Auxin plays a pivotal role in the co-evolution of plants and microorganisms. Xanthomonas oryzae pv. oryzicola (Xoc) stands as a significant factor that affects rice yield and quality. However, the current understanding of Xoc's capability for indole 3-acetic acid (IAA) synthesis and its mechanistic implications remains elusive. In this study, we performed a comprehensive genomic analysis of Xoc strain RS105, leading to the identification of two nitrilase enzyme family (NIT) genes, designated as AKO15524.1 and AKO15829.1, subsequently named NIT24 and NIT29, respectively. Our investigation unveiled that the deletion of NIT24 and NIT29 resulted in a notable reduction in IAA synthesis capacity within RS105, thereby impacting extracellular polysaccharide production. This deficiency was partially ameliorated through exogenous IAA supplementation. The study further substantiated that NIT24 and NIT29 have nitrilase activity and the ability to catalyse IAA production in vitro. The lesion length and bacterial population statistics experiments confirmed that NIT24 and NIT29 positively regulated the pathogenicity of RS105, suggesting that NIT24 and NIT29 may regulate Xoc invasion by affecting IAA synthesis. Furthermore, our analysis corroborated mutant strains, RS105_ΔNIT24 and RS105_ΔNIT29, which elicited the outbreak of reactive oxygen species, the deposition of callose and the upregulation of defence-related gene expression in rice. IAA exerted a significant dampening effect on the immune responses incited by these mutant strains in rice. In addition, the absence of NIT24 and NIT29 affected the growth-promoting effect of Xoc on rice. This implies that Xoc may promote rice growth by secreting IAA, thus providing a more suitable microenvironment for its own colonization. In summary, our study provides compelling evidence for the existence of a nitrilase-dependent IAA biosynthesis pathway in Xoc. IAA synthesis-related genes promote Xoc colonization by inhibiting rice immune defence response and affecting rice growth by increasing IAA content in Xoc.

中文翻译：

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NIT24 和 NIT29 介导的米黄单胞菌 IAA 合成。oryzicola 抑制免疫力并促进水稻生长

生长素在植物和微生物的共同进化中发挥着关键作用。米黄单胞菌pv. oryzicola (Xoc) 是影响水稻产量和品质的重要因素。然而，目前对 Xoc 合成吲哚 3-乙酸 (IAA) 的能力及其机制影响的理解仍然难以捉摸。在这项研究中，我们对 Xoc 菌株 RS105 进行了全面的基因组分析，鉴定出了两个腈水解酶家族 (NIT) 基因，分别命名为AKO15524.1和AKO15829.1，随后分别命名为NIT24和NIT29。我们的研究表明， NIT24和NIT29的缺失导致 RS105 内 IAA 合成能力显着降低，从而影响细胞外多糖的产生。通过补充外源 IAA 可以部分改善这种缺陷。研究进一步证实NIT24和NIT29具有腈水解酶活性以及在体外催化IAA产生的能力。病斑长度和细菌种群统计实验证实NIT24和NIT29正向调节RS105的致病性，提示NIT24和NIT29可能通过影响IAA合成来调节Xoc侵袭。此外，我们的分析证实了突变菌株RS105_ΔNIT24和RS105_ΔNIT29，它们引发了水稻中活性氧的爆发、胼胝质的沉积以及防御相关基因表达的上调。IAA 对水稻中这些突变菌株引发的免疫反应具有显着的抑制作用。此外，NIT24和NIT29的缺失影响了Xoc对水稻的促生长作用。这意味着Xoc可能通过分泌IAA促进水稻生长，从而为其自身定植提供更合适的微环境。总之，我们的研究为 Xoc 中存在腈水解酶依赖性 IAA 生物合成途径提供了令人信服的证据。IAA合成相关基因通过抑制水稻免疫防御反应促进Xoc定植，并通过增加Xoc中IAA含量影响水稻生长。