Multiple Mechanisms Drive the Evolutionary Adaptation of <i>Phytophthora infestans</i> Effector Avr1 to Host Resistance
Effectors, a group of small proteins secreted by pathogens, play a central role in antagonistic interactions between plant hosts and pathogens. The evolution of effector genes threatens plant disease management and sustainable food production, but population genetic analyses to understand evolutiona...
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MDPI AG
2021-09-01
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| author | Lin-Lin Shen Abdul Waheed Yan-Ping Wang Oswald Nkurikiyimfura Zong-Hua Wang Li-Na Yang Jiasui Zhan |
| author_facet | Lin-Lin Shen Abdul Waheed Yan-Ping Wang Oswald Nkurikiyimfura Zong-Hua Wang Li-Na Yang Jiasui Zhan |
| author_sort | Lin-Lin Shen |
| collection | DOAJ |
| description | Effectors, a group of small proteins secreted by pathogens, play a central role in antagonistic interactions between plant hosts and pathogens. The evolution of effector genes threatens plant disease management and sustainable food production, but population genetic analyses to understand evolutionary mechanisms of effector genes are limited compared to molecular and functional studies. Here we investigated the evolution of the <i>Avr1</i> effector gene from 111 <i>Phytophthora infestans</i> isolates collected from six areas covering three potato cropping regions in China using a population genetic approach. High genetic variation of the effector gene resulted from diverse mechanisms including base substitution, pre-termination, intragenic recombination and diversifying selection. Nearly 80% of the 111 sequences had a point mutation in the 512th nucleotide (T512G), which generated a pre-termination stop codon truncating 38 amino acids in the C-terminal, suggesting that the C-terminal may not be essential to ecological and biological functions of <i>P. infestans.</i> A significant correlation between the frequency of <i>Avr1</i> sequences with the pre-termination and annual mean temperature in the collection sites suggests that thermal heterogeneity might be one of contributors to the diversifying selection, although biological and biochemical mechanisms of the likely thermal adaptation are not known currently. Our results highlight the risk of rapid adaptation of <i>P. infestans</i> and possibly other pathogens as well to host resistance, and the application of eco-evolutionary principles is necessary for sustainable disease management in agricultural ecosystems. |
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| spelling | doaj.art-097a4ae4e0a145b98c9b30c8c581de922023-11-22T18:46:28ZengMDPI AGJournal of Fungi2309-608X2021-09-0171078910.3390/jof7100789Multiple Mechanisms Drive the Evolutionary Adaptation of <i>Phytophthora infestans</i> Effector Avr1 to Host ResistanceLin-Lin Shen0Abdul Waheed1Yan-Ping Wang2Oswald Nkurikiyimfura3Zong-Hua Wang4Li-Na Yang5Jiasui Zhan6Key Lab for Biopesticide and Chemical Biology, Fujian Agriculture and Forestry University, Ministry of Education, Fuzhou 350002, ChinaKey Lab for Biopesticide and Chemical Biology, Fujian Agriculture and Forestry University, Ministry of Education, Fuzhou 350002, ChinaCollege of Chemistry and Life Sciences, Sichuan Provincial Key Laboratory for Development and Utilization of Characteristic Horticultural Biological Resources, Chengdu Normal University, Chengdu 611130, ChinaKey Lab for Biopesticide and Chemical Biology, Fujian Agriculture and Forestry University, Ministry of Education, Fuzhou 350002, ChinaKey Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaKey Lab for Biopesticide and Chemical Biology, Fujian Agriculture and Forestry University, Ministry of Education, Fuzhou 350002, ChinaDepartment of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, 75007 Uppsala, SwedenEffectors, a group of small proteins secreted by pathogens, play a central role in antagonistic interactions between plant hosts and pathogens. The evolution of effector genes threatens plant disease management and sustainable food production, but population genetic analyses to understand evolutionary mechanisms of effector genes are limited compared to molecular and functional studies. Here we investigated the evolution of the <i>Avr1</i> effector gene from 111 <i>Phytophthora infestans</i> isolates collected from six areas covering three potato cropping regions in China using a population genetic approach. High genetic variation of the effector gene resulted from diverse mechanisms including base substitution, pre-termination, intragenic recombination and diversifying selection. Nearly 80% of the 111 sequences had a point mutation in the 512th nucleotide (T512G), which generated a pre-termination stop codon truncating 38 amino acids in the C-terminal, suggesting that the C-terminal may not be essential to ecological and biological functions of <i>P. infestans.</i> A significant correlation between the frequency of <i>Avr1</i> sequences with the pre-termination and annual mean temperature in the collection sites suggests that thermal heterogeneity might be one of contributors to the diversifying selection, although biological and biochemical mechanisms of the likely thermal adaptation are not known currently. Our results highlight the risk of rapid adaptation of <i>P. infestans</i> and possibly other pathogens as well to host resistance, and the application of eco-evolutionary principles is necessary for sustainable disease management in agricultural ecosystems.https://www.mdpi.com/2309-608X/7/10/789effector proteinmutation mechanismspopulation geneticsnatural selectionoomycete pathogenintragenic recombination |
| spellingShingle | Lin-Lin Shen Abdul Waheed Yan-Ping Wang Oswald Nkurikiyimfura Zong-Hua Wang Li-Na Yang Jiasui Zhan Multiple Mechanisms Drive the Evolutionary Adaptation of <i>Phytophthora infestans</i> Effector Avr1 to Host Resistance Journal of Fungi effector protein mutation mechanisms population genetics natural selection oomycete pathogen intragenic recombination |
| title | Multiple Mechanisms Drive the Evolutionary Adaptation of <i>Phytophthora infestans</i> Effector Avr1 to Host Resistance |
| title_full | Multiple Mechanisms Drive the Evolutionary Adaptation of <i>Phytophthora infestans</i> Effector Avr1 to Host Resistance |
| title_fullStr | Multiple Mechanisms Drive the Evolutionary Adaptation of <i>Phytophthora infestans</i> Effector Avr1 to Host Resistance |
| title_full_unstemmed | Multiple Mechanisms Drive the Evolutionary Adaptation of <i>Phytophthora infestans</i> Effector Avr1 to Host Resistance |
| title_short | Multiple Mechanisms Drive the Evolutionary Adaptation of <i>Phytophthora infestans</i> Effector Avr1 to Host Resistance |
| title_sort | multiple mechanisms drive the evolutionary adaptation of i phytophthora infestans i effector avr1 to host resistance |
| topic | effector protein mutation mechanisms population genetics natural selection oomycete pathogen intragenic recombination |
| url | https://www.mdpi.com/2309-608X/7/10/789 |
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