A Tonoplast P3B-ATPase Mediates Fusion of Two Types of Vacuoles in Petal Cells

Faraco, Marianna; Li, Yanbang; Li, Shuangjiang; Spelt, Cornelis; Sansebastiano, Gian Pietro Di; Reale, Lara; Ferranti, Francesco; Verweij, Walter; Koes, Ronald; Quattrocchio, Francesca

doi:10.1016/j.celrep.2017.05.076

Cited by 24 publications

(41 citation statements)

References 45 publications

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“…The tannin‐related genes ANR and LAR were not affected by ASRs M1 overexpression, indicating that these MYBs are specific for the anthocyanin pathway. Similarly, no expression of the flavonol synthase gene ( FLS) was induced in ASRs‐ OE lines, and no induction was observed for the expression of PH1 and PH5 , the two P‐ATPases required for vacuolar hyperacidification in the epidermis of petals (Faraco et al., , ; Quattrocchio et al., ; Verweij et al., ), consistent with the pH values measured in petals.…”

Section: Resultssupporting

confidence: 56%

Identification and functional analysis of three new anthocyanin R2R3‐MYB genes in Petunia

et al. 2019

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We identified three novel members of the R2R3‐ MYB clade of anthocyanin regulators in the genome of the purple flowering Petunia inflata S6 wild accession, and we called them ANTHOCYANIN SYNTHESIS REGULATOR ( ASR ). Two of these genes, ASR 1 and ASR 2, are inactivated by two different single base mutations in their coding sequence. All three of these genes are absent in the white flowering species P. axillaris N and P. parodii , in the red flowering P. exserta , and in several Petunia hybrida lines, including R27 and W115. P. violacea and other P . hybrida lines (M1, V30, and W59) instead harbor functional copies of the ASR genes. Comparative, functional and phylogenic analysis of anthocyanin R2R3‐ MYB genes strongly suggest that the ASR genes cluster is a duplication of the genomic fragment containing the other three R2R3‐ MYB genes with roles in pigmentation that were previously defined, the ANTHOCYANIN 4‐ DEEP PURPLE ‐ PURPLE HAZE ( AN 4 ‐ DPL ‐ PHZ ) cluster. An investigation of the genomic fragments containing anthocyanin MYB s in different Petuni a accessions reveals that massive rearrangements have taken place, resulting in large differences in the regions surrounding these genes, even in closely related species. Yeast two‐hybrid assays showed that the ASR proteins can participate in the WMBW ( WRKY , MYB , B‐ HLH , and WDR ) anthocyanin regulatory complex by interacting with the transcription factors AN 1 and AN 11. All three ASR s can induce anthocyanin synthesis when ectopically expressed in P. hybrida lines, but ASR 1 appeared to be the most effective. The expression patterns of ASR 1 and ASR 2 cover several different petunia tissues with higher expression at early stages of bud development. In contrast, ASR 3 is only weakly expressed in the stigma, ovary, and anther filaments. The characterization of these novel ASR MYB genes completes the picture of the MYB members of the petunia anthocyanin regulatory ...

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Section: Resultssupporting

confidence: 56%

Identification and functional analysis of three new anthocyanin R2R3‐MYB genes in Petunia

et al. 2019

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“…Interestingly, a proteomics screen for the Arabidopsis SYP132 interactome has identified the H + -ATPase proteins as one of the SNARE binding partners (Fujiwara et al, 2014). Indeed, some interesting interactions of trafficking SNAREs with non-SNARE proteins are noted to affect cellular traffic and plant physiology (Honsbein et al, 2009;Faraco et al, 2017;Barozzi et al, 2019). We are currently investigating the dynamics of SYP132 interactions and their relationship to H + -ATPase traffic as well as the physiology of plant growth.…”

Section: Resultsmentioning

confidence: 99%

Unusual Roles of Secretory SNARE SYP132 in Plasma Membrane H⁺-ATPase Traffic and Vegetative Plant Growth

et al. 2019

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The plasma membrane proton (H +)-ATPases of plants generate steep electrochemical gradients and activate osmotic solute uptake. H +-ATPase-mediated proton pumping orchestrates cellular homeostasis and is a prerequisite for plastic cell expansion and plant growth. All evidence suggests that the population of H +-ATPase proteins at the plasma membrane reflects a balance of their roles in exocytosis, endocytosis, and recycling. Auxin governs both traffic and activation of the plasma membrane H +-ATPase proteins already present at the membrane. As in other eukaryotes, in plants, SNARE-mediated membrane traffic influences the density of several proteins at the plasma membrane. Even so, H +-ATPase traffic, its relationship with SNAREs, and its regulation by auxin have remained enigmatic. Here, we identify the Arabidopsis (Arabidopsis thaliana) Qa-SNARE SYP132 (Syntaxin of Plants132) as a key factor in H +-ATPase traffic and demonstrate its association with endocytosis. SYP132 is a low-abundant, secretory SNARE that primarily localizes to the plasma membrane. We find that SYP132 expression is tightly regulated by auxin and that augmented SYP132 expression reduces the amount of H +-ATPase proteins at the plasma membrane. The physiological consequences of SYP132 overexpression include reduced apoplast acidification and suppressed vegetative growth. Thus, SYP132 plays unexpected and vital roles in auxin-regulated H +-ATPase traffic and associated functions at the plasma membrane.

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“…Two KCO channels ( VIT_12s0028g00140 and VIT_12s0028g00130 ) are also among the identified targets. Most TPK/KCO proteins localize on the tonoplast (Voelker et al ., ; Faraco et al ., ; Appelhagen et al ., ) and in petunia epidermal petal cells are trafficked to the central vacuole via additional vacuoles, known as vacuolinos, the genesis of which are dependent on PH3 and PH4 (Faraco et al ., ). It is possible that a similar subcellular route is taken by their grapevine counterparts; the identification of putative MBWW target genes encoding proteins involved in membrane recognition, fusion and remodelling, as a RabGAP/TBC ( VIT_11s0016g05350 ) domain protein and three patatin‐like phospholipases ( VIT_18s0001g10900 ; VIT_18s0001g10830 and VIT_18s0001g10870 ), strongly suggested that vacuolar trafficking in grapevine is under the same type of regulation as in petunia.…”

Section: Discussionmentioning

confidence: 97%

The MYB5‐driven MBW complex recruits a WRKY factor to enhance the expression of targets involved in vacuolar hyper‐acidification and trafficking in grapevine

et al. 2019

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† These authors contributed equally to this work. SUMMARYThe accumulation of secondary metabolites and the regulation of tissue acidity contribute to the important traits of grape berry and influence plant performance in response to abiotic and biotic factors. In several plant species a highly conserved MYB-bHLH-WD (MBW) transcriptional regulatory complex controls flavonoid pigment synthesis and transport, and vacuolar acidification in epidermal cells. An additional component, represented by a WRKY-type transcription factor, physically interacts with the complex increasing the expression of some target genes and adding specificity for other targets. Here we investigated the function of MBW(W) complexes involving two MYBs (VvMYB5a and VvMYB5b) and the WRKY factor VvWRKY26 in grapevine (Vitis vinifera L.). Using transgenic grapevine plants we showed that these complexes affected different aspects of morphology, plant development, pH regulation, and pigment accumulation. Transcriptomic analysis identified a core set of putative target genes controlled by VvMYB5a, VvMYB5b, and VvWRKY26 in different tissues. Our data indicated that VvWRKY26 enhances the expression of selected target genes induced by VvMYB5a/b. Among these targets are genes involved in vacuolar hyper-acidification, such as the P-type ATPases VvPH5 and VvPH1, and trafficking, and genes involved in the biosynthesis of flavonoids. In addition, VvWRKY26 is recruited specifically by VvMYB5a, reflecting the functional diversification of VvMYB5a and VvMYB5b. The expression of MBWW complexes in vegetative organs, such as leaves, indicates a possible function of vacuolar hyper-acidification in the repulsion of herbivores and/or in developmental processes, as shown by defects in transgenic grape plants where the complex is inactivated.

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A Tonoplast P3B-ATPase Mediates Fusion of Two Types of Vacuoles in Petal Cells

Cited by 24 publications

References 45 publications

Identification and functional analysis of three new anthocyanin R2R3‐MYB genes in Petunia

Identification and functional analysis of three new anthocyanin R2R3‐MYB genes in Petunia

Unusual Roles of Secretory SNARE SYP132 in Plasma Membrane H⁺-ATPase Traffic and Vegetative Plant Growth

The MYB5‐driven MBW complex recruits a WRKY factor to enhance the expression of targets involved in vacuolar hyper‐acidification and trafficking in grapevine

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A Tonoplast P3B-ATPase Mediates Fusion of Two Types of Vacuoles in Petal Cells

Cited by 24 publications

References 45 publications

Identification and functional analysis of three new anthocyanin R2R3‐MYB genes in Petunia

Identification and functional analysis of three new anthocyanin R2R3‐MYB genes in Petunia

Unusual Roles of Secretory SNARE SYP132 in Plasma Membrane H+-ATPase Traffic and Vegetative Plant Growth

The MYB5‐driven MBW complex recruits a WRKY factor to enhance the expression of targets involved in vacuolar hyper‐acidification and trafficking in grapevine

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Unusual Roles of Secretory SNARE SYP132 in Plasma Membrane H⁺-ATPase Traffic and Vegetative Plant Growth