Armillaria root rot (ARR) caused by Desarmillaria caespitosa and Armillaria mellea represents the main cause of premature stone fruit and nut tree decline in the United States. A. mellea is a primary concern for almond and peach growers in California, while D. caespitosa threatens peach production in the southeast region of the U.S. These fungi survive as facultative necrotrophs and colonize roots of several agriculturally important crops, including peach, almond, and sweet cherry. This colonization ultimately kills the woody roots and therefore host, severely limiting the tree’s lifespan and ability to provide a return on investment for the grower. Few management options are available to slow down ARR disease progression, and no management practice eliminates ARR fungi presence in an infested field. Additionally, most of the commercially available rootstocks are susceptible to infection, with only two peach/plum hybrid commercial rootstocks (Prunus umbellata × P. persica ‘MP-29’ and P. cerasifera × P. persica ‘Krymsk® 86’) showing partial resistance to ARR. The shared plum genetic background in these hybrids, paired with the lack of ARR resistance observed in peach germplasm suggests the source of resistance originated from plum. In this work, induced genetic responses in one susceptible accession, P. persica ‘Guardian®’, and two resistant accessions, P. cerasifera ’14-4’ and ‘MP-29’, when infected with D. tabescens and A. mellea were analyzed. Additionally, expression of genes encoding effectors and cell wall degrading enzymes (CWDEs) were investigated in the ARR fungi while infecting the three hosts. The results of the infection assays revealed unique responses between each of the three hosts in their progression of disease symptoms over time and in their transcriptomes while under infection by the two ARR fungi. Analysis identified key hub genes expressed by the two resistant Prunus accessions involved in the sensing and enzymatic degradation of chitin and the upregulation of GSTs, oxidoreductases, and transcription factors. Investigation of the ARR fungi transcriptomes similarly identified host-dependent expression of fungal effectors and CWDEs responsible for degrading the cell wall components cellulose, hemicellulose and pectin. Comprehensive analyses considering transcriptomes produced by both the host and pathogen during the infection course provides a deeper understanding of the factors driving resistant and susceptible responses to ARR infection, and their effects on the infecting pathogen’s gene expression.
