Independent Control by Each Female Gamete Prevents the Attraction of Multiple Pollen Tubes

Maruyama, Daisuke; Hamamura, Yuki; Takeuchi, Hidenori; Susaki, Daichi; Nishimaki, Moe; Kurihara, Daisuke; Kasahara, Ryushiro D.; Higashiyama, Tetsuya

doi:10.1016/j.devcel.2013.03.013

Cited by 131 publications

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“…Maternal defects in transmitting tract differentiation or morphology as well as defects in chemotactic signaling can disrupt pollen tube development or produce defects in guidance even for wild-type (WT) pollen (Crawford and Yanofsky 2011;Leydon et al 2014;Ngo et al 2014). The guidance and development signals from the sporophyte are dynamic, ensuring that a successful double fertilization results in inhibition of additional pollen tubes growing toward the fertilized ovule (Beale et al 2012;Kasahara et al 2012;Maruyama et al 2013).The extent to which epigenetic regulatory pathways contribute to coordinated development of sporophytic and gametophytic compartments in plant reproductive tissues remains to be determined. Precedent for a possible role is provided by the important contribution of epigenetic machinery to the development of the seed after fertilization (Jiang and Kohler 2012;Gehring 2013).…”

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Cross-Talk Between Sporophyte and Gametophyte Generations Is Promoted by CHD3 Chromatin Remodelers inArabidopsis thaliana

et al. 2016

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Angiosperm reproduction requires the integrated development of multiple tissues with different genotypes. To achieve successful fertilization, the haploid female gametophytes and diploid ovary must coordinate their development, after which the male gametes must navigate through the maternal sporophytic tissues to reach the female gametes. After fertilization, seed development requires coordinated development of the maternal diploid integuments, the triploid endosperm, and the diploid zygote. Transcription and signaling factors contribute to communication between these tissues, and roles for epigenetic regulation have been described for some of these processes. Here we identify a broad role for CHD3 chromatin remodelers in Arabidopsis thaliana reproductive development. Plants lacking the CHD3 remodeler, PICKLE, exhibit various reproductive defects including abnormal development of the integuments, female gametophyte, and pollen tube, as well as delayed progression of ovule and embryo development. Genetic analyses demonstrate that these phenotypes result from loss of PICKLE in the maternal sporophyte. The paralogous gene PICKLE RELATED 2 is preferentially expressed in the endosperm and acts antagonistically with respect to PICKLE in the seed: loss of PICKLE RELATED 2 suppresses the large seed phenotype of pickle seeds. Surprisingly, the alteration of seed size in pickle plants is sufficient to determine the expression of embryonic traits in the seedling primary root. These findings establish an important role for CHD3 remodelers in plant reproduction and highlight how the epigenetic status of one tissue can impact the development of genetically distinct tissues. KEYWORDS PICKLE; PKR2; ovule; pollen tube; seed size D EVELOPMENT in multicellular organisms requires coordinated morphogenesis and communication between tissues with distinct gene expression profiles and occasionally distinct genotypes. Mutations in epigenetic regulators can perturb mutually dependent cell types and therefore complicate interpretation of the resulting phenotypes. The reproductive system of flowering plants presents an attractive context in which to distinguish autonomous phenotypes from those arising from defects in ancillary tissues. The haploid male and female gametophyte generation is contained within the diploid sporophyte, and development of these genetically distinct tissues is highly interdependent (Ma and Sundaresan 2010;Niklas and Kutschera 2010). The female gametophyte develops within the sporophytic ovary, where it forms into an embryo sac as it is surrounded by the diploid sporophytic integuments of the ovule (Bencivenga et al. 2011;Chevalier et al. 2011). Characterization of ovule-defective mutants in Arabidopsis thaliana has revealed that female gametophyte development is dependent on the sporophyte, particularly integument development, and has also identified a variety of factors that contribute to this relationship including transcription factors, kinases, and components of plant hormone signal transduction pathwa...

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Cross-Talk Between Sporophyte and Gametophyte Generations Is Promoted by CHD3 Chromatin Remodelers inArabidopsis thaliana

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“…Pollen tube reception is completed by pollen tube burst, SC release, and degeneration of synergid cells (12). If this process fails, a second pollen tube can be attracted to the same ovule for a second attempt, resulting in polytubey (19). The SCs [or their progenitor the generative cell (GC)] are enclosed by an endocytic membrane tethered to the pollen vegetative nucleus (VN) (20).…”

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Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins

Zhou

Meier

2014

Proc. Natl. Acad. Sci. U.S.A.

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Increasing evidence suggests that nuclear migration is important for eukaryotic development. Although nuclear migration is conserved in plants, its importance for plant development has not yet been established. The most extraordinary plant nuclear migration events involve plant fertilization, which is starkly different from that of animals. Instead of evolving self-propelled sperm cells (SCs), plants use pollen tubes to deliver SCs, in which the pollen vegetative nucleus (VN) and the SCs migrate as a unit toward the ovules, a fundamental but barely understood process. Here, we report that WPP domain-interacting proteins (WIPs) and their binding partners the WPP domain-interacting tail-anchored proteins (WITs) are essential for pollen nuclear migration. Loss-offunction mutations in WIT and/or WIP gene families resulted in impaired VN movement, inefficient SC delivery, and defects in pollen tube reception. WIPs are Klarsicht/ANC-1/Syne-1 Homology (KASH) analogs in plants. KASH proteins are key players in animal nuclear migration. Thus, this study not only reveals an important nuclear migration mechanism in plant fertilization but also, suggests that similar nuclear migration machinery is conserved between plants and animals.nuclear envelope | Arabidopsis | male gametophyte | LINC complex N uclear migration is essential for cell differentiation, polarization, and migration, which influence organism development (1-3). Examples range from Caenorhabditis elegans P-cell development to mammalian neural development (1-3). The key players in opisthokont nuclear migration are the inner nuclear membrane Sad1/UNC-84 (SUN) proteins and outer nuclear membrane Klarsicht/ANC-1/Syne-1 Homology (KASH) proteins. SUN and KASH proteins form the linkers of the nucleoskeleton and the cytoskeleton complexes at the nuclear envelope (NE) and transfer cytoplasmic forces to the nucleus (1-3). In plants, nuclear migration is associated with a number of developmental events and environmental responses, including fertilization, root and leaf hair formation, and plant-microbe interactions (4, 5). So far, little is known about the mechanism of plant nuclear migration. Although SUN proteins are conserved in plants (6, 7), absence of animal KASH homologs in plants suggests that plants may have evolved different molecular solutions to achieve nuclear migration. Recently, WPP domaininteracting proteins (WIPs) were identified as KASH proteins in plants (8), and their outer nuclear membrane binding partners WPP domain-interacting tail anchored proteins (WITs) were shown to interact with myosin XI-I (9). The WIT-myosin XI

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“…Fusion of the two sperm cells with the female gametes (egg and central cell) is required to stimulate the degeneration of the second synergid, and the termination of attractant production (Beale et al, 2012;Kasahara et al, 2012). These events have been shown to require both the chromatin-remodeling Polycomb repressive complex 2 (PRC2) (Maruyama et al, 2013) and ethylene signaling (Völz et al, 2013).…”

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Live and let die: a REM complex promotes fertilization through synergid cell death in Arabidopsis

et al. 2016

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Fertilization in flowering plants requires a complex series of coordinated events involving interaction between the male and female gametophyte. We report here molecular data on one of the key events underpinning this process -the death of the receptive synergid cell and the coincident bursting of the pollen tube inside the ovule to release the sperm. We show that two REM transcription factors, VALKYRIE (VAL) and VERDANDI (VDD), both targets of the ovule identity MADS-box complex SEEDSTICK-SEPALLATA3, interact to control the death of the receptive synergid cell. In vdd-1/+ mutants and VAL_RNAi lines, we find that GAMETOPHYTIC FACTOR 2 (GFA2), which is required for synergid degeneration, is downregulated, whereas expression of FERONIA (FER) and MYB98, which are necessary for pollen tube attraction and perception, remain unaffected. We also demonstrate that the vdd-1/+ phenotype can be rescued by expressing VDD or GFA2 in the synergid cells. Taken together, our findings reveal that the death of the receptive synergid cell is essential for maintenance of the following generations, and that a complex comprising VDD and VAL regulates this event.

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Independent Control by Each Female Gamete Prevents the Attraction of Multiple Pollen Tubes

Cited by 131 publications

References 46 publications

Cross-Talk Between Sporophyte and Gametophyte Generations Is Promoted by CHD3 Chromatin Remodelers inArabidopsis thaliana

Cross-Talk Between Sporophyte and Gametophyte Generations Is Promoted by CHD3 Chromatin Remodelers inArabidopsis thaliana

Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins

Live and let die: a REM complex promotes fertilization through synergid cell death in Arabidopsis

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