Specific selection on XEG1 and XLP1 genes correlates with host range and adaptability in Phytophthora

In diverse Phytophthora-plant pathosystems, Phytophthora secretes XLP1 (PsXEG1-Like Protein), a non-enzymatic paralog that functions as a decoy to protect XEG1 (Xyloglucan-specific Endoglucanase) from host inhibitors. Here, we show that the genus-specific selection pressures on the XEG1/XLP1 gene pair are crucial for host adaptation and are closely linked to Phytophthora host range. Our findings reveal that the XEG1/XLP1 gene pair originated within Phytophthora and subsequently evolved into genus-specific genes, undergoing functional divergence driven by preferential selection. Positive selection sites within the XEG1/XLP1 gene pair in Phytophthora contribute to this functional divergence and are associated with the host range variability of Phytophthora as evidenced by multivariate statistical analyses. Furthermore, mutations at key selection sites in Phytophthora sojae and Phytophthora capsici significantly impair their pathogenicity, with P. capsici exhibiting almost no colonization expansion on tobacco and pea. Notably, natural Phytophthora populations harbor mutations at the positive selection sites, indicating ongoing evolutionary pressures on the XEG1/XLP1 gene pair.