A Diverse Membrane Interaction Network for Plant Multivesicular Bodies: Roles in Proteins Vacuolar Delivery and Unconventional Secretion

Abstract

Vesicle trafficking between the membrane-bound organelles in plant cells plays crucial roles in the precise transportation of various materials, and thus supports cell proliferation and cellular polarization. Conventionally, plant prevacuolar compartments (PVCs), identified as multivesicular bodies (MVBs), play important roles in both the secretory pathway as intermediate compartments and the endocytic pathway as late endosomes. In recent years, the PVC/MVBs have been proposed to play important roles in both protein vacuolar delivery and unconventional secretion, but several important questions on the new regulators and environmental cues that coordinate the PVC/MVB-organelle membrane interactions and their biological significances remain. In this review, we first summarize the identity and nature of the plant PVC/MVBs, and then we present an update on our current understanding on the interaction of PVC/MVBs with other organelles in the plant endomembrane system with focus on the vacuole, autophagosome, and plasma membrane (PM) in plant development and stress responses. Finally, we raise some open questions and present future perspectives in the study of PVC/MVB-organelle interactions and associated biological functions.

Gland cell responses to feeding in Drosera capensis, a carnivorous plant

“…These observations support the report of Adlassnig et al (2012) concerning endocytosis in several glands of carnivorous plants including Drosera. They clearly underline the findings of Baluska et al (2004), Samaj et al (2004), Exteberria et al (2009), Exteberria (2012, and recently Narasimhan et al (2020) that fluid-phase endocytosis is a primary route for the exchange of solutes between the apoplast and cytoplasm, and the further trafficking of endomembranes as was summarized, e.g., by Hu et al (2020). Clathrin-mediated endocytosis similar to animal cells was discussed also for plant cells, and indeed, we did find vesicles in the cytoplasm bearing proteins structurally similar to clathrin (Fig.…”

Organelle Visualization With Multicolored Fluorescent Markers in Bamboo

“…The plant prevacuolar compartment (PVC) or multivesicular body (MVB) is an organelle that not only participates in the secretory pathway that mediates protein trafficking to vacuoles but also serves in the endocytic pathway as a late endosome (LE) in plants (Hu et al, 2020a). Because VSRs are mainly concentrated on PVC/MVBs in sorting acid hydrolases to vacuoles (Sanderfoot et al, 1998), VSR reporter proteins, containing the TMD and CT regions of VSRs, were first used as an organelle marker to define the PVC (Tse et al, 2004).…”

“…The transient gene expression system, either in plant protoplasts or specific tissues, is a powerful tool in cell biology researches in plant systems. Taking the advantage of its convenience, rapidity, and flexibility, the transient gene expression in protoplasts has been the most efficient and widely used method in model plants for various functional studies including subcellular localization (Miao and Jiang, 2007;Yoo et al, 2007;Shen et al, 2014b;Falter et al, 2019), proteinprotein interaction (Yang et al, 2014;Hu et al, 2020a;Xiao et al, 2020), investigation of promoters and regulatory elements that are involved in transcription and translation (Jacobsen and Beach, 1985), and high-throughput examination of cell signaling transduction pathways in response to phytohormones, environmental cues, and pathogen-derived elicitors (Assmann et al, 1985;Sheen, 2001;Li et al, 2013;Fraiture et al, 2014;Lin et al, 2014). Due to the versatility and convenience to detect physiological and biochemical responses, protoplast-based transformation systems have also been recently established and applied to non-model plants whose transgenic platforms are not yet available or for which regeneration of transgenic plants is difficult, such as wheat (Hensel et al, 2011), maize (Zea mays) (Sheen, 2001), carrot (Daucus carota) (Rasmussen and Rasmussen, 1993), perennial ryegrass (Lolium perenne) (Yu et al, 2017), pineapple (Ananas comosus) (Priyadarshani et al, 2018), and soybean (Glycine max) (Xiong et al, 2019).…”

Unconventional Pathways of Protein Secretion: Mammals vs. Plants

“…Another aspect related to the UPS definition is that some mechanisms involved in this process are superimposable with other cellular processes such as autophagy or programmed cell death (PCD). Even if the crosstalk between organelles of different pathways may occur in specific situations, UPS is clearly determined by literature as a distinct pathway from the conventional exo–endocytic trafficking which regulates the turnover of plasma membrane proteins ( Zhang et al, 2019 ) and the autophagic route as well ( Hu et al, 2020 ). Currently investigated in many organisms, UPS seems to be related to several physiological processes like immune responses, abiotic stress responses and cell proliferation in normal growth conditions ( Pallotta and Nickel, 2020 ; Balmer and Faso, 2021 ).…”

“…Plant MVBs (alternatively named prevacuolar compartments or late endosomes) are organelles of conventional secretion pathway mediating the transport from the Golgi to vacuoles ( Hu et al, 2020 ), but MVBs can also participate in UPS pathways by fusing with the plasma membrane to release their ILVs to the apoplast. These ILVs, referred to as exosomes, take part in intercellular communication and carry small RNAs and proteins ( Cai et al, 2018 ).…”