K63-linked ubiquitin chains are a global signal for endocytosis and contribute to selective autophagy in plants

Saeed, Bushra; Deligne, Florian; Brillada, Carla; Dünser, Kai; Ditengou, Franck Aniset; Turek, Ilona; Allahham, Alaa; Grujic, Nenad; Dagdas, Yasin; Ott, Thomas; Kleine‐Vehn, Jürgen; Vert, Grégory; Trujillo, Marco

doi:10.1016/j.cub.2023.02.024

Cited by 15 publications

(5 citation statements)

References 66 publications

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“…However, K11‐ or K29‐ubiquitin chains, as well as multiple mono‐ubiquitination, are also commonly known as degradation signals (Swatek & Komander, 2016; Yau & Rape, 2016). By contrast, K63‐linked polyubiquitination is involved in various cellular processes such as signal transduction, DNA repair, endocytosis, and selective autophagy (Silva et al ., 2015; Saeed et al ., 2023). K63‐linked ubiquitination regulates the correct MVB sorting of proteins, which may ultimately affect protein trafficking and quality, especially membrane proteins.…”

Section: Discussionmentioning

confidence: 99%

Potato E3 ubiquitin ligase StRFP1 positively regulates late blight resistance by degrading sugar transporters StSWEET10c and StSWEET11

Wu,

Lin,

Zhou

et al. 2024

New Phytologist

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Summary Potato (Solanum tuberosum) is the fourth largest food crop in the world. Late blight, caused by oomycete Phytophthora infestans, is the most devastating disease threatening potato production. Previous research has shown that StRFP1, a potato Arabidopsis Tóxicos en Levadura (ATL) family protein, positively regulates late blight resistance via its E3 ligase activity. However, the underlying mechanism is unknown. Here, we reveal that StRFP1 is associated with the plasma membrane (PM) and undergoes constitutive endocytic trafficking. Its PM localization is essential for inhibiting P. infestans colonization. Through in vivo and in vitro assays, we investigated that StRFP1 interacts with two sugar transporters StSWEET10c and StSWEET11 at the PM. Overexpression (OE) of StSWEET10c or StSWEET11 enhances P. infestans colonization. Both StSWEET10c and StSWEET11 exhibit sucrose transport ability in yeast, and OE of StSWEET10c leads to an increased sucrose content in the apoplastic fluid of potato leaves. StRFP1 ubiquitinates StSWEET10c and StSWEET11 to promote their degradation. We illustrate a novel mechanism by which a potato ATL protein enhances disease resistance by degrading susceptibility (S) factors, such as Sugars Will Eventually be Exported Transporters (SWEETs). This offers a potential strategy for improving disease resistance by utilizing host positive immune regulators to neutralize S factors.

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Section: Discussionmentioning

confidence: 99%

Potato E3 ubiquitin ligase StRFP1 positively regulates late blight resistance by degrading sugar transporters StSWEET10c and StSWEET11

Wu,

Lin,

Zhou

et al. 2024

New Phytologist

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“…Notably, all polyubiquitin linkage types were present in chloroplasts, and K63 was shown to be one of the most abundant types, second only to K48 (Sun et al , 2022), implying that ubiquitinated chloroplast proteins can have fates other than proteasomal degradation. Ubiquitination is a key mechanism governing cellular signaling, and K63‐linked polyubiquitination is particularly involved in the determination of autophagic substrate specificity in mammals and plants (Kwon & Ciechanover, 2017; Saeed et al , 2023). However, little is known about the role of K63 ubiquitination in plant autophagy, and it remained unclear how chloroplast protein cargos are regulated by this modification.…”

Section: Discussionmentioning

confidence: 99%

Selective autophagy regulates chloroplast protein import and promotes plant stress tolerance

Wan,

Zhang,

Cheng

et al. 2023

The EMBO Journal

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Chloroplasts are plant organelles responsible for photosynthesis and environmental sensing. Most chloroplast proteins are imported from the cytosol through the translocon at the outer envelope membrane of chloroplasts (TOC). Previous work has shown that TOC components are regulated by the ubiquitin‐proteasome system (UPS) to control the chloroplast proteome, which is crucial for the organelle's function and plant development. Here, we demonstrate that the TOC apparatus is also subject to K63‐linked polyubiquitination and regulation by selective autophagy, potentially promoting plant stress tolerance. We identify NBR1 as a selective autophagy adaptor targeting TOC components, and mediating their relocation into vacuoles for autophagic degradation. Such selective autophagy is shown to control TOC protein levels and chloroplast protein import and to influence photosynthetic activity as well as tolerance to UV‐B irradiation and heat stress in Arabidopsis plants. These findings uncover the vital role of selective autophagy in the proteolytic regulation of specific chloroplast proteins, and how dynamic control of chloroplast protein import is critically important for plants to cope with challenging environments.

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“…qPCR was done in a 15 µL final volume containing 10 ng cDNA, 0.3 µM of each gene-specific primer (Supplemental Table 6), and Maxima SYBR green qPCR (Thermo Fisher Scientific). Primer efficiency has already been validated (Barberon et al, 2011;Oh et al, 2012;Saeed et al, 2023;Spielmann et al, 2020). PCRs were performed using real-time PCR system CFX Opus 384.…”

Section: Quantitative Real-time Pcrmentioning

confidence: 99%

Direct non-transcriptional link between brassinosteroid perception and cortical microtubule reorientation drives hypocotyl growth

Delesalle,

Montiel-Jorda,

Neveu

et al. 2024

Preprint

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Brassinosteroids (BRs) are steroid-type phytohormones that are essential for plant growth, development and adaptation to environmental stresses. BRs promote cell wall remodelling through extensive reprogramming of gene expression, thus impacting on cell elongation and hypocotyl growth. The existence of non-genomic responses to BRs is however still unclear. Here we identified and characterized a new family of BRI1-interacting proteins identified by yeast two hybrid named MBAPs. We confirmed using several complementary approaches that MBAPs are genuine BRI1 partners in plant cells. We demonstrated that MBAPs are localized to cortical microtubules (CMTs) underlying the plasma membrane using a short conserved helix and where they contact with and are phosphorylated by BRI1. Combinations ofmbaploss-of-function mutants showed hypersensitivity to BRs and establish MBAPs as negative regulators of BR responses. Surprisingly,mbapmutants showed unaffected typical downstream BR signaling readouts and BR target gene expression. Rather,mbapmutants displayed disordered CMT network and enhanced CMT reorganization upon BR perception. Altogether, our work shed light on the direct non-transcriptional connection between BR perception at the cell surface and CMT organization in the control of hypocotyl elongation.

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K63-linked ubiquitin chains are a global signal for endocytosis and contribute to selective autophagy in plants

Cited by 15 publications

References 66 publications

Potato E3 ubiquitin ligase StRFP1 positively regulates late blight resistance by degrading sugar transporters StSWEET10c and StSWEET11

Potato E3 ubiquitin ligase StRFP1 positively regulates late blight resistance by degrading sugar transporters StSWEET10c and StSWEET11

Selective autophagy regulates chloroplast protein import and promotes plant stress tolerance

Direct non-transcriptional link between brassinosteroid perception and cortical microtubule reorientation drives hypocotyl growth

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