Rapid adaptation of the Irish potato famine pathogen Phytophthora infestans to changing temperature

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.

Altitudinal Heterogeneity of UV Adaptation in Phytophthorainfestans Is Associated with the Spatial Distribution of a DNA Repair Gene

“…The contribution of DNA repair genes in enhancing the adaptation of a species to high altitudes has also been reported in other organisms, including animals and plants [ 79 , 80 , 81 , 82 ]. Although these inferences indicate that many species are fully equipped to respond to UV stresses, experimental evolution combined with genomic approaches, such as passaging [ 39 ], GWAS [ 83 ]. and proteomics [ 84 ], may be required to confirm the results and to determine how quickly adaptation could occur and which other genes may be involved.…”

“…It has a worldwide distribution and can quickly adapt to environmental stresses, such as host resistance and climate change; this is likely attributable to large genomes and a high density of transposable elements [ 37 , 38 ]. For example, the pathogen increased by ~20% fitness after it was acclimated either at low (13 °C) or high temperature (25 °C) conditions for 200 days [ 39 ]. Germination and viability of P. infestans sporangia and other reproductive units can be significantly decreased even when exposed to only short periods of UV conditions [ 39 , 40 ].…”

“…For example, the pathogen increased by ~20% fitness after it was acclimated either at low (13 °C) or high temperature (25 °C) conditions for 200 days [ 39 ]. Germination and viability of P. infestans sporangia and other reproductive units can be significantly decreased even when exposed to only short periods of UV conditions [ 39 , 40 ]. Interestingly, even though the pathogen is generally very sensitive to UV irradiation, experimental data have shown that it can adapt to the environmental stress through both genetic and quasi-genetic mechanisms [ 41 ].…”

Climate change and disease in plant communities

“…In areas where changes favor the pathogen, genetic change in invasive traits such as aggressiveness (and/or infectivity), fungicide sensitivity, and eco-niche breadth and preference [ 5 , 8 , 9 ] can occur rapidly. Equally, there is evidence supporting the possibility of genetically based temperature adaptation [ 10 ] that may make the prospect of expansion of a pathogen’s geographic range more concerning. However, human-directed evolution can ensure corresponding changes in the defensive traits of crops.…”

“…This occurs against potential shifts in the niche breadth of pathogens and their host plants [ 5 ]. There is then an urgent need to empirically study the adaptive responses of pathogens and their hosts to climate changes using cutting-edge technology applied to a combination of approaches such as experimental evolution in the laboratory or field [ 10 , 41 ]. Such studies built around long-term, real-world pathogen–host epidemiological and evolutionary studies will help the development of new models that account for the future climatic preferences and niche breadths of plants, pathogens, and their interactions.…”