Job Sharing in the Endomembrane System: Vacuolar Acidification Requires the Combined Activity of V-ATPase and V-PPase

Kriegel, Anne; Andrés, Zaida; Medzihradszky, Anna; Krüger, Friedrich; Scholl, Stefan; Delang, Simon; Patir-Nebioglu, M. Görkem; Gute, Gezahegn; Yang, Haibing; Murphy, Angus S.; Peer, Wendy Ann; Pfeiffer, Anne; Krebs, Melanie; Lohmann, Jan U.; Schumacher, Karin

doi:10.1105/tpc.15.00733

Cited by 90 publications

(107 citation statements)

References 70 publications

(91 reference statements)

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“…A recent study indicated that vacuolar acidification is collectively contributed by the TGN/ EE-associated and the tonoplast-associated V-ATPases (40). Thus, the effect of VHA-A loss of function could be from the TGN/EE and the vacuoles (39).…”

Section: Discussionmentioning

confidence: 99%

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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Section: Discussionmentioning

confidence: 99%

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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“…In fugu5-1, a knockout of the PP i -ase AtAVP1, the vacuolar pH was increased by 0.25 units compared with the wildtype pH of 5.8 (Ferjani et al, 2011). The triple mutant vha2 3 vha3 3 avp1 shows that these two kinds of proton pumps present an additive function only in some cell types (Kriegel et al, 2015). In petunia (Petunia hybrida) petals, the vacuolar membrane also contains ATPases of the P-type, the type found at the plasma membrane (Verweij et al, 2008;Faraco et al, 2014), but there is no report for such a function in Arabidopsis guard cells.…”

Section: Vacuolar Ph During Stomatal Movementmentioning

confidence: 98%

“…Hence, part of the proton gradient necessary for stomatal opening must be generated elsewhere. It has been suggested that vacuolar acidity originates during vacuolar biogenesis and, thus, relies on other acidic compartments, such as the transGolgi network/early endosome (Schumacher, 2014;Kriegel et al, 2015). The det3 mutant, a knockout of the trans-Golgi network/early endosome-localized V-type ATPase, however, shows impaired stomatal closure (Allen et al, 2000;Brüx et al, 2008), but stomatal opening was not reported to be affected in this mutant.…”

Section: Vacuolar Ph During Stomatal Movementmentioning

confidence: 98%

“…The fact that mutants of the H + -coupled antiporters AtNHX1, AtNHX2, AtCLCa, and AtCLCc all show impaired stomatal opening phenotypes demonstrates that the existence of a proton gradient is necessary for opening. Therefore, it is surprising that AtVHA and AtAVP1 knockout mutants do not show impaired stomatal opening (Bak et al, 2013), and triple mutants defective in both proton pumps show vacuolar pH values that are still slightly acidic (Schumacher, 2014;Kriegel et al, 2015). Hence, part of the proton gradient necessary for stomatal opening must be generated elsewhere.…”

Section: Vacuolar Ph During Stomatal Movementmentioning

confidence: 99%

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Ion Transport at the Vacuole during Stomatal Movements

Eisenach

Angeli

2017

Plant Physiol.

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Plant gas exchange with the environment is facilitated by stomata, small pores found on most aerial surfaces of land plants. Stomatal pores are formed between a pair of specialized guard cells. In C3 plants, open stomata allow the uptake of CO 2 for photosynthesis during the day and at the same time the loss of water vapor, maintaining the transpiration stream. At night and during drought, plants close their stomata to conserve water, while they open them in response to low CO 2 and at high temperatures to allow for evaporative cooling. The opening and closure of stomata depends on guard cell turgor, which, in turn, relies on fluxes of osmotically active solutes in and out of the guard cell. During stomatal opening, osmotically active solutes enter guard cells via the plasma membrane or are produced inside the cell and ultimately are stored in the vacuole (Roelfsema and Hedrich, 2005;Kollist et al., 2014;Santelia and Lawson, 2016). This causes water influx, a concomitant increase in turgor and swelling of the guard cell pair, resulting in the opening of the stomatal pore. K + and its charge-balancing anions Cl 2 , NO 3 2 , and malate (Mal 22 ), as well as sugars, are the osmotica accumulating in guard cell vacuoles for stomatal opening. The ions are transported across the vacuolar membrane (also, the tonoplast) by ion channels and secondary active transporters, while vacuolar proton pumps generate the necessary proton motive force and acidify the vacuolar lumen.With the dawn of the patch-clamp technique, many ion channels were characterized in the 1980s and 1990s. A lot of these early studies were conducted with the broad bean Vicia faba and the monocotyledon dayflower plant Commelina communis because of the large size of their guard cells. It was only with the era of molecular genetics that the proteins responsible for the characterized transport were identified in Arabidopsis (Arabidopsis thaliana), and this review focuses almost exclusively on vacuolar transport proteins of this species with a role in stomatal physiology (Table I; Fig. 1).Nevertheless, many discoveries about guard cell function were made using V. faba, C. communis, and other species but were carried over into Arabidopsis guard cell research and now shape our reasoning. For example, Mal 22 is often listed as an important osmoticum. This is true for some species such as V. faba (Outlaw and Lowry, 1977;Outlaw and Kennedy, 1978; Raschke, 1978a, 1978b) and in certain growth conditions (Raschke and Schnabl, 1978;Van Kirk and Raschke, 1978a). But in Arabidopsis guard cells, on average, K + is charge balanced to 50% by Cl 2 and only to 5% by Mal 22 , with Mal 22 concentrations in the range of 1 to 2 mM

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“…The authors wondered whether the remaining proton gradient in the mutant was entirely due to V-PPase activity or whether other pumps contributed to vacuolar acidification. Now, Kriegel et al (2015) have dissected the contribution of V-ATPases and V-PPases to vacuolar acidification using a panel of Arabidopsis mutants. In addition to vha-a2 vha-a3, they obtained mutants lacking the tonoplast-localized K 1 -stimulated V-PPase (fugu5-1) and generated plants in which the K 1 -stimulated V-PPase was overexpressed in the vha-a2 vha-a3 background (UBQ:AVP1 vha-a2 vha-a3) and a triple mutant lacking both V-ATPases and the V-PPase (fugu5-1 vha-a2 vha-a3).…”

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confidence: 99%

A TGN/EE-Localized V-ATPase Contributes to Vacuolar Acidification

Farquharson

2015

Plant Cell

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Job Sharing in the Endomembrane System: Vacuolar Acidification Requires the Combined Activity of V-ATPase and V-PPase

Cited by 90 publications

References 70 publications

AP1G mediates vacuolar acidification during synergid-controlled pollen tube reception

AP1G mediates vacuolar acidification during synergid-controlled pollen tube reception

Ion Transport at the Vacuole during Stomatal Movements

A TGN/EE-Localized V-ATPase Contributes to Vacuolar Acidification

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