A plant receptor domain with functional analogies to animal malectin disables ER stress responses upon infection

Giordano, Laïla; Allasia, Valérie; Cremades, Alexandra; Hok, Sophie; Panabières, Franck; Bailly-Maître, Béatrice; Keller, Harald

doi:10.1016/j.isci.2022.103877

Cited by 3 publications

(18 citation statements)

References 60 publications

(89 reference statements)

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“…These mutants still produce HAP6 transcripts and exhibit relatively mild phenotypes with respect to the UPR and their interaction with pathogens, such as Hpa (Giordano et al, 2022) and the powdery mildew fungus (Weis et al, 2013). These phenotypes were more strongly pronounced in rpn2-2 than in rpn2-1 (Giordano et al, 2022;Weis et al, 2013).…”

Section: Hap6 Stimulates Aba Signalling On Infectionmentioning

confidence: 99%

“…Tunicamycin inhibits N-glycosylation of proteins in the ER and triggers the UPR in Arabidopsis (Nagashima et al, 2011). To analyse whether or not a stimulation of the UPR may influence ABA signalling, we treated seedlings from the Arabidopsis Ler wild-type (Wt), the ios1-1 mutant, and a line that expresses the IOS1 exodomain in the ios1-1 mutant background (line ED3.6; Giordano et al, 2022) with this drug. In ios1-1 mutant plants, the accumulation of transcripts from previously described UPR marker genes, such as PDI5 and SAR1 (Giordano et al, 2022), was significantly increased (Figure 1a).…”

Section: Er Stress-mediated Aba Signalling Is Attenuated By the Ios1 ...mentioning

confidence: 99%

“…To analyse whether or not a stimulation of the UPR may influence ABA signalling, we treated seedlings from the Arabidopsis Ler wild-type (Wt), the ios1-1 mutant, and a line that expresses the IOS1 exodomain in the ios1-1 mutant background (line ED3.6; Giordano et al, 2022) with this drug. In ios1-1 mutant plants, the accumulation of transcripts from previously described UPR marker genes, such as PDI5 and SAR1 (Giordano et al, 2022), was significantly increased (Figure 1a). This increased mRNA accumulation in the absence of IOS1 was repressed in line ED3.6 (Figure 1a), confirming that the exodomain of IOS1 attenuates UPR signalling.…”

Section: Er Stress-mediated Aba Signalling Is Attenuated By the Ios1 ...mentioning

confidence: 99%

“…IOS1 interacts with the ER-residing ribophorin HAP6, which positively regulates the UPR during infection with Hpa and thus antagonizes the activity of IOS1 in the ER (Giordano et al, 2022). We therefore addressed the question of whether HAP6, similar to IOS1, also affects ABA signalling.…”

Section: Hap6 Stimulates Aba Signalling On Infectionmentioning

confidence: 99%

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The exodomain of the impaired oomycete susceptibility 1 receptor mediates both endoplasmic reticulum stress responses and abscisic acid signalling during downy mildew infection of Arabidopsis

Giordano

Schimmerling

Panabières

et al. 2022

Molecular Plant Pathology

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The phytohormone abscisic acid (ABA) regulates cell growth and plant development, and contributes to defence responses to pathogens. We previously showed that the Arabidopsis malectin‐like domain leucine‐rich repeat receptor‐like kinase (MLD‐LRR‐RLK) impaired oomycete susceptibility 1 (IOS1) attenuates ABA signalling during infection with the oomycete downy mildew pathogen Hyaloperonospora arabidopsidis. The exodomain of IOS1 with its MLD retains the receptor in the endoplasmic reticulum (ER), where it interacts with the ribophorin HAP6 to dampen a pathogen‐induced ER stress response called the unfolded protein response (UPR). The down‐regulation of both ABA and UPR signalling probably provides the pathogen with an advantage for infection. Here, we show that ABA‐related phenotypes of the ios1‐1 mutant, such as up‐regulated expression of ABA‐responsive genes and hypersensitivity to exogenous ABA application, were reverted by expression of the IOS1 exodomain in the mutant background. Furthermore, knockdown mutants for ER‐resident HAP6 showed similarly reduced UPR and ABA signalling, indicating that HAP6 positively regulates both pathways. Our data suggest that the IOS1 exodomain and HAP6 contribute in the ER to the IOS1‐mediated interference with ABA and UPR signalling.

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Section: Hap6 Stimulates Aba Signalling On Infectionmentioning

confidence: 99%

Section: Er Stress-mediated Aba Signalling Is Attenuated By the Ios1 ...mentioning

confidence: 99%

Section: Er Stress-mediated Aba Signalling Is Attenuated By the Ios1 ...mentioning

confidence: 99%

Section: Hap6 Stimulates Aba Signalling On Infectionmentioning

confidence: 99%

See 2 more Smart Citations

The exodomain of the impaired oomycete susceptibility 1 receptor mediates both endoplasmic reticulum stress responses and abscisic acid signalling during downy mildew infection of Arabidopsis

Giordano

Schimmerling

Panabières

et al. 2022

Molecular Plant Pathology

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“…More recently, a tomato malectin (referred to as malectin-like domain protein, SlRLK-like, in the original publication), was shown to affect the localization and abundance of the LeEIX2 receptor, resulting in the suppression of EIX-induced immune responses in tomato [ 54 ]. Moreover, recent research has revealed that the MLD of the MLD-containing receptor IOS1 retains IOS1 in the ER of plant cells and attenuates the infection-induced UPR in Arabidopsis thaliana [ 55 ].…”

Section: Introductionmentioning

confidence: 99%

The Rice Malectin Regulates Plant Cell Death and Disease Resistance by Participating in Glycoprotein Quality Control

Feng

Qiu

Yin

et al. 2022

IJMS

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In animals, malectin is well known to play an essential role in endoplasmic reticulum quality control (ERQC) by interacting with ribophorin I, one unit of the oligosaccharyltransferase (OST) complex. However, the functions of malectin in plants remain largely unknown. Here, we demonstrate the rice OsMLD1 is an ER- and Golgi-associated malectin protein and physically interacts with rice homolog of ribophorin I (OsRpn1), and its disruption leads to spontaneous lesion mimic lesions, enhanced disease resistance, and prolonged ER stress. In addition, there are many more N-glycosites and N-glycoproteins identified from the mld1 mutant than wildtype. Furthermore, OsSERK1 and OsSERK2, which have more N-glycosites in mld1, were demonstrated to interact with OsMLD1. OsMLD1 can suppress OsSERK1- or OsSERK2-induced cell death. Thus, OsMLD1 may play a similar role to its mammalian homologs in glycoprotein quality control, thereby regulating cell death and immunity of rice, which uncovers the function of malectin in plants.

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The Phytophthora parasitica effector AVH195 interacts with ATG8, attenuates host autophagy, and promotes biotrophic infection

Testi,

Kuhn,

Allasia

et al. 2024

BMC Biol

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Background Plant pathogens secrete effector proteins into host cells to suppress immune responses and manipulate fundamental cellular processes. One of these processes is autophagy, an essential recycling mechanism in eukaryotic cells that coordinates the turnover of cellular components and contributes to the decision on cell death or survival. Results We report the characterization of AVH195, an effector from the broad-spectrum oomycete plant pathogen, Phytophthora parasitica. We show that P. parasitica expresses AVH195 during the biotrophic phase of plant infection, i.e., the initial phase in which host cells are maintained alive. In tobacco, the effector prevents the initiation of cell death, which is caused by two pathogen-derived effectors and the proapoptotic BAX protein. AVH195 associates with the plant vacuolar membrane system and interacts with Autophagy-related protein 8 (ATG8) isoforms/paralogs. When expressed in cells from the green alga, Chlamydomonas reinhardtii, the effector delays vacuolar fusion and cargo turnover upon stimulation of autophagy, but does not affect algal viability. In Arabidopsis thaliana, AVH195 delays the turnover of ATG8 from endomembranes and promotes plant susceptibility to P. parasitica and the obligate biotrophic oomycete pathogen Hyaloperonospora arabidopsidis. Conclusions Taken together, our observations suggest that AVH195 targets ATG8 to attenuate autophagy and prevent associated host cell death, thereby favoring biotrophy during the early stages of the infection process.

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A plant receptor domain with functional analogies to animal malectin disables ER stress responses upon infection

Cited by 3 publications

References 60 publications

The exodomain of the impaired oomycete susceptibility 1 receptor mediates both endoplasmic reticulum stress responses and abscisic acid signalling during downy mildew infection of Arabidopsis

The exodomain of the impaired oomycete susceptibility 1 receptor mediates both endoplasmic reticulum stress responses and abscisic acid signalling during downy mildew infection of Arabidopsis

The Rice Malectin Regulates Plant Cell Death and Disease Resistance by Participating in Glycoprotein Quality Control

The Phytophthora parasitica effector AVH195 interacts with ATG8, attenuates host autophagy, and promotes biotrophic infection

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