Abstract
Our research provides new insights into how the low and steady-state levels of nitric oxide (NO) and reactive oxygen species (ROS) in potato leaves are altered after the challenge with the hemibiotroph Phytophthora infestans or the necrotroph Botrytis cinerea, with the subsequent rapid and invader-dependent modification of defense responses with opposite effects. Mainly in the avirulent (avr) P. infestans–potato system, NO well balanced with the superoxide level was tuned with a battery of SA-dependent defense genes, leading to the establishment of the hypersensitive response (HR) successfully arresting the pathogen. Relatively high levels of S-nitrosoglutathione and S-nitrosothiols concentrated in the main vein of potato leaves indicated the mobile function of these compounds as a reservoir of NO bioactivity. In contrast, low-level production of NO and ROS during virulent (vr) P. infestans-potato interactions might be crucial in the delayed up-regulation of PR-1 and PR-3 genes and compromised resistance to the hemibiotrophic pathogen. In turn, B. cinerea triggered huge NO overproduction and governed inhibition of superoxide production by blunting NADPH oxidase. Nevertheless, a relatively high level of H2O2 was found owing to the germin-like activity in cooperation with NO-mediated HR-like cell death in potato genotypes favorable to the necrotrophic pathogen. Moreover, B. cinerea not only provoked cell death, but also modulated the host redox milieu by boosting protein nitration, which attenuated SA production but not SA-dependent defense gene expression. Finally, based on obtained data the organismal cost of having machinery for HR in plant resistance to biotrophs is also discussed, while emphasizing new efforts to identify other components of the NO/ROS cell death pathway and improve plant protection against pathogens of different lifestyles.
Highlights
Both plants and pathogens of different lifestyles have adopted sophisticated strategies to secure their survival and reproduction
An approximately 4-fold rise in nitric oxide (NO) production was found in the potato Bintje–B. cinerea interaction, in which it was significantly more abundant when compared to the virulent P. infestans–potato response (Fig 1B)
The most intensive fluorescence related to the cellular S-nitrosothiol (SNO) pool was observed in the avr P. infestans–potato interaction, as well as in the B. cinerea–genotype Bzura interaction at 48 hpi (Fig 2B and 2C)
Summary
Both plants and pathogens of different lifestyles have adopted sophisticated strategies to secure their survival and reproduction. The Role of NO in the Battle of Potato against Pathogens have shown that necrotrophic pathogens impart an ecological cost on plant resistance to biotrophic pathogens. Studies on ecological costs, defined as resulting from any plant mechanisms that provide resistance to biotrophs or hemibiotrophs, but increasing their susceptibility to necrotrophs, are based on the concept that the plant immune system possesses an ability to self-regulate programmed cell death with reference to a “threshold for the hypersensitive response” [1]. In view of the observation by the cited authors, if the environment is abundant in biotrophic pathogens, plants may be subjected to evolutionary pressure to activate a hypersensitive response at a lower threshold. Necrotrophs dominant in an environment kill host cells using toxic compounds by overcoming the threshold for the initiation of the hypersensitive response, facilitating infection. It has been found that the host defense system against a biotroph or hemibiotroph attack might be targeted by toxins of necrotrophic pathogens to enhance virulence and provide susceptibility [3]
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