Autophagy-Related Direct Membrane Import from ER/Cytoplasm into the Vacuole or Apoplast: A Hidden Gateway also for Secondary Metabolites and Phytohormones?

Abstract

Transportation of low molecular weight cargoes into the plant vacuole represents an essential plant cell function. Several lines of evidence indicate that autophagy-related direct endoplasmic reticulum (ER) to vacuole (and also, apoplast) transport plays here a more general role than expected. This route is regulated by autophagy proteins, including recently discovered involvement of the exocyst subcomplex. Traffic from ER into the vacuole bypassing Golgi apparatus (GA) acts not only in stress-related cytoplasm recycling or detoxification, but also in developmentally-regulated biopolymer and secondary metabolite import into the vacuole (or apoplast), exemplified by storage proteins and anthocyanins. We propose that this pathway is relevant also for some phytohormones’ (e.g., auxin, abscisic acid (ABA) and salicylic acid (SA)) degradation. We hypothesize that SA is not only an autophagy inducer, but also a cargo for autophagy-related ER to vacuole membrane container delivery and catabolism. ER membrane localized enzymes will potentially enhance the area of biosynthetic reactive surfaces, and also, abundant ER localized membrane importers (e.g., ABC transporters) will internalize specific molecular species into the autophagosome biogenesis domain of ER. Such active ER domains may create tubular invaginations of tonoplast into the vacuoles as import intermediates. Packaging of cargos into the ER-derived autophagosome-like containers might be an important mechanism of vacuole and exosome biogenesis and cytoplasm protection against toxic metabolites. A new perspective on metabolic transformations intimately linked to membrane trafficking in plants is emerging.

Autophagy Modulates Articular Cartilage Vesicle Formation in Primary Articular Chondrocytes

“…Recent work supports a potential association of autophagy with exosome formation (9). Autophagy is a constitutive degradative pathway of cellular homeostasis and organelle turnover, and involves formation of autophagosomes containing unwanted proteins and organelles, which fuse with lysosomes to recycle the energy-rich components of these materials (10).…”

Subcellular compartmentalization in protoplasts from Artemisia annua cell cultures: Engineering attempts using a modified SNARE protein

“…The sorting and accumulation mechanism was not sufficiently investigated but it would not be a surprising mechanism. Anthocyanin autophagy-related vesicular import pathway from ER into the vacuole is an example of compartmentation with the help of autophagocitosis (Kulich and Zarsky, 2014).…”

“…The accumulation of the metabolite occurs in the apoplast of glandular trichomes and it seems to arrive there by autophagy-related exosome secretion (Krause et al, 2013). Several examples of this mechanism were recently reviewed (Kulich and Zarsky, 2014) and are well represented in maize cells where autofluorescent membrane-bound bodies derived from the ER were induced and secreted upon the induction of the P1 transcription factor (Lin et al, 2003). Similarly to those autofluorescent compounds, phenylpropanoids are found in the cell walls esterified to the polysaccharides, but they reach the apoplast travelling from the ER to plasma membrane (PM) in small membrane vesicles aggregating into bigger structures before fusing with the PM.…”

“…Similarly to those autofluorescent compounds, phenylpropanoids are found in the cell walls esterified to the polysaccharides, but they reach the apoplast travelling from the ER to plasma membrane (PM) in small membrane vesicles aggregating into bigger structures before fusing with the PM. These compartments might be generated by autophagy-related process similar to that observed in epidermal cells of leaves invaded by pathogens, where the mechanism is based on multivesicular bodies (MVB)-derived exosomes (Meyer et al, 2009;Kulich and Zarsky, 2014).…”

Vacuolar Sorting Mechanisms are Differently Influenced by Detoxification Processes

“…This pathway needs to be supported by transporters on the tonoplast and by an adequate vacuolar compartmentalization; in fact it shares many features and problematics with the pathway for vacuolar secondary metabolites accumulation. As for secondary metabolites, such as anthocyanins [1,2], specific compartmentalization adaptations could be observed and the sequence of traffic events remains unclear [3]. Here we investigated the alteration induced by GST overexpression and/or glyphosate treatment on the vacuolar sorting pathway using two known vacuolar markers: AleuGFP (Sar1 dependent sorting) and GFPChi (Sar1 independent sorting) [4].…”