Proteolytic degradation pathways and their role in plant immunity

• Applicant: Professor Dr. Suayib Üstün
• Subject Area: Organismic Interactions, Chemical Ecology and Microbiomes of Plant Systems
• Term: from 2018 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 400923110

• Final Report Year: 2024

Final Report Abstract

It is well established that proteolytic pathways such as autophagy and the ubiquitin-proteasome system are involved in a broad array of cellular pathways including development, protein quality control, signal transduction and response to various stimuli. However, despite recent efforts, there is a lack of knowledge how pathogens modulate these pathways and what target proteins are degraded implicated in plant immunity. Here we show how Xanthomonas suppresses autophagy via the type-III effector XopL to escape its own degradation. We have identified that XopL from Xanthomonas exhibits E3 ligase activity to degrade autophagy component SH3P2 for autophagy suppression. We have profound evidence that the effector blocks autophagy to escape its own degradation by the autophagy pathway and to increase virulence of Xanthomonas in plants. Additionally, our research identifies the ARF-GEF protein BIG5, also known as MIN7, as a novel modulator of autophagy, linking vesicle trafficking to autophagic processes. The loss of BIG5 was shown to activate autophagy, indicating its regulatory role in this pathway. Overall, our study deepened the understanding of how these degradation pathways function in plant immunity and how pathogens may exploit them, ultimately contributing to improved agricultural resilience against diseases.

Publications

• Microbial Effector Proteins – A Journey through the Proteolytic Landscape. Trends in Microbiology, 28(7), 523-535.
  Langin, Gautier; Gouguet, Paul & Üstün, Suayib
  
• A bacterial effector counteracts host autophagy by promoting degradation of an autophagy component. The EMBO Journal, 41(13).
  Leong, Jia Xuan; Raffeiner, Margot; Spinti, Daniela; Langin, Gautier; Franz‐Wachtel, Mirita; Guzman, Andrew R.; Kim, Jung‐Gun; Pandey, Pooja; Minina, Alyona E.; Macek, Boris; Hafrén, Anders; Bozkurt, Tolga O.; Mudgett, Mary Beth; Börnke, Frederik; Hofius, Daniel & Üstün, Suayib
  
• Crossing paths: recent insights in the interplay between autophagy and intracellular trafficking in plants. FEBS Letters, 596(17), 2305-2313.
  Gouguet, Paul & Üstün, Suayib
  
• Selective autophagy: adding precision in plant immunity. Essays in Biochemistry, 66(2), 189-206.
  Leong, Jia Xuan; Langin, Gautier & Üstün, Suayib
  
• The Arabidopsis SAC9 enzyme is enriched in a cortical population of early endosomes and restricts PI(4,5)P2 at the plasma membrane. eLife, 11.
  Lebecq, Alexis; Doumane, Mehdi; Fangain, Aurelie; Bayle, Vincent; Leong, Jia Xuan; Rozier, Frédérique; Marques-Bueno, Maria del; Armengot, Laia; Boisseau, Romain; Simon, Mathilde Laetitia; Franz-Wachtel, Mirita; Macek, Boris; Üstün, Suayib; Jaillais, Yvon & Caillaud, Marie-Cécile
  
• Interplay between autophagy and proteasome during protein turnover. Trends in Plant Science, 28(6), 698-714.
  Raffeiner, Margot; Zhu, Shanshuo; González-Fuente, Manuel & Üstün, Suayib
  
• The Plant Ubiquitin–Proteasome System as a Target for Microbial Manipulation. Annual Review of Phytopathology, 61(1), 351-375.
  Langin, Gautier; González-Fuente, Manuel & Üstün, Suayib
  
• XopM, An FFAT Motif‐Containing Type III Effector Protein From Xanthomonas, Suppresses MTI Responses at the Plant Plasma Membrane. Molecular Plant Pathology, 25(12).
  Brinkmann, Charlotte; Bortlik, Jennifer; Raffeiner, Margot; González‐Fuente, Manuel; Börnke, Linus F.; Üstün, Suayib & Börnke, Frederik
  
• ATG8 delipidation is not universally critical for autophagy in plants. Nature Communications, 16(1).
  Zou, Yong; Ohlsson, Jonas A.; Holla, Sanjana; Sabljić, Igor; Leong, Jia Xuan; Ballhaus, Florentine; Krebs, Melanie; Schumacher, Karin; Moschou, Panagiotis N.; Stael, Simon; Üstün, Suayib; Dagdas, Yasin; Bozhkov, Peter V. & Minina, Elena A.
  
• Autophagy restricts tomato fruit ripening via a general role in ethylene repression. New Phytologist, 246(6), 2392-2404.
  Kumaran, Girishkumar; Pathak, Pradeep Kumar; Quandoh, Ebenezer; Devi, Jyoti; Mursalimov, Sergey; Alkalai‐Tuvia, Sharon; Leong, Jia Xuan; Schenstnyi, Kyrylo; Levin, Elena; Üstün, Suayib & Michaeli, Simon