Endogenous RALF peptide function is required for powdery mildew host colonization

New Phytologist, vol. 251, pp. 2073–2090

Abstract

Summary The receptor kinase FERONIA (FER) is a susceptibility factor for biotrophic powdery mildew fungal pathogens in Arabidopsis thaliana , but the underlying molecular mechanisms remain largely unknown. FER is required for the perception of endogenous RAPID ALKALINIZATION FACTOR (RALF) peptides to control various aspects of plant growth, development and immunity. RALFs are either perceived by FER/LORELEI‐LIKE GPI‐ANCHORED PROTEIN (LLG) heterocomplexes to induce cellular responses or bind to LEUCINE‐RICH REPEAT EXTENSIN (LRX) proteins as cell wall structural components. Combining genetics, cell biology and biochemistry, we found that FER's endogenous RALF ligands are necessary for full colonization success of the powdery mildew‐species Erysiphe cruciferarum . We reveal that LLGs and LRXs are also powdery mildew susceptibility factors. We show that cell wall remodeling and apoplastic pH homeostasis, hallmark features of RALF function, support powdery mildew reproductive success. We provide data that RALF‐dependent powdery mildew pathogenesis is partially independent of FER. Powdery mildew fungi likely do not produce RALF peptide mimics, suggesting their reliance on endogenous RALFs for successful host colonization. We propose that powdery mildew fungi require RALF‐mediated modulation of apoplastic pH and pectin remodeling for successful host colonization, highlighting a new susceptibility mechanism by obligate biotrophic fungi.

Authors 18

1. Henriette Leicher

   Technical University of Munich

   Affiliation as printed

   Phytopathology, TUM School of Life Sciences Technical University of Munich (TUM) 85354 Freising Germany

2. Sebastian D. Schade

   Technical University of Munich

   Affiliation as printed

   Phytopathology, TUM School of Life Sciences Technical University of Munich (TUM) 85354 Freising Germany

3. Jan Hübbers Aachen Unit of Plant Molecular Cell Biology Institute for Biology I

   RWTH Aachen University

   Affiliation as printed

   Unit of Plant Molecular Cell Biology, Institute for Biology I RWTH Aachen University 52056 Aachen Germany

4. Kristina S. Munzert‐Eberlein

   Philipps University of Marburg

   Affiliation as printed

   Molecular Plant Physiology, Department of Biology Philipps‐Universität Marburg 35043 Marburg Germany

5. Genc Haljiti

   Technical University of Munich

   Affiliation as printed

   Bavarian Center for Biomolecular Mass Spectrometry (BayBioMS), TUM School of Life Science Technical University of Munich (TUM) 85354 Freising Germany

6. David Biermann

   Technical University of Munich

   Affiliation as printed

   Plant Cell Biology, TUM School of Life Sciences Technical University of Munich (TUM) 85354 Freising Germany

7. Athanasios Makris

   Leibniz Institute of Plant Biochemistry

   Affiliation as printed

   Leibniz‐Institute of Plant Biochemistry 06120 Halle Germany

8. Xiaoxuan Zhu

   Université Côte d'Azur · Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · Institut Sophia Agrobiotech

   Affiliation as printed

   Université Côte d'Azur INRAE, Institut Sophia Agrobiotech 06903 Sophia Antipolis Cedex France

9. Yashank Chauhan

   Technical University of Munich

   Affiliation as printed

   Phytopathology, TUM School of Life Sciences Technical University of Munich (TUM) 85354 Freising Germany

10. Christina Ludwig

    Technical University of Munich

    Affiliation as printed

    Bavarian Center for Biomolecular Mass Spectrometry (BayBioMS), TUM School of Life Science Technical University of Munich (TUM) 85354 Freising Germany

11. Marion Claudia Müller

    Technical University of Munich

    Affiliation as printed

    Phytopathology, TUM School of Life Sciences Technical University of Munich (TUM) 85354 Freising Germany

12. Toshinori Kinoshita

    Nagoya University

    Affiliation as printed

    Graduate School of Science Nagoya University Chikusa 464‐8602 Nagoya Japan

    Institute of Transformative Bio‐Molecules (WPI‐ITbM) Nagoya University Chikusa 464‐8602 Nagoya Japan

13. Timo Engelsdorf

    Philipps University of Marburg

    Affiliation as printed

    Molecular Plant Physiology, Department of Biology Philipps‐Universität Marburg 35043 Marburg Germany

14. Julien Gronnier

    Technical University of Munich

    Affiliation as printed

    Plant Cell Biology, TUM School of Life Sciences Technical University of Munich (TUM) 85354 Freising Germany

15. Martina Katharina Ried

    Leibniz Institute of Plant Biochemistry

    Affiliation as printed

    Leibniz‐Institute of Plant Biochemistry 06120 Halle Germany

16. Aurélien Boisson‐Dernier

    Université Côte d'Azur · Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · Institut Sophia Agrobiotech

    Affiliation as printed

    Université Côte d'Azur INRAE, Institut Sophia Agrobiotech 06903 Sophia Antipolis Cedex France

17. Ralph Hückelhoven

    Technical University of Munich

    Affiliation as printed

    Phytopathology, TUM School of Life Sciences Technical University of Munich (TUM) 85354 Freising Germany

18. Martin Stegmann corresponding

    Technical University of Munich

    Affiliation as printed

    Phytopathology, TUM School of Life Sciences Technical University of Munich (TUM) 85354 Freising Germany