A Plant Immune Receptor Degraded by Selective Autophagy

Abstract

Plants recycle non-activated immune receptors to maintain a functional immune system. The Arabidopsis immune receptor kinase FLAGELLIN-SENSING 2 (FLS2) recognizes bacterial flagellin. However, the molecular mechanisms by which non-activated FLS2 and other non-activated plant PRRs are recycled remain not well understood. Here, we provide evidence showing that Arabidopsis orosomucoid (ORM) proteins, which have been known to be negative regulators of sphingolipid biosynthesis, act as selective autophagy receptors to mediate the degradation of FLS2. Arabidopsis plants overexpressing ORM1 or ORM2 have undetectable or greatly diminished FLS2 accumulation, nearly lack FLS2 signaling, and are more susceptible to the bacterial pathogen Pseudomonas syringae. On the other hand, ORM1/2 RNAi plants and orm1 or orm2 mutants generated by the CRISPR/Cas9-mediated gene editing have increased FLS2 accumulation and enhanced FLS2 signaling, and are more resistant to P. syringae. ORM proteins interact with FLS2 and the autophagy-related protein ATG8. Interestingly, overexpression of ORM1 or ORM2 in autophagydefective mutants showed FLS2 abundance that is comparable to that in wild-type plants. Moreover, FLS2 levels were not decreased in Arabidopsis plants overexpressing ORM1/2 derivatives that do not interact with ATG8. Taken together, these results suggest that selective autophagy functions in maintaining the homeostasis of a plant immune receptor and that beyond sphingolipid metabolic regulation ORM proteins can also act as selective autophagy receptors.

Dehydrin MtCAS31 promotes autophagic degradation under drought stress

“…NBR1 was shown to promote the selective autophagic degradation of ubiquitinated targets via interacting with AtATG8 [51]. Orosomucoid ORM1/2 can maintain the function of the plant immune system by interacting with FLS2 (flagellin-sensing 2) and ATG8 [53]. Under drought and starvation stress, DSK2 is phosphorylated by BIN2 (a GSK3-like kinase) to promote the DSK2-ATG8 interaction and then enhances BES1 (BRI1-EMS suppressor 1) autophagic degradation [14].…”

Emerging Roles of the Selective Autophagy in Plant Immunity and Stress Tolerance

“…Under non-elicited conditions, non-activated plasma membrane (PM)-localized AtFLS2 constitutively recycles between the PM and endosomes via a clathrin-dependent endocytic trafficking route [80]. Intriguingly, it has been reported recently that orosomucoid (ORM) proteins regulate the stability of non-activated FLS2 [81]. ORMs have been reported regulating sphingolipid biosynthesis through suppressing the activity of serine palmitoyltransferase (SPT), which is a key enzyme in the sphingolipid synthesis pathway [82,83].…”

“…ORMs have been reported regulating sphingolipid biosynthesis through suppressing the activity of serine palmitoyltransferase (SPT), which is a key enzyme in the sphingolipid synthesis pathway [82,83]. In addition to participating in sphingolipid synthesis, ORM proteins interact with both FLS2 and the ATG8s via an AIM and act as a selective autophagy receptor to mediate the degradation of FLS2 [81]. These results indicate that ORM proteins serve as selective autophagy receptors for non-activated FLS2 to modulate plant immunity.…”

Diversity, Function and Regulation of Cell Surface and Intracellular Immune Receptors in Solanaceae

“…The use of mass spectrometry-based interactomic screens targeting various immune receptor protein of interest (under both mock and elicited conditions) could provide clues on downstream interacting proteins (both activator and repressor). Furthermore, newly discovered players in plant immunity are related to diverse processes like autophagy, vesicular trafficking and cytoskeleton [184][185][186]. Characterization of homologous solanaceous plant genes through CRISPR/Cas9 genome editing would expand our knowledge of genes that perturbs host resistance responses [187].…”