there is no detectable auxin gradient in the angiosperm female gametophyte

“…Therefore, it was proposed that the phytohormone auxin is distributed in a gradient and serves as the morphogen driving cell specification in the Arabidopsis FG ( Fig. 1) (Pagnussat et al, 2009;Sundaresan and Alandete-Saez, 2010).…”

Female gametophytic cell specification and seed development require the function of the putativeArabidopsisINCENP orthologWYRD

“…Although genetic and molecular approaches have identified many factors involved in male and female gametophyte development (for reviews, see Borg et al, 2009;Brukhin et al, 2005;Dresselhaus and Marton, 2009;Kägi and Gross-Hardt, 2007;Liu and Qu, 2008;Sundaresan and Alandete-Saez, 2010;Yadegari and Drews, 2004;Yang et al, 2010) and maternal effects on seed formation (for reviews, see Berger and Chaudhury, 2009;Grossniklaus, 2005;Huh et al, 2008;North et al, 2010), the molecular processes underlying cell specification and differentiation are still poorly understood. Only a small number of genes involved in the cellular differentiation of gametophytic cell types has been described.…”