Genomic insights into bamboo witches’ broom disease: pathogenicity and phytohormone biosynthesis in Aciculosporium take

Bamboo witches' broom disease (WBD), caused by <i>Aciculosporium take</i> Miyake, devastates bamboo forests. Understanding the genome and pathogenic factors of pathogen is crucial for disease control. We employed single-molecule real-time sequencing, Illumina paired-end sequencing, and chromatin interaction mapping techniques to assemble the genome of <i>A. take</i> CCTCC-M2023413, analyze pathogenicity- and phytohormone-biosynthesis-related genes, and compare it to 12 other WBD pathogens. The genome of <i>A. take</i> is 59.24 Mb in size, with 54.32% repeats, 7 chromosomes, 7,105 protein-coding genes, 84 ribosomal RNAs, and 115 transfer RNAs. Predictive analysis of pathogenicity genes found 237 carbohydrate-active enzymes, 1,069 membrane transport proteins, 1,040 pathogen-host interaction genes, 315 virulence factors, and 70 effectors. Most of pathogenicity genes overlapped with repeat-rich regions. Additionally, 172 genes were linked to auxin biosynthesis, 53 to brassinosteroid biosynthesis, and 2 to <i>cis</i>-zeatin biosynthesis. Comparative genomic analysis identified 77 core orthogroups shared by 13 WBD pathogens, played roles in metabolites, genetic information processing, pathogenesis, <i>cis</i>-zeatin biosynthesis, lifespan, and quorum sensing. The <i>miaA</i> gene, crucial for <i>cis</i>-zeatin biosynthesis, is structurally conserved and sequence-diverse among 13 WBD pathogens, with upregulated expression during bamboo WBD pathogenesis. This highlights that <i>cis</i>-zeatin is significant contributor to host pathogenesis, and miaA is a new potential target for controlling WBD. This study provides important insights on preventing and controlling bamboo WBD.