The Lesson Learned from the Unique Evolutionary Story of Avirulence Gene AvrPii of Magnaporthe oryzae

Xing Wang; Weihuai Wu; Yaling Zhang; Cheng Li; Jinyan Wang; Jianqiang Wen; Shulin Zhang; Yongxiang Yao; Weisheng Lu; Zhenghong Zhao; Jiasui Zhan; Qinghua Pan

doi:10.3390/genes14051065

The Lesson Learned from the Unique Evolutionary Story of Avirulence Gene AvrPii of Magnaporthe oryzae

Genes (Basel). 2023 May 11;14(5):1065. doi: 10.3390/genes14051065.

Authors

Xing Wang¹, Weihuai Wu^{1

2}, Yaling Zhang^{1

3}, Cheng Li¹, Jinyan Wang¹, Jianqiang Wen¹, Shulin Zhang^{1

4}, Yongxiang Yao^{1

5}, Weisheng Lu¹, Zhenghong Zhao⁶, Jiasui Zhan⁷, Qinghua Pan¹

Affiliations

¹ Rice Blast Research Center, South China Agricultural University, Guangzhou 510642, China.
² Hainan Key Laboratory for Monitoring and Control of Tropical Agricultural Pests, Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China.
³ College of Agronomy, Heilongjiang Bayi Agricultural University, Daqing 163319, China.
⁴ Department of Plant Pathology, College of Plant Protection, Anhui Agricultural University, Hefei 230036, China.
⁵ Corn Research Institute, Dandong Academy of Agricultural Sciences, Dandong 118109, China.
⁶ State Key Laboratory of Hybrid Rice, Rice Research Institute, Hunan Academy of Agricultural Sciences, Changsha 410125, China.
⁷ Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden.

Abstract

Blast, caused by Magnaporthe oryzae, is one of the most destructive diseases affecting rice production. Understanding population dynamics of the pathogen's avirulence genes is pre-required for breeding and then deploying new cultivars carrying promising resistance genes. The divergence and population structure of AvrPii was dissected in the populations of southern (Guangdong, Hunan, and Guizhou) and northern (Jilin, Liaoning, and Heilongjiang) China, via population genetic and evolutionary approaches. The evolutionary divergence between a known haplotype AvrPii-J and a novel one AvrPii-C was demonstrated by haplotype-specific amplicon-based sequencing and genetic transformation. The different avirulent performances of a set of seven haplotype-chimeric mutants suggested that the integrity of the full-length gene structures is crucial to express functionality of individual haplotypes. All the four combinations of phenotypes/genotypes were detected in the three southern populations, and only two in the northern three, suggesting that genic diversity in the southern region was higher than those in the northern one. The population structure of the AvrPii family was shaped by balancing, purifying, and positive selection pressures in the Chinese populations. The AvrPii-J was recognized as the wild type that emerged before rice domestication. Considering higher frequencies of avirulent isolates were detected in Hunan, Guizhou, and Liaoning, the cognate resistance gene Pii could be continuously used as a basic and critical resistance resource in such regions. The unique population structures of the AvrPii family found in China have significant implications for understanding how the AvrPii family has kept an artful balance and purity among its members (haplotypes) those keenly interact with Pii under gene-for-gene relationships. The lesson learned from case studies on the AvrPii family is that much attention should be paid to haplotype divergence of target gene.

Keywords: Magnaporthe oryzae; avirulence gene; divergence; haplotype; population structure.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Biological Evolution
Genetic Variation* / genetics
Magnaporthe* / genetics
Plant Breeding

Supplementary concepts

Pyricularia oryzae

Grants and funding

The project was supported by the Key Areas Research and Development Programs of Guangdong Province, China (2022B0202060005), the National Natural Science Foundation (31870137), and the Ministry of Science and Technology, China (2015ZX08001-002, 2016YDF0100601).