Pollen Tube Discharge Completes the Process of Synergid Degeneration That Is Initiated by Pollen Tube-Synergid Interaction in Arabidopsis

Leydon, Alexander R.; Tsukamoto, Tatsuya; Dunatunga, Damayanthi; Qin, Yuan; Johnson, Mark A.; Palanivelu, Ravishankar

doi:10.1104/pp.15.00528

Cited by 42 publications

(32 citation statements)

References 48 publications

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“…We present here structural and molecular data demonstrating that the receptive synergid is also responsible for inducing the bursting of the pollen tube. As proposed by SandaklieNikolova et al (2007), Ngo et al (2014) and later, Leydon et al (2015), our results confirm that cell death of the receptive synergid is coordinated with that of the pollen tube. Furthermore, we show that VDD and VAL, two REM transcription factors and direct targets of the MADS domain complex -STK and SEP3 -are able to interact in vivo, indicating that cell death in the receptive synergid requires a complex containing both VDD and VAL, possibly as a heterodimer.…”

Section: Discussionsupporting

confidence: 79%

“…Other mutants known to have an overgrowing pollen tube phenotype such as lre show increased synergid degeneration 48 h after fertilization, suggesting that physical contact with the pollen tube may trigger synergid cell death (Leydon et al, 2015). In our mutants lines, even 48 h after fertilization, we found both ovules with intact synergids (vdd gametophyte) and ovules containing a developing endosperm (VDD gametophyte), which demonstrates that even if the pollen tube remains in contact with the synergid for a long period, cell death does not occur.…”

Section: Discussionmentioning

confidence: 99%

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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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Section: Discussionsupporting

confidence: 79%

Section: Discussionmentioning

confidence: 99%

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

et al. 2016

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“…CLSM of ovules at different HAP showed that synergid degeneration was impaired by AP1G loss of function, which is further supported by that fact that nondischarging pollen tubes always correlated with the failure of synergid degeneration. However, synergid degeneration could be initiated without pollen tube discharge (17), which explains the comparable ratio of ovules with two intact synergids at 8 HAP and one intact synergid at 12 HAP within ap1g/+ pistils. The impaired degeneration of the remaining synergid in ap1g/+ might be a secondary effect due to the failure of pollen tube discharge (23,24).…”

Section: Discussionmentioning

confidence: 97%

“…In Arabidopsis, the degeneration of the receptive synergid usually accompanies the discharge of the incoming pollen tube (18). Synergid degeneration can also be initiated without pollen tube discharge (17). The degeneration and removal of the persistent synergid are mediated by ethylene signaling and the central cell (19,20).…”

mentioning

confidence: 99%

“…Between the two synergid cells, a receptive synergid cell is the one that succeeds in interacting with the pollen tube and induces it to burst and undergoes cell death first. The other synergid cell that continues to persist and then undergoes cell death orchestrated by the fertilized egg cell and the central cell is the persistent synergid (3,11,17). In Arabidopsis, the degeneration of the receptive synergid usually accompanies the discharge of the incoming pollen tube (18).…”

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confidence: 99%

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AP1G mediates vacuolar acidification during synergid-controlled pollen tube reception

Wang

Feng

Liu

et al. 2017

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

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Double fertilization in angiosperms requires the delivery of immotile sperm through pollen tubes, which enter embryo sacs to initiate synergid degeneration and to discharge. This fascinating process, called pollen tube reception, involves extensive communications between pollen tubes and synergids, within which few intracellular regulators involved have been revealed. Here, we report that vacuolar acidification in synergids mediated by AP1G and V-ATPases might be critical for pollen tube reception. Functional loss of AP1G or VHA-A, encoding the γ subunit of adaptor protein 1 or the shared component of two endomembrane V-ATPases, respectively, impaired synergid-controlled pollen tube reception and caused partial female sterility. AP1G works in parallel to the plasma membrane-associated receptor FERONIA in synergids, suggesting that synergid-mediated pollen tube reception requires proper sorting of vacuolar cargos by AP1G. Although AP1G did not mediate the targeting of V-ATPases, AP1G loss of function or the expression of AP1G-RNAi compromised vacuolar acidification mediated by V-ATPases, implying their genetic interaction. We propose that vacuolar acidification might represent a distinct cell-death mechanism specifically adopted by the plant phylum, which is critical for synergid degeneration during pollen tube reception. . The female gametophyte (FG), i.e., the embryo sac, is formed inside the ovules and contains an egg cell, a central cell, two synergid cells, and three antipodal cells (3). Upon landing on a receptive pistil, a pollen grain forms a long cylindrical extension, called a pollen tube, which extends inside female sporophytic tissues. To deliver immotile sperm, pollen tubes perceive attractive signals sent out by the FG, change their growth axis, and finally enter the embryo sacs through the micropyle (1-4). A process called "pollen tube reception" instructs the cessation and discharge of the penetrating pollen tube, leading to sperm release and fertilization (1-4).Studies have uncovered key female factors controlling pollen tube reception, including FERONIA (FER) (5-7), LORELEI (LRE) (8, 9), and early nodulin-like proteins (ENODLs) (10) and NORTIA (NTA) (11). These synergid receptors likely operate in the same genetic pathway (10-12) whose functional loss caused the failure of pollen tube discharge and led to reduced female fertility (5-9, 11). Male ligands are yet to be identified. However, recent studies showed that the production of reactive oxygen species (ROS) and Ca 2+ spiking are downstream events of FER-controlled pollen tube reception (13-16).Synergid degeneration, a form of programmed cell death (PCD), is a key step during pollen tube reception. Between the two synergid cells, a receptive synergid cell is the one that succeeds in interacting with the pollen tube and induces it to burst and undergoes cell death first. The other synergid cell that continues to persist and then undergoes cell death orchestrated by the fertilized egg cell and the central cell is the persistent synergid (3,11,1...

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Directional Growth for Sperm Delivery

Sankaranarayanan

Higashiyama

2017

Pollen Tip Growth

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Pollen Tube Discharge Completes the Process of Synergid Degeneration That Is Initiated by Pollen Tube-Synergid Interaction in Arabidopsis

Cited by 42 publications

References 48 publications

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

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

AP1G mediates vacuolar acidification during synergid-controlled pollen tube reception

Directional Growth for Sperm Delivery

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