First Report of Armillaria Root Disease Pathogen, Armillaria gallica, on Rhododendron and Quercus rubra in Georgia, USA.

Armillaria root and butt diseases, which are a global issue, can be influenced by changing environmental conditions. Armillaria gallica is a well-known pathogen of diverse trees worldwide (Brazee and Wick 2009). Besides A. gallica causing root rot of Hemerocallis sp. and Cornus sp. in South Carolina (Schnabel et al. 2005), little is reported on the distribution and host range of A. gallica in the southeastern USA. In July 2017, three Armillaria isolates were obtained from two naturally occurring hosts in Georgia, USA and cultured on malt extract medium (3% malt extract, 3% dextrose, 1% peptone, and 1.5% agar). One isolate (GA3) was obtained in Unicoi State Park near Helen, Georgia (Lat. 34.712275, Long. -83.727765, elev. 498 m) from the basal portion of Rhododendron sp. with extensive root/butt decay, but no crown symptoms were evident (Supplementary Figure 1). GA4 and GA5 (Lat. 33.902433, Long. -83.382453, elev. 215 m) were isolated from wind-felled Quercus rubra (red oak) with root disease at the State Botanical Gardens in Athens, Georgia. GA4 was associated with a large root ball (ca. 4-m diameter) (Supplementary Figure 2), and GA5 was obtained from a mature tree with infected roots, with characteristic spongy rot of Armillaria root disease. Crown symptoms could not be evaluated because the crowns had been removed before the collections. Several other oaks with Armillaria root disease were noted throughout the State Botanical Gardens. Pairing tests reduced these three isolates (whiteish mycelia with a dark, brownish crust and rhizomorphs), to two genets with GA4 = GA5. Both genets (GA3 and GA4) were identified as A. gallica using translation elongation factor 1α (tef1) sequences (Genbank Nos. MT761697 and MT761698, respectively) that showed ≥ 97% identity (≥ 98% coverage) with A. gallica sequences (KF156772, KF156775). Also, nine replications of somatic pairing tests showed 33 - 67% compatibility with A. gallica (occurs in southeastern USA), compared with 0 - 22% for A. mexicana, A. mellea (occurs in southeastern USA), A. solidipes, and Desarmillaria tabescens (occurs in southeastern USA). To our knowledge, this note represents the first report of A. gallica on Rhododendron and Q. rubra in Georgia, USA, which has experienced severe drought in recent decades (e.g., Park Williams et al. 2017) that could predispose trees to Armillaria infection (e.g., Wargo 1996). Quercus rubra was previously reported as a host of A. gallica in Arkansas (Kelley et al. 2009) and Massachusetts (Brazee and Wick 2009), USA. In Missouri, USA, A. gallica has been reported as a weak pathogen with potential biological control against A. mellea (Bruhn et al. 2000). Other reports from several regions on various hosts suggest pathogenicity of A. gallica is associated with changing climate (Nelson et al. 2013, Kim et al. 2017, Kubiak et al. 2017). Wide genetic variation and/or cryptic speciation within A. gallica may account for differences in ecological behavior (Klopfenstein et al. 2017), but this is difficult to evaluate because Armillaria pathogenicity tests cannot be used on most forest tree seedlings. This study suggests that A. gallica is more widespread than previously known and its adverse impacts on woody plants may intensify over time, depending on the environmental conditions. Further studies are needed to determine environmental influences on A. gallica, the full distribution of A. gallica, and its effects in forests of the southeastern USA.