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Graft-transmissible resistance of cherry pepper (Capsicum annuum var. cerasiforme) to powdery mildew (Leveillula taurica) is associated with elevated superoxide accumulation, NADPH oxidase activity and pathogenesis-related gene expression

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Abstract

We found that resistance to pepper powdery mildew (PM) (Leveillula taurica) develops in a sweet pepper (Capsicum annuum) cultivar (‘Totál’) when grafted on a resistant cherry pepper (C. annuum var. cerasiforme) rootstock (cv. Szentesi). Resistance is manifested both towards PM symptoms and pathogen accumulation. In healthy, uninfected plants PM-resistance can be predicted by enhanced accumulation of the reactive oxygen species (ROS) superoxide (O .−2 ) and activity of NADPH oxidase, the enzyme mainly responsible for pathogenesis-related superoxide generation. In L. taurica-inoculated PM-resistant ‘Szentesi’ high levels of superoxide and NADPH oxidase activity are sustained even 45 days after inoculation, as opposed to PM-susceptible ‘Totál’. This is also true for ‘Totál’ grafted on resistant ‘Szentesi’ rootstocks, where PM resistance, enhanced superoxide production and NADPH oxidase activity is likely due to an unknown, graft-transmitted signal. To further elucidate the mechanisms of graft-transmissible PM-resistance we monitored expression of pathogenesis-related (PR) genes in healthy and infected plants. In healthy plants, expression of CaPR-1 is several times higher in leaves of PM-resistant pepper than in sensitive plants, while high expression of CaPR-2 (glucanase) does not entirely correlate with PM-resistance, being detectable only in PM-resistant ‘Szentesi’. However, during advanced stages of PM-pathogenesis (45 DAI) expression of CaPR-1 and CaPR-2 is by far the highest in PM-susceptible ‘Totál’. Our results suggest that the direct biochemical cause of graft-transmissible PM-resistance in pepper is the enhanced accumulation of NADPH oxidase-generated superoxide. To our knowledge, this is the first report on the role of ROS (superoxide) in graft-transmissible, pathogen-specific disease resistance.

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Acknowledgements

The help of Dr. József Fodor (Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences) in NADPH oxidase activity assays is gratefully acknowledged. Thanks are also due to Prof. Zoltán Király (PPI, CAR, HAS) for his valuable suggestions in the initial stages of the work. This research was supported by grants of the Hungarian National Research, Development and Innovation Office (NKFIH K111995, K112146 and PD108455).

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    1. Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, 15 Herman O. Street, 1022, Budapest, Hungary

      Réka Albert, András Künstler, Attila L. Ádám & Lóránt Király

    2. Faculty of Agriculture, Institute of Plant Science and Environmental Studies, University of Szeged, 15 Andrássy Street, 6800, Hódmezővásárhely, Hungary

      Ferenc Lantos

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    Albert, R., Künstler, A., Lantos, F. et al. Graft-transmissible resistance of cherry pepper (Capsicum annuum var. cerasiforme) to powdery mildew (Leveillula taurica) is associated with elevated superoxide accumulation, NADPH oxidase activity and pathogenesis-related gene expression. Acta Physiol Plant 39, 53 (2017). https://doi.org/10.1007/s11738-017-2353-5

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