The evolution and patterning of male gametophyte development

Abstract

1. The evolutionary history of the male gametophyte 1.1. The origins of spermatogenesis in green plants 1.2. The sporophyte was key for terrestrial plant evolution 1.3. Heterospory and the origin of microgametophytes 1.4. Adaptations of seed plant microgametophytes 2. Male germline development in angiosperms 2.1. Asymmetric division and cell fate determination 2.2. Cell cycle control and male gametophyte patterning 2.3. Transcriptional control of male gametophyte patterning 2.4. Chromatin remodelling in male gametophyte development 2.5. Communication between non-germ and germ cells 3. Molecular evolution of the male germline 3.1. Motile plant and animal sperm share common features 3.2. Gene expression in male germ cells 3.3. The evolution of transcription factors regulating male gametogenesis 4. Perspective 5. Acknowledgements 2 6. References Abstract: The reproductive adaptations of land plants have played a key role in their terrestrial colonization and radiation. These encompass mechanisms used for the production, dispersal and union of gametes to support sexual reproduction. The production of small motile male gametes and larger immotile female gametes (oogamy) in specialized multicellular gametangia evolved in the charophyte algae, the closest extant relatives of land plants.Reliance on water and motile male gametes for sexual reproduction was retained by bryophytes and basal vascular plants, but was overcome in seed plants by the dispersal of pollen and the guided delivery of non-motile sperm to the female gametes. Here we discuss the evolutionary history of male gametogenesis in streptophytes (green plants) and the underlying developmental biology, including recent advances in bryophyte and angiosperm models. We conclude with a perspective on research trends that promise to deliver a deeper understanding of the evolutionary and developmental mechanisms of male gametogenesis in plants.

Role of Autophagy in Male Reproductive Processes in Land Plants

“…Conversely, bryophytes, lycophytes, monilophytes, and some gymnosperms such as ginkgoes and cycads utilize motile male gametes called spermatozoids, which are equipped with two or more flagella, for sexual reproduction (Southworth and Cresti, 1997;Renzaglia and Garbary, 2001). In both cases, drastic reorganization of cellular components occurs during male gamete development (Hackenberg and Twell, 2019). In the angiosperm, A. thaliana, four haploid microspores are produced by meiosis of a diploid pollen mother A B FIGURE 1 | Scheme of macroautophagy.…”

“…Spermatozoids move toward female gametes in water to accomplish fertilization (Shimamura, 2016). Although the molecular mechanisms of male reproduction in angiosperms are well-documented, molecular mechanisms of spermatozoid formation in basal land plants remain mostly ambiguous (Hackenberg and Twell, 2019).…”

Characterization of evolutionarily conserved key players affecting eukaryotic flagellar motility and fertility using a moss model

“…In the unicellular algal model organism Chlamydomonas reinhardtii flagella are responsible for motility of the organism and serve during sexual reproduction to mediate a species-specific adhesion between two cells of different mating types (van den Ende et al 1990). In streptophyte algae (Streptophyta comprise charophycean green algae as well as land plants), male gametes (spermatozoids) are the only motile cells of sessile multicellular algae, swimming to the oogonia to fertilize the egg cell (Hackenberg et al 2019, McCourt et al 2004. After the water-to-land-transition of plants this system was retained, i.e.…”

MYB81, a microspore‐specific GAMYB transcription factor, promotes pollen mitosis I and cell lineage formation in Arabidopsis

“…Phylogenetic analysis has revealed that the R2R3 S18 GAMYB family is sister to the DUO1 R2R3 MYB family (Du et al , ; Higo et al , ). The GAMYB and DUO1 R2R3 MYB family are clearly separated in moss and liverworts, with DUO1 directing male germline development and the GAMYB clade specializing male reproductive roles in angiosperms (Higo et al , ; Hackenberg and Twell, ).…”