ABSTRACTPeas carrying thecyv1recessive resistance gene are resistant to clover yellow vein virus (ClYVV) isolates No.30 (Cl-No.30) and 90-1 (Cl-90-1) but can be infected by a derivative of Cl-90-1 (Cl-90-1 Br2). The main determinant for the breaking ofcyv1resistance by Cl-90-1 Br2 is P3N-PIPO produced from theP3gene via transcriptional slippage, and the higher level of P3N-PIPO produced by Cl-90-1 Br2 than by Cl-No.30 contributes to the breaking of resistance. Here we show that P3N-PIPO is also a major virulence determinant in susceptible peas that possess another resistance gene,Cyn1, which does not inhibit systemic infection with ClYVV but causes hypersensitive reaction-like lethal systemic cell death. We previously assumed that the susceptible pea cultivar PI 226564 has a weak allele ofCyn1. Cl-No.30 did not induce cell death, but Cl-90-1 Br2 killed the plants. Our results suggest that P3N-PIPO is recognized byCyn1and induces cell death. Unexpectedly, heterologously strongly expressed P3N-PIPO of Cl-No.30 appears to be recognized byCyn1in PI 226564. The level of P3N-PIPO accumulation from theP3gene of Cl-No.30 was significantly lower than that of Cl-90-1 Br2 in aNicotiana benthamianatransient assay. Therefore,Cyn1-mediated cell death also appears to be determined by the level of P3N-PIPO. The more efficiently a ClYVV isolate brokecyv1resistance, the more it induced cell death systemically (resulting in a loss of the environment for virus accumulation) in susceptible peas carryingCyn1, suggesting that antagonistic pleiotropy of P3N-PIPO controls the resistance breaking of ClYVV.IMPORTANCEControl of plant viral disease has relied on the use of resistant cultivars; however, emerging mutant viruses have broken many types of resistance. Recently, we revealed that Cl-90-1 Br2 breaks the recessive resistance conferred bycyv1, mainly by accumulating a higher level of P3N-PIPO than that of the nonbreaking isolate Cl-No.30. Here we show that a susceptible pea line recognized the increased amount of P3N-PIPO produced by Cl-90-1 Br2 and activated the salicylic acid-mediated defense pathway, inducing lethal systemic cell death. We found a gradation of virulence among ClYVV isolates in acyv1-carrying pea line and two susceptible pea lines. This study suggests a trade-off between breaking of recessive resistance (cyv1) and host viability; the latter is presumably regulated by the dominantCyn1gene, which may impose evolutionary constraints uponP3N-PIPOfor overcoming resistance. We propose a working model of the host strategy to sustain the durability of resistance and control fast-evolving viruses.
The central and C-terminal domains of VPg of Clover yellow vein virus are important for VPg–HCPro and VPg–VPg interactions
