Apple scar skin viroid causes dapple and scar skin apple diseases by disrupting phenylpropanoid-mediated metabolic pathways

Abstract

Apple scar skin viroid (ASSVd) causes dapple and scar skin apple diseases, posing serious threats to apple production. The molecular mechanisms underlying disease induction remain poorly understood, primarily due to the long period required for apple trees to exhibit fruit symptoms. Here, we found that the two fruit disorders are associated with alterations in phenylpropanoid metabolic pathways. Transcriptomic analyses revealed that anthocyanin biosynthesis pathway was downregulated in dapple apples, whereas suberin biosynthesis pathway was upregulated in scar skin apples, aligning with the development of dapple and scar skin symptoms. Both pathways act as parallel branches of the core phenylpropanoid pathway, suggesting that ASSVd interferes with upstream metabolic steps. Infection experiments using the established apple callus system revealed that ASSVd infection inhibited the development of red pigment in the callus and suppressed key structural genes in the anthocyanin biosynthesis pathway. Moreover, no specific ASSVd variant was detected in apple fruit skins exhibiting dapple symptoms. It seems unlikely that the expression of regulatory genes in the anthocyanin biosynthesis pathway is inhibited via RNA silencing. Collectively, these findings deepen the understanding of the pathogenesis of dapple and scar skin apple diseases and provide a suitable infection system for studying ASSVd and apple interactions.

Keywords

apple / metabolic pathway / phenylpropanoid / transcriptome / viroid

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