Hyperacidification of Vacuoles by the Combined Action of Two Different P-ATPases in the Tonoplast Determines Flower Color

Faraco, Marianna; Spelt, Cornelis; Bliek, Mattijs; Verweij, Walter; Hoshino, Atsushi; Espen, Luca; Prinsi, Bhakti; Jaarsma, Rinse; Tarhan, Eray; Boer, Albertus H. de; Sansebastiano, Gian Pietro Di; Koes, Ronald; Quattrocchio, Francesca

doi:10.1016/j.celrep.2013.12.009

Cited by 117 publications

(170 citation statements)

References 52 publications

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“…V-ATPase and V-PPase have long been considered to be the only tonoplast proton pumps, but it is by now clear that members of the P3A subgroup of P-type ATPases previously assumed to be exclusively present at the plasma membrane can also be found at the tonoplast (Verweij et al, 2008;Faraco et al, 2014). In Arabidopsis, AHA10 is required for the vacuolar accumulation of proanthocyanidins (Baxter et al, 2005) and has recently been shown to be localized at the tonoplast of seed coat endothelial cells (Appelhagen et al, 2015).…”

Section: How Can Vacuoles Be Acidic Without V-atpase and V-ppase?mentioning

confidence: 99%

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

et al. 2015

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The presence of a large central vacuole is one of the hallmarks of a prototypical plant cell, and the multiple functions of this compartment require massive fluxes of molecules across its limiting membrane, the tonoplast. Transport is assumed to be energized by the membrane potential and the proton gradient established by the combined activity of two proton pumps, the vacuolar H + -pyrophosphatase (V-PPase) and the vacuolar H + -ATPase (V-ATPase). Exactly how labor is divided between these two enzymes has remained elusive. Here, we provide evidence using gain-and loss-of-function approaches that lack of the V-ATPase cannot be compensated for by increased V-PPase activity. Moreover, we show that increased V-ATPase activity during cold acclimation requires the presence of the V-PPase. Most importantly, we demonstrate that a mutant lacking both of these proton pumps is conditionally viable and retains significant vacuolar acidification, pointing to a so far undetected contribution of the trans-Golgi network/early endosome-localized V-ATPase to vacuolar pH.

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Section: How Can Vacuoles Be Acidic Without V-atpase and V-ppase?mentioning

confidence: 99%

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

et al. 2015

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“…Anthocyanins are thought to be synthesized on the cytoplasmic face of the endoplasmic reticulum (ER) (Hrazdina et al, 1987;Saslowsky and Winkel-Shirley, 2001;Winkel, 2004) from where they are transported to the vacuolar lumen. Vacuolar localization prevents anthocyanin oxidation and the low pH environment confers the typical intense anthocyanin coloration (Marrs et al, 1995;Verweij et al, 2008;Faraco et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Anthocyanin Vacuolar Inclusions Form by a Microautophagy Mechanism

et al. 2015

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Anthocyanins are flavonoid pigments synthesized in the cytoplasm and stored inside vacuoles. Many plant species accumulate densely packed, 3-to 10-mm diameter anthocyanin deposits called anthocyanin vacuolar inclusions (AVIs). Despite their conspicuousness and importance in organ coloration, the origin and nature of AVIs have remained controversial for decades. We analyzed AVI formation in cotyledons of different Arabidopsis thaliana genotypes grown under anthocyanin inductive conditions and in purple petals of lisianthus (Eustoma grandiorum). We found that cytoplasmic anthocyanin aggregates in close contact with the vacuolar surface are directly engulfed by the vacuolar membrane in a process reminiscent of microautophagy. The engulfed anthocyanin aggregates are surrounded by a single membrane derived from the tonoplast and eventually become free in the vacuolar lumen like an autophagic body. Neither endosomal/prevacuolar trafficking nor the autophagy ATG5 protein is involved in the formation of AVIs. In Arabidopsis, formation of AVIs is promoted by both an increase in cyanidin 3-O-glucoside derivatives and by depletion of the glutathione S-transferase TT19. We hypothesize that this novel microautophagy mechanism also mediates the transport of other flavonoid aggregates into the vacuole.

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“…To date, seven such PH genes have been identified in petunia via mutants that all show a similar phenotype: petals with a bluish color and an increased pH of petal homogenates (de Vlaming et al, 1983;van Houwelingen et al, 1998). Molecular analysis revealed that ph6 mutants represent specific an1 alleles that lost the capacity to acidify the vacuole but can still drive anthocyanin biosynthesis (Spelt et al, 2002) and that PH5 and PH1 are direct target genes of the AN11-AN1-PH4 complex that encodes two interacting P-ATPase transmembrane transporters that reside in the tonoplast (Verweij et al, 2008;Faraco et al, 2014).The AN1-AN11-PH4 triumvirate is also required for the stability of anthocyanins in the vacuole, as in certain genetic backgrounds ph4 and specific an1 alleles (formerly known as ph6 alleles) trigger the complete disappearance of anthocyanins and "fading" of the flower color after opening of the bud (de Vlaming et al, 1982(de Vlaming et al, , 1983Quattrocchio et al, 2006;Passeri et al, 2016). Fading is not triggered by the pH shift alone because it is not seen in ph5 and ph2 mutants but seems due to a different vacuolar defect caused by the misregulation of distinct AN1-AN11-PH4 target genes (Quattrocchio et al, 2006).…”

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confidence: 99%

Functionally Similar WRKY Proteins Regulate Vacuolar Acidification in Petunia and Hair Development in Arabidopsis

Verweij¹,

et al. 2016

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The WD40 proteins ANTHOCYANIN11 (AN11) from petunia (Petunia hybrida) and TRANSPARENT TESTA GLABRA1 (TTG1) from Arabidopsis thaliana and associated basic helix-loop-helix (bHLH) and MYB transcription factors activate a variety of differentiation processes. In petunia petals, AN11 and the bHLH protein AN1 activate, together with the MYB protein AN2, anthocyanin biosynthesis and, together with the MYB protein PH4, distinct genes, such as PH1 and PH5, that acidify the vacuole. To understand how AN1 and AN11 activate anthocyanin biosynthetic and PH genes independently, we isolated PH3. We found that PH3 is a target gene of the AN11-AN1-PH4 complex and encodes a WRKY protein that can bind to AN11 and is required, in a feed-forward loop, together with AN11-AN1-PH4 for transcription of PH5. PH3 is highly similar to TTG2, which regulates hair development, tannin accumulation, and mucilage production in Arabidopsis. Like PH3, TTG2 can bind to petunia AN11 and the Arabidopsis homolog TTG1, complement ph3 in petunia, and reactivate the PH3 target gene PH5. Our findings show that the specificity of WD40-bHLH-MYB complexes is in part determined by interacting proteins, such as PH3 and TTG2, and reveal an unanticipated similarity in the regulatory circuitry that controls petunia vacuolar acidification and Arabidopsis hair development. INTRODUCTIONRegulatory complexes consisting of a MYB, basic helix-loop-helix (bHLH), and WD40 protein (MBW complexes) control multiple pathways involved in the differentiation of epidermal cells in angiosperms (reviewed in Broun, 2005;Koes et al., 2005;Ramsay and Glover, 2005;Ishida et al., 2008). The best understood function of this complex involves the biosynthesis of anthocyanin pigments that color many flowers and fruits. Closely related, and in most cases functionally exchangeable, MYB, bHLH, and WD40 proteins collaboratively activate the transcription of genes that encode enzymes of the anthocyanin pathway in a broad range of species, including distantly related dicots like Arabidopsis thaliana (a Rosid) and petunia (Petunia hybrida; an Asterid) and monocots like maize (Zea mays; Koes et al., 2005;Hichri et al., 2011;Petroni and Tonelli, 2011). In addition, related MBW complexes activate numerous other pathways and processes, such as vacuolar acidification, formation of seed mucilage, and the development of hair cells, a process that seems restricted to smaller sets of species (Koes et al., 2005;Ramsay and Glover, 2005;Serna and Martin, 2006).In petunia flowers, the WD40 protein ANTHOCYANIN11 (AN11) and the bHLH factor AN1 activate structural anthocyanin genes in floral tissues, such as petals and anthers, and a few vegetative tissues (Quattrocchio et al., 1993;de Vetten et al., 1997;Spelt et al., 2000). To this end, AN11 and AN1 interact with paralogous and exchangeable MYB proteins, which are encoded by AN2, AN4, and DEEP PURPLE and are expressed in different tissues (Quattrocchio et al., 1999(Quattrocchio et al., , 2006Albert et al., 2011). Furthermore, AN1 and AN11 activate, in concert...

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Hyperacidification of Vacuoles by the Combined Action of Two Different P-ATPases in the Tonoplast Determines Flower Color

Cited by 117 publications

References 52 publications

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

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

Anthocyanin Vacuolar Inclusions Form by a Microautophagy Mechanism

Functionally Similar WRKY Proteins Regulate Vacuolar Acidification in Petunia and Hair Development in Arabidopsis

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