Population Genetics Suggests That the Resurgence of Pine Blister Rust Caused by Cronartium pini in the Landes Forest of France Was Triggered by the Recent Cultivation of Alternate Hosts

Abstract

Two-needle pine blister rust is caused by Cronartium pini, a fungus that can have one of two forms. One requires an alternate host plant to achieve sexual reproduction and thus complete its life cycle (heteroecious), while the other is able to maintain itself clonally on pines (autoecious). Pine blister rust is widely distributed across Eurasia and may cause significant damage in infected natural forests and plantations. In France, the fungus may cause sporadic, local damage to plantations under certain environmental conditions, such as the presence of wild alternate hosts and particular weather conditions. A recent outbreak of this disease was observed on young pine stands in the Landes forest in South-West France, with prevalence levels reaching up to 80% in some stands. This outbreak emerged contemporaneously with the planting of a large peony field in the middle of young pine plantations. Peonies being one of the many alternate hosts for C. pini, this work aimed to investigate whether the latter was present in its alternating or non-alternating form and to study the relationship between the fungal populations attacking both pine trees and peonies. A total of 522 samples of aecia on pines and 108 samples of uredia on peonies were genotyped in 2021 and 2022 by studying seven microsatellite loci. The results showed that the heteroecious form of C. pini largely predominated in both the populations of the two sites sampled in the Landes forest and at the two more distant sites. In addition, the populations sampled from peonies did not differ genetically from those sampled in the pine plots surrounding them, which suggests that peonies participate in the completion of the biological cycle of C. pini on these sites. On the other hand, the populations in the Landes differ from the populations at the more distant sites in France. This study demonstrates that the establishment of natural hosts in the form of peony crops in the middle of pine plantations allowed the fungus inoculum to multiply in its heteroecious form, to increase the disease pressure and, consequently, the severity of damage to pine saplings. The complete removal of peony plots in late 2023 should help reduce the intensity of the disease in the years to come.