A plant Bro1 domain protein BRAF regulates multivesicular body biogenesis and membrane protein homeostasis

Shen, Jinbo; Zhao, Qiong; Wang, Xiangfeng; Gao, Caiji; Zhu, Ying; Zeng, Yonglun; Jiang, Liwen

doi:10.1038/s41467-018-05913-y

Cited by 46 publications

(39 citation statements)

References 63 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Col-0, RabF2b-YFP (Wave2Y), Got1p homolog-YFP (Wave 22Y) seeds were obtained from the Arabidopsis Resource Center (ABRC) stock centre (Ohio, U.S.A.). Arabidopsis FLS2-GFP, pREM1.2::YFP:REM1.2, CLC-GFP, BRI1-GFP and BOR1-GFP marker lines were described previously (18, 57; 108, 109,110). Sterol mutants fkX224 , smt1-1 and their WT ecotypes were described previously (111, 112).…”

Section: Experimental Model and Subject Detailsmentioning

confidence: 99%

The bacterial quorum sensing signal DSF hijacksArabidopsis thalianasterol biosynthesis to suppress plant innate immunity

Tran

Triebl

et al. 2020

Preprint

View full text Add to dashboard Cite

36Quorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-37 related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is 38 largely under-studied. In this work, we show that the QS molecule DSF (cis-11-methyl-dodecenoic acid) 39 produced by Xanthomonas campestris pv. campestris can suppress pathogen-associated molecular 40 pattern (PAMP)-triggered immunity (PTI) in Arabidopsis thaliana, mediated by flagellin-induced activation 41 of flagellin receptor FLS2. The DSF-mediated attenuation of innate immunity results from the alteration of 42 oligomerization states and endocytic internalization of plasma membrane FLS2. DSF altered the lipid 43 profile of Arabidopsis, with a particular increase of the phytosterol species, which impairs the general 44 endocytosis pathway mediated by clathrin and FLS2 nano-clustering on the plasma membrane. The DSF 45 effect on receptor dynamics and host immune responses could be entirely reversed by sterol removal. 46Together, our results highlighted the importance of sterol homeostasis to plasma membrane organization 47 and demonstrate a novel mechanism by which pathogenic bacteria use their communicating molecule to 48 manipulate PAMP-triggered host immunity. 49 50 Keywords: quorum sensing, plasma membrane, endocytosis, plant-pathogen interaction 51 52 SIGNIFICANCE STATEMENT 53Bacteria rely on small signalling molecules called quorum sensing (QS) signals to communicate 54 and coordinate their behaviors. QS is known to regulate gene expression, production of virulence factors, 55 and biofilm formation for pathogenic bacteria to effectively colonize their hosts and cause diseases. In this 56 work, we found a class of QS molecule called diffusible-signal factor (DSF), produced by devastating 57 phytopathogenic bacteria such as Xanthomonas spp. and Xylella fastidiosa, could communicate directly 58 with plant host and subvert plant innate immunity by inducing plant sterol production and thereby, 59 attenuating receptor signalling through hindering the receptor clustering and plant endocytosis. The 60 results significantly enrich our understanding of the mechanisms in the tug-of-war between bacterial 61 pathogenesis and host immunity. 62 63 infection (4). The 3OC12-HSL was also shown to be recognized by the bitter taste receptor, T2R family 73 protein, T2R38 in neutrophils, lymphocytes and monocytes to activate innate immune responses (5). 74Similarly, plant pathogenic bacteria also secrete small-molecule virulence factors to cross-talk with host 75 and manipulate host immunity during infection. QS molecules produced by several bacterial 76 phytopathogens showed a wide range of interference in host development and defence mechanisms, 77including the root morphological development in an auxin-dependent manner or callose deposition during 78 immune responses (6-8). However, the detailed mechanisms of how QS molecules directly influence 79 plant host development and pathology, especially the PAMP-mediated host immunity,...

show abstract

Section: Experimental Model and Subject Detailsmentioning

confidence: 99%

The bacterial quorum sensing signal DSF hijacksArabidopsis thalianasterol biosynthesis to suppress plant innate immunity

Tran

Triebl

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Plantspecific substitutes for this subunit could be several ubiquitin receptors in the early endocytic pathway of plants (Mosesso et al, 2019). In Arabidopsis the conserved scaffolding protein, apoptosis-linked gene-2 interacting protein X (ALIX), binds membranes, ubiquitin, and K63-linked ubiquitin chains, and interacts with Vacuolar Sorting Protein 23A (VPS23A) and FYVE1 (Fab1, YOTB, Vac1, and EEA1)/FREE1 (FYVE DOMAIN PROTEIN REQUIRED FOR ENDOSOMAL SORTING 1), essential for ESCRT-I as well as ESCRT-III function (Cardona-Lopez et al, 2015;Kalinowska et al, 2015;Shen et al, 2018). The plantspecific FYVE1/FREE1 localizes to MVBs and binds ubiquitin as well as PtdIns(3)P, and furthermore interacts with the Src homology-3 (SH3) domain-containing protein 2 (SH3P2), VPS23A/B, and the ESCRT-III complex (Barberon et al, 2014;Gao et al, 2014;Kolb et al, 2015;Belda-Palazon et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

TOLs Function as Ubiquitin Receptors in the Early Steps of the ESCRT Pathway in Higher Plants

et al. 2020

View full text Add to dashboard Cite

Protein abundance and localization at the plasma membrane (PM) shapes plant development and mediates adaptation to changing environmental conditions. It is regulated by ubiquitination, a post-translational modification crucial for the proper sorting of endocytosed PM proteins to the vacuole for subsequent degradation. To understand the significance and the variety of roles played by this reversible modification, the function of ubiquitin receptors, which translate the ubiquitin signature into a cellular response, needs to be elucidated. In this study, we show that TOL (TOM1-like) proteins function in plants as multivalent ubiquitin receptors, governing ubiquitinated cargo delivery to the vacuole via the conserved Endosomal Sorting Complex Required for Transport (ESCRT) pathway. TOL2 and TOL6 interact with components of the ESCRT machinery and bind to K63-linked ubiquitin via two tandemly arranged conserved ubiquitin-binding domains. Mutation of these domains results not only in a loss of ubiquitin binding but also altered localization, abolishing TOL6 ubiquitin receptor activity. Function and localization of TOL6 is itself regulated by ubiquitination, whereby TOL6 ubiquitination potentially modulates degradation of PM-localized cargoes, assisting in the fine-tuning of the delicate interplay between protein recycling and downregulation. Taken together, our findings demonstrate the function and regulation of a ubiquitin receptor that mediates vacuolar degradation of PM proteins in higher plants.

show abstract

“…Studies using state-of-the-art techniques revealed many details on the underlying mechanisms of plant membrane transport (reviewed in Paez . Although many conserved trafficking regulators have been found to be as important in plants as in other organisms, at the same time, plant-specific regulators have also been identified (Gao et al, 2014;Kolb et al, 2015;Nagel et al, 2017;Reyes et al, 2014;Shen et al, 2018), providing a glimpse into the intriguing adaptation and evolution of this pathway.…”

Section: Tom1-like Proteins Are Ub Adaptor Proteins Expanded In Plantsmentioning

confidence: 99%

“…In mammals, an additional Bro1 domain-containing protein, His domain phosphotyrosine phosphatase (HD-PTP, also known as PTPN23), has been reported to be involved in ESCRT-dependent intracellular trafficking events (Ali et al, 2013; Gahloth et al, 2016). Besides ALIX, four Bro1 domain-containing proteins can be found in the Arabidopsis genome (Shen et al, 2018). Although a second Bro1 domain-containing protein named BRO1-DOMAIN PROTEIN AS FYVE1/FREE1 SUPPRESSOR (BRAF) has been shown to be involved in plant endosomal protein degradation, there is no obvious homolog of HD-PTP in the Arabidopsis genome (Shen et al, 2018).…”

Section: Tom1-like Proteins Are Ub Adaptor Proteins Expanded In Plantsmentioning

confidence: 99%

“…Besides ALIX, four Bro1 domain-containing proteins can be found in the Arabidopsis genome (Shen et al, 2018). Although a second Bro1 domain-containing protein named BRO1-DOMAIN PROTEIN AS FYVE1/FREE1 SUPPRESSOR (BRAF) has been shown to be involved in plant endosomal protein degradation, there is no obvious homolog of HD-PTP in the Arabidopsis genome (Shen et al, 2018).…”

Section: Tom1-like Proteins Are Ub Adaptor Proteins Expanded In Plantsmentioning

confidence: 99%

See 1 more Smart Citation

Ubiquitin recognition in endocytic trafficking – with or without ESCRT-0

Mosesso

Nagel

Isono

2019

Journal of Cell Science

View full text Add to dashboard Cite

The ability to sense and adapt to the constantly changing environment is important for all organisms. Cell surface receptors and transporters are key for the fast response to extracellular stimuli and, thus, their abundance on the plasma membrane has to be strictly controlled. Heteromeric endosomal sorting complexes required for transport (ESCRTs) are responsible for mediating the post-translational degradation of endocytosed plasma membrane proteins in eukaryotes and are essential both in animals and plants. ESCRTs bind and sort ubiquitylated cargoes for vacuolar degradation. Although many components that comprise the multi-subunit ESCRT-0, ESCRT-I, ESCRT-II and ESCRT-III complexes are conserved in eukaryotes, plant and animal ESCRTs have diverged during the course of evolution. Homologues of ESCRT-0, which recognises ubiquitylated cargo, have emerged in metazoan and fungi but are not found in plants. Instead, the Arabidopsis genome encodes plant-specific ubiquitin adaptors and a greater number of target of Myb protein 1 (TOM1) homologues than in mammals. In this Review, we summarise and discuss recent findings on ubiquitin-binding proteins in Arabidopsis that could have equivalent functions to ESCRT-0. We further hypothesise that SH3 domain-containing proteins might serve as membrane curvature-sensing endophilin and amphiphysin homologues during plant endocytosis.

show abstract

A plant Bro1 domain protein BRAF regulates multivesicular body biogenesis and membrane protein homeostasis

Cited by 46 publications

References 63 publications

The bacterial quorum sensing signal DSF hijacksArabidopsis thalianasterol biosynthesis to suppress plant innate immunity

The bacterial quorum sensing signal DSF hijacksArabidopsis thalianasterol biosynthesis to suppress plant innate immunity

TOLs Function as Ubiquitin Receptors in the Early Steps of the ESCRT Pathway in Higher Plants

Ubiquitin recognition in endocytic trafficking – with or without ESCRT-0

Contact Info

Product

Resources

About