Plant immunity is antagonized by pathogenic effectors during interactions with bacteria, viruses or oomycetes. These effectors target core plant processes to promote infection. One such core plant process is autophagy, a conserved proteolytic pathway involved in ensuring cellular homeostasis. It involves the formation of autophagosomes around proteins destined for autophagic degradation. Many cellular components from organelles, aggregates, inactive or misfolded proteins have been found to be degraded via autophagy. Increasing evidence points to a high degree of specificity during the targeting of these components, strengthening the idea of selective autophagy. Selective autophagy receptors bridge the gap between target proteins and the forming autophagosome. To achieve this, the receptors are able to recognize specifically their target proteins in a ubiquitin-dependent or -independent manner, and to bind to ATG8 via canonical or non-canonical ATG8-interacting motifs. Some receptors have also been shown to require oligomerization to achieve their function in autophagic degradation. We summarize the recent advances in the role of selective autophagy in plant immunity and highlight NBR1 as a key player. However, not many selective autophagy receptors, especially those functioning in immunity, have been characterized in plants. We propose an in silico approach to identify novel receptors, by screening the Arabidopsis proteome for proteins containing features theoretically needed for a selective autophagy receptor. To corroborate these data, the transcript levels of these proteins during immune response are also investigated using public databases. We further highlight the novel perspectives and applications introduced by immunity-related selective autophagy studies, demonstrating its importance in research.

Plant immunity centers around the plant-pathogen interface, where an intriguing arms race occurs at the molecular level. Plants defend themselves against pathogens using their innate immunity, where broad resistance to pathogens is conferred by pathogen-associated-molecular-pattern (PAMP)-triggered immunity (PTI), which involves recognition of conserved molecules shared by pathogens by surface-localized pattern-recognition receptors (PRRs) [1–3]. For a successful infection, plant pathogens such as bacteria, fungi or oomycetes colonize the plant extracellular space and secrete effector proteins into the host cell cytoplasm, which then target essential pathways in the plant [2,4,5]. Plant viruses are rather obligate intracellular parasites, but likewise utilize effectors for manipulating host processes from within the plant cell, and to facilitate cell-to-cell movement [6–8]. Effectors have been shown to target key plant processes such as PTI signaling, cytoskeleton localization and endocytic trafficking, in a process termed “effector-targeted pathways (ETP)” [4]. Effectors can in turn be recognized by nucleotide-binding leucine-rich repeat receptors (NLRs), which guard host immune components and induce effector-triggered immunity (ETI) [1–3].

As cellular processes are mediated to a great extent by proteins, plant proteostasis i.e. the homeostasis of the plant proteome is an important factor to consider in immunity. Proteostasis is the dynamic and constant interplay between protein synthesis and degradation, which can be influenced by factors such as protein translation, folding, localization, post-translational modifications, proteasome and autophagic activity [9]. A major hub where effectors converge for ETP are the main protein degradation pathways, autophagy and the ubiquitin–proteasome system (UPS) [5]. Both proteolytic pathways have been shown to be essential, where knockouts of some genes involved in these processes result in severe growth defects, especially under nutrient limiting conditions [10,11]. Autophagy also functions directly in immunity to limit infection [7,8,12]. It follows that targeting of autophagy and UPS pathways through ETP could be highly effective in perturbing host cell during infection, and indeed many examples of this has been described, as reviewed in Langin et al. [5].

Macroautophagy (henceforth autophagy) is essential for cellular homeostasis through intracellular constituent recycling and mediates degradation of large protein complexes, insoluble protein aggregates and dysfunctional organelles [11]. The mechanism behind autophagy is generally conserved in eukaryotes and involves the coordinated action of around 40 autophagy-related (ATG) genes to direct formation of the autophagosome, a double-membraned vesicle that envelops cytosolic material such as proteins and organelles destined for degradation [11,13,14]. In brief, during plant autophagy, ATG1 and ATG13 take in signals from Target of Rapamycin (TOR) kinase which is influenced by both developmental and nutritional signals, although it is to note that TOR-independence exists for oxidative or ER stress-related autophagy [15]. During TOR-dependent autophagy, TOR blocks autophagy by phosphorylating ATG13, which prevents its association with ATG1. Upon nutrient deficiency or other TOR-inactivating conditions, ATG13 is rapidly dephosphorylated which results in ATG1 binding. Additional hypo-and hyperphosphorylation events allow the assembly of the ATG1, ATG13 and the accessory subunits ATG11 and ATG101. The active ATG1 kinase complex then promotes the ATG9-mediated delivery of lipids and membrane sources derived from the ER to the developing phagophore. Nucleation and expansion of the phagophore also involves the VPS34 lipid kinase, which generates PI3P on the phagophore membrane. In parallel, a ubiquitin-like conjugation system (ATG5/ATG12/ATG16) drives the conjugation of ATG8 to PE, which decorates the autophagosome membrane. The autophagosome is further sealed by recruitment of SH3 domain-containing protein 2 (SH3P2) that stimulates phagophore curvature. Mature autophagosomes are delivered to the lytic vacuole for degradation by vacuolar hydrolases.

Many steps in this pathway have been shown to be modulated during plant–pathogen interactions, with excellent reviews summarizing the known examples [5,7,12]. Effectors from plant pathogens were also shown to target different components of the host autophagic machinery, strengthening the idea that autophagy is a key cellular process in immunity [16]. Autophagy has been shown play both pro- and anti-pathogen roles [7,8,12]. Thus, there must be a high degree of regulation behind plant-pathogen interactions. In this review, we focus on protein degradation via selective autophagy, and its role in adding specificity to plant immunity.

Our early understanding of autophagy characterized it as a non-specific “bulk” process, where cell cytoplasmic contents are “randomly” engulfed and degraded. Although it was already suggested then that autophagy displays selectivity toward cargo [17], only with the characterization of selective autophagy receptors (SARs, abbreviation not to be confused with systemic acquired resistance) there is strong proof of substrate specificity in autophagy [18]. Receptors have been identified for the selective autophagy of many cellular components across a range of eukaryotic organisms, for example proteasomes (proteaphagy), endoplasmic reticulum (ER-phagy), intracellular pathogens (xenophagy), protein aggregates (aggrephagy) and mitochondria (mitophagy) [19–22] (Figure 1). Particularly relevant to immunity, xenophagy of intracellular bacteria, viruses, protozoa and fungi have been well-described in mammalian systems, whereas for plants most research is directed at xenophagy of viruses [7,8,23,24]. Research on receptors and their identified substrates have been well-summarized for plants [20,25] and for the yeast model system [19]. Thus, in this review, we rather summarize common patterns behind domain organization of SARs and highlight recent advances in plant research regarding selective autophagy and immunity.

Selective autophagy is involved in the degradation of cellular and pathogenic components

Figure 1
Selective autophagy is involved in the degradation of cellular and pathogenic components

Selective autophagy receptors (SARs) bring their substrate to the nascent autophagosome ATG8 interaction. Substrate binding can be ubiquitin-dependent or -independent. The cargo for xenophagy and effectorphagy includes viral proteins and bacterial effectors. Protein aggregates are targeted in aggrephagy. Organelles such as endoplasmic reticulum (ER), proteasome, and mitochondria are the cargo for ER-phagy, proteaphagy and mitophagy respectively. Specific proteins such as FLS2 and BES1 have also been found to be targeted by SARs. Examples were highlighted based on data availability on ubiquitin-binding and AIM/LIR/UIM-containing. For a comprehensive review on receptors and their substrates see [19,20,25].

Figure 1
Selective autophagy is involved in the degradation of cellular and pathogenic components

Selective autophagy receptors (SARs) bring their substrate to the nascent autophagosome ATG8 interaction. Substrate binding can be ubiquitin-dependent or -independent. The cargo for xenophagy and effectorphagy includes viral proteins and bacterial effectors. Protein aggregates are targeted in aggrephagy. Organelles such as endoplasmic reticulum (ER), proteasome, and mitochondria are the cargo for ER-phagy, proteaphagy and mitophagy respectively. Specific proteins such as FLS2 and BES1 have also been found to be targeted by SARs. Examples were highlighted based on data availability on ubiquitin-binding and AIM/LIR/UIM-containing. For a comprehensive review on receptors and their substrates see [19,20,25].

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One component underlying the mechanism of action behind selective autophagy is the receptor, and the study of these SARs has been a substantial driving force behind our understanding of selective autophagy. Despite the wide range of targets and functions, there are nonetheless common patterns that can be established in the mechanism of selective autophagy. In principle, SARs should be able to achieve two tasks. First—to recognize its substrate, either directly or via polyubiquitin chains on the substrate, and second—be able to bring the bound substrate to the autophagy machinery by binding ATG8, for example via ATG8-interacting motifs (AIMs), LC3-interacting motifs (LIR) or ubiquitin-interacting motifs (UIM) [19,20,25–27] (Figure 2).

Domain organization of selective autophagy receptors (SAR)

Figure 2
Domain organization of selective autophagy receptors (SAR)

SARs can have ubiquitin-binding domains (UBD) that aids in substrate recognition. ATG8-, LC3- or ubiquitin- interacting motif (AIM/LIR/UIM) of the SAR contacts the LC3 docking site (LDS) on ATG8. Some SARs also contain domains that promote oligomerization.

Figure 2
Domain organization of selective autophagy receptors (SAR)

SARs can have ubiquitin-binding domains (UBD) that aids in substrate recognition. ATG8-, LC3- or ubiquitin- interacting motif (AIM/LIR/UIM) of the SAR contacts the LC3 docking site (LDS) on ATG8. Some SARs also contain domains that promote oligomerization.

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Ubiquitin-dependent substrate recognition

Many SARs recognize polyubiquitinated substrates, and contain ubiquitin-binding domains for the recognition of their target substrate [26]. The post-translational modification ubiquitination, also known as ubiquitylation, is described as “eat me” signal due to its role in targeting proteins toward degradative processes [28]. Ubiquitin is conjugated on a lysine residue of a target protein based on the enzymatic cascade of ubiquitin-activating (E1), ubiquitin-conjugating (E2) and ubiquitin-ligase (E3) enzymes [29]. The presence of internal lysine residues allows further conjugation of ubiquitin with itself to form polyubiquitinated chains which mark proteins for degradation [28], although targeting toward non-degradative processes such as the regulation of protein interactions and signal transduction also possible [29,30]. Domains known to bind ubiquitin include UBA (ubiquitin associated), UIM (ubiquitin-interacting motif), CUE (coupling of ubiquitin conjugation to endoplasmic reticulum degradation), TOM (target of Myb) and more as reviewed in [31].

One well-characterized plant SAR is NEIGHBOR OF BRCA1 gene 1 (NBR1), also known as Joka2 in solanaceous plants, which is a homolog of mammalian NBR1 and functionally similar to p62 [32,33]. NBR1 contains two UBA domains, but it was shown that only the C-terminal UBA domain of A. thaliana NBR1 could bind ubiquitin, and is thought to be involved in recognition of ubiquitinated targets for selective autophagy [32].

DOMINANT SUPPRESSOR OF KAR 2 (DSK2) is another SAR which acts as a ubiquitin receptor for BRI1-EMS SUPRESSOR 1 (BES1), the master regulator of the brassinosteroid (BR) pathway. Degradation of BES1 by DSK2 requires its UBA domain that can bind polyubiquitin chains, and AIM motif [34].

Similarly, proteasome subunit RPN10 which directs the 26S proteasome towards selective autophagy can bind both ubiquitin and ATG8 [35]. Additionally some proteasome subunits were found to be ubiquitinated thus strengthening RPN10 as a ubiquitin-dependent SAR [35,36].

Considering the role of ubiquitination as a degradation signal and the ubiquitin-binding ability of some SARs, many selective autophagy targets likely undergo ubiquitination. In fact, ubiquitinated proteins are observed to hyperaccumulate in nbr1 or atg5 mutants upon infection conditions shown to induce autophagy [37]. Thus, we hypothesize there are additional SARs with ubiquitin binding ability, and investigate this in more detail below.

Ubiquitin-independent substrate recognition

In plant-pathogen interactions, there is evolutionary pressure on the host side to recognize pathogenic components, and on the pathogen side to escape this recognition. Indirect substrate recognition via ubiquitination is intuitively an effective strategy in which xenophagy-related SARs can participate in the xenophagy of a wide range of molecules, from viral capsids to oomycete and bacterial effectors. However, there are exceptions where substrate recognition is still achieved independently of ubiquitin association.

The turnip mosaic virus (TuMV) subunit P4 is recognized by the A. thaliana NBR1, and this interaction is still observed with a truncated NBR1 variant missing its UBA domain, suggesting for ubiquitin-independence in the interaction [38].

A study from our lab showed that a bacterial effector XopL is recognized by NBR1 through both ubiquitin-dependent and independent mechanisms. We show through co-immunoprecipitation that XopL interacted with full-length NBR1 and UBA deletion mutants, but a higher molecular weight species hypothesized to be ubiquitinated XopL, only interacted with NBR1 when a functional UBA domain is present [39].

Both these examples of ubiquitin-independence during NBR1-mediated xenophagy are intriguing as NBR1 is the only xenophagy receptor identified so far in plants. Are there more similar examples to be discovered, and if so how would NBR1 recognize the diverse effectors and viral subunits that could be present within the host cell? Are there some conserved features such as structure, that can drive the recognition of these foreign molecules by xenophagy receptors? Indeed, this could be a possibility, given that plant ER-phagy receptors ATG8-interacting proteins 1 and 2 (ATI1/2) share structural similarity with other ER-phagy receptors, where their AIM is located at the end of long, intrinsically disordered cytosolic regions [40]. The structure to function relationship is proposed as the disordered domain could bridge the membrane of the rough ER to ATG8 on phagophores or endolysosomes [40].

Although not shown to be a SAR, exocyst subunit Exo70B2 was found to interact with ATG8 via two AIMs, and is subject to autophagic transport to the vacuole upon treatment with defense-related compounds salicylic acid (SA) and benzothiadiazole (BTH) or immunogenic peptide flg22 [41]. We speculate that Exo70B2 could function as a SAR, directing cargo toward autophagic degradation. Interestingly, Exo70B2 is phosphorylated by the immunity-related kinase MPK3 that enhances its interaction with ATG8 [41]. Thus, if Exo70B2 acts as a SAR, this phosphorylation could present a novel way in which SARs are regulated.

Although not related to immunity, plant mitophagy receptor, FRIENDLY (FMT) does not have UBA domain yet mediates the recycling of damaged mitochondria in Arabidopsis [42]. Furthermore, plant ER-phagy receptors ATI1/2, Sec62, C53, reticulon proteins 1 and 2 (Rtn1/2) and degrade specific proteins in the ER during proteotoxic stress [43–45] or dark-induced starvation [46]. These proteins do not have any predicted ubiquitin-binding functions, thus future work should confirm their ubiquitin-independence and characterize the mechanism.

For mammalian systems as well, under specific conditions receptors link their cargo to autophagosomes during mitophagy, pexophagy, and virophagy in a ubiquitin-independent manner [47]. Thus, is entirely possible that there are more examples of ubiquitin-independent selective autophagy involved in immunity.

Motifs for ATG8 interaction

Once a target substrate is bound, the subsequent role of a SAR is to bring its bound substrate to the autophagic machinery, usually the nascent autophagosome. To achieve this, canonical ATG8-interacting motif (AIM), otherwise known as LC3-interacting region (LIR), or the non-canonical ubiquitin-interacting motif (UIM) on a SAR is crucial, since the autophagosome is decorated with ATG8 proteins to facilitate this specific binding [48,49]. Mechanistically, this binding between the SAR and ATG8 occurs as the AIM/LIR contacts a hydrophobic patch on ATG8 known as the LIR docking site (LDS) [50,51].

Plant NBR1 has a canonical AIM facilitating its interaction with ATG8 on autophagosomes [32,33]. Svenning et al. additionally showed that AtNBR1 during co-expression with AtATG8 or human GABARAPL2, required its AIM to be recognized as an autophagic substrate in HeLa cells [32].

Many other SARs have been found to contain AIMs which are crucial for their function in selective autophagy, for example as mentioned above DSK2, RPN10 and potentially Exo70B2 [34,35,41].

RPN10 was additionally shown to have a UIM, which is a non-canonical motif for ATG8 interaction named for its similarity to existing UIM [35,52]. The authors further screened known ATG8-binding proteins for UIM, and identified three PUX proteins, thus raising the possibility that novel SARs with UIM are yet to be characterized [52].

The importance of the AIM in autophagy has inspired tools for AIM prediction to aid in discovery of novel autophagy targets [53,54]. This has potential in aiding in the identification of novel SARs, and will be discussed below.

Oligomerization

Oligomerization of SARs have been shown to be especially important during selective autophagy of aggregates [55,56]. This is because protein aggregates are present as biomolecular condensates, which are membraneless assemblies where certain cellular components such as biopolymers are concentrated [57]. Domains such as Phox and Bem1p (PB1) are present on some SARs which enable their oligomerization [58]. It is rather intuitive that SARs involved in aggrephagy would oligomerize, so that they more easily localize into condensates where their targets reside. Indeed, this idea holds true when we consider the receptors Dsk2 and Cue2, which play a role in both proteasome- and autophagy-dependent protein degradation [59]. Lu and colleagues designed artificial ubiquitin- and Atg8-binding receptors, with or without the ability to oligomerize, and found that only oligomeric receptors could function in aggrephagy. Although direct evidence was not shown, a previous study suggest that Joka2 aggregates contain its multimeric form, and that in the nucleus and cytoplasm it is in a monomeric form [60].

The ubiquitin-binding domains of SARs can also contribute to their oligomerization. For example, a PB1 domain is present on plant NBR1, which allows it to form oligomers with other molecules of itself, but this oligomerization is also partially dependent on its UBA domains [32,60]. In a similar way, human p62 is the main driver of ubiquitin condensate formation, but NBR1 also promotes the p62 condensation through its PB1 and UBA domains [61].

SAR oligomerization may have wider implications beyond aggrephagy, and may function generally in promoting the interaction with ATG8. It was shown that oligomerization of mammalian p62 has an important role in stabilizing the binding to LC3 on the autophagosome membrane [55,56]. Furthermore, the DIX domain of Dishevelled (Dvl) mediates its self-oligomerization, which is ultimately required for interaction with LC3 [62]. There is also increasing evidence that autophagosome formation during autophagy involves liquid-liquid phase separation, which can be promoted by the oligomerization of SARs [63].

Plant–viral interactions

The pro-plant role of xenophagy during plant–viral interactions is well-characterized. The SAR NBR1 functions in the targeted degradation of viral particles and proteins. For example, cauliflower mosaic virus (CaMV) capsid and P4 proteins, and Turnip mosaic virus (TuMV) HcPro have been shown to be removed by NBR1 [37,38]. In turn, TuMV evolved viral proteins VPg and 6K2 to counteract NBR1-driven host xenophagy by blocking the degradation of HcPro [64]. More recently, it has been reported that nuclear autophagy degrades geminivirus nuclear protein C1 to restrict viral infection in solanaceous plants [65]. In the present study, viral protein C1 harbors an AIM which facilitates its interaction with ATG8, leading to its degradation via autophagy in the cytoplasm. Considering that AIM-containing proteins can act as autophagy adaptors or receptors it is tempting to speculate whether C1, similar to Phytophtora infestans effector PexRD54 elaborated on below, functions to target nuclear proteins upon viral infection.

A recent study identified that autophagy core component ATG6/Beclin1 might act as a SAR, as it mediates the degradation of a TuMV RNA-dependent RNA polymerase Nlb to restrict virus infection [66]. ATG6/Beclin1 was also shown to be involved in autophagy-like protein degradation of tobacco calmodulin-like protein rgs-CaM which bound to viral RNA silencing suppressor proteins, thus enhancing host antiviral RNAi [67]. Additionally, Jiang et al. identified a new cargo receptor NbP3IP with a previously unknown function, which specifically interacts with the P3 protein (VSR) of Rice stripe virus (RSV) and NbATG8f. These interactions mediate the selective degradation of the P3 protein and limit RSV infection [68].

Pro-viral effects of selective autophagy have also been described. P0 from Turnip yellows virus (TuYV) was found to manipulate selective autophagy for the degradation of ARGONAUTE1 (AGO1), exploiting ATI1 and ATI2 mediate the delivery of host AGO1 from the ER to the vacuole, ultimately down-regulating host antiviral RNA silencing [69].

Although the majority of the studies identified how SARs contribute to plant–virus interactions, further mechanistic details, such as oligomerization state of the SAR or whether substrate recognition is mediated by ubiquitin, remain still elusive.

Plant–bacterial interactions

During interactions with bacteria, plant autophagy can also function in a pro-plant or pro-bacterial manner. FLAGELLIN-SENSING 2 (FLS2), a receptor kinase which recognizes bacterial flagellin, was found to be degraded by selective autophagy [70]. Orosomucoid (ORM) proteins ORM1 and 2 act as SARs in the degradation of non-activated FLS2, which ensures sufficient amounts of activated FLS2 for signaling [70]. The pathway is hijacked for pro-pathogen effects, for example during Pseudomonas syringae infection, where it was found that a T3E HopM1 causes the targeted degradation of the host proteasome by inducing proteaphagy, which could involve the proteaphagy receptor RPN10 since Pst bacterial growth was elevated in the rpn10 mutant [37].

As viruses are the only described intracellular pathogens in plants, we propose that xenophagy includes degradation of viruses, “virophagy” and of effectors, “effectorphagy”. During effectorphagy, bacterial effectors are recognized in the plant cell and degraded via the autophagy pathway, for example as in Leong et al. [39]. The study showed that NBR1/Joka2 interacts with and causes the autophagic degradation of a Xanthomonas campestris pv. vesicatoria (Xcv) effector XopL which are present in aggregates, providing a link between aggrephagy in immunity [39]. This is a novel example in plants of selective autophagy targeting bacterial effectors, and there is a possibility that NBR1 is involved in degradation of other bacterial effectors. Evidence for this include increased bacterial growth and disease progression of Pseudomonas syringae pathovar tomato DC3000 (Pst) in the nbr1 mutant compared with WT, which indicates for a role of NBR1 in Pst infection [37]. The same study further shows that overexpression of NBR1 reduces water soaking caused by HopM1. Both of these results led the authors to speculate that NBR1 is involved in the degradation of other Pst effectors.

Plant–oomycete interactions

Phytophtora infestans, the causal pathogen of potato late blight, was shown to secrete an effector PexRD54 which, via its AIM motif, associates with ATG8CL to antagonize Joka2, ultimately enhancing oomycete virulence [71]. Further studies showed that this interaction between oomycete effector and host SAR takes place at the extrahaustorial membrane (EHM), where defense-related Rab8a-vesicles labelled with Joka2 and ATG8CL accumulated [72,73]. Apart from providing more insight to the role of autophagy during plant–oomycete interactions, the authors additionally developed a tool for autophagy suppression. The AIM from PexRD54 was used to create an AIM peptide, which was shown to compete with ATG8-binding and thus blocks autophagy progression. The peptide has already been applied in competition assays to reinforce AIM-dependent ATG8 interactions identified in an immunoprecipitation coupled to mass spectrometry (IP-MS) screen [43]. It was also used to block autophagy by transient expression in Nicotiana benthamiana, as it is more specific to autophagy compared with other tools such as Concanamycin A which inhibits vacuolar degradation [39]. In summary, this highlights that studying the role of autophagy in the context of plant–microbe interaction may result in the discovery of novel tools to study the pathway in more detail.

Identification of new receptors

We have established that SARs mediate substrate specificity during selective autophagy. Identifying and characterization of new SARs related to immunity can help advance our understanding of plant–pathogen interactions. We propose to identify new plant immunity-related SARs by mining the Arabidopsis database for proteins that bind to ubiquitin and/or ATG8, and further investigate these candidates by looking into their gene expression during infection using publicly available data.

Ubiquitin-binding proteins were identified based on the presence of characterized ubiquitin-binding domains (INTERPRO/PFAM/SMART) or with the Gene Ontology annotation “ubiquitin-binding” (GO:0043130). From these 106 ubiquitin-binding proteins, we further cross-checked previously published screens for ATG8-interacting proteins [52,53]. We identified 25 ubiquitin-binding proteins that was also found in Marshall et al.’s UIM-interaction dataset [52], and 15 that were found in Jacomin et al.'s LIR prediction for A. thaliana proteome [53], with 5 proteins found in both datasets (Table 1). Among the identified receptors include the known SARs NBR1/Joka2, RPN10 and DSK2 with both ubiquitin-binding and ATG8-interacting abilities (Table 1).

Table 1
Ubiquitin-binding proteins identified based on presence of ubiquitin-binding domains or Gene Ontology annotation
EntryEntry.nameProtein.namesGene. namesLengthAgi_ CodeUBQ. binding. PredictionATG8_ Y2HiLIR. prediction
Q9SIV2 PSD2A_ARATH 26S proteasome non-ATPase regulatory subunit 2 homolog A (26S proteasome regulatory subunit RPN1a) (AtRPN1a) (26S proteasome regulatory subunit S2 homolog A) RPN1A 891 AT2G20580 GO   
Q9ZT95 R7SL1_ARATH Ubiquitin domain-containing protein 7SL RNA1 (At7SL-1) 7SL1 275 AT4G02970 GO   
Q9ZQZ6 R7SL2_ARATH Ubiquitin domain-containing protein 7SL RNA2 (At7SL-2) (Protein ETERNALLY VEGETATIVE PHASE 1) EVE1 263 AT4G03350 GO   
Q9ZQZ4 Q9ZQZ4_ARATH Putative ubiquitin-like protein (Ubiquitin family protein) (Uncharacterized protein AT4g03370) At4g03370 295 AT4G03370 GO  
Q9XIP2 OTU6_ARATH OVARIAN TUMOR DOMAIN-containing deubiquitinating enzyme 6 (OTU domain-containing protein 6) (EC 3.4.19.12) (Deubiquitinating enzyme OTU6) (Otubain-like deubiquitinase 1) OTU6 505 AT2G27350 UBA   
Q9SZD6 PETS_ARATH Polyprotein of EF-Ts, chloroplastic (150 kDa pro-protein) (Protein EMBRYO DEFECTIVE 2726) [Cleaved into: Plastid-specific ribosomal protein-7, chloroplastic; Elongation factor Ts, chloroplastic (EF-Ts)] PETs 953 AT4G29060 UBA-like   
Q9SUG6 PUX3_ARATH Plant UBX domain-containing protein 3 (PUX3) (CDC48-interacting UBX-domain protein 3) PUX3 302 AT4G22150 UBX  
Q9SSD3 Q9SSD3_ARATH F18B13.13 protein (Ubiquitin system component Cue) (Uncharacterized protein At1g80040) At1g80040 248 AT1G80040 CUE  
Q9SJJ5 CKS2_ARATH Cyclin-dependent kinases regulatory subunit 2 CKS2 83 AT2G27970 GO   
Q9SB64 NBR1_ARATH Protein NBR1 homolog (AtNBR1) (At4g24690) NBR1 704 AT4G24690 UBA  
Q9M9U7 Q9M9U7_ARATH At1g18760 (F6A14.13 protein) (Zinc finger, C3HC4 type (RING finger) family protein) At1g18760 224 AT1G18760 UIM   
Q9M548 DRM2_ARATH DNA (cytosine-5)-methyltransferase DRM2 (EC 2.1.1.37) (Protein DOMAINS REARRANGED METHYLASE 2) DRM2 626 AT5G14620 UBA   
Q9M0X2 Q9M0X2_ARATH Ubiquitin-like superfamily protein At4g05230 206 AT4G05230 GO   
Q9M0X1 Q9M0X1_ARATH Ubiquitin-like superfamily protein At4g05240 197 AT4G05240 GO   
Q9M0X0 Q9M0X0_ARATH Ubiquitin-like superfamily protein At4g05250 318 AT4G05250 GO   
Q9M0W9 Q9M0W9_ARATH Ubiquitin-like superfamily protein (Uncharacterized protein AT4g05260) At4g05260 259 AT4G05260 GO   
Q9M0W8 Q9M0W8_ARATH Ubiquitin-like superfamily protein (Uncharacterized protein AT4g05270) At4g05270 129 AT4G05270 GO   
Q9M0W4 Q9M0W4_ARATH Ubiquitin-like superfamily protein At4g05310 415 AT4G05310 GO   
Q9M0N1 PUX10_ARATH Plant UBX domain-containing protein 10 (PUX10) PUX10 480 AT4G10790 UBA/UBX  
Q9LYE5 CID5_ARATH Polyadenylate-binding protein-interacting protein 5 (PABP-interacting protein 5) (Poly(A)-binding protein-interacting protein 5) (PAM2-containing protein CID5) (Protein CTC-INTERACTING DOMAIN 5) (Protein INCREASED POLYPLOIDY LEVEL IN DARKNESS 1) CID5 155 AT5G11440 CUE   
Q9LYC2 NPL41_ARATH NPL4-like protein 1 At3g63000 413 AT3G63000 NPL4   
Q9LXE5 DRM1L_ARATH DNA (cytosine-5)-methyltransferase DRM1 (EC 2.1.1.37) (Protein DOMAINS REARRANGED METHYLASE 1) DRM1 624 AT5G15380 UBA   
Q9LVR6 DAR3_ARATH Protein DA1-related 3 DAR3 450 AT5G66640 DA1-like   
Q9LPL6 TOL3_ARATH TOM1-like protein 3 TOL3 506 AT1G21380 VHS-GAT  
Q9LNC6 TOL2_ARATH TOM1-like protein 2 TOL2 383 AT1G06210 VHS-GAT  
Q9LJN8 BUB31_ARATH Mitotic checkpoint protein BUB3.1 (Protein BUDDING UNINHIBITED BY BENZYMIDAZOL 3.1) BUB3.1 340 AT3G19590 WD40   
Q9LHS5 Q9LHS5_ARATH Cell division related protein-like (DnaJ and myb-like DNA-binding domain-containing protein) At5g06110 663 AT5G06110 UBD   
Q9LHN3 Q9LHN3_ARATH AT3g18860/MCB22_3 (Transducin family protein / WD-40 repeat family protein)  760 AT3G18860 WD40/PFU/ PUL 
Q9LHG8 ELC_ARATH Protein ELC (AtELC) (ESCRT-I complex subunit VPS23 homolog 1) (Protein VACUOLAR PROTEIN SORTING 23A) (Vacuolar protein-sorting-associated protein 23 homolog 1) ELC 398 AT3G12400 UEV   
Q9LFL3 TOL1_ARATH TOM1-like protein 1 TOL1 407 AT5G16880 VHS-GAT   
Q9LET3 RBL20_ARATH Rhomboid-like protein 20 (AtRBL20) RBL20 293 AT3G56740 UBA   
Q9FMQ0 Q9FMQ0_ARATH AT5g12120/MXC9_8 (At5g12120) (Ubiquitin-associated/translation elongation factor EF1B protein) (Uncharacterized protein At5g12120) MXC9.8 619 AT5G12120 UBA  
Q9FLZ3 KIN12_ARATH SNF1-related protein kinase catalytic subunit alpha KIN12 (AKIN12) (EC 2.7.11.1) (AKIN alpha-3) (AKINalpha3) (SNF1-related kinase 1.3) (SnRK1.3) KIN12 494 AT5G39440 UBA   
Q9FKZ1 DRL42_ARATH Probable disease resistance protein At5g66900 At5g66900 809 AT5G66900 GO   
Q9FKZ0 DRL43_ARATH Probable disease resistance protein At5g66910 At5g66910 815 AT5G66910 GO   
Q9FKN7 DAR4_ARATH Protein DA1-related 4 (Protein CHILLING SENSITIVE 3) DAR4 1613 AT5G17890 DA1-like   
Q9FJX9 DAR7_ARATH Protein DA1-related 7 DAR7 560 AT5G66610 UIM  
Q9FJX8 DAR6_ARATH Protein DA1-related 6 DAR6 644 AT5G66620 UIM  
Q9FFQ0 TOL5_ARATH TOM1-like protein 5 TOL5 447 AT5G63640 VHS-GAT   
Q9FF81 VPS36_ARATH Vacuolar protein sorting-associated protein 36 (AtVPS36) (ESCRT-II complex subunit VPS36) VPS36 440 AT5G04920 VPS36   
Q9FDZ8 Q9FDZ8_ARATH At1g73440 (Calmodulin-like protein) (Uncharacterized protein T9L24.51) T9L24.51 254 AT1G73440 UIM  
Q9C9Y1 TOL8_ARATH TOM1-like protein 8 TOL8 607 AT3G08790 VHS   
Q9C9U5 SIS8_ARATH Probable serine/threonine-protein kinase SIS8 (EC 2.7.11.1) (MAPKK kinase SIS8) (Protein SUGAR INSENSITIVE 8) SIS8 1030 AT1G73660 UIM  
Q9C701 BUB32_ARATH Mitotic checkpoint protein BUB3.2 (Protein BUDDING UNINHIBITED BY BENZYMIDAZOL 3.2) BUB3.2 339 AT1G49910 WD40   
Q9C5H4 MTV1_ARATH Protein MODIFIED TRANSPORT TO THE VACUOLE 1 MTV1 690 AT3G16270 VHS-GAT   
Q9C5G7 PUX13_ARATH Plant UBX domain-containing protein 13 (PUX13) PUX13 525 AT4G23040 UBA/UBX  
Q9ASS2 FREE1_ARATH Protein FREE1 (FYVE domain protein required for endosomal sorting 1) (FYVE domain-containing protein 1) FREE1 601 AT1G20110 Experimentally proven  
Q94JZ8 PUX7_ARATH Plant UBX domain-containing protein 7 (PUX7) PUX7 468 AT1G14570 UIM/UBA/UBX  
Q93ZS6 Q93ZS6_ARATH AT3g05090/T12H1_5 (Transducin/WD40 repeat-like superfamily protein) (Uncharacterized protein At3g05090) LRS1 753 AT3G05090 WD40   
Q8W4Q5 RIN3_ARATH E3 ubiquitin protein ligase RIN3 (EC 2.3.2.27) (RING-type E3 ubiquitin transferase RIN3) (RPM1-interacting protein 3) RIN3 577 AT5G51450 CUE   
Q8W4F0 DAR1_ARATH Protein DA1-related 1 DAR1 553 AT4G36860 UIM/DA1  
Q8VZS6 GIP1_ARATH GBF-interacting protein 1 GIP1 567 AT3G13222 UBA-like   
Q8VYC8 RIN2_ARATH E3 ubiquitin protein ligase RIN2 (EC 2.3.2.27) (AMF receptor-like protein 1A) (RING-type E3 ubiquitin transferase RIN2) (RPM1-interacting protein 2) RIN2 578 AT4G25230 CUE   
Q8VWF1 SH3P2_ARATH SH3 domain-containing protein 2 (AtSH3P2) SH3P2 368 AT4G34660 SH3  
Q8RWY8 Q8RWY8_ARATH Nucleic acid binding protein (Uncharacterized protein At1g27750) At1g27750 1075 AT1G27750 GO  
Q8RWU7 PUX4_ARATH Plant UBX domain-containing protein 4 (PUX4) (CDC48-interacting UBX-domain protein 4) PUX4 303 AT4G04210 UBX  
Q8LG98 OTU1_ARATH OVARIAN TUMOR DOMAIN-containing deubiquitinating enzyme 1 (OTU domain-containing protein 1) (EC 3.4.19.12) (Deubiquitinating enzyme OTU1) OTU1 306 AT1G28120 GO   
Q8LG11 Q8LG11_ARATH Proline-rich cell wall protein-like (Ubiquitin-associated/translation elongation factor EF1B protein) At5g53330 221 AT5G53330 UBA   
Q8L860 TOL9_ARATH TOM1-like protein 9 TOL9 675 AT4G32760 VHS-GAT  
Q8L6Y1 UBP14_ARATH Ubiquitin carboxyl-terminal hydrolase 14 (EC 3.4.19.12) (Deubiquitinating enzyme 14) (AtUBP14) (TITAN-6 protein) (Ubiquitin thioesterase 14) (Ubiquitin-specific-processing protease 14) UBP14 797 AT3G20630 UBA   
Q8H0T4 UPL2_ARATH E3 ubiquitin-protein ligase UPL2 (Ubiquitin-protein ligase 2) (EC 2.3.2.26) (HECT-type E3 ubiquitin transferase UPL2) UPL2 3658 AT1G70320 UIM/UBA 
Q8GY23 UPL1_ARATH E3 ubiquitin-protein ligase UPL1 (Ubiquitin-protein ligase 1) (EC 2.3.2.26) (HECT-type E3 ubiquitin transferase UPL1) UPL1 3681 AT1G55860 UIM/UBA 
Q84WJ0 DAR5_ARATH Protein DA1-related 5 DAR5 702 AT5G66630 DA1-like   
Q84L33 RD23B_ARATH Ubiquitin receptor RAD23b (AtRAD23b) (Putative DNA repair protein RAD23-1) (RAD23-like protein 1) (AtRAD23-1) RAD23B 371 AT1G79650 UBA  
Q84L32 RD23A_ARATH Probable ubiquitin receptor RAD23a (AtRAD23a) (Putative DNA repair protein RAD23-2) (RAD23-like protein 2) (AtRAD23-2) RAD23A 368 AT1G16190 UBA  
Q84L31 RD23C_ARATH Ubiquitin receptor RAD23c (AtRAD23c) (Putative DNA repair protein RAD23-3) (RAD23-like protein 3) (AtRAD23-3) RAD23C 419 AT3G02540 UBA   
Q84L30 RD23D_ARATH Ubiquitin receptor RAD23d (AtRAD23d) (Putative DNA repair protein RAD23-4) (RAD23-like protein 4) (AtRAD23-4) RAD23D 378 AT5G38470 UBA   
Q7Y175 PUX5_ARATH Plant UBX domain-containing protein 5 (PUX5) PUX5 421 AT4G15410 UBA/UBX  
Q6NQK0 TOL4_ARATH TOM1-like protein 4 TOL4 446 AT1G76970 VHS-GAT   
Q6NQH9 CID6_ARATH Polyadenylate-binding protein-interacting protein 6 (PABP-interacting protein 6) (Poly(A)-binding protein-interacting protein 6) (PAM2-containing protein CID6) (Protein CTC-INTERACTING DOMAIN 6) CID6 175 AT5G25540 CUE   
Q5XF75 EFTS_ARATH Elongation factor Ts, mitochondrial (EF-Ts) (EF-TsMt) EFTS 395 AT4G11120 UBA-like   
Q4V3D3 PUX9_ARATH Plant UBX domain-containing protein 9 (PUX9) PUX9 469 AT4G00752 UIM/UBA-like/ UBX  
Q38997 KIN10_ARATH SNF1-related protein kinase catalytic subunit alpha KIN10 (AKIN10) (EC 2.7.11.1) (AKIN alpha-2) (AKINalpha2) (SNF1-related kinase 1.1) (SnRK1.1) KIN10 512 AT3G01090 UBA   
Q38942 RAE1_ARATH Protein RAE1 (RNA export factor 1) RAE1 349 AT1G80670 WD40   
Q0WSN2 DAR2_ARATH Protein DA1-related 2 (Protein LATERAL ROOT DEVELOPMENT 3) DAR2 528 AT2G39830 UIM  
Q0WL28 Q0WL28_ARATH Ubiquitin system component Cue protein (Uncharacterized protein At1g27750) At1g27752 656 AT1G27752 CUE  
P92958 KIN11_ARATH SNF1-related protein kinase catalytic subunit alpha KIN11 (AKIN11) (EC 2.7.11.1) (AKIN alpha-1) (AKINalpha1) (SNF1-related kinase 1.2) (SnRK1.2) KIN11 512 AT3G29160 UBA   
P55034 PSMD4_ARATH 26S proteasome non-ATPase regulatory subunit 4 homolog (26S proteasome regulatory subunit RPN10) (AtRPN10) (26S proteasome regulatory subunit S5A homolog) (Multiubiquitin chain-binding protein 1) (AtMCB1) RPN10 386 AT4G38630 UIM  
P0DKI4 PUX14_ARATH Putative plant UBX domain-containing protein 14 (PUX14) PUX14 417 AT4G14250 UBX  
P0C7Q8 DA1_ARATH Protein DA1 (Protein SUPPRESSOR OF LARGE SEED AND ORGAN PHENOTYPES OF DA1-1 1) DA1 532 AT1G19270 UIM  
O82264 NPL42_ARATH NPL4-like protein 2 At2g47970 413 AT2G47970 UBQ-like/MPN   
O81015 O81015_ARATH At2g26920 (Ubiquitin-associated/translation elongation factor EF1B protein) (Uncharacterized protein At2g26920) At2g26920 646 AT2G26920 UBA  
O80996 BRIZ2_ARATH BRAP2 RING ZnF UBP domain-containing protein 2 (EC 2.3.2.27) BRIZ2 479 AT2G26000 Znf_UBP-like   
O80910 TOL6_ARATH TOM1-like protein 6 TOL6 671 AT2G38410 VHS-GAT   
O65506 O65506_ARATH Disease resistance protein (TIR-NBS-LRR class) (Putative disease resistance protein) At4g36140 1607 AT4G36140 GO   
O48726 RPN13_ARATH 26S proteasome regulatory subunit RPN13 (AtRPN13) (26S proteasome non-ATPase regulatory subunit 13) RPN13 300 AT2G26590 PH   
O48696 O48696_ARATH AAA-type ATPase family protein (F3I6.23 protein) At1g24290 525 AT1G24290 UBA   
O23249 CKS1_ARATH Cyclin-dependent kinases regulatory subunit 1 (CKS1-At) CKS1 87 AT2G27960 GO   
F4KED5 F4KED5_ARATH Ubiquitin system component Cue protein At5g32440 265 AT5G32440 CUE   
F4KCN6 F4KCN6_ARATH Ubiquitin receptor RAD23 (DNA repair protein RAD23) At5g16090 171 AT5G16090 UBA   
F4KAU9 TOL7_ARATH TOM1-like protein 7 TOL7 542 AT5G01760 VHS-GAT   
F4JPR7 PUX8_ARATH Plant UBX domain-containing protein 8 (PUX8) (Ara4-interacting protein) (Suppressor of ARA4-induced defect of ypt1) (SAY1) PUX8 564 AT4G11740 UIM/UBA-like/UBX 
F4JI85 F4JI85_ARATH Ubiquitin family protein At4g03360 322 AT4G03360 GO   
F4IXN6 PUX6_ARATH Plant UBX domain-containing protein 6 (PUX6) PUX6 435 AT3G21660 UBX 
F4ITP6 F4ITP6_ARATH Ubiquitin-like superfamily protein At2g32350 242 AT2G32350 GO   
F4I241 BUB33_ARATH Mitotic checkpoint protein BUB3.3 (Protein BUDDING UNINHIBITED BY BENZYMIDAZOL 3.3) BUB3.3 314 AT1G69400 WD40   
F4HXZ1 BRO1_ARATH Vacuolar-sorting protein BRO1 (BRO domain-containing protein 1) (AtBRO1) BRO1 846 AT1G15130 BRO1   
A4FVR1 GIP1L_ARATH GBF-interacting protein 1-like (Protein GIP1-like) GIP1L 575 AT1G55820 UBA-like   
A0A1P8AW60 A0A1P8AW60_ARATH Ubiquitin-associated (UBA)/TS-N domain-containing protein At1g04850 324 AT1G04850 UBA   
Q9SII9 DSK2A_ARATH Ubiquitin domain-containing protein DSK2a DSK2A 538 AT2G17190 UBA  
Q9SII8 DSK2B_ARATH Ubiquitin domain-containing protein DSK2b DSK2B 551 AT2G17200 UBA   
Q8RXQ2 RBL18_ARATH Rhomboid-like protein 18, AtRBL18 RBL18 287 AT2G41160 UBA   
Q9FT69 RQSIM_ARATH ATP-dependent DNA helicase Q-like SIM, EC 3.6.4.12†(RecQ-like protein SIM, AtRecQsim, Similar to RecQ protein) RECQSIM 858 AT5G27680 UBA   
Q500V3 Q500V3_ARATH At2g12550 (Ubiquitin-associated (UBA)/TS-N domain-containing protein) NUB1 562 AT2G12550 UBA   
Q8LB17 RBL15_ARATH Rhomboid-like protein 15, AtRBL15, EC 3.4.21.- RBL15 403 AT3G58460 UBA   
Q1EBV4 DDI1_ARATH Protein DNA-DAMAGE INDUCIBLE 1, EC 3.4.23.- DDI1 414 AT3G13235 UBA   
EntryEntry.nameProtein.namesGene. namesLengthAgi_ CodeUBQ. binding. PredictionATG8_ Y2HiLIR. prediction
Q9SIV2 PSD2A_ARATH 26S proteasome non-ATPase regulatory subunit 2 homolog A (26S proteasome regulatory subunit RPN1a) (AtRPN1a) (26S proteasome regulatory subunit S2 homolog A) RPN1A 891 AT2G20580 GO   
Q9ZT95 R7SL1_ARATH Ubiquitin domain-containing protein 7SL RNA1 (At7SL-1) 7SL1 275 AT4G02970 GO   
Q9ZQZ6 R7SL2_ARATH Ubiquitin domain-containing protein 7SL RNA2 (At7SL-2) (Protein ETERNALLY VEGETATIVE PHASE 1) EVE1 263 AT4G03350 GO   
Q9ZQZ4 Q9ZQZ4_ARATH Putative ubiquitin-like protein (Ubiquitin family protein) (Uncharacterized protein AT4g03370) At4g03370 295 AT4G03370 GO  
Q9XIP2 OTU6_ARATH OVARIAN TUMOR DOMAIN-containing deubiquitinating enzyme 6 (OTU domain-containing protein 6) (EC 3.4.19.12) (Deubiquitinating enzyme OTU6) (Otubain-like deubiquitinase 1) OTU6 505 AT2G27350 UBA   
Q9SZD6 PETS_ARATH Polyprotein of EF-Ts, chloroplastic (150 kDa pro-protein) (Protein EMBRYO DEFECTIVE 2726) [Cleaved into: Plastid-specific ribosomal protein-7, chloroplastic; Elongation factor Ts, chloroplastic (EF-Ts)] PETs 953 AT4G29060 UBA-like   
Q9SUG6 PUX3_ARATH Plant UBX domain-containing protein 3 (PUX3) (CDC48-interacting UBX-domain protein 3) PUX3 302 AT4G22150 UBX  
Q9SSD3 Q9SSD3_ARATH F18B13.13 protein (Ubiquitin system component Cue) (Uncharacterized protein At1g80040) At1g80040 248 AT1G80040 CUE  
Q9SJJ5 CKS2_ARATH Cyclin-dependent kinases regulatory subunit 2 CKS2 83 AT2G27970 GO   
Q9SB64 NBR1_ARATH Protein NBR1 homolog (AtNBR1) (At4g24690) NBR1 704 AT4G24690 UBA  
Q9M9U7 Q9M9U7_ARATH At1g18760 (F6A14.13 protein) (Zinc finger, C3HC4 type (RING finger) family protein) At1g18760 224 AT1G18760 UIM   
Q9M548 DRM2_ARATH DNA (cytosine-5)-methyltransferase DRM2 (EC 2.1.1.37) (Protein DOMAINS REARRANGED METHYLASE 2) DRM2 626 AT5G14620 UBA   
Q9M0X2 Q9M0X2_ARATH Ubiquitin-like superfamily protein At4g05230 206 AT4G05230 GO   
Q9M0X1 Q9M0X1_ARATH Ubiquitin-like superfamily protein At4g05240 197 AT4G05240 GO   
Q9M0X0 Q9M0X0_ARATH Ubiquitin-like superfamily protein At4g05250 318 AT4G05250 GO   
Q9M0W9 Q9M0W9_ARATH Ubiquitin-like superfamily protein (Uncharacterized protein AT4g05260) At4g05260 259 AT4G05260 GO   
Q9M0W8 Q9M0W8_ARATH Ubiquitin-like superfamily protein (Uncharacterized protein AT4g05270) At4g05270 129 AT4G05270 GO   
Q9M0W4 Q9M0W4_ARATH Ubiquitin-like superfamily protein At4g05310 415 AT4G05310 GO   
Q9M0N1 PUX10_ARATH Plant UBX domain-containing protein 10 (PUX10) PUX10 480 AT4G10790 UBA/UBX  
Q9LYE5 CID5_ARATH Polyadenylate-binding protein-interacting protein 5 (PABP-interacting protein 5) (Poly(A)-binding protein-interacting protein 5) (PAM2-containing protein CID5) (Protein CTC-INTERACTING DOMAIN 5) (Protein INCREASED POLYPLOIDY LEVEL IN DARKNESS 1) CID5 155 AT5G11440 CUE   
Q9LYC2 NPL41_ARATH NPL4-like protein 1 At3g63000 413 AT3G63000 NPL4   
Q9LXE5 DRM1L_ARATH DNA (cytosine-5)-methyltransferase DRM1 (EC 2.1.1.37) (Protein DOMAINS REARRANGED METHYLASE 1) DRM1 624 AT5G15380 UBA   
Q9LVR6 DAR3_ARATH Protein DA1-related 3 DAR3 450 AT5G66640 DA1-like   
Q9LPL6 TOL3_ARATH TOM1-like protein 3 TOL3 506 AT1G21380 VHS-GAT  
Q9LNC6 TOL2_ARATH TOM1-like protein 2 TOL2 383 AT1G06210 VHS-GAT  
Q9LJN8 BUB31_ARATH Mitotic checkpoint protein BUB3.1 (Protein BUDDING UNINHIBITED BY BENZYMIDAZOL 3.1) BUB3.1 340 AT3G19590 WD40   
Q9LHS5 Q9LHS5_ARATH Cell division related protein-like (DnaJ and myb-like DNA-binding domain-containing protein) At5g06110 663 AT5G06110 UBD   
Q9LHN3 Q9LHN3_ARATH AT3g18860/MCB22_3 (Transducin family protein / WD-40 repeat family protein)  760 AT3G18860 WD40/PFU/ PUL 
Q9LHG8 ELC_ARATH Protein ELC (AtELC) (ESCRT-I complex subunit VPS23 homolog 1) (Protein VACUOLAR PROTEIN SORTING 23A) (Vacuolar protein-sorting-associated protein 23 homolog 1) ELC 398 AT3G12400 UEV   
Q9LFL3 TOL1_ARATH TOM1-like protein 1 TOL1 407 AT5G16880 VHS-GAT   
Q9LET3 RBL20_ARATH Rhomboid-like protein 20 (AtRBL20) RBL20 293 AT3G56740 UBA   
Q9FMQ0 Q9FMQ0_ARATH AT5g12120/MXC9_8 (At5g12120) (Ubiquitin-associated/translation elongation factor EF1B protein) (Uncharacterized protein At5g12120) MXC9.8 619 AT5G12120 UBA  
Q9FLZ3 KIN12_ARATH SNF1-related protein kinase catalytic subunit alpha KIN12 (AKIN12) (EC 2.7.11.1) (AKIN alpha-3) (AKINalpha3) (SNF1-related kinase 1.3) (SnRK1.3) KIN12 494 AT5G39440 UBA   
Q9FKZ1 DRL42_ARATH Probable disease resistance protein At5g66900 At5g66900 809 AT5G66900 GO   
Q9FKZ0 DRL43_ARATH Probable disease resistance protein At5g66910 At5g66910 815 AT5G66910 GO   
Q9FKN7 DAR4_ARATH Protein DA1-related 4 (Protein CHILLING SENSITIVE 3) DAR4 1613 AT5G17890 DA1-like   
Q9FJX9 DAR7_ARATH Protein DA1-related 7 DAR7 560 AT5G66610 UIM  
Q9FJX8 DAR6_ARATH Protein DA1-related 6 DAR6 644 AT5G66620 UIM  
Q9FFQ0 TOL5_ARATH TOM1-like protein 5 TOL5 447 AT5G63640 VHS-GAT   
Q9FF81 VPS36_ARATH Vacuolar protein sorting-associated protein 36 (AtVPS36) (ESCRT-II complex subunit VPS36) VPS36 440 AT5G04920 VPS36   
Q9FDZ8 Q9FDZ8_ARATH At1g73440 (Calmodulin-like protein) (Uncharacterized protein T9L24.51) T9L24.51 254 AT1G73440 UIM  
Q9C9Y1 TOL8_ARATH TOM1-like protein 8 TOL8 607 AT3G08790 VHS   
Q9C9U5 SIS8_ARATH Probable serine/threonine-protein kinase SIS8 (EC 2.7.11.1) (MAPKK kinase SIS8) (Protein SUGAR INSENSITIVE 8) SIS8 1030 AT1G73660 UIM  
Q9C701 BUB32_ARATH Mitotic checkpoint protein BUB3.2 (Protein BUDDING UNINHIBITED BY BENZYMIDAZOL 3.2) BUB3.2 339 AT1G49910 WD40   
Q9C5H4 MTV1_ARATH Protein MODIFIED TRANSPORT TO THE VACUOLE 1 MTV1 690 AT3G16270 VHS-GAT   
Q9C5G7 PUX13_ARATH Plant UBX domain-containing protein 13 (PUX13) PUX13 525 AT4G23040 UBA/UBX  
Q9ASS2 FREE1_ARATH Protein FREE1 (FYVE domain protein required for endosomal sorting 1) (FYVE domain-containing protein 1) FREE1 601 AT1G20110 Experimentally proven  
Q94JZ8 PUX7_ARATH Plant UBX domain-containing protein 7 (PUX7) PUX7 468 AT1G14570 UIM/UBA/UBX  
Q93ZS6 Q93ZS6_ARATH AT3g05090/T12H1_5 (Transducin/WD40 repeat-like superfamily protein) (Uncharacterized protein At3g05090) LRS1 753 AT3G05090 WD40   
Q8W4Q5 RIN3_ARATH E3 ubiquitin protein ligase RIN3 (EC 2.3.2.27) (RING-type E3 ubiquitin transferase RIN3) (RPM1-interacting protein 3) RIN3 577 AT5G51450 CUE   
Q8W4F0 DAR1_ARATH Protein DA1-related 1 DAR1 553 AT4G36860 UIM/DA1  
Q8VZS6 GIP1_ARATH GBF-interacting protein 1 GIP1 567 AT3G13222 UBA-like   
Q8VYC8 RIN2_ARATH E3 ubiquitin protein ligase RIN2 (EC 2.3.2.27) (AMF receptor-like protein 1A) (RING-type E3 ubiquitin transferase RIN2) (RPM1-interacting protein 2) RIN2 578 AT4G25230 CUE   
Q8VWF1 SH3P2_ARATH SH3 domain-containing protein 2 (AtSH3P2) SH3P2 368 AT4G34660 SH3  
Q8RWY8 Q8RWY8_ARATH Nucleic acid binding protein (Uncharacterized protein At1g27750) At1g27750 1075 AT1G27750 GO  
Q8RWU7 PUX4_ARATH Plant UBX domain-containing protein 4 (PUX4) (CDC48-interacting UBX-domain protein 4) PUX4 303 AT4G04210 UBX  
Q8LG98 OTU1_ARATH OVARIAN TUMOR DOMAIN-containing deubiquitinating enzyme 1 (OTU domain-containing protein 1) (EC 3.4.19.12) (Deubiquitinating enzyme OTU1) OTU1 306 AT1G28120 GO   
Q8LG11 Q8LG11_ARATH Proline-rich cell wall protein-like (Ubiquitin-associated/translation elongation factor EF1B protein) At5g53330 221 AT5G53330 UBA   
Q8L860 TOL9_ARATH TOM1-like protein 9 TOL9 675 AT4G32760 VHS-GAT  
Q8L6Y1 UBP14_ARATH Ubiquitin carboxyl-terminal hydrolase 14 (EC 3.4.19.12) (Deubiquitinating enzyme 14) (AtUBP14) (TITAN-6 protein) (Ubiquitin thioesterase 14) (Ubiquitin-specific-processing protease 14) UBP14 797 AT3G20630 UBA   
Q8H0T4 UPL2_ARATH E3 ubiquitin-protein ligase UPL2 (Ubiquitin-protein ligase 2) (EC 2.3.2.26) (HECT-type E3 ubiquitin transferase UPL2) UPL2 3658 AT1G70320 UIM/UBA 
Q8GY23 UPL1_ARATH E3 ubiquitin-protein ligase UPL1 (Ubiquitin-protein ligase 1) (EC 2.3.2.26) (HECT-type E3 ubiquitin transferase UPL1) UPL1 3681 AT1G55860 UIM/UBA 
Q84WJ0 DAR5_ARATH Protein DA1-related 5 DAR5 702 AT5G66630 DA1-like   
Q84L33 RD23B_ARATH Ubiquitin receptor RAD23b (AtRAD23b) (Putative DNA repair protein RAD23-1) (RAD23-like protein 1) (AtRAD23-1) RAD23B 371 AT1G79650 UBA  
Q84L32 RD23A_ARATH Probable ubiquitin receptor RAD23a (AtRAD23a) (Putative DNA repair protein RAD23-2) (RAD23-like protein 2) (AtRAD23-2) RAD23A 368 AT1G16190 UBA  
Q84L31 RD23C_ARATH Ubiquitin receptor RAD23c (AtRAD23c) (Putative DNA repair protein RAD23-3) (RAD23-like protein 3) (AtRAD23-3) RAD23C 419 AT3G02540 UBA   
Q84L30 RD23D_ARATH Ubiquitin receptor RAD23d (AtRAD23d) (Putative DNA repair protein RAD23-4) (RAD23-like protein 4) (AtRAD23-4) RAD23D 378 AT5G38470 UBA   
Q7Y175 PUX5_ARATH Plant UBX domain-containing protein 5 (PUX5) PUX5 421 AT4G15410 UBA/UBX  
Q6NQK0 TOL4_ARATH TOM1-like protein 4 TOL4 446 AT1G76970 VHS-GAT   
Q6NQH9 CID6_ARATH Polyadenylate-binding protein-interacting protein 6 (PABP-interacting protein 6) (Poly(A)-binding protein-interacting protein 6) (PAM2-containing protein CID6) (Protein CTC-INTERACTING DOMAIN 6) CID6 175 AT5G25540 CUE   
Q5XF75 EFTS_ARATH Elongation factor Ts, mitochondrial (EF-Ts) (EF-TsMt) EFTS 395 AT4G11120 UBA-like   
Q4V3D3 PUX9_ARATH Plant UBX domain-containing protein 9 (PUX9) PUX9 469 AT4G00752 UIM/UBA-like/ UBX  
Q38997 KIN10_ARATH SNF1-related protein kinase catalytic subunit alpha KIN10 (AKIN10) (EC 2.7.11.1) (AKIN alpha-2) (AKINalpha2) (SNF1-related kinase 1.1) (SnRK1.1) KIN10 512 AT3G01090 UBA   
Q38942 RAE1_ARATH Protein RAE1 (RNA export factor 1) RAE1 349 AT1G80670 WD40   
Q0WSN2 DAR2_ARATH Protein DA1-related 2 (Protein LATERAL ROOT DEVELOPMENT 3) DAR2 528 AT2G39830 UIM  
Q0WL28 Q0WL28_ARATH Ubiquitin system component Cue protein (Uncharacterized protein At1g27750) At1g27752 656 AT1G27752 CUE  
P92958 KIN11_ARATH SNF1-related protein kinase catalytic subunit alpha KIN11 (AKIN11) (EC 2.7.11.1) (AKIN alpha-1) (AKINalpha1) (SNF1-related kinase 1.2) (SnRK1.2) KIN11 512 AT3G29160 UBA   
P55034 PSMD4_ARATH 26S proteasome non-ATPase regulatory subunit 4 homolog (26S proteasome regulatory subunit RPN10) (AtRPN10) (26S proteasome regulatory subunit S5A homolog) (Multiubiquitin chain-binding protein 1) (AtMCB1) RPN10 386 AT4G38630 UIM  
P0DKI4 PUX14_ARATH Putative plant UBX domain-containing protein 14 (PUX14) PUX14 417 AT4G14250 UBX  
P0C7Q8 DA1_ARATH Protein DA1 (Protein SUPPRESSOR OF LARGE SEED AND ORGAN PHENOTYPES OF DA1-1 1) DA1 532 AT1G19270 UIM  
O82264 NPL42_ARATH NPL4-like protein 2 At2g47970 413 AT2G47970 UBQ-like/MPN   
O81015 O81015_ARATH At2g26920 (Ubiquitin-associated/translation elongation factor EF1B protein) (Uncharacterized protein At2g26920) At2g26920 646 AT2G26920 UBA  
O80996 BRIZ2_ARATH BRAP2 RING ZnF UBP domain-containing protein 2 (EC 2.3.2.27) BRIZ2 479 AT2G26000 Znf_UBP-like   
O80910 TOL6_ARATH TOM1-like protein 6 TOL6 671 AT2G38410 VHS-GAT   
O65506 O65506_ARATH Disease resistance protein (TIR-NBS-LRR class) (Putative disease resistance protein) At4g36140 1607 AT4G36140 GO   
O48726 RPN13_ARATH 26S proteasome regulatory subunit RPN13 (AtRPN13) (26S proteasome non-ATPase regulatory subunit 13) RPN13 300 AT2G26590 PH   
O48696 O48696_ARATH AAA-type ATPase family protein (F3I6.23 protein) At1g24290 525 AT1G24290 UBA   
O23249 CKS1_ARATH Cyclin-dependent kinases regulatory subunit 1 (CKS1-At) CKS1 87 AT2G27960 GO   
F4KED5 F4KED5_ARATH Ubiquitin system component Cue protein At5g32440 265 AT5G32440 CUE   
F4KCN6 F4KCN6_ARATH Ubiquitin receptor RAD23 (DNA repair protein RAD23) At5g16090 171 AT5G16090 UBA   
F4KAU9 TOL7_ARATH TOM1-like protein 7 TOL7 542 AT5G01760 VHS-GAT   
F4JPR7 PUX8_ARATH Plant UBX domain-containing protein 8 (PUX8) (Ara4-interacting protein) (Suppressor of ARA4-induced defect of ypt1) (SAY1) PUX8 564 AT4G11740 UIM/UBA-like/UBX 
F4JI85 F4JI85_ARATH Ubiquitin family protein At4g03360 322 AT4G03360 GO   
F4IXN6 PUX6_ARATH Plant UBX domain-containing protein 6 (PUX6) PUX6 435 AT3G21660 UBX 
F4ITP6 F4ITP6_ARATH Ubiquitin-like superfamily protein At2g32350 242 AT2G32350 GO   
F4I241 BUB33_ARATH Mitotic checkpoint protein BUB3.3 (Protein BUDDING UNINHIBITED BY BENZYMIDAZOL 3.3) BUB3.3 314 AT1G69400 WD40   
F4HXZ1 BRO1_ARATH Vacuolar-sorting protein BRO1 (BRO domain-containing protein 1) (AtBRO1) BRO1 846 AT1G15130 BRO1   
A4FVR1 GIP1L_ARATH GBF-interacting protein 1-like (Protein GIP1-like) GIP1L 575 AT1G55820 UBA-like   
A0A1P8AW60 A0A1P8AW60_ARATH Ubiquitin-associated (UBA)/TS-N domain-containing protein At1g04850 324 AT1G04850 UBA   
Q9SII9 DSK2A_ARATH Ubiquitin domain-containing protein DSK2a DSK2A 538 AT2G17190 UBA  
Q9SII8 DSK2B_ARATH Ubiquitin domain-containing protein DSK2b DSK2B 551 AT2G17200 UBA   
Q8RXQ2 RBL18_ARATH Rhomboid-like protein 18, AtRBL18 RBL18 287 AT2G41160 UBA   
Q9FT69 RQSIM_ARATH ATP-dependent DNA helicase Q-like SIM, EC 3.6.4.12†(RecQ-like protein SIM, AtRecQsim, Similar to RecQ protein) RECQSIM 858 AT5G27680 UBA   
Q500V3 Q500V3_ARATH At2g12550 (Ubiquitin-associated (UBA)/TS-N domain-containing protein) NUB1 562 AT2G12550 UBA   
Q8LB17 RBL15_ARATH Rhomboid-like protein 15, AtRBL15, EC 3.4.21.- RBL15 403 AT3G58460 UBA   
Q1EBV4 DDI1_ARATH Protein DNA-DAMAGE INDUCIBLE 1, EC 3.4.23.- DDI1 414 AT3G13235 UBA   

The list of proteins were cross-checked with previously published screens for ATG8-interacting proteins conducted by Marshall et al. [52] and Jacomin et al. [53] and indicated if they were found in these screens.

Expression level of candidate receptors were then analyzed using data available from public Arabidopsis RNAseq libraries [74]. In brief, five representative datasets were used for the analysis based on following criteria: (1) Dataset contains only one treatment. (2) There are at least three biological replicates in control and treated conditions. (3) Datasets are non-redundant. FPKM values for each gene and replicate were extracted from the five datasets, and subsequent Log2 Fold-change (Log2FC) and false discovery rate (FDR) for each gene comparing treated samples to control samples were assessed using Rstudio software (https://www.rstudio.com/). Only, genes with FDR < 0.05 were considered statistically significant. Log2FC of statistically significant genes are displayed as a heatmap with a dendrogram representing genes sorting based on expression pattern similarity from the different dataset (Figure 3).

Differential gene expression of candidate SARs during immune responses represented in a heatmap

Figure 3
Differential gene expression of candidate SARs during immune responses represented in a heatmap

Expression values are represented as Log2FC, and the color key is indicated at the bottom. The dendrogram on the left clusters together genes with similar expression pattern. Columns correspond to the different dataset extracted from the public online database (http://ipf.sustech.edu.cn/pub/athrna/) as following: flg22 1h (PRJNA491484); flg22 2h (PRJNA429781); P. syringae pv. maculicola (Pma) (PRJNA390966); S. sclerotiorum (PRJNA418121) and B. cinerea (PRJNA276444).

Figure 3
Differential gene expression of candidate SARs during immune responses represented in a heatmap

Expression values are represented as Log2FC, and the color key is indicated at the bottom. The dendrogram on the left clusters together genes with similar expression pattern. Columns correspond to the different dataset extracted from the public online database (http://ipf.sustech.edu.cn/pub/athrna/) as following: flg22 1h (PRJNA491484); flg22 2h (PRJNA429781); P. syringae pv. maculicola (Pma) (PRJNA390966); S. sclerotiorum (PRJNA418121) and B. cinerea (PRJNA276444).

Close modal

As NBR1 is well-characterized, we first investigated the data on NBR1 presented by the heatmap. Notably, expression of NBR1 displayed a high positive log fold change during infection with P. syringae pv. maculicola (Pma) but showed no significant expression differences during flg22 treatment or Sclerotinia sclerotiorum and Botrytis cinerea infection (Figure 3).

We draw focus to the proteins which display expression patterns evidently different from NBR1, as they could be novel immune-related SARs with specialized functions different from the well-characterized NBR1. For example, the subset of proteins ATMCB1, VPS36, LRS1, SH3P2 and RIN2 were up-regulated during infection with S. sclerotiorum and B. cinerea, and could be novel ubiquitin- and/or AIM- binding receptors with functions in immunity. In contrast, there is a high negative log fold change in the expression of proteins AT1G24290, DMT7, ATG4G00752, and AT1G73660 during S. sclerotiorum and B. cinerea infection (Figure 3). This indicates for a possibility that these proteins could be targeted during infection, perhaps because they as well play a role in immunity.

S. sclerotiorum and B. cinerea are necrotrophic in contrast with the hemibiotrophic P. syringae. Past studies have shown autophagy plays different roles during immunity against biotrophic and necrotrophic pathogens, due in part to its cross-talk with salicylic-acid signalling which mediates resistance against biotrophic pathogens [75]. It is therefore plausible that these putative SARs which respond specifically to necrotrophic pathogens could mediate resistance in a novel manner.

We have identified here many ubiquitin- and/or ATG8- binding receptors with significant expression differences upon flg22 treatment or pathogen challenge. Further investigation should be directed at validating the role of these proteins as SARs, and characterizing how they mediate pathogen interactions and immune responses. The molecular mechanisms that drive their substrate recognition and interaction with autophagic machinery should also be studied so we gain more insight into these interactions.

ATG8 isoforms

We have discussed in depth how SARs can promote the specificity of substrate degradation via autophagy. On the other hand, recent research has shown that different ATG8 isoforms can also add specificity to autophagy. This was already hinted at in earlier publications where Arabidopsis NBR1 showed different levels of interaction with different members from the ATG8 family of proteins [32]. A study into potato ATG8 isoforms showed that the isoforms display differential gene expression under a range of conditions, and interact with distinct sets of proteins with varying degrees of overlap, which suggests some degree of functional specialization of the isoforms [76]. In addition, a yeast-two-hybrid screen revealed differential preference of A. thaliana ATG8 isoforms to associate with the UIM [52]. In an immunity context, Leong et al. found that in N. benthamiana transcript levels of NbATG8-2 increased earlier than that of NbATG8-1 during Xcv infection [39]. P. infestans effector PexRD54 also showed a preference for ATG8CL over ATG8IL [72].

To strengthen the idea that ATG8 isoforms add specificity during autophagic responses in immunity, we analyzed publicly available data on the gene expression of A. thaliana ATG8 isoforms during responses to immunogenic peptide flg22 and pathogens Pma, B. cinerea, and S. sclerotiorum (Figure 4). The analysis method and datasets used are the same as above for identification of putative novel SARs. We found differential gene expression patterns of the ATG8 isoforms during these conditions. Notably, the ATG8 isoforms show different expression patterns compared to each other and under different pathogenic contexts. As previously mentioned, potato ATG8 isoforms show differential gene expression and interact with distinct subsets of proteins, which suggests functionalization [76]. We build upon this hypothesis and apply it to our analysis of A. thaliana ATG8 isoforms, and suggest that the differential expression patterns in ATG8 isoforms strengthen the idea that the isoforms have specific functions. Some ATG8 isoforms could be grouped according to the similarity in which they behave. For example, ATG8B, ATG8E, and ATG8I were up-regulated during Pma infection and but did not show significant log fold change during S. sclerotiorum or B. cinerea infection. ATG8A and ATG8H responded to both hemibiotrophic Pma and necrotrophic S. sclerotiorum. In contrast, ATG8C and ATG8G displayed negative log fold change during infection with S. sclerotiorum. These patterns, where a subset of isoforms could specifically respond to the different pathogenic contexts, are similar to the patterns presented by putative ubiquitin- and/or ATG8- binding proteins analyzed above. This strongly supports a scenario where receptor and ATG8 works together to add specificity during immunity.

Differential gene expression of ATG8 isoforms during immune responses represented in a heatmap

Figure 4
Differential gene expression of ATG8 isoforms during immune responses represented in a heatmap

Expression values are represented as Log2FC, and the color key is indicated at the bottom. The dendrogram on the left clusters together isoforms with similar expression pattern. Columns correspond to the different dataset extracted from the public online database (http://ipf.sustech.edu.cn/pub/athrna/) as following: flg22 1h (PRJNA491484); flg22 2h (PRJNA429781); P. syringae pv. maculicola (Pma) (PRJNA390966); S. sclerotiorum (PRJNA418121) and B. cinerea (PRJNA276444).

Figure 4
Differential gene expression of ATG8 isoforms during immune responses represented in a heatmap

Expression values are represented as Log2FC, and the color key is indicated at the bottom. The dendrogram on the left clusters together isoforms with similar expression pattern. Columns correspond to the different dataset extracted from the public online database (http://ipf.sustech.edu.cn/pub/athrna/) as following: flg22 1h (PRJNA491484); flg22 2h (PRJNA429781); P. syringae pv. maculicola (Pma) (PRJNA390966); S. sclerotiorum (PRJNA418121) and B. cinerea (PRJNA276444).

Close modal

Spatiotemporal control

Studies in selective autophagy and immunity have also revealed the importance of spatiotemporal regulation in cellular processes. Infection and autophagy are dynamic processes involving many players which constantly display changes in expression, localization, and stability. Dagdas et al. showed that during P. infestans infection, the effector PexRD54 caused a diversion of Joka2-ATG8CL defense-related vesicles to haustoria [72]. Leong et al. further showed that the protein accumulation of NBR1 occurs earlier than its increase in transcription [39]. In the same study, it was also shown that knockdown of NBR1 expression via virus-induced gene silencing (VIGS) reduced Xcv growth at 3 days-post-inoculation (dpi) compared with WT but not at 6dpi, thus indicating for a role in selective autophagy during the earlier steps of infection [39].

Selective autophagy research has contributed much to our understanding of plant–pathogen interactions. During infection, autophagy is targeted by pathogens due to its central role in plant homeostasis but can also function in clearing pathogenic components and reducing infection. The SARs mediate selective autophagy, and studying these receptors gives us more mechanistic insight into how selective autophagy interacts with immunity. We have highlighted many excellent studies which have shed more light on the role of selective autophagy during immunity. There are nevertheless still many questions to answer, giving great potential for further investigation.

In a classical immunity concept of the “zig-zag” model, gene-for-gene resistance is mediated by cell surface PRRs and cytoplasmic NLRs, which recognize pathogenic components in an extracellular and intracellular manner respectively [1,3]. In this review, we have highlighted the role of SARs in recognizing pathogenic components and their downstream effects within the cell. We draw parallels between NLRs-mediated immunity (NMI) and the role of immune-related SARs reviewed here, and propose that SARs can confer immunity to pathogens through SAR-mediated immunity (SMI) which results in effectorphagy (Figure 5). In both scenarios, effectors and/or their downstream effects are recognized by intracellular proteins with various features leading to effector-triggered immunity (ETI). In fact, Deretic et al. proposed, in the context of mammalian SARs, that they could represent a new paradigm in innate immunity as a new class of PRRs [77]. We support this view, and further emphasize the mechanistic details behind SAR function–how substrate recognition can be both ubiquitin-dependent and -independent, and how SARs directly bridge their substrate to the autophagosome thus immediately targeting them for degradation. This allows SARs to recognize a wide range of pathogenic effectors that are more directly involved in modulation of cellular processes.

Parallels between SAR-mediated immunity (SMI) and NLR-mediated immunity (NMI)

Figure 5
Parallels between SAR-mediated immunity (SMI) and NLR-mediated immunity (NMI)

Both pathways depend on recognition of microbial effectors by receptors. SARs and NLRs are different by structure and domain organization. Both receptors inactivate the effector function either by inducing cell death (NMI) or by degrading the effector via autophagy (SMI) and leading to effector-triggered immunity.

Figure 5
Parallels between SAR-mediated immunity (SMI) and NLR-mediated immunity (NMI)

Both pathways depend on recognition of microbial effectors by receptors. SARs and NLRs are different by structure and domain organization. Both receptors inactivate the effector function either by inducing cell death (NMI) or by degrading the effector via autophagy (SMI) and leading to effector-triggered immunity.

Close modal
  • Due to its central role in ensuring plant cellular homeostasis, autophagy is targeted by plant pathogens during infection

  • Selective autophagy has been found to play pro-plant or pro-pathogen roles during immunity

  • Similarities can be found across selective autophagy receptor domain organization and function

  • Selective autophagy receptors are emerging as key players in plant interaction with bacteria, viruses, and oomycetes.

  • The interplay between selective autophagy and pathogenic effectors can present new perspectives on the molecular mechanisms behind plant–pathogen interactions

The authors declare that there are no competing interests associated with the manuscript.

This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme [grant number 948996, DIVERSIPHAGY] and Emmy Noether Fellowship GZ: UE188/2-1 from the Deutsche Forschungsgemeinschaft.

J.X.L. and S.Ü. wrote the manuscript. J.X.L. S.Ü. and G.L designed figures. G.L. performed in silico analysis to identify novel SARs.

We thank all members of the Üstün Lab for fruitful discussions.

     
  • CaMV

    cauliflower mosaic virus

  •  
  • ETI

    effector-triggered immunity

  •  
  • NMI

    NLR-mediated immunity

  •  
  • PAMP

    pathogen-associated-molecular-pattern

  •  
  • PRR

    pattern-recognition receptor

  •  
  • PTI

    PAMP-triggered immunity

  •  
  • SAR

    selective autophagy receptor

  •  
  • SMI

    SAR-mediated immunity

  •  
  • TuMV

    Turnip mosaic virus

  •  
  • TuYV

    Turnip yellows virus

  •  
  • VIGS

    virus-induced gene silencing

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