Copy Number Variation and Transcriptional Polymorphisms of Phytophthora sojae RXLR Effector Genes Avr1a and Avr3a

Abstract

The importance of segmental duplications and copy number variants as a source of genetic and phenotypic variation is gaining greater appreciation, in a variety of organisms. Now, we have identified the Phytophthora sojae avirulence genes Avr1a and Avr3a and demonstrate how each of these Avr genes display copy number variation in different strains of P. sojae. The Avr1a locus is a tandem array of four near-identical copies of a 5.2 kb DNA segment. Two copies encoding Avr1a are deleted in some P. sojae strains, causing changes in virulence. In other P. sojae strains, differences in transcription of Avr1a result in gain of virulence. For Avr3a, there are four copies or one copy of this gene, depending on the P. sojae strain. In P. sojae strains with multiple copies of Avr3a, this gene occurs within a 10.8 kb segmental duplication that includes four other genes. Transcriptional differences of the Avr3a gene among P. sojae strains cause changes in virulence. To determine the extent of duplication within the superfamily of secreted proteins that includes Avr1a and Avr3a, predicted RXLR effector genes from the P. sojae and the P. ramorum genomes were compared by counting trace file matches from whole genome shotgun sequences. The results indicate that multiple, near-identical copies of RXLR effector genes are prevalent in oomycete genomes. We propose that multiple copies of particular RXLR effectors may contribute to pathogen fitness. However, recognition of these effectors by plant immune systems results in selection for pathogen strains with deleted or transcriptionally silenced gene copies.

Oomycete Interactions with Plants: Infection Strategies and Resistance Principles

“…Several oomycete effectors have been shown to contribute to pathogen virulence. Variations in the copy numbers of P. sojae AvrI and Avr3a (94), as well as knockdown of transcript levels of Avr3a (49), PsAvh172, PsAvh238 (95), PsAvr3b (96), PsCRN63, and PsCRN115 (97), have negative impacts on virulence.…”

Transcriptional Programming and Functional Interactions within the Phytophthora sojae RXLR Effector Repertoire

“…Thus, presence of the RXLR-dEER motifs in the Avh proteins makes them all candidate effectors. The importance of the Avh proteins is underlined by the finding that 10 recently cloned oomycete Avr genes all encode RXLR-dEER proteins, including Avr1a, Avr3a, Avr3c, and Avr4/6 from P. sojae (Shan et al, 2004;Dong et al, 2009;Qutob et al, 2009;Dou et al, 2010), Avr2, Avr4, Avr-blb1, and Avr-blb2 from P. infestans van Poppel et al, 2008;Vleeshouwers et al, 2008;Oh et al, 2009), and ATR1 and ATR13 from H. arabidopsidis (Allen et al, 2004;Rehmany et al, 2005). Due to selection pressure from the hosts, the avirulence genes show extensive variations, including amino acid changes indicative of strong positive selection, gene truncations and deletions, and transcriptional silencing (Jiang et al, 2008;Qutob et al, 2009).…”

R/Avr gene expression study of Rpi-vnt1.1 transgenic potato resistant to the Phytophthora infestans clonal lineage EC-1

“…Across all these studies, including ours, Avrvnt1 gene expression has been very low in the virulent isolates and no clear evidence exists yet as to whether its detection in potato plants without the Rpi-vnt1.1 or Rpiphu1 genes reflect a real change in expression. Oomycete pathogens can evade recognition by silencing Avr gene which could be the explanation of the EC-1 virulence (Qutob et al 2009(Qutob et al , 2013Vetukuri et al 2013;Na et al 2014). Sub-clonal variation in virulence is typical for P. infestans such that isolates belonging to the same clonal lineage have different virulence patterns.…”

“…Gain of virulence resulting from Avr gene transcript differences has been described for the Avr2 and Avr-vnt1 genes in P. infestans (Gilroy et al 2011;Pel 2010). Gene silencing of effector genes to gain virulence is found in other oomycete pathogens such as Phytophthora sojae (Qutob et al 2009(Qutob et al , 2013Vetukuri et al 2013;Na et al 2014).…”