Ubiquitination during Plant Immune Signaling
Year: 2012
Type: review
Abstract: Plant responses to pathogens depend on the rapid and effective coordination of microbial perception and downstream signal transduction events. Detection of pathogen invasion starts by the recognition of conserved microbial molecules called pathogen-associated molecular patterns (PAMPs), mainly by plant membrane-associated extracellular receptors, which results in PAMP-triggered immunity (PTI). Using a type III secretion system, plant pathogenic bacteria are able to inject type III effectors (T3Es) directly inside host cells, thereby overcoming PTI and favoring bacterial growth. Recognition of T3Es by plant resistance (R) proteins leads to effector-triggered immunity (ETI), a more efficient form of resistance that is regularly associated with the development of hypersensitive cell death (HR) at the site of pathogen penetration (Jones and Dangl, 2006). In addition, the onset of the HR typically triggers systemic acquired resistance (SAR), an inducible form of plant defense that spreads resistance to systemic tissues through mobilization of salicylic acid (SA)-mediated defenses and confers broad-spectrum immunity to secondary infection (Spoel and Dong, 2012). Plant hormones are crucial systemic signals that strongly influence the level of plant resistance. Indeed, significant changes in hormone levels and hormonal cross talk occur in plant cells interacting with microbes and are essential to the efficient integration of biotic stress cues (Pieterse et al., 2009). The intricate molecular mechanisms that govern plant immune responses engage a high degree of proteomic plasticity to which posttranslational protein modification through ubiquitination contributes crucially. Ubiquitin is a small (8.5 kD) and highly conserved protein modifier that, covalently linked to target proteins, leads to their proteasomal degradation or to other fates including relocalization or endocytosis. Typically, proteins modified by sequential linkage of multiple ubiquitin residues via the ubiquitin residue Lys-48 are targeted for degradation by the 26S proteasome, a highly conserved proteolytic complex composed of two subparticles (Smalle and Vierstra, 2004): (1) the barrel-shaped 20S proteasome that is a stack of two outer rings formed by seven α-subunits (α1–α7) and two inner rings of seven β-subunits (β1–β7) enclosing a cavity with the active sites for protein degradation and (2) the 19S regulatory particles that are attached at both ends of the 20S cylinder and recognize the protein targeted for degradation. The ubiquitin-26S proteasome system (UPS) involves the sequential action of three enzymes, namely E1 (ubiquitin activating), E2 (ubiquitin conjugating), and E3 (ubiquitin ligase), to ultimately ligate one or more ubiquitin molecules to specific target proteins (Vierstra, 2009). Ubiquitin is first activated for transfer by the E1 enzyme and activated ubiquitin is then transferred to a Cys residue in the E2. The ubiquitin-E2 intermediate generally serves as the proximal ubiquitin donor, using the E3 to identify the target and catalyze ubiquitin transfer. E3 enzymes are key factors that determine substrate specificity and are classified into four main subfamilies depending on their subunit composition and mechanism of action: Homologous to E6-associated protein Carboxyl Terminus (HECT), Really Interesting New Gene (RING), U-box, and cullin-RING ligases (CRLs; Vierstra, 2009). HECT proteins are single polypeptides that, unlike other E3 ligases, form a thioester intermediate with ubiquitin before ubiquitination of the target (Downes et al., 2003). RING and U-box proteins are structurally related single polypeptides that respectively use zinc chelation and hydrogen bonds/salt bridges to transfer ubiquitin from the E2-ubiquitin intermediate to the substrate (Stone et al., 2005; Yee and Goring, 2009). CRLs are multisubunit E3 ligases that contain a cullin, a RING-BOX1 that binds to ubiquitin, and a variable module for target recognition (Vierstra, 2009). The modular S-phase Kinase-associated Protein1 (SKP1)/CULLIN1 (CUL1)/F-Box (SCF) group is the best-characterized CRL. Arabidopsis (Arabidopsis thaliana) SKP1-like proteins are known as Arabidopsis SKP1-like (ASK). In SCF complexes, CUL1 acts as a molecular scaffold by interacting at its C terminus with RING-BOX1 (which is linked to the E2-ubiquitin intermediate) and at the N terminus with SKP1/ASK (which is linked to the F-box protein, responsible for recruiting the target) thereby promoting the transfer of ubiquitin from the E2 to the target (Vierstra, 2009). Here, we discuss the involvement of different UPS-related components during the regulation of plant immune responses, paying special attention to the well-characterized family of E3 ubiquitin ligases. Strikingly, targeted protein turnover through the UPS is a shared feature by most hormone signaling pathways (Santner and Estelle, 2009; Vierstra, 2009). Due to space limitations, we refer the reader to recently published reviews for a detailed account on the control of hormone signaling by ubiquitination during plant immunity (Trujillo and Shirasu, 2010; Robert-Seilaniantz et al., 2011). Finally, we also review our current knowledge about the exploitation of the host UPS by plant parasite proteins. Direct studies involving ubiquitin gene disruption may lead to severe effects in plant performance and eventually to plant lethality. To counteract this problem, several studies have used ubiquitin variants or transient silencing strategies. The use of a ubiquitin variant containing Arg instead of Lys at position 48 (UbR48) impairs polyubiquitination, and thus proteolytic degradation, but allows monoubiquitination to occur. Expression of UbR48 in tobacco (Nicotiana tabacum) plants induced the development of necrotic lesions and altered plant responses to infection with Tobacco mosaic virus (TMV; Becker et al., 1993), whereas in Arabidopsis, expression of UbR48 led to spontaneous cell death symptoms, reactive oxygen species (ROS) production, and constitutive induction of defense-related genes (Schlögelhofer et al., 2006). However, Arabidopsis plants expressing UbR48 did not present altered resistance to virulent or avirulent Pseudomonas syringae bacterial strains (Schlögelhofer et al., 2006). Partial depletion of ubiquitin levels by transient-induced silencing of the ubiquitin-encoding gene in barley (Hordeum vulgare) epidermal cells resulted in enhanced susceptibility to the powdery mildew fungus Blumeria graminis f. sp. hordei (Dong et al., 2006). Moreover, complementation studies suggested a role for Lys-48-linked polyubiquitination in defense signaling (Dong et al., 2006). The importance of proteasomal subunits for the regulation of the plant response to microbes has also been documented. In tobacco, expression of three genes encoding subunits of the 20S proteasome (α3, α6, β1) is induced after treatment with the elicitor cryptogein (Dahan et al., 2001; Suty et al., 2003). Tobacco cell lines overexpressing the β1 subunit showed a drastic reduction of the NtRbohD (NADPH oxidase) gene induction and of its associated oxidative burst after cryptogein treatment, suggesting that the β1 subunit acts as a negative regulator of early plant responses to cryptogein (Lequeu et al., 2005). In addition, RNA interference (RNAi) stable Arabidopsis lines the proteasome β1 subunit altered cell death responses bacterial pathogens et al., 2009). cell death associated with the of the with the proteins to the of the cells bacteria this response by plants with avirulent but not virulent suggesting that this type of cell death is related to resistance et al., 2009). In this proteasome protein degradation to for cell death but not for defense as cell death not by altered or expression of defense-related genes et al., 2009). In to the of the 20S of genes encoding subunits of the 19S proteasome regulatory did not the defense response graminis f. hordei (Dong et al., 2006). that the role by Lys-48-linked protein polyubiquitination in barley defense is from the proteasome the defense to in defense responses and in resistance bacterial but not in host defense thus suggesting that the proteasome may in susceptibility in E1 enzymes have been in The Arabidopsis modifier of a in the which of resistance et al., plants a in an gene that results in constitutive of defense responses et al., 2001; et al., 2003). plants more to a virulent Pseudomonas and susceptibility with bacteria different factors et al., a role of ubiquitination in defense bacterial pathogens and a specific role of this E1 in but not resistance of did not the suggesting of the two E1 enzymes and a for Arabidopsis resistance et al., In tobacco, expression of and induced in response to and defense-related hormones as and acid and the et al., 2005). on the induction of their expression E2 enzymes have been suggested to to plant resistance. expression of the gene but not its induced in cells with elicitor et al., enzymes are able to catalyze of a E3 that is also induced elicitor treatment et al., However, involvement of E2 proteins in plant defense responses to and genes proteins in of the expression of RING genes different has been et al., et al., et al., 2005; et al., 2006). 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In the of plant defense responses, a role of F-box proteins in the regulation of hormone signaling pathways has been and (Trujillo and Shirasu, 2010; Robert-Seilaniantz et al., 2011). their control of hormone production, F-box proteins have also been to during the regulation of plant defense to expression of the F-box encoding gene enhanced treatment with a of defense responses, and the plant hormone acid et al., of in tobacco resulted in acid and enhanced resistance and bacterial is protein that has been in the regulation of Arabidopsis a form of defense that is by and by the protein and highly to infection by the The showed of resistance both and in also in a in which is to that not of and of the Arabidopsis F-box encoding gene led to constitutive defense responses to syringae and et al., 2009). The a to the which a in a and this in the suggesting a both genes et al., 2012). 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Finally, also with and the plant resistance protein a key in the resistance and et al., syringae proteasomal degradation of Arabidopsis a plant by a ubiquitin et al., 2006). degradation and a of plant PTI Finally, an by plant pathogenic bacteria to the host UPS is by the that syringae syringae a called that and the host The of of strongly the of this on its host that of the proteasome is for et al., F-box encoding genes have also been to present in of two plant The cell F-box protein of the small virus family has been to with plant SKP1-like and proteins. is for a level of that of proteins by a complex cell and by of by is of its F-box and of protein ubiquitination and degradation is et al., et al., The protein of is an F-box protein that acts as a silencing and is for et al., et al., 2006). by by the degradation of a key in the silencing of not to on the proteasome et al., et al., In to its proteolytic the UPS associated with the subunit and is able to suggesting that this may of a defense et al., et al., 2011). a has been by the that the protein a of RNA with different 20S proteasomal subunits and with the of the 20S proteasome et al., 2005; et al., et al., 2011). Moreover, Arabidopsis for of the two genes encoding the subunit of the 20S proteasome more to infection by mosaic et al., 2011). In a protein to with modification of in the of the RING protein, this a mechanism to defense of et al., 2003). 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To our the that effectors may with their host UPS is the that the in with four different plant proteins in the ubiquitination the of this are et al., the protein of the a of ubiquitin with an et al., to the two ubiquitin a enzyme as as an SKP1-like protein et al., In a to the protein composition of the by into host cells, a et al., 2011). is to that and proteins may with the plant UPS during the infection The have the of a significant of UPS-related components that plant immune components to in of plant from pathogen recognition to downstream signaling during both PTI and E3 proteins have been as plant immunity in most their and of target proteins into the molecular mechanisms associated to plant In addition, our knowledge about the of monoubiquitination and other of ubiquitination their to plant immunity is and in Arabidopsis, the RING E3 that and with a subunit of the complex that the of RNA has been in resistance pathogens et al., 2009). of of other proteasomal protein degradation, thus a more of the regulatory associated to this posttranslational enzymes Arabidopsis and have been as negative of plant through of target as immunity et al., 2011). to determine of ubiquitin by enzymes the and of Finally, the that most microbes to have a to the host UPS (1) the importance of during the regulation of plant responses to pathogen and (2) a of the degree of by pathogens in their to the In for which ubiquitination has been In for which ubiquitination has been to not of space pathogen-associated molecular patterns RNA interference PAMP-triggered immunity effectors effector-triggered immunity hypersensitive cell death systemic acquired resistance salicylic acid ubiquitin-26S proteasome system cullin-RING ligases Tobacco mosaic virus reactive oxygen species
Source: PLANT PHYSIOLOGY
Authors: Daniel Marino, Nemo Peeters, Susana Rivas
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: green
OpenAlex ID: W1986921906