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. 2022 Jul 30;8(8):808.
doi: 10.3390/jof8080808.

Elevating Air Temperature May Enhance Future Epidemic Risk of the Plant Pathogen Phytophthora infestans

E-Jiao Wu  1 , Yan-Ping Wang  2 , Li-Na Yang  3 , Mi-Zhen Zhao  1 , Jiasui Zhan  4
Affiliations

Elevating Air Temperature May Enhance Future Epidemic Risk of the Plant Pathogen Phytophthora infestans

E-Jiao Wu et al. J Fungi (Basel). .

Abstract

Knowledge of pathogen adaptation to global warming is important for predicting future disease epidemics and food production in agricultural ecosystems; however, the patterns and mechanisms of such adaptation in many plant pathogens are poorly understood. Here, population genetics combined with physiological assays and common garden experiments were used to analyze the genetics, physiology, and thermal preference of pathogen aggressiveness in an evolutionary context using 140 Phytophthora infestans genotypes under five temperature regimes. Pathogens originating from warmer regions were more thermophilic and had a broader thermal niche than those from cooler regions. Phenotypic plasticity contributed ~10-fold more than heritability measured by genetic variance. Further, experimental temperatures altered the expression of genetic variation and the association of pathogen aggressiveness with the local temperature. Increasing experimental temperature enhanced the variation in aggressiveness. At low experimental temperatures, pathogens from warmer places produced less disease than those from cooler places; however, this pattern was reversed at higher experimental temperatures. These results suggest that geographic variation in the thermal preferences of pathogens should be included in modeling future disease epidemics in agricultural ecosystems in response to global warming, and greater attention should be paid to preventing the movement of pathogens from warmer to cooler places.

Keywords: AUDPC; counter-gradient variation; ecological sustainability; natural selection; pathogen evolution; plant disease; thermal adaptation.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Frequency distribution of aggressiveness in the 140 Phytophthora infestans isolates sampled from seven geographic locations with different annual mean temperatures in China. The aggressiveness, represented by AUDPC, was estimated from the lesion sizes of 140 Phytophthora infestans isolates at 2–6 days post-inoculation.
Figure 2
Figure 2
Influence of annual mean temperature at the collection site on the thermal preference of Phytophthora infestans aggressiveness. The thermal preference of aggressiveness of each isolate was estimated from the fitted thermal reaction norm. (A) Maximum temperature; (B) optimum temperature; (C) minimum temperature; and (D) temperature breadth.
Figure 3
Figure 3
The thermal adaptation pattern of Phytophthora infestans aggressiveness estimated from 140 isolates sampled from seven geographic locations with different annual mean temperatures: (A) the thermal reaction norm estimated from AUDPC of isolates at the five temperature regimes; (B) the spectrum estimated from the difference between isolates with the highest and lowest aggressiveness in the populations; (C) standard deviation of aggressiveness of the 140 isolates.
Figure 4
Figure 4
The interactive impact of experimental and historical temperature (i.e., the air temperature at the pathogen collection site) on the development of Phytophthora infestans aggressiveness. Pathogen aggressiveness was quantified from 140 isolates sampled from seven geographic locations in China. The aggressiveness, measured by AUDPC, was estimated from lesion size at 2–6 days post-inoculation at five experimental temperatures. NOTE: The bar color shows the change in aggressiveness value from low (blue) to high (red).
Figure 5
Figure 5
Impact of experimental temperature on the thermal adaptation of Phytophthora infestans. Thermal adaptation was quantified by analyzing the linear association (correlation coefficient) between the aggressiveness of Phytophthora infestans and the annual mean temperature at its collection site.
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