Interkingdom multi-omics analysis reveals the enhancing effects of magnesium oxide nanoparticles and Piriformospora indica co-application on tobacco growth and Ralstonia solanacearum resistance

Tobacco ( Nicotiana tabacum L.) is an important cash crop, but its yield, quality, and profitability are severely affected by bacterial wilt caused by Ralstonia solanacearum . There is currently no effective means to control tobacco bacterial wilt. This study reported a novel strategy to improve resistance to bacterial wilt and enhance the growth of tobacco. Magnesium oxide nanoparticles with concentrations of > 250 mg/L inhibited the growth of Ralstonia solanacearum while promoting Piriformospora indica growth. Magnesium oxide nanoparticles can bind to Piriformospora indica through electric field force. Compared with the single application of magnesium oxide nanoparticles or Piriformospora indica , co-application of magnesium oxide nanoparticles (250 mg/L) and Piriformospora indica (10 7 cfu/mL) demonstrated a superior promoting effect on tobacco growth and resistance to bacterial wilt. The magnesium oxide nanoparticles– Piriformospora indica combination strengthened the functions of magnesium oxide nanoparticles or Piriformospora indica on tobacco by inducing expression of the genes involved in pathogenesis (such as PTI and PR10a ), immunity, reactive oxygen species detoxification, hormone signaling, and transcriptional regulation (such as WRKY ). This combination shapes the microbial community to improve tobacco resistance to Ralstonia solanacearum , resulting in an increase in the abundance of beneficial bacteria such as Streptomyces , Nocardioides , and Micromonospora . Furthermore, an integrated analysis of the transcriptome, metagenomics, and soil metabolomics revealed the root–microbe interactional networks driven by the magnesium oxide nanoparticles– Piriformospora indica combination under Ralstonia solanacearum attack. This work highlights the advantages of the magnesium oxide nanoparticles– Piriformospora indica combination in tobacco production, providing an potential nanobiofertilizer for controlling tobacco bacterial wilt. • MgO NPs– P. indica combination enhances tobacco growth and disease resistance. • MgO NPs inhibited the growth of R. solanacearum while promoting P. indica survival. • MgO NPs– P. indica combination shapes the microbial community to improve tobacco resistance to R. solanacearum . • The root–microbe interactional networks driven by the MgO NPs– P. indica combination under R. solanacearum attack were revealed.