Whole-genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Neoscytalidium dimidiatum on pitaya

Abstract

ABSTRACT Neoscytalidium dimidiatum (class Dothideomycetes ) is a fungus responsible for canker disease in pitaya stems and fruits, leading to significant economic losses. However, little is known about the pathogenesis, family evolution, and genetic variants of this species. In this study, we report a high-quality genome sequence of N. dimidiatum based on the Nanopore sequencing technology platform for sequencing and Hi-C assembly technology for genome assembly. The genome contains 12 chromosomes (2 n = 2× = 12; diploid), with a sequencing depth of 186.1×, encoding 12,349 proteins. Molecular phylogenetic analysis showed that N. dimidiatum is evolutionarily close to Botryosphaeria dothidea . Compared to other fungi, the N. dimidiatum genome contains many carbohydrate-active enzymes and secondary metabolites. Additionally, we predict that N. dimidiatum contains 121 candidate effectors that may play important roles in infection and colonization, promoting pathogenicity in pitaya. Nine of these effectors were confirmed to contain signal peptides and inhibit BAX/INF1-induced necrosis in Nicotiana benthamiana , demonstrating their importance during infection. Finally, we also confirm that N. dimidiatum does not form an appressorium or infection thread but instead infects pitaya via open stomata. In conclusion, the results provide a foundation for future research on N. dimidiatum and the control of pitaya canker. IMPORTANCE Pitaya canker is a significant disease in the pitaya industry in China, causing significant economic losses. Therefore, systematic research on Neoscytalidium dimidiatum , the fungus implicated in pitaya canker, is essential for comprehending the pathogenesis of this disease and developing effective control strategies. We applied comparative genomics to reveal the genetic evolution, metabolic diversity, environmental adaptation, and pathogenicity of N. dimidiatum , providing ideal targets for studies of pathogenesis and molecular targets for fungicide development. Moreover, the systematic study of the N. dimidiatum growth cycle, morphological characteristics, and molecular phylogenetic analysis can promote a comprehensive understanding of its genetic basis.