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. 2019 Dec 3;13(4):768-780.
doi: 10.1111/eva.12899. eCollection 2020 Apr.

Rapid Adaptation of the Irish Potato Famine Pathogen Phytophthora infestans to Changing Temperature

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Free PMC article

Rapid Adaptation of the Irish Potato Famine Pathogen Phytophthora infestans to Changing Temperature

E-Jiao Wu et al. Evol Appl. .
Free PMC article

Abstract

Temperature plays a multidimensional role in host-pathogen interactions. As an important element of climate change, elevated world temperature resulting from global warming presents new challenges to sustainable disease management. Knowledge of pathogen adaptation to global warming is needed to predict future disease epidemiology and formulate mitigating strategies. In this study, 21 Phytophthora infestans isolates originating from seven thermal environments were acclimated for 200 days under stepwise increase or decrease of experimental temperatures and evolutionary responses of the isolates to the thermal changes were evaluated. We found temperature acclimation significantly increased the fitness and genetic adaptation of P. infestans isolates at both low and high temperatures. Low-temperature acclimation enforced the countergradient adaptation of the pathogen to its past selection and enhanced the positive association between the pathogen's intrinsic growth rate and aggressiveness. At high temperatures, we found that pathogen growth collapsed near the maximum temperature for growth, suggesting a thermal niche boundary may exist in the evolutionary adaptation of P. infestans. These results indicate that pathogens can quickly adapt to temperature shifts in global warming. If this is associated with environmental conditions favoring pathogen spread, it will threaten future food security and human health and require the establishment of mitigating actions.

Keywords: Phytophthora infestans; acclimation; aggressiveness; fitness; thermal adaptation.

Conflict of interest statement

None declared.

Figures

Figure 1
Figure 1
Map showing the geographic locations of the seven Phytophthora infestans populations included in this study
Figure 2
Figure 2
The flowchart of Phytophthora infestans temperature acclimatization: The yellow cylinder represents the parental isolates preserved in microtubes at 13°C for long‐term storage. The black circles represent the parental isolates revived and maintained on rye B plates at 19°C (the optimum temperature of the pathogen); gray circles represent parental isolates without trained (controls); blue circles represent isolates continuously trained under increasing temperatures; and green circles represent isolates continuously trained under reducing temperatures. Arrows represent the transfer of isolates to fresh rye B plates after 10 days (one generation), and orange circles indicate the stages when aggressiveness of acclimated isolates was tested. The acclimation lasted for 20 generations (transfers) with 10 days in each generation
Figure 3
Figure 3
Temporal changes (fitted smoother) of mean colony size and its 95% confidence interval (CI) in the acclimated and unacclimated Phytophthora infestans isolates. The mean colony sizes were estimated over all 21 isolates collected from the seven locations. Acclimation was carried out in two directions under continuing increase or decrease of temperatures over 20 generations (10 days per generation). At the high‐temperature acclimation, the pathogen was continually trained under a steady increase of experimental temperatures at 1°C interval starting from 26°C and ending at 30°C (total five temperature regimes). In each temperature regime, the pathogen was acclimated for four generations. Similarly, at the low‐temperature acclimation, the pathogen was continually trained under a steady decrease of experimental temperatures at 1°C interval starting from 12°C. The acclimation was also executed under five temperature regimes (ending at 8°C) each with four generations: (a) high‐temperature acclimation; and (b) low‐temperature acclimation
Figure 4
Figure 4
Temporal changes in mean relative colony size, aggressiveness, and their associated 95% confidence intervals of acclimated to unacclimated Phytophthora infestans isolates growing in the low‐ and high‐temperature acclimation treatments. The aggressiveness of the isolates was assessed at the end of each four generations, and the mean relative colony sizes and mean aggressiveness were estimated over all 21 isolates collected from the seven locations. Acclimations were carried out in two directions under continuing increase or decrease of temperatures over 20 generations (10 days per generation). At the high‐temperature acclimation, pathogen was continually trained under a steady increase of experimental temperatures at 1°C interval starting from 26°C and ending at 30°C (total five temperature regimes). In each temperature regime, the pathogen was acclimated for four generations. Similarly, at the low‐temperature acclimation, pathogen was continually trained under a steady decrease of experimental temperatures at 1°C interval starting from 12°C. The acclimation was also executed under five temperature regimes (ending at 8°C) each with four generations: (a) relative colony size under high‐ and low‐temperature acclimation; and (b) relative lesion size under low‐temperature acclimation
Figure 5
Figure 5
Temporal changes of mean lesion size (aggressiveness) and its associated 95% confidence interval (CI) in the acclimated and unacclimated Phytophthora infestans isolates. Aggressiveness of the isolates was assessed at the end of each four generations at a particular temperature regime, and the mean aggressiveness was estimated over all 21 isolates collected from the seven locations
Figure 6
Figure 6
The response of the association between pathogen colony size or lesion size and the annual mean temperature at collection sites to the changing experimental temperatures in acclimated and unacclimated isolates: (a) without high‐temperature acclimation for mycelial growth; (b) with high‐temperature acclimation for mycelial growth; (c) without low‐temperature acclimation for mycelial growth; (d) with low‐temperature acclimation for mycelial growth; (e) without low‐temperature acclimation for aggressiveness; and (f) with low‐temperature acclimation for aggressiveness
Figure 7
Figure 7
The impact of low‐temperature acclimation on the association between colony size and aggressiveness of 21 Phytophthora infestans isolates collected from seven potato field geographic sites in China: (a) unacclimated; and (b) acclimated

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