Bamboo mosaic virus-induced metabolic reprogramming engages mitochondrial function to regulate redox homeostasis and defense responses in Nicotiana benthamiana

竹子花叶病毒诱导的代谢重编程通过线粒体功能调节本氏烟草的氧化还原稳态和防御反应

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Abstract

Plants possess a remarkable capacity to reprogram their metabolism in response to pathogen attacks. However, how virus-induced metabolic shifts intersect with redox dynamics and defense signaling remains incompletely understood. In this study, we leveraged a multifaceted omics approach to investigate the metabolic shifts induced by Bamboo mosaic virus (BaMV), a positive-sense single-stranded RNA virus, in Nicotiana benthamiana—a model host widely used for dissecting plant–virus interactions due to its high susceptibility and amenability to genetic manipulation. Metabolic profiling revealed the accumulation of hexose phosphates and Krebs cycle intermediates following BaMV infection, while fluxomic analysis uncovered an orchestrated redirection of carbon flux toward glycolysis and the Krebs cycle. Proteomic data further highlighted a concerted upregulation of mitochondrial enzymes, with three mitochondrial proteins showing markedly increased accumulation in BaMV-infected tissues. Together, these integrated omics analyses indicate that BaMV infection induces a metabolic shift toward energy-generating pathways, possibly to meet the elevated metabolic demands of infection. Notably, functional analysis revealed that silencing mitochondrial NAD(+)-dependent malic enzyme 1 significantly enhanced BaMV accumulation, accompanied by alterations in cytoplasmic NADH-to-NAD(+) ratio and changes in the landscape of defense gene expression. Collectively, our findings underscore the pivotal role of mitochondrial metabolism in governing cytoplasmic redox balance and finely tuning defense responses during BaMV infection. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-025-07996-4.

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