First Report of the Armillaria Root Disease Pathogen, Armillaria solidipes, on Black Oak (Quercus velutina) in North Carolina, USA.

Armillaria root disease is among the largest causes of mortality and lost productivity of widely ranging horticultural, urban, and forest trees/shrubs in diverse boreal, temperate, and tropical regions around the world (Kim et al. 2022). Damage from Armillaria root disease will likely increase in response to changing climate and extreme weather because environmental stress can predispose host trees to Armillaria root disease (Murray and Leslie 2021; Kim et al. 2021). On August 14, 2021, a mature black oak (Quercus velutina) ca. 29 m in height and 64 cm DBH experienced a complete structural failure originating at the root plate, falling onto a major highway within the Pisgah National Forest near Brevard, North Carolina (35°16'50.876"N, 82°42'51.785"W, elevation 680 m) during sunny, calm conditions. No above-ground indications of predisposing disturbance, injury, or insect/disease activity were observed. Advanced wood decay, however, was present in many structural roots of the exposed root plate; abundant rhizomorphs attached to the surfaces of most roots were noted (Supplemental Figure 1). One large primary root (ca. 23 cm in diameter) exhibited clear signs of Armillaria root disease at the point of failure as evidenced by an extensive decay column, abundant black rhizomorphs on the root surface, and white mycelial fans (a sign of pathogenicity) within the root itself (Supplemental Figure 1). Rhizomorph samples were established in culture, two Armillaria isolates (PNF#001R-1 and PNF#001R-2) were examined, and pairing tests showed that both isolates belonged to the same genet (PNF#001R-1 = PNF#001R-2). Based on translation elongation factor 1α (tef1) sequences, both isolates (one genet) were identified as A. solidipes (GenBank accession no. OP823701), showing 98% similarity with A. solidipes tef1 sequences (e.g., MH879015) in GenBank. Also, nine replications of somatic incompatibility tests of the isolate with five North American Armillaria spp. [A. solidipes, A. mellea, A. gallica, A. mexicana, and Desarmillaria caespitosa (= North American A. tabescens)] showed 67% compatibility with A. solidipes, compared with 0-22% for A. mellea, D. caespitosa, A. gallica, and A. mexicana. All test species but A. mexicana are reported to occur in the eastern and/or southern USA, while A. mexicana occurs in a similar environment in Mexico (Elías-Román et al. 2018). To our knowledge, this is the first confirmed report of A. solidipes in North Carolina, USA, where it was causing disease on black oak, and this is the most southerly confirmed case of A. solidipes in eastern North America. Although Armillaria inoculation tests are impractical, black oak was previously reported as a host of A. solidipes in Massachusetts, USA (Brazee and Wick 2009). Armillaria solidipes is considered as the most important Armillaria root disease pathogen of conifer forests in western USA (Lockman and Kearns 2016), but it has been suggested that A. solidipes can thrive in northern hardwood forests that reside near conifer forests (Brazee and Wick 2009). Climate change is predicted to increase damage caused by A. solidipes on conifers in the western USA (Kim et al. 2021); however, it is undetermined if the occurrence of A. solidipes-caused disease in North Carolina is related to climate change or how climate change could influence this disease across the region. More surveys are needed to assess the impact of Armillaria root disease on health of mixed forests in the eastern USA.