Abstract
Key message
Comparative genetics and genomics among green plants, including algae, provide deep insights into the evolution of land plant sexual reproduction.
Abstract
Land plants have evolved successive changes during their conquest of the land and innovations in sexual reproduction have played a major role in their terrestrialization. Recent years have seen many revealing dissections of the molecular mechanisms of sexual reproduction and much new genomics data from the land plant lineage, including early diverging land plants, as well as algae. This new knowledge is being integrated to further understand how sexual reproduction in land plants evolved, identifying highly conserved factors and pathways, but also molecular changes that underpinned the emergence of new modes of sexual reproduction. Here, we review recent advances in the knowledge of land plant sexual reproduction from an evolutionary perspective and also revisit the evolution of angiosperm double fertilization.
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Introduction
The land is covered by green plants such as bryophytes, ferns, and seed-bearing plants. They have improved the environment for other organisms (e.g., more oxygen, temperate climates, and balanced O2–CO2 levels), and animals, including humans, can live on land due to its successful conquest by plants (Dahl and Arens 2020). The terrestrialization of plants was a long process, during which plants have undergone many innovations, including evolution of land plant-type cell walls with phragmoplasts, more control over plastids by the nucleus, the haplodiplontic life cycle (both gametophytic and sporophytic stages are multicellular), and new tissue/organ systems such as vasculature, the leaf, root, pollen, seed and flowers (Pires and Dolan 2012; Rensing 2018). The vascular system functions as the means to transport resources such as water and nutrients to different parts of the plant, including leaves that provide more surface area for photosynthesis.
In particular, features associated with sexual reproduction like pollen, seeds, and flowers have helped terrestrialization. Evolution of the pollen grain and the formation of flowers have increased the range of environments over which fertilization can occur efficiently. The evolution of seeds extended the scope for dispersing offspring in time and space as they could survive for longer periods, until conditions were favorable for germination and were able to spread in novel ways. In seed-bearing plants such as gymnosperms and angiosperms (flowering plants), sperm cells are encapsuled in the pollen grain that protects them until they reach the female. After pollination, an extruded tube from the pollen grain conveys male gametes to female gametes, thus allowing fertilization without environmental water. Compared to gymnosperms, a further innovation occurred in angiosperms; an additional fertilization besides that of the egg cell occurs to initiate the development of an embryo nourishing tissue, called the endosperm. This phenomenon is generally termed “double fertilization” and this simultaneous development of the endosperm alongside the embryo ensures the proper allocation of nutrients for the successful generation of offspring.
Rapid collection of genomic resources from many species spanning not only land plants but also green algae (Wong et al. 2019) enable us to revisit the relationship between reproductive phenotype and genotype from an evolutionary perspective. Furthermore, the emergence of a new dioecious model plant, Marchantia polymorpha, for molecular dissection (Bowman et al. 2017) has accelerated our understanding of sexual reproduction in early diverging land plants. These new data bridge accumulated knowledge in different species and have further elucidated land plant evolution. In this review, we introduce our current understanding of land plant fertilization from an evolutionary perspective. Especially, recent updates on regulation of sperm morphogenesis, fertilization processes, and the mystery of the evolution of double fertilization in angiosperms, are highlighted. The evolution of gametogenesis in land plants (Hackenberg and Twell 2019; Hisanaga et al. 2019) and flowers (Simonini and Østergaard 2019; Woźniak and Sicard 2018) has been reviewed elsewhere.
Changes in the sperm cell
The transition of the mode of sexual reproduction has been intensively studied in the Chlorophyta, the sister group to the Streptophyta (the land plant lineage of green plants) (Fig. 1). The Chlorophyta show a sequential shift from isogamy to anisogamy to oogamy (Mori et al. 2015; Umen and Coelho 2019). Isogamous species reproduce via fusion of two motile gametes of similar size and morphology. Anisogamous species have two motile gametes dissimilar in size, and oogamous species generate a large, sessile female gamete and a smaller, motile male gamete. Transition from isogamy to anisogamy to oogamy is correlated with an increase in size and complexity of the genome as well as a transition from unicellular to multicellular species among the Chlorophyta (Fang et al. 2017; Herron et al. 2010; Nozaki et al. 2014). One important characteristic of oogamous species is the evolution of specialized female organs that provide an environment where the sessile egg cell is maintained and protected maternally and is fertilized internally. These provide controlled conditions where the development of the zygote can be supported maternally against environmental and natural threats, increasing the chance of survival (Fernando et al. 2010; Gasser and Skinner 2019; Hackenberg and Twell 2019; Nishiyama et al. 2018).
Streptophyte algae also show a transition from isogamy to oogamy (Fig. 1); however, the evolution of this group is not yet clear. One of the most early diverging streptophyte algal groups, the Mesostigmatophyceae, is unicellular (Lemieux et al. 2007) and appears to sexually reproduce via isogamy (Mori et al. 2015). Another early diverging streptophyte algal group, the Chlorokybophyceae, has genes involved in meiosis, suggesting sexual reproduction in its sole species (Wang et al. 2020). It still remains unknown what type of gametes it produces. The Charophyceae, a more complex, multicellular group, reproduce via oogamy with biflagellate sperm fertilizing a sessile egg cell present inside an oogonium, which is more complex than that of Chlorophyceae (Graham and McBride 1979; Nishiyama et al. 2018). Oogamy has been maintained in the Coleochaetophyceae and the early diverging land plants such as bryophytes and ferns (Cove and Knight 1993; Graham and McBride 1979; Lopez-Smith and Renzaglia 2008; Nishiyama et al. 2018).
Due to land plant-like features such as three-dimensional growth, and the presence of plasmodesmata and oogamy, the Charophyceae was thought to be the sister group to land plants (Evert and Eichhorn 2013). With the accumulation of molecular and genomic information, the Zygnematophyceae is now considered as the closest lineage to land plants (Cheng et al. 2019; Wickett et al. 2014; Wodniok et al. 2011). Although the loss of flagellated gametes in the Zygnematophyceae (Fig. 1) is still puzzling, the study of the DUO POLLEN 1 (DUO1) gene shed light on this enigma. DUO1 is a MYB-domain transcription factor (Rotman et al. 2005) that controls sperm morphogenesis in land plants (Borg et al. 2011; Higo et al. 2018). Gene duplication and neo-functionalization of an ancestral MYB transcription factor occurred in the common ancestor to the Charophyceae, Zygnematophyceae, and land plants, and led to the innovation of DUO1 (Fig. 1). DUO1 orthologs are present in land plants (Brownfield et al. 2009) as well as oogamous Charophyceae species, but not in early diverging streptophyte algae Mesostigma viride and Klebsormidium flaccidum (Higo et al. 2018). Although the precise function of DUO1 in these algae is still not clear, DUO1 coincides with sperm morphogenesis (i.e., spermatid formation) and Chara DUO1 can partly function as DUO1 in Marchantia (Higo et al. 2018). Interestingly, DUO1 is also present in the Zygnematophyceae; however, its expression is minimized and the key amino acid residues of the MYB DNA binding domain have been intensively altered. These changes in DUO1 in the Zygnematophyceae may account for their loss of sperm morphogenesis and may have led to conjugation reproduction (Higo et al. 2018; Hisanaga et al. 2019). In contrast to these insights into sperm morphogenesis, how female gametes in the Streptophyta became sessile is still unclear.
It is estimated that the conquest of land by ancient green plants was achieved ~ 470–515 MYA (Harris et al. 2020). Early diverging land plants show oogamy with motile sperm which require conditions wet with environmental water for sperm to swim for fertilization. The number of flagella on sperm in ferns has increased (> 40) compared to (biflagellate) sperm in bryophytes. This increased number of flagella in ferns aids fertilization by helping sperm penetrate venter canal cells of the archegonium and thus reach the egg cells (Lopez-Smith and Renzaglia 2008; Southworth and Cresti 1997). During the evolution of seed-bearing plants, a game-changing innovation occurred: the generation of the pollen grain and tube (Fernando et al. 2010; Friedman 1993). In seed-bearing plants, sperm cells are encapsulated in the pollen grain, which is conveyed to a female organ via wind, insects, or self-pollination. Once the pollen grain lands on the female organ, a pollen tube extrudes from the grain and delivers sperm cells to the female gametophyte for fertilization; thus, environmental water is no longer required. Early diverging gymnosperms such as Ginkgo biloba and cycads still produce flagellated sperm in the pollen (Southworth and Cresti 1997). In these species, the extended pollen tube discharges sperm into secreted fluid near the egg cell and sperm, with numbers of flagella ranging from up to 1,000 in Ginkgo and 40,000 in cycads, swim a short distance within the fluid for fertilization (Southworth and Cresti 1997). Sperm cells in later-diverging gymnosperms such as Gnetum gnemon, Ephedra nevadensis, and conifers are not motile, possibly displaying an evolutionary change in sperm from motile to non-motile (Fig. 2).
The terrestrial conquest by angiosperms has covered many different environments around the globe with a vast number of species. This success was possible in part due to advances in reproductive mechanisms including the innovation of flowers and the internalization of ovules into maternal tissues (Baum and Hileman 2018; Specht and Bartlett 2009). Formation of flowers has led to evolution of flower-pollinator interactions, which greatly enhanced sexual reproduction efficiency. The harboring of ovules in carpels provides them further protection from the environment and predators (Simonini and Østergaard 2019). Sperm cells in all angiosperms are immotile and are transported directly to the female gametophyte by the pollen tube. In Arabidopsis thaliana, two sperm cells along with the vegetative nucleus in the pollen tube form the male germ unit that is conveyed to the female gametophyte for fertilization.
Although DUO1 in Marchantia clearly has essential functions in sperm morphogenic processes such as flagella formation and chromatin condensation (Higo et al. 2018), angiosperm sperm cells do not generate flagella, raising the question of how DUO1 is involved in sperm morphogenesis in angiosperms. The analysis of DUO1 downstream target genes (Borg et al. 2011) as well as investigation of DUO1s binding to cis-elements (Higo et al. 2018) showed that the DUO1 gene regulatory network evolved concomitantly with changes in the mode of sperm delivery in land plants. In Marchantia, genes encoding components of the flagella and motility apparatus, as well as protamine-like proteins for chromatin condensation, are under DUO1 control. Flowering plants have lost these genes and, instead, have incorporated new targets involved in gamete attachment (GEX2) and fusion (HAP2/GCS1) (see Plasmogamy section for details) (Higo et al. 2018). A sperm-specific histone (H3.10) (Ingouff et al. 2010), important for epigenetic memory reset (Borg et al. 2020), has also been integrated into the DUO1 network.
Evolution of double fertilization
Double fertilization in angiosperms was first discovered by Guignard (1899), Nawaschin (1898). One sperm cell fuses with the egg cell to form an embryo while the other fuses with the central cell forming the endosperm, which provides nourishment to the developing embryo (Shin et al. 2020). Thus, in angiosperms, nutrient supply becomes dependent on the second fertilization that happens only after the egg cell has been successfully fertilized, allowing plants to focus nutrient/energy allocation only on viable offspring. Interestingly, orchids in general produce tiny seeds compared to other angiosperms, and a significant reduction of the endosperm has been observed. In some orchid species, there is no sign of endosperm development from the fertilized central cell (Kolomeitseva et al. 2020). These species likely underwent a different evolutionary direction in sexual reproduction and further molecular characterizations will provide a better insight into their embryo and seed development.
Differing ploidy levels have been observed among angiosperm endosperms. Diploid (maternal to paternal = 1:1) endosperm is seen in the Nymphaeaceae (basal angiosperm) and Onagraceae (eudicot) (Baroux and Grossniklaus 2019; Williams and Friedman 2002). Species of the basal angiosperm Amborellaceae and also Arabidopsis thaliana are triploid (maternal to paternal = 2:1) (Baroux and Grossniklaus 2019; Kordyum and Mosyakin 2020). Maternal to paternal genomic content of the endosperm guides how nourishment is provided and used. Seeds with higher paternal to maternal ratios in their endosperms selfishly and aggressively derive more nutrition from the maternal sporophyte, causing defects in other developing embryos (Friedman and Ryerson 2009). While endosperm ploidy could be thought to have contributed to the direction of endosperm development, there is no obvious correlation with angiosperm evolution. Endosperm ploidy differences among different taxa could simply be attributed to the difference in embryo sac development (i.e., the number of polar nuclei) (Baroux et al. 2002; Kordyum and Mosyakin 2020). Further analyses are needed to further understand endosperm ploidy from an evolutionary perspective.
In gymnosperms, different forms of double fertilization have been observed (Fig. 2). In the order Gnetales, the female gametophyte of Ephedra contains two egg cells. Each egg cell is binucleate with a venter canal nucleus and egg nucleus. After the release of the binucleate sperm cell from the pollen tube, the two sperm nuclei enter the egg cell. One sperm nucleus fuses with the venter canal nucleus to form a supernumerary zygote while the other fuses with the egg nucleus. Both fused nuclei start to develop an embryo; thus, two embryos are formed per egg cell (polyembryony). Only one of the developing embryo matures while the other degenerates (Carmichael and Friedman 1996; Friedman and Carmichael 1996). A rudimentary polyembryony type of double fertilization has also been observed in Gnetum gnemon where the functional female gametophyte does not contain an egg cell per se but has a cell with free nuclei that act as individual gamete nuclei. During fertilization, each of the two sperm nuclei released from the pollen tube can fertilize any two free nuclei in their vicinity to form two zygotes. Ultimately, only one embryo survives at the end of seed maturation (Carmichael and Friedman 1996; Friedman and Carmichael 1996). In Welwitschia mirabilis, the micropyle-most cells form tubular projections called prothalial tubes. The egg nuclei are carried in the prothalial tubes, which protrude into the nucellus, to meet the incoming pollen tube. Each prothalial tube carries two to three egg nuclei and one of the two sperm released from the pollen tube enters the prothalial cell and fertilizes an egg nucleus. In some rare conditions, double fertilization happens from a single pollen tube but generally only one sperm nucleus fuses with the egg nucleus while the other remains outside the prothalial cell (Friedman 2015).
In the early diverging gymnosperms, such as Ginkgo and cycads, two motile flagellated sperm are released from the pollen tube into the archegonium but only one sperm fertilizes the egg to form a zygote. Like in Ginkgo and cycads, double fertilization is not observed in the Pinaceae. In the Pinaceae, one ovule contains many archegonia and each archegonium harbors an egg cell that contains the egg nucleus and venter canal cells. A pollen tube reaches each archegonium, grows through the venter canal cell, ruptures it and releases two sperm nuclei. The leading sperm nucleus fuses with the egg nucleus, forming a proembryo. The other sperm nucleus deteriorates (Runions and Owens 1999). More than one embryo starts to develop from each fertilized egg cell in each ovule, but only one survives and matures as the others undergo programmed cell death (Filonova et al. 2002).
Although the end products are supernumerary zygotes/embryos, the second fertilization does therefore exist in gymnosperms (Fig. 2). Based on the current understanding of gymnosperm evolution (Fig. 2), the presence of “double fertilization” events in Gnetales and angiosperms is likely the result of convergent evolution and several hypotheses have been made to relate them to the origin of angiosperm double fertilization. One is that formation of the supernumerary embryo could be the key to the origin of the endosperm in the ancestral angiosperm and that a supernumerary embryo took on the function of embryo nourishing tissue. As it otherwise degenerates, like in Ephedra, one of the embryos instead might have become altruistic and switched its role to support its twin embryo’s development. Another hypothesis is that the origin of the angiosperm endosperm was not the supernumerary embryo and the fertilization process happened to be incorporated into an already existing embryo nourishing tissue. In the case of Gnetum and Welwitschia, free nuclei are present at the chalazal end of the developing female gametophyte and provide nourishment to the embryo (Baroux and Grossniklaus 2019; Friedman 2015; Friedman and Carmichael 1996; Wang et al. 2014). This chalazal tissue with free nuclei becomes cellularized later, resembling the development of the endosperm in angiosperms. In Arabidopsis, the initiation of endosperm development can be independent of the fertilization event (Hands et al. 2016). Many different types of cells accept sperm at the time of fertilization in extant gymnosperms (Carmichael and Friedman 1996; Friedman 2015; Friedman and Carmichael 1996), thus incorporation of the fertilization process into a non-gametic cell appears not so uncommon. There are several key factors essential for fertilization processes such as gamete attachment and fusion, that underwent regulatory network rewiring during land plant evolution (see Changes in Sperm Cells section for details). In either scenario, such rewiring of gene regulatory networks (Halfon 2017; Lai et al. 2020) should play a major role in the origin of angiosperm double fertilization. Comparing gene regulatory networks that control egg cell and central cell fertilization will further elucidate the evolutionary events that determined the angiosperm central cell’s fate to be sexual.
One of the key pre-requisites for the innovation of double fertilization may be the presence of two male gametes in one pollen grain. Two sperm are also present in one pollen grain in gymnosperms and the incorporation of an additional mitotic division prior to sperm morphogenesis likely occurred before the divergence and gymnosperms and angiosperms. In early diverging land plants such as Marchantia and ferns, sperm morphogenesis coincides with the mitotic division of spermatid mother cells, and in Arabidopsis, major gene regulatory pathways controlling sperm differentiation and mitotic division are interlinked (Hackenberg and Twell 2019). More elucidation on the male side of reproductive evolution including the relationship between divisions and morphogenesis should shed light on the evolution of angiosperm double fertilization.
Fertilization mechanism
Plasmogamy
Discovery of GAMETE EXPRESSED 2 (GEX2) in Arabidopsis sperm cells localized on the plasma membrane (Mori et al. 2014) provided insights into the adhesion of the sperm cell membrane with that of the egg cell. GEX2 protein contains a filamin-like domain. A filamin-like domain is also present in FUS1 protein of Chlamydomonas where it helps in adhesion of two mating types to complete fertilization (Mori et al. 2014). A gene encoding a protein with a filamin-like domain is also found in Selaginella (Maruyama et al. 2016), and the GEX2 homolog in Zea mays is important for fertilization (Mori et al. 2014; Warman et al. 2020). In Arabidopsis, DUO1 controls the expression of GEX2 and GEX2 is specifically found on the male germ cells (Maruyama et al. 2016; Sprunck 2020). Sperm cell specific expression of GEX2 was also observed in rice (Sharma et al. 2011) and GEX2 promoters in angiosperms contain several DUO1 binding motifs (Higo et al. 2018), implying the incorporation of GEX2 in the DUO1 regulatory network predates the divergence of monocots and eudicots.
HAPLESS 2 (HAP2)/GENERATIVE CELL SPECIFIC 1 (GCS1) encodes a transmembrane protein that is specifically expressed in the gametes and essential for the gamete membrane fusion process. The mutant phenotype of HAP2 was first discovered in a genetic screen of Arabidopsis that identified haploid disrupting (hapless) mutations of pollen development and function (Johnson et al. 2004). Independently, a strongly expressed sperm-specific GCS1 transcript was identified and shown to accumulate in the plasma membrane of generative cells of Lilium longiflorum (Mori et al. 2006). In their seminal study, Mori et al. identified that gcs1 mutant sperm cells failed to fuse with the female gametes in Arabidopsis and also recognized that homologs are found in rice and, further afield, in green and red algae, social amoeba and protists including Plasmodium falciparum (Mori et al. 2006). von Besser et al. (2006) identified that HAP2 is allelic with GCS1.
HAP2/GCS1 is redistributed from the sperm cell endomembrane system to the cell surface in response to the release of small Egg Cell 1 (EC1) proteins by the egg cell in Arabidopsis (Sprunck et al. 2012). EC1-like proteins are found in flowering plants, including basal angiosperm Amborella trichopoda, but not in gymnosperms, ferns or bryophytes (Sprunck et al. 2012). Mutant analyses confirmed that, once on the sperm cell membrane, HAP2/GCS1 has a role in the fusion of the gamete membranes rather than attachment to them as hap2/gcs1 sperm cells were able to adhere to Arabidopsis female gametes but membrane fusion did not occur (Mori et al. 2014). Attachment of gametes, bringing membranes within 10 nm of each other, is a prerequisite for fusion (Sprunck 2020). HAP2’s function as a fusogen was confirmed by its ability to cause fusion in heterologous systems (Valansi et al. 2017).
The ancient origins of HAP2/GCS1 became even clearer following X-ray crystallographic structural studies. HAP2 of Chlamydomonas has a conserved fold similar to viral class II fusogens (Fédry et al. 2017). Based on well-studied viral fusogens (Fedry et al. 2018), HAP2 is proposed to trimerize and undergo a conformational shift driving membrane bending and pore formation during plasmogamy. HAP2s in various eukaryotes have a fusion loop or loops that is/are inserted into the lipid bilayer during membrane fusion. In the protozoan Trypanosoma cruzi, the three loops that are suggested to contact the female gamete contain nonpolar residues and are expected to interact together. In Arabidopsis, while the same three loops are present, one of them, containing an amphipathic helix, protrudes beyond the others and would be expected to enter the female gamete membrane (Fedry et al. 2018). While the overall fold of HAP2 is thought to be well conserved, based on amino acid alignment further differences are seen in the residues of the prominent surface loops and their helices among different flowering plants. Larger differences are found among Selaginella moellendorffii, Physcomitrium patens, and Marchantia (Fedry et al. 2018). These structural differences have been suggested to have evolved as those organisms diverged (Fedry et al. 2018) and, as well as those found in Chlamydomonas (Baquero et al. 2019; Feng et al. 2018), could relate to differences in the membranes and proteins they interact with. Further, detailed investigations of the changes in interactions of HAP2, if any, that have occurred during evolution and speciation are awaited. Genes involved in reproduction and responsible for speciation evolve relatively quickly (Swanson and Vacquier 2002). Interestingly, comparing the relative divergence of Arabidopsis and the closely related A. lyrata, HAP2/GCS1 evolved more slowly than the GEX2 gene for gamete attachment (Mori et al. 2014). Maybe attachment genes evolve faster than those involved in fusion and are more usually responsible for speciation (Mori et al. 2014). Even if so, how the structural changes that have evolved in HAP2 may account for speciation remains to be explored in detail.
Sperm membrane proteins DUF679 DOMAIN MEMBRANE PROTEIN 8 and 9 (DMP8/9) are other key regulators of sperm-egg cell fusion in Arabidopsis (Cyprys et al. 2019; Takahashi et al. 2018). Like HAP2/GCS1 and GEX2, at least DMP9 is regulated by DUO1 (Borg et al. 2011), and dmp8/dmp9 mutants show a defect in fertilization, yet with normal sperm-egg cell adhesion, indicating their functions particularly in the egg-sperm fusion. DMP9 orthologs are present in Chlamydomonas (Ning et al. 2013), which suggests that there are conserved DMP8/9 sperm-egg cell interaction pathways among green plants. Interestingly, dmp8/9 mutants show no or minimal effect on sperm-central cell fusion (Cyprys et al. 2019; Takahashi et al. 2018). These findings indicate that the fertilization process between the egg and central cells are not exactly the same, and these differences might be contributing to the stronger polyspermy block observed in the egg cell compared to the central cell (Nagahara et al. 2021; Scott et al. 2008).
Gamete nuclear migration
In most animals, not only the sperm pronucleus, but also the sperm centrioles are delivered to the fertilized egg. The inheritance of paternal centrioles has been also observed in brown algae (Nagasato 2005; Nagasato et al. 1999) and these sperm derived centrioles generate a centrosome, which then establishes a microtubule sperm aster that facilitates pronuclear migration for the completion of fertilization. The importance of microtubules for pronuclear migration has been evident genetically and pharmacologically (Fatema et al. 2019). Likewise, early diverging land plants such as bryophytes and ferns produce flagellated motile sperm, and pharmacological studies using a fern, Marsilea vestita, suggested the important role of microtubules in early events of fertilization including gamete nuclear migration (Kuligowski et al. 1987, 1985). Flowering plants, on the other hand, have evolved non-motile sperm cells and have lost components essential to centriole organization (Carvalho-Santos et al. 2011), raising the question of how do flowering plants control gamete nuclear migration for fertilization? Pharmacological studies in rice, tobacco, and maize show that microtubules are dispensable and, instead, F-actin plays the critical role in sperm nuclear migration (Ohnishi et al. 2014; Peng et al. 2017). This was confirmed by genetics in Arabidopsis (Kawashima et al. 2014). Interestingly, F-actin in the female gamete cells generate constant inward movement prior to fertilization: F-actin is assembled at the plasma membrane periphery and migrates toward the center of the cell where the female nucleus resides (Fig. 3a). Upon sperm delivery to the female gamete cell, the sperm nucleus starts moving, together with F-actin, for karyogamy.
In Arabidopsis, the small Rho GTPase of plants 8 (ROP8) controls the dynamic F-actin inward movement in the central cell (Fig. 3b) (Kawashima et al. 2014). ROPs are associated with the plasma membrane and activate the WAVE/SCAR signaling pathway that controls cytoskeleton organization (Craddock et al. 2012; Uhrig et al. 2007). For somatic F-actin dynamics, WAVE/SCAR relays to ARP2/3 and activates branching of F-actin in vitro (Frank et al. 2004; Zhang et al. 2008) and in trichomes (Basu et al. 2005; Zhang et al. 2005). Very recently, it has been discovered that SCAR2 plays a role in the F-actin inward movement in the central cell, and surprisingly, that not ARP2/3, but another actin nucleator group, formin, is involved in this process (Fig. 3b) (Ali et al. 2020; Ali and Kawashima 2021). These data show that there is a novel gametophyte-specific ARP2/3-independent WAVE/SCAR signaling pathway, controlling fertilization processes. In addition, the class XI myosin, XI-G was identified to play an important role in the F-actin inward movement in the Arabidopsis central cell (Fig. 3b) (Ali et al. 2020). Class XI myosins in plants walk on F-actin and transport molecules and organelles as cargo (Duan and Tominaga 2018). In the central cell, XI-G appears to generate forces to move F-actin per se. This action is independent from the organelle movement function of myosins (Ali et al. 2020), indicating a novel non-canonical class XI myosin function in the female gametophytic cell.
All factors identified for sperm nuclear migration in Arabidopsis (i.e., ROP8, SCAR2, and XI-G) are from the central cell (Ali et al. 2020; Kawashima et al. 2014); however, the egg cell also requires proper sperm nuclear migration for successful fertilization. Furthermore, the function of WAVE/SCAR and myosin is also important in the egg cell (Ohnishi et al. 2014; Peng et al. 2017). Because the expression of ROP8 and XI-G are not detected in the egg cell (Ali et al. 2020; Kawashima et al. 2014), the simplest scenario is that other members of ROP, SCAR, and myosin XI are responsible for sperm nuclear migration in the egg cell. If this is the case, another interesting question would arise: what are the biological and evolutionary reasons why the egg and central cells utilize different members of factors for the same function? The fertilization processes of the egg and central cells are also different, like in the case of DMP8/9 (see Plasmogamy section for details). Understanding the evolutionary changes in these factors in the egg and central cells will also elucidate the origin of angiosperm double fertilization.
Karyogamy
After sperm nuclear migration, fusion of gamete nuclei (karyogamy) takes place, ending fertilization and initiating embryo and endosperm development in angiosperms. The nuclear envelope consists of two lipid bilayer membranes (inner and outer nuclear membranes). The immunoglobulin binding protein (BiP), a molecular chaperone of the Hsp70 family of proteins in the endoplasmic reticulum (ER), and its partner, J-domain-containing protein, play roles in each nuclear membrane fusion during karyogamy. The fusion of the outer nuclear membranes is critical for sperm chromatin decondensation in the Arabidopsis central cell and the onset of endosperm development (Maruyama et al. 2020). The involvement of BiP and J-proteins in karyogamy has also been evident in yeast (Ng and Walter 1996; Nishikawa and Endo 1997; Rose et al. 1989). Other karyogamy factors highly conserved among organisms are the integral nuclear membrane protein, Kar5 family proteins. Kar5 was first identified in yeast (Beh et al. 1997) and is required for outer nuclear membrane fusion. The ortholog of Kar5 has been found in many species including zebrafish, Chlamydomonas, and Arabidopsis (Abrams et al. 2012; Ning et al. 2013; Nishikawa et al. 2020; Speijer et al. 2015), indicating that, while the mechanism of gamete nuclear migration has diverged, the molecular repertoire for karyogamy is highly conserved and has been maintained during evolution.
Concluding remarks
With the rapid accumulation of omics data in many species, both conserved and altered molecular processes in sexual reproduction in land plants have become gradually evident. In particular, DUO1 functions in the Streptophyta have highlighted how neo-functionalization of transcription factors and rewiring of gene regulatory networks can explain a part of evolution in land plant sexual reproduction (Higo et al. 2018). Further molecular dissections of streptophyte algae will further advance our understanding of land plants. Extant gymnosperms display evolutionary changes in sperm motility and some species show an early form of double fertilization. In orchid species, the endosperm has been largely reduced and some species do not appear to have endosperm development. Thus, not only model plants like Marchantia and Arabidopsis, but such species should also be further investigated, and this would provide new insights into the evolution of sexual reproduction in land plants. In addition, it would be useful to know the biological and/or evolutionary meanings of the egg and central cell’s utilization of different genes for controlling sperm nuclear migration in Arabidopsis. Together with sperm evolution, plasmogamic paternal contributions to fertilization and the onset of embryo/endosperm development (Ohnishi and Kawashima 2020) is also an exciting field to study from an evolutionary perspective. We have now many resources and methods available to address these questions and revealing the remaining evolutionary mystery of angiosperm sexual reproduction could be a big step in the fundamental understanding of overall green plant evolution.
Author contribution statement
V.S. and T.K. conceived the work and V.S., A.J.C., and T.K. wrote the manuscript.
References
Abrams EW, Zhang H, Marlow FL, Kapp L, Lu S, Mullins MC (2012) Dynamic assembly of brambleberry mediates nuclear envelope fusion during early development. Cell 150(3):521–532. https://doi.org/10.1016/j.cell.2012.05.048
Ali MF, Fatema U, Peng X, Hacker SW, Maruyama D, Sun MX, Kawashima T (2020) ARP2/3-independent WAVE/SCAR pathway and class XI myosin control sperm nuclear migration in flowering plants. Proc Natl Acad Sci U S A 117(51):32757–32763. https://doi.org/10.1073/pnas.2015550117
Ali MF, Kawashima T (2021) Formins control dynamics of F-actin in the central cell of Arabidopsis thaliana. Plant Signal Behav. https://doi.org/10.1080/15592324.2021.1920192
Baquero E, Fedry J, Legrand P, Krey T, Rey FA (2019) Species-specific functional regions of the green alga gamete fusion protein HAP2 revealed by structural studies. Structure 27(1):113–124114. https://doi.org/10.1016/j.str.2018.09.014
Baroux C, Grossniklaus U (2019) Seeds—An evolutionary innovation underlying reproductive success in flowering plants. Current topics in developmental biology, vol 131. Elsevier, pp 605–642. https://doi.org/10.1016/bs.ctdb.2018.11.017
Baroux C, Spillane C, Grossniklaus U (2002) Evolutionary origins of the endosperm in flowering plants. Genome Biol 3(9):reviews1026. https://doi.org/10.1186/gb-2002-3-9-reviews1026
Basu D et al (2005) DISTORTED3/SCAR2 is a putative Arabidopsis WAVE complex subunit that activates the Arp2/3 complex and is required for epidermal morphogenesis. Plant Cell 17(2):502–524. https://doi.org/10.1105/tpc.104.027987
Baum DA, Hileman LC (2018) A developmental genetic model for the origin of the flower. Ann Plant Rev Online. https://doi.org/10.1002/9780470988602.ch1
Beh CT, Brizzio V, Rose MD (1997) KAR5 encodes a novel pheromone-inducible protein required for homotypic nuclear fusion. J Cell Biol 139(5):1063–1076. https://doi.org/10.1083/jcb.139.5.1063
Borg M, Brownfield L, Khatab H, Sidorova A, Lingaya M, Twell D (2011) The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell 23(2):534–549. https://doi.org/10.1105/tpc.110.081059
Borg M et al (2020) Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin. Nat Cell Biol 22(6):621–629. https://doi.org/10.1038/s41556-020-0515-y
Bowman JL et al (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171(2):287-304. e215. https://doi.org/10.1016/j.cell.2017.09.030
Brownfield L, Hafidh S, Borg M, Sidorova A, Mori T, Twell D (2009) A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet 5(3):e1000430. https://doi.org/10.1371/journal.pgen.1000430
Carmichael JS, Friedman WE (1996) Double fertilization in Gnetum gnemon (Gnetaceae): its bearing on the evolution of sexual reproduction within the Gnetales and the anthophyte clade. Am J Bot 83(6):767–780. https://doi.org/10.1002/j.1537-2197.1996.tb12766.x
Carvalho-Santos Z, Azimzadeh J, Pereira-Leal JB, Bettencourt-Dias M (2011) Evolution: tracing the origins of centrioles, cilia, and flagella. J Cell Biol 194(2):165–175. https://doi.org/10.1083/jcb.201011152
Cheng S et al (2019) Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell 179(5):1057-1067. e1014. https://doi.org/10.1016/j.cell.2019.10.019
Cove DJ, Knight CD (1993) The moss Physcomitrella patens, a model system with potential for the study of plant reproduction. Plant Cell 5(10):1483–1488
Craddock C, Lavagi I, Yang Z (2012) New insights into Rho signaling from plant ROP/Rac GTPases. Trends Cell Biol 22(9):492–501. https://doi.org/10.1016/j.tcb.2012.05.002
Cyprys P, Lindemeier M, Sprunck S (2019) Gamete fusion is facilitated by two sperm cell-expressed DUF679 membrane proteins. Nat Plants 5(3):253–257. https://doi.org/10.1038/s41477-019-0382-3
Dahl TW, Arens SK (2020) The impacts of land plant evolution on Earth’s climate and oxygenation state—an interdisciplinary review. Chem Geol. https://doi.org/10.1016/j.chemgeo.2020.119665
Duan Z, Tominaga M (2018) Actin-myosin XI: an intracellular control network in plants. Biochem Biophys Res Commun 506(2):403–408. https://doi.org/10.1016/j.bbrc.2017.12.169
Evert RF, Eichhorn SE (2013) Raven: biology of plants, vol 581. RAV
Fang L, Leliaert F, Zhang ZH, Penny D, Zhong BJ (2017) Evolution of the Chlorophyta: insights from chloroplast phylogenomic analyses. J Syst Evol 55(4):322–332. https://doi.org/10.1111/jse.12248
Fatema U, Ali MF, Hu Z, Clark AJ, Kawashima T (2019) Gamete nuclear migration in animals and plants. Front Plant Sci 10:517. https://doi.org/10.3389/fpls.2019.00517
Fedry J et al (2018) Evolutionary diversification of the HAP2 membrane insertion motifs to drive gamete fusion across eukaryotes. PLoS Biol 16(8):e2006357. https://doi.org/10.1371/journal.pbio.2006357
Fédry J et al (2017) The ancient gamete fusogen HAP2 is a eukaryotic class II fusion protein. Cell 168(5):904-915. e910. https://doi.org/10.1016/j.cell.2017.01.024
Feng J et al (2018) Fusion surface structure, function, and dynamics of gamete fusogen HAP2. Elife 7:e39772. https://doi.org/10.7554/eLife.39772
Fernando DD, Quinn CR, Brenner ED, Owens JN (2010) Male gametophyte development and evolution in extant gymnosperms. Int J Plant Dev Biol 4(Special Issue 1):47–63
Filonova L, Von Arnold S, Daniel G, Bozhkov P (2002) Programmed cell death eliminates all but one embryo in a polyembryonic plant seed. Cell Death Differ 9(10):1057–1062. https://doi.org/10.1038/sj.cdd.4401068
Frank M, Egile C, Dyachok J, Djakovic S, Nolasco M, Li R, Smith LG (2004) Activation of Arp2/3 complex-dependent actin polymerization by plant proteins distantly related to Scar/WAVE. Proc Natl Acad Sci U S A 101(46):16379–16384. https://doi.org/10.1073/pnas.0407392101
Friedman WE (1993) The evolutionary history of the seed plant male gametophyte. Trends Ecol Evol 8(1):15–21. https://doi.org/10.1016/0169-5347(93)90125-9
Friedman WE (2015) Development and evolution of the female gametophyte and fertilization process in Welwitschia mirabilis (Welwitschiaceae). Am J Bot 102(2):312–324. https://doi.org/10.3732/ajb.1400472
Friedman WE, Carmichael JS (1996) Double fertilization in Gnetales: implications for understanding reproductive diversification among seed plants. Int J Plant Sci 157(S6):S77–S94. https://doi.org/10.1086/297405
Friedman WE, Ryerson KC (2009) Reconstructing the ancestral female gametophyte of angiosperms: insights from Amborella and other ancient lineages of flowering plants. Am J Bot 96(1):129–143. https://doi.org/10.3732/ajb.0800311
Gasser CS, Skinner DJ (2019) Development and evolution of the unique ovules of flowering plants. Current topics in developmental biology, vol 131. Elsevier, pp 373–399. https://doi.org/10.1016/bs.ctdb.2018.10.007
Graham LE, McBride GE (1979) The occurrence and phylogenetic significance of a multilayered structure in Coleochaete spermatozoids. Am J Bot 66(8):887–894. https://doi.org/10.1002/j.1537-2197.1979.tb06297.x
Guignard L (1899) Sur les antherozoides et la double copulation sexuelle chez les vegetaux angiosperms. CR Acad Sci Paris 128:864–871
Hackenberg D, Twell D (2019) The evolution and patterning of male gametophyte development. Current topics in developmental biology, vol 131. Elsevier, pp 257–298. https://doi.org/10.1016/bs.ctdb.2018.10.008
Halfon MS (2017) Perspectives on gene regulatory network evolution. Trends Genet 33(7):436–447. https://doi.org/10.1016/j.tig.2017.04.005
Hands P, Rabiger DS, Koltunow A (2016) Mechanisms of Endosperm Initiation. Plant Reprod 29(3):215–225. https://doi.org/10.1007/s00497-016-0290-x
Harris BJ, Harrison CJ, Hetherington AM, Williams TA (2020) Phylogenomic evidence for the monophyly of bryophytes and the reductive evolution of stomata. Curr Biol 30(11):2001-2012 e2002. https://doi.org/10.1016/j.cub.2020.03.048
Herron MD, Desnitskiy AG, Michod RE (2010) Evolution of developmental programs in volvox (chlorophyta) 1. J Phycol 46(2):316–324. https://doi.org/10.1111/j.1529-8817.2009.00803.x
Higo A et al (2018) Transcription factor DUO1 generated by neo-functionalization is associated with evolution of sperm differentiation in plants. Nat Commun 9(1):1–13. https://doi.org/10.1038/s41467-018-07728-3
Hisanaga T et al (2019) Building new insights in plant gametogenesis from an evolutionary perspective. Nat Plants 5(7):663–669. https://doi.org/10.1038/s41477-019-0466-0
Ingouff M et al (2010) Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol 20(23):2137–2143. https://doi.org/10.1016/j.cub.2010.11.012
Johnson MA et al (2004) Arabidopsis hapless mutations define essential gametophytic functions. Genetics 168(2):971–982. https://doi.org/10.1534/genetics.104.029447
Kawashima T et al (2014) Dynamic F-actin movement is essential for fertilization in Arabidopsis thaliana. Elife 3:e04501. https://doi.org/10.7554/eLife.04501
Kolomeitseva GL, Babosha AV, Ryabchenko AS, Tsavkelova EA (2020) Megasporogenesis, megagametogenesis, and embryogenesis in Dendrobium nobile (Orchidaceae). Protoplasma. https://doi.org/10.1007/s00709-020-01573-2
Kordyum EL, Mosyakin SL (2020) Endosperm of Angiosperms and Genomic Imprinting. Life (Basel) 10(7):104. https://doi.org/10.3390/life10070104
Kuligowski J, Chenou E, Ferrand M (1987) Les effets de la colchicine sur le gamète mâle d’une fougère, le Marsilea vestita; Devenir de la chromatine spermatique au cours de la fécondation. Bull Soc Bot France Lett Bot 134(3):257–268. https://doi.org/10.1080/01811797.1987.10824751
Kuligowski J, Ferrand M, Chenou E, Tourte Y (1985) Fertilization of a colchicine-treated gamete of the fern Marsilea vestita. Exp Biol 43(4):263–276
Lai X, Chahtane H, Martin-Arevalillo R, Zubieta C, Parcy F (2020) Contrasted evolutionary trajectories of plant transcription factors. Curr Opin Plant Biol 54:101–107. https://doi.org/10.1016/j.pbi.2020.03.002
Lemieux C, Otis C, Turmel M (2007) A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biol 5(1):2. https://doi.org/10.1186/1741-7007-5-2
Lopez-Smith R, Renzaglia K (2008) Sperm cell architecture, insemination, and fertilization in the model fern, Ceratopteris Richardii. Sex Plant Reprod 21(3):153–167. https://doi.org/10.1007/s00497-008-0068-x
Maruyama D, Higashiyama T, Endo T, Nishikawa S-i (2020) Fertilization-coupled sperm nuclear fusion is required for normal endosperm nuclear proliferation. Plant Cell Physiol 61(1):29–40. https://doi.org/10.1093/pcp/pcz158
Maruyama D, Ohtsu M, Higashiyama T (2016) Cell fusion and nuclear fusion in plants. Semin Cell Dev Biol. Elsevier, pp 127–135. https://doi.org/10.1016/j.semcdb.2016.07.024
Mori T, Igawa T, Tamiya G, Miyagishima SY, Berger F (2014) Gamete attachment requires GEX2 for successful fertilization in Arabidopsis. Curr Biol 24(2):170–175. https://doi.org/10.1016/j.cub.2013.11.030
Mori T, Kawai-Toyooka H, Igawa T, Nozaki H (2015) Gamete dialogs in green lineages. Mol Plant 8(10):1442–1454. https://doi.org/10.1016/j.molp.2015.06.008
Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2006) GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8(1):64–71. https://doi.org/10.1038/ncb1345
Nagahara S, Takeuchi H, Higashiyama T (2021) Polyspermy block in the central cell during double fertilization of Arabidopsis thaliana. Front Plant Sci 11:2164. https://doi.org/10.3389/fpls.2020.588700
Nagasato C (2005) Behavior and function of paternally inherited centrioles in brown algal zygotes. J Plant Res 118(6):361–369. https://doi.org/10.1007/s10265-005-0244-0
Nagasato C, Motomura T, Ichimura T (1999) Influence of centriole behavior on the first spindle formation in zygotes of the brown AlgaFucus distichus (Fucales, Phaeophyceae). Dev Biol 208(1):200–209. https://doi.org/10.1006/dbio.1998.9183
Nawaschin S (1898) Resultate einer Revision der Befruchtungsvorgange bei Lilium martagon und Fritillaria tenella. Извecтия Poccийcкoй Aкaдeмии Нayк Cepия Мaтeмaтичecкaя 9(4):377–382
Ng DT, Walter P (1996) ER membrane protein complex required for nuclear fusion. J Cell Biol 132(4):499–509. https://doi.org/10.1083/jcb.132.4.499
Ning J et al (2013) Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates. Genes Dev 27(10):1198–1215. https://doi.org/10.1101/gad.212746.112
Nishikawa S-i, Endo T (1997) The yeast JEM1p is a DnaJ-like protein of the endoplasmic reticulum membrane required for nuclear fusion. J Biol Chem 272(20):12889–12892. https://doi.org/10.1074/jbc.272.20.12889
Nishikawa S-I et al (2020) Arabidopsis Gex1 is a nuclear membrane protein of gametes required for nuclear fusion during reproduction. Front Plant Sci 11:548032
Nishiyama T et al (2018) The chara genome: secondary complexity and implications for plant terrestrialization. Cell 174(2):448-464 e424. https://doi.org/10.1016/j.cell.2018.06.033
Nozaki H, Yamada TK, Takahashi F, Matsuzaki R, Nakada T (2014) New “missing link” genus of the colonial volvocine green algae gives insights into the evolution of oogamy. BMC Evol Biol 14(1):1–11. https://doi.org/10.1186/1471-2148-14-37
Ohnishi Y, Hoshino R, Okamoto T (2014) Dynamics of male and female chromatin during Karyogamy in Rice Zygotes. Plant Physiol 165(4):1533–1543. https://doi.org/10.1104/pp.114.236059
Ohnishi Y, Kawashima T (2020) Plasmogamic paternal contributions to early zygotic development in flowering plants. Front Plant Sci 11:871. https://doi.org/10.3389/fpls.2020.00871
Peng X, Yan T, Sun M (2017) The WASP-Arp2/3 complex signal cascade is involved in actin-dependent sperm nuclei migration during double fertilization in tobacco and maize. Sci Rep 7:43161. https://doi.org/10.1038/srep43161
Pires ND, Dolan L (2012) Morphological evolution in land plants: new designs with old genes. Philos Trans R Soc Lond B Biol Sci 367(1588):508–518. https://doi.org/10.1098/rstb.2011.0252
Rensing SA (2018) Great moments in evolution: the conquest of land by plants. Curr Opin Plant Biol 42:49–54. https://doi.org/10.1016/j.pbi.2018.02.006
Rose MD, Misra LM, Vogel JP (1989) KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57(7):1211–1221. https://doi.org/10.1016/0092-8674(89)90058-5
Rotman N et al (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr Biol 15(3):244–248. https://doi.org/10.1016/j.cub.2005.01.013
Runions CJ, Owens JN (1999) Sexual reproduction of interior spruce (Pinaceae). II. Fertilization to early embryo formation. Int J Plant Sci 160(4):641–652. https://doi.org/10.1086/314171
Scott RJ, Armstrong SJ, Doughty J, Spielman M (2008) Double fertilization in Arabidopsis thaliana involves a polyspermy block on the egg but not the central cell. Mol Plant 1(4):611–619. https://doi.org/10.1093/mp/ssn016
Sharma N, Russell SD, Bhalla PL, Singh MB (2011) Putative cis-regulatory elements in genes highly expressed in rice sperm cells. BMC Res Notes 4(1):319. https://doi.org/10.1186/1756-0500-4-319
Shin JM, Yuan L, Ohme-Takagi M, Kawashima T (2020) Cellular dynamics of double fertilization and early embryogenesis in flowering plants. J Exp Zool B Mol Dev Evol. https://doi.org/10.1002/jez.b.22981
Simonini S, Østergaard L (2019) Female reproductive organ formation: a multitasking endeavor. Current topics in developmental biology, vol 131. Elsevier, Berlin, pp 337–371. https://doi.org/10.1016/bs.ctdb.2018.10.004
Southworth D, Cresti M (1997) Comparison of flagellated and nonflagellated sperm in plants. Am J Bot 84(9):1301. https://doi.org/10.2307/2446056
Specht CD, Bartlett ME (2009) Flower evolution: the origin and subsequent diversification of the angiosperm flower. Annu Rev Ecol Evol Syst. https://doi.org/10.1146/annurev.ecolsys.110308.120203
Speijer D, Lukeš J, Eliáš M (2015) Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proc Natl Acad Sci 112(29):8827–8834. https://doi.org/10.1073/pnas.1501725112
Sprunck S (2020) Twice the fun, double the trouble: gamete interactions in flowering plants. Curr Opin Plant Biol 53:106–116. https://doi.org/10.1016/j.pbi.2019.11.003
Sprunck S, Rademacher S, Vogler F, Gheyselinck J, Grossniklaus U, Dresselhaus T (2012) Egg cell-secreted EC1 triggers sperm cell activation during double fertilization. Science 338(6110):1093–1097. https://doi.org/10.1126/science.1223944
Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3(2):137–144. https://doi.org/10.1038/nrg733
Takahashi T et al (2018) The male gamete membrane protein DMP9/DAU2 is required for double fertilization in flowering plants. Development. https://doi.org/10.1242/dev.170076
Uhrig JF et al (2007) The role of Arabidopsis SCAR genes in ARP2-ARP3-dependent cell morphogenesis. Development 134(5):967–977. https://doi.org/10.1242/dev.02792
Umen J, Coelho S (2019) Algal sex determination and the evolution of anisogamy. Annu Rev Microbiol 73:267–291. https://doi.org/10.1146/annurev-micro-020518-120011
Valansi C et al (2017) Arabidopsis HAP2/GCS1 is a gamete fusion protein homologous to somatic and viral fusogens. J Cell Biol 216(3):571–581. https://doi.org/10.1083/jcb.201610093
von Besser K, Frank AC, Johnson MA, Preuss D (2006) Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133(23):4761–4769. https://doi.org/10.1242/dev.02683
Wang D, Lu Y, Zhang M, Lu Z, Luo K, Cheng F, Wang L (2014) Structure and function of the neck cell during fertilization in Ginkgo biloba L. Trees 28(4):995–1005. https://doi.org/10.1007/s00468-014-1013-2
Wang S et al (2020) Genomes of early-diverging streptophyte algae shed light on plant terrestrialization. Nat Plants 6(2):95–106. https://doi.org/10.1038/s41477-019-0560-3
Warman C et al (2020) High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements. PLoS Genet 16(4):e1008462. https://doi.org/10.1371/journal.pgen.1008462
Wickett NJ et al (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc Natl Acad Sci U S A 111(45):E4859-4868. https://doi.org/10.1073/pnas.1323926111
Williams JH, Friedman WE (2002) Identification of diploid endosperm in an early angiosperm lineage. Nature 415(6871):522–526. https://doi.org/10.1038/415522a
Wodniok S, Brinkmann H, Glöckner G, Heidel AJ, Philippe H, Melkonian M, Becker B (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evol Biol 11(1):1–10. https://doi.org/10.1186/1471-2148-11-104
Wong GK-S et al (2019) Sequencing and analyzing the transcriptomes of a thousand species across the tree of life for green plants. Annu Rev Plant Biol. https://doi.org/10.1146/annurev-arplant-042916-041040
Woźniak NJ, Sicard A (2018) Evolvability of flower geometry: convergence in pollinator-driven morphological evolution of flowers. Semin Cell Dev Biol. Elsevier, pp 3–15. https://doi.org/10.1016/j.semcdb.2017.09.028
Zhang C et al (2008) Arabidopsis SCARs function interchangeably to meet actin-related protein 2/3 activation thresholds during morphogenesis. Plant Cell 20(4):995–1011. https://doi.org/10.1105/tpc.107.055350
Zhang X, Dyachok J, Krishnakumar S, Smith LG, Oppenheimer DG (2005) IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubule organization. Plant Cell 17(8):2314–2326. https://doi.org/10.1105/tpc.104.028670
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This work was supported by NSF Grant IOS-1928836 (to T.K.) and National Institute of Food and Agriculture, US Department of Agriculture Hatch Program Grant 1014280 (to T.K.).
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Sharma, V., Clark, A.J. & Kawashima, T. Insights into the molecular evolution of fertilization mechanism in land plants. Plant Reprod 34, 353–364 (2021). https://doi.org/10.1007/s00497-021-00414-3
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DOI: https://doi.org/10.1007/s00497-021-00414-3