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<p>Cereal cyst nematodes (CCNs, <i>Heterodera filipjevi</i>) are major constraints to global wheat productivity. Beneficial microbes such as arbuscular mycorrhizal fungi (AMF) and <i>Trichoderma</i> are known to enhance plant stress tolerance, yet their combined effects on CCN resistance in wheat remain largely unexplored. This study investigated the individual and synergistic roles of AMF and <i>Trichoderma</i> in conferring resistance to <i>H. filipjevi</i> in the susceptible wheat cultivar Bezostaya using integrated ionomics, metabolomics, and transcriptomics approaches. The combined AMF + <i>Trichoderma</i> treatment most effectively suppressed CCN populations (reproduction factor: 1.17) compared with the untreated control (4.50) and single-agent treatments. Successful root colonization by both symbionts was confirmed. Ionomic profiling revealed synergistic enhancement of nitrate, potassium, iron, manganese, and zinc uptake, suggesting improved nutritional status and stress resilience. Metabolomic analysis identified significant elevation of 2-descarboxy-betanidin and reduction of N-(3-acetamidopropyl)-4-aminobutanal in combined-treatment plants, with additional shifts in defense-related amino acids and secondary metabolites supporting antimicrobial biosynthesis. Transcriptomic profiling revealed 1,110 upregulated and 1,718 downregulated genes. Key upregulated defense genes included <i>PRB1-2</i>, <i>PRB1-3</i>, <i>RPM1</i>, <i>BTB</i> domain-containing protein, <i>MAPK kinase substrate protein</i>, and <i>cinnamoyl-CoA reductase 1-like</i>, reflecting activation of salicylic acid-mediated immunity, MAPK cascades, and hormone signaling. Downregulated pathways included phenylpropanoid biosynthesis and starch/sucrose metabolism. Promoter analysis of <i>PRB1-2</i> confirmed cis-elements responsive to symbiosis and pathogen elicitors, and subcellular localization confirmed its apoplastic defense role. The synergistic AMF–<i>Trichoderma</i> consortium orchestrates a robust, multi-layered defense response, offering significant potential for sustainable nematode management and improved wheat productivity.</p>

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AMF and Trichoderma Confer Cereal Cyst Nematode ‘Heterodera filipjevi’ Resistance in Wheat by Fine-tuning Ionomics, Metabolomics, and Transcriptomics

  • 期刊论文

  • 发表日期：

    2026年7月11日

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  • Özgenur Arslanoğlu,
  • Muhammad Sameeullah,
  • Ayşegül Yaman,
  • Nagihan Duman,
  • Furkan Ulaş,
  • Ebubekir Yüksel,
  • Mustafa İmren,
  • Abdelfattah A. Dababat

摘要

Cereal cyst nematodes (CCNs, Heterodera filipjevi) are major constraints to global wheat productivity. Beneficial microbes such as arbuscular mycorrhizal fungi (AMF) and Trichoderma are known to enhance plant stress tolerance, yet their combined effects on CCN resistance in wheat remain largely unexplored. This study investigated the individual and synergistic roles of AMF and Trichoderma in conferring resistance to H. filipjevi in the susceptible wheat cultivar Bezostaya using integrated ionomics, metabolomics, and transcriptomics approaches. The combined AMF + Trichoderma treatment most effectively suppressed CCN populations (reproduction factor: 1.17) compared with the untreated control (4.50) and single-agent treatments. Successful root colonization by both symbionts was confirmed. Ionomic profiling revealed synergistic enhancement of nitrate, potassium, iron, manganese, and zinc uptake, suggesting improved nutritional status and stress resilience. Metabolomic analysis identified significant elevation of 2-descarboxy-betanidin and reduction of N-(3-acetamidopropyl)-4-aminobutanal in combined-treatment plants, with additional shifts in defense-related amino acids and secondary metabolites supporting antimicrobial biosynthesis. Transcriptomic profiling revealed 1,110 upregulated and 1,718 downregulated genes. Key upregulated defense genes included PRB1-2, PRB1-3, RPM1, BTB domain-containing protein, MAPK kinase substrate protein, and cinnamoyl-CoA reductase 1-like, reflecting activation of salicylic acid-mediated immunity, MAPK cascades, and hormone signaling. Downregulated pathways included phenylpropanoid biosynthesis and starch/sucrose metabolism. Promoter analysis of PRB1-2 confirmed cis-elements responsive to symbiosis and pathogen elicitors, and subcellular localization confirmed its apoplastic defense role. The synergistic AMF–Trichoderma consortium orchestrates a robust, multi-layered defense response, offering significant potential for sustainable nematode management and improved wheat productivity.