The evolution of the Gp‐Rbp‐1 gene in Globodera pallida includes multiple selective replacements

Abstract

The Globodera pallida SPRYSEC Gp-Rbp-1 gene encodes a secreted protein which induces effector-triggered immunity (ETI) mediated by the Solanum tuberosum disease resistance gene Gpa2. Nonetheless, it is not known how the Andes orogeny, the richness in Solanum species found along the Cordillera or the introduction of the nematode into Europe have affected the diversity of Gp-Rbp-1 and its recognition by Gpa2. We generated a dataset of 157 highly polymorphic Gp-Rbp-1 sequences and identified three Gp-Rbp-1 evolutionary pathways: the ‘Northern Peru’, ‘Peru clade I/European’ and ‘Chilean’ paths. These may have been shaped by passive dispersion of the nematode and by climatic variations that have influenced the nature and diversity of wild host species. We also confirmed that, by an analysis of the selection pressures acting on Gp-Rbp-1, this gene has evolved under positive/diversifying selection, but differently among the three evolutionary pathways described. Using this extended sequence dataset, we were able to detect eight sites under positive selection. Six sites appear to be of particular interest because of their predicted localization to the extended loops of the B30.2 domain and/or support by several computational methods. The P/S 187 position was previously identified for its effect on the interaction with GPA2. The functional importance of the other five amino acid polymorphisms observed was investigated using Agrobacterium transient transformation assays. None of these new residues, however, appears to be directly involved in Gpa2-mediated plant defence mechanisms. Thus, the P/S polymorphism observed at position 187 remains the sole variation sufficient to explain the recognition of Gp-Rbp-1 by Gpa2.

Evolution and variability of Solanum RanGAP2, a cofactor in the incompatible interaction between the resistance protein GPA2 and the Globodera pallida effector Gp-RBP-1

“…RanGAP2 shows less sequence size variations and a lower polymorphism rate (31.4% vs 19%) than Gp-Rbp-1 [20], the gene encoding for the effector recognized by GPA2. Furthermore RanGAP2 also appears to be less variable than the housekeeping gene nitrate reductase, whose variability was evaluated in various Solanum species [28].…”

“…Compared to Rx, Gpa2 induces a much weaker hypersensitive response (HR) when transiently expressed with its effector counterpart (the avirulence protein Gp-RBP-1 of G. pallida ) in tobacco [19]. Unexpectedly, numerous variants of the G. pallida avirulence protein GP-RBP-1 are recognized by GPA2, even those from nematode populations described as virulent against S. tuberosum cultivars expressing Gpa2 [20]. Thus, other proteins involved in the recognition of GP-RBP-1 by GPA2 may explain these results and RanGAP2 has been thought to mediate recognition of the avirulence protein GP-RBP-1 by GPA2.…”

“…The genetic diversity of the genes encoding both the avirulence proteins (PVX CP and Gp-RBP-1) and the resistance proteins (Rx and GPA2) has been well characterized. A high frequency of polymorphic sites in the four genes has been identified, including key residues necessary for recognition of the CP and GP-RBP-1 by Rx and GPA2, respectively [19,20,23,24]. On the other hand, the genetic diversity or sequence polymorphism of the co-factor RanGAP2 has not yet been reported.…”

Resistance genes against plant-parasitic nematodes: a durable control strategy?

“…The study revealed that eight sites are under positive selection in Gp-RBP-1, six of which were predicted to localise to the SPRY domain, including the P/S polymorphism at position 187 known to be required for recognition by Gpa2. The five novel sites in the SPRY domain were not involved in Gpa recognition but are hypothesised potentially to interact with other plant host proteins (Carpentier et al, 2012). Hallmarks of positive selection have been demonstrated in effector genes of the oomycete Phytophthora and implicated in host adaptation (Raffaele et al, 2010).…”

“…The SPRY domain was shown to be involved in the recognition of Gp-RBP-1 by Gpa2, as the polymorphism correlating to Avr gene recognition was localised to a single amino acid in the Gp-RBP-1 SPRY domain (Sacco et al, 2009). In another study, the diversity and evolution of Gp-RBP-1 was investigated using a dataset of 157 highly polymorphic Gp-RBP-1 sequences obtained from numerous G. pallida populations collected in Peru and Chile (Carpentier et al, 2012). The study revealed that eight sites are under positive selection in Gp-RBP-1, six of which were predicted to localise to the SPRY domain, including the P/S polymorphism at position 187 known to be required for recognition by Gpa2.…”