Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans

Abstract

Phytophthora infestans is the most destructive pathogen of potato and a model organism for the oomycetes, a distinct lineage of fungus-like eukaryotes that are related to organisms such as brown algae and diatoms. As the agent of the Irish potato famine in the mid-nineteenth century, P. infestans has had a tremendous effect on human history, resulting in famine and population displacement. To this day, it affects world agriculture by causing the most destructive disease of potato, the fourth largest food crop and a critical alternative to the major cereal crops for feeding the world's population. Current annual worldwide potato crop losses due to late blight are conservatively estimated at $6.7 billion. Management of this devastating pathogen is challenged by its remarkable speed of adaptation to control strategies such as genetically resistant cultivars. Here we report the sequence of the P. infestans genome, which at approximately 240 megabases (Mb) is by far the largest and most complex genome sequenced so far in the chromalveolates. Its expansion results from a proliferation of repetitive DNA accounting for approximately 74% of the genome. Comparison with two other Phytophthora genomes showed rapid turnover and extensive expansion of specific families of secreted disease effector proteins, including many genes that are induced during infection or are predicted to have activities that alter host physiology. These fast-evolving effector genes are localized to highly dynamic and expanded regions of the P. infestans genome. This probably plays a crucial part in the rapid adaptability of the pathogen to host plants and underpins its evolutionary potential.

Evidence for intragenic recombination and selective sweep in an effector gene of Phytophthora infestans

“…Although nucleotide substitution was the main mechanism, other types of mutations account for ~15% of haplotype variation observed. Avr3a proteins secreted from P. infestans during infection trigger defense responses in hosts carrying corresponding resistance genes (Lo Presti et al., 2015) and are also important for the pathogenicity of plant pathogens by increasing host susceptibility or suppressing host immunity (Bos et al., 2010; Haas et al., 2009; Vetukuri et al., 2011). Although increasing the invasive opportunity of P. infestans due to the prevention of its recognition by potato hosts carrying with R3a gene, high mutation rates in Avr3a particular through pseudogenization also abruptly disrupt the normal biochemical functions of the gene.…”

“…Effector genes commonly lie in gene‐sparse, transposon‐rich regions of the pathogen genome (Haas et al., 2009; Raffaele & Kamoun, 2012). This physical location provides effector genes a unique opportunity to generate sequence duplication.…”

“…Molecular genomic analyses confirm that P. infestans secretes a wide range of effector proteins into extracellular space (apoplastic effectors) or cell cytoplasm (cytoplasmic effectors). The pathogen genome contains at least 550 effectors all earmarked with a conserved N‐terminal motif of Arginine–X–Leucine–Arginine (RXLR), where X can be one of any 20 amino acids (Haas et al., 2009). However, this RXLR effector repertoire is likely expanding, contributing to the enormous size of the P. infestans genome (Haas et al., 2009; Raffaele & Kamoun, 2012).…”

“…The pathogen genome contains at least 550 effectors all earmarked with a conserved N‐terminal motif of Arginine–X–Leucine–Arginine (RXLR), where X can be one of any 20 amino acids (Haas et al., 2009). However, this RXLR effector repertoire is likely expanding, contributing to the enormous size of the P. infestans genome (Haas et al., 2009; Raffaele & Kamoun, 2012). Biochemical and virulent functions of some RXLR effectors in P. infestans have been characterized recently (Bozkurt et al., 2011; King et al., 2014; McLellan et al., 2013; Wang et al., 2015; Yang, McLellan, et al., 2016).…”

“…It is a RXLR effector containing conserved W, Y, and L motifs in C‐terminal domains. These conserved motifs are believed to be generated by purifying selection imposed by the plant host over the course of the co‐evolutionary history of host and pathogen (Dou et al., 2008; Haas et al., 2009; Jiang & Tyler, 2008). The effector gene is also essential to pathogen infection.…”