Whole Genome Re-sequencing Reveals Natural Variation and Adaptive Evolution of Phytophthora sojae.

Xiong Zhang,Yuanchao Wang,Daolong Dou,Rongbo Wang,Wei Fan,Wanqiang Qian,Feng He,Danyu Shen,Brett M Tyler,Zhiyuan Yin,Fen Zou,Bo Liu

doi:10.3389/fmicb.2019.02792

Abstract

Due to the monocultural basis of agricultural crops, mutated plant microbes with increased pathogenicity can easily spread in the field and lead to serious yield losses. As a major threat to a wide range of crop plants, oomycete pathogens continuously undergo adaptive evolution to overcome plant defense barriers. However, the genetic basis of their evolution at the molecular level remains largely unknown. Here, we investigated the nature variation and the population genomics of the soybean pathogen Phytophthora sojae by high-throughput genome re-sequencing. Genomic variation analysis revealed uneven “two-speed” evolutionary pattern with genes in gene-sparse regions (GSRs) showing higher rates of structural polymorphisms and positive selection. GSRs are enriched in effector genes and transposase-related genes. Our results also suggested that the NADH oxidase and MIP transporter gene families undergo rapid and diversifying selection. Furthermore, we demonstrated that P. sojae isolates possess varying numbers of RxLR effectors with diverse sequences, totaling 471 members. Among them, 42 core RxLR effectors are assumed to be important for infection. Finally, we observed that Avr genes exhibit abundant sequence variation in P. sojae isolates. Several novel variants lead to the evading of host resistance, including a complete deletion in Avr3c and amino acid mutations in Avr1a. Taken together, our results provide an adaptive landscape of P. sojae at single-nucleotide resolution, as well as resources for further resistance breeding and disease prevention against this important plant pathogen.

Highlights

Oomycetes are fungal-like eukaryotic organisms classified into the Stramenopila kingdom, which includes multiple plant- and animal-infecting pathogens (Fawke et al, 2015)
Little is known about the genetic basis of adaptive evolution, especially pathogen adaptation, in Phytophthora
Previous studies indicate that several Phytophthora genomes contain a typical “two-speed” architecture, with gene-sparse regions (GSRs) being more plastic than gene dense regions (GDRs) and serving as a cradle for adaptive evolution (Raffaele and Kamoun, 2012; Dong et al, 2015)

Summary

Introduction

Oomycetes are fungal-like eukaryotic organisms classified into the Stramenopila kingdom, which includes multiple plant- and animal-infecting pathogens (Fawke et al, 2015). Oomycetes cause devastating diseases on a wide range of crop plants and result in severe yield loss (Jiang and Tyler, 2012). The most notorious plant-infecting oomycete pathogens belong to the genus Phytophthora, which includes over 100 species (Hansen et al, 2012). Population Genomics of Phytophthora sojae (Glycine max), Phytophthora sojae is one of the most economically important Phytophthora pathogens (Tyler et al, 2006). As the second most destructive pathogen and a major yield-limiting factor for soybean, P. sojae can cause up to 100% yield loss in individual fields, resulting in around $2 billion of annual loss worldwide (Tyler, 2007). Despite the importance of P. sojae in soybean disease control, the molecular details of its pathogenesis and population genomics remain elusive

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Conclusion