Effector Avr4 in Phytophthora infestans Escapes Host Immunity Mainly Through Early Termination
Effector genes play critical roles in the antagonistic interactions between plants and pathogens. However, knowledge of mutation mechanisms and evolutionary processes in effector genes and the contribution of climatic factors to the evolution of effector genes are fragmented but important in sustain...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2021-05-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.646062/full |
| _version_ | 1818730219362582528 |
|---|---|
| author | Abdul Waheed Yan-Ping Wang Oswald Nkurikiyimfura Wen-Yang Li Shi-Ting Liu Yahuza Lurwanu Yahuza Lurwanu Guo-Dong Lu Guo-Dong Lu Zong-Hua Wang Zong-Hua Wang Li-Na Yang Li-Na Yang Jiasui Zhan |
| author_facet | Abdul Waheed Yan-Ping Wang Oswald Nkurikiyimfura Wen-Yang Li Shi-Ting Liu Yahuza Lurwanu Yahuza Lurwanu Guo-Dong Lu Guo-Dong Lu Zong-Hua Wang Zong-Hua Wang Li-Na Yang Li-Na Yang Jiasui Zhan |
| author_sort | Abdul Waheed |
| collection | DOAJ |
| description | Effector genes play critical roles in the antagonistic interactions between plants and pathogens. However, knowledge of mutation mechanisms and evolutionary processes in effector genes and the contribution of climatic factors to the evolution of effector genes are fragmented but important in sustainable management of plant diseases and securing food supply under changing climates. Here, we used a population genetic approach to explore the evolution of the Avr4 gene in Phytophthora infestans, the causal agent of potato blight. We found that the Avr4 gene exhibited a high genetic diversity generated by point mutation and sequence deletion. Frameshifts caused by a single base-pair deletion at the 194th nucleotide position generate two stop codons, truncating almost the entire C-terminal, which is important for effector function and R4 recognition in all sequences. The effector is under natural selection for adaptation supported by comparative analyses of population differentiation (FST) and isolation-by-distance between Avr4 sequences and simple sequence repeat marker loci. Furthermore, we found that local air temperature was positively associated with pairwise FST in the Avr4 sequences. These results suggest that the evolution of the effector gene is influenced by local air temperature, and the C-terminal truncation is one of the main mutation mechanisms in the P. infestans effector gene to circumvent the immune response of potato plants. The implication of these results to agricultural and natural sustainability in future climate conditions is discussed. |
| first_indexed | 2024-12-17T22:58:18Z |
| format | Article |
| id | doaj.art-ce4ed6f113344a0998e5c5d2986375a0 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-17T22:58:18Z |
| publishDate | 2021-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-ce4ed6f113344a0998e5c5d2986375a02022-12-21T21:29:29ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-05-011210.3389/fmicb.2021.646062646062Effector Avr4 in Phytophthora infestans Escapes Host Immunity Mainly Through Early TerminationAbdul Waheed0Yan-Ping Wang1Oswald Nkurikiyimfura2Wen-Yang Li3Shi-Ting Liu4Yahuza Lurwanu5Yahuza Lurwanu6Guo-Dong Lu7Guo-Dong Lu8Zong-Hua Wang9Zong-Hua Wang10Li-Na Yang11Li-Na Yang12Jiasui Zhan13Key Lab for Bio Pesticide and Chemical Biology, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, ChinaKey Lab for Bio Pesticide and Chemical Biology, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, ChinaKey Lab for Bio Pesticide and Chemical Biology, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, ChinaKey Lab for Bio Pesticide and Chemical Biology, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, ChinaKey Lab for Bio Pesticide and Chemical Biology, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, ChinaKey Lab for Bio Pesticide and Chemical Biology, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, ChinaDepartment of Crop Protection, Bayero University Kano, Kano, NigeriaKey Lab for Bio Pesticide and Chemical Biology, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, ChinaKey Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, ChinaKey Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, ChinaInstitute of Oceanography, Minjiang University, Fuzhou, ChinaKey Lab for Bio Pesticide and Chemical Biology, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, ChinaInstitute of Oceanography, Minjiang University, Fuzhou, ChinaDepartment of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Uppsala, SwedenEffector genes play critical roles in the antagonistic interactions between plants and pathogens. However, knowledge of mutation mechanisms and evolutionary processes in effector genes and the contribution of climatic factors to the evolution of effector genes are fragmented but important in sustainable management of plant diseases and securing food supply under changing climates. Here, we used a population genetic approach to explore the evolution of the Avr4 gene in Phytophthora infestans, the causal agent of potato blight. We found that the Avr4 gene exhibited a high genetic diversity generated by point mutation and sequence deletion. Frameshifts caused by a single base-pair deletion at the 194th nucleotide position generate two stop codons, truncating almost the entire C-terminal, which is important for effector function and R4 recognition in all sequences. The effector is under natural selection for adaptation supported by comparative analyses of population differentiation (FST) and isolation-by-distance between Avr4 sequences and simple sequence repeat marker loci. Furthermore, we found that local air temperature was positively associated with pairwise FST in the Avr4 sequences. These results suggest that the evolution of the effector gene is influenced by local air temperature, and the C-terminal truncation is one of the main mutation mechanisms in the P. infestans effector gene to circumvent the immune response of potato plants. The implication of these results to agricultural and natural sustainability in future climate conditions is discussed.https://www.frontiersin.org/articles/10.3389/fmicb.2021.646062/fullPhytophthora infestanseffector genemutation mechanismpopulation genomicsprotein truncationthermal adaptation |
| spellingShingle | Abdul Waheed Yan-Ping Wang Oswald Nkurikiyimfura Wen-Yang Li Shi-Ting Liu Yahuza Lurwanu Yahuza Lurwanu Guo-Dong Lu Guo-Dong Lu Zong-Hua Wang Zong-Hua Wang Li-Na Yang Li-Na Yang Jiasui Zhan Effector Avr4 in Phytophthora infestans Escapes Host Immunity Mainly Through Early Termination Frontiers in Microbiology Phytophthora infestans effector gene mutation mechanism population genomics protein truncation thermal adaptation |
| title | Effector Avr4 in Phytophthora infestans Escapes Host Immunity Mainly Through Early Termination |
| title_full | Effector Avr4 in Phytophthora infestans Escapes Host Immunity Mainly Through Early Termination |
| title_fullStr | Effector Avr4 in Phytophthora infestans Escapes Host Immunity Mainly Through Early Termination |
| title_full_unstemmed | Effector Avr4 in Phytophthora infestans Escapes Host Immunity Mainly Through Early Termination |
| title_short | Effector Avr4 in Phytophthora infestans Escapes Host Immunity Mainly Through Early Termination |
| title_sort | effector avr4 in phytophthora infestans escapes host immunity mainly through early termination |
| topic | Phytophthora infestans effector gene mutation mechanism population genomics protein truncation thermal adaptation |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.646062/full |
| work_keys_str_mv | AT abdulwaheed effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT yanpingwang effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT oswaldnkurikiyimfura effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT wenyangli effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT shitingliu effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT yahuzalurwanu effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT yahuzalurwanu effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT guodonglu effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT guodonglu effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT zonghuawang effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT zonghuawang effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT linayang effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT linayang effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination AT jiasuizhan effectoravr4inphytophthorainfestansescapeshostimmunitymainlythroughearlytermination |