A New Threat to Limber Pine (Pinus flexilis) Restoration in Alberta and Beyond: First Documentation of a Cronartium ribicola race (vcr4) Virulent to Cr4-Controlled Major Gene Resistance

The coevolution of virulence reduces the effectiveness of host resistance to pathogens, posing a direct threat to forest species and their key ecosystem functions. This exacerbates the threat to limber pine (Pinus flexilis), an endangered species in Canada due to rapid declines mainly driven by white pine blister rust (WPBR) as caused by Cronartium ribicola. We present the first report on a new C. ribicola virulent race (designated vcr4) that overcomes limber pine major gene (Cr4) resistance (MGR). Field surveys found that three parental trees (pf-503, pf-508 and pf-2015-0070) were cankered with WPBR in Alberta, but their progenies showed MGR-related phenotypic segregation post-inoculation of avirulent race (Avcr4). Genotyping of their progenies using Cr4-linked DNA markers and genome-wide association study (GWAS) provided additional support that these cankered parental trees had Cr4-controlled MGR. To confirm the presence of vcr4, aeciospores were collected from the cankered pf-503 tree to inoculate resistant seedlings that had survived prior inoculation using Avcr4 race, as well as seedlings of two US seed parents, one previously confirmed with MGR (Cr4) and one non-MGR, respectively. All inoculated seedlings showed clear stem symptoms, confirming the virulent race is vcr4. These results provide insights into evolution of C. ribicola virulence, and reinforces caution on deployment of Cr4-controlled MGR. The information will be useful for designing a breeding program for durable resistance by layering both R genes with quantitative trait loci (QTLs) for resistance to WPBR in North America.