<p>The interaction between maize (<i>Zea mays</i>) and <i>Aspergillus</i> species poses a huge threat to global food safety due to the production of aflatoxins, the toxic secondary metabolites that contaminate maize and pose health risks to humans and animals. The molecular basis of maize defense to <i>Aspergillus</i> <i>flavus</i>&#xa0;infection was studied through the integration of transcriptome-wide differential expression, functional enrichment, network analysis and DNA methylation profiling combined with machine learning, and finally, these patterns were compared with normal seed germination. <i>Aspergillus</i> infection triggered a rapid reprogramming of maize gene expression, replacing germination-associated pathways—most notably starch hydrolysis via α-amylase—with the massive induction of seed storage protein genes. Concurrently, <i>Aspergillus</i> manipulates maize metabolism, degrades tissues, and exploits nutrient reserves, including zein proteins, to support its proliferation and aflatoxin production. Major down-regulated genes under fungal infection compared to normal germination that led to the weakening of maize defenses include acidic endochitinase, CRRSP and AFP1. Up-regulation of rRNA N-glycosylases and ricin-like lectin genes, key ribosome-inactivating proteins (RIPs), highlights their critical role in maize defense against <i>Aspergillus</i> infection, offering potential for crop protection through advanced strategies like transgenic expression and CRISPR/Cas9 editing. Metabolic changes were reflected in the altered expression of hydrolytic enzymes (e.g., alpha-amylase, phytase) and stress response proteins with a huge impact on seed germination and resistance. DNA methylation plays a significant role in regulating maize responses to fungal invasion, including zein metabolism, with hypomethylation activating defense genes and epigenetic stress memory priming plants for future challenges. Differential gene expression was correlated with promoter methylation in pathogenesis-related (PR) genes as well as zein and alpha-amylase genes. ML algorithms identified <i>Zm00001eb115030</i>, <i>Zm00001eb078730</i>, <i>Zm00001eb089460</i>, <i>Zm00001eb375640</i> and <i>Zm00001eb201830</i> as the most methylation-sensitive defense genes affecting maize reactions. This study identifies key players in the maize-<i>Aspergillus</i> crosstalk, focusing on the molecular and epigenetic mechanisms that underpin this interaction, with implications for developing resistant maize varieties.</p>

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The essential role of methylation in maize (Zea mays) defense against the seed-colonizing fungus Aspergillus flavus

  • Ramya Parakkunnel,
  • S. Aravindan,
  • K. Bhojaraja Naik,
  • C. S. Shantharaja,
  • Anjitha George,
  • K. V. Sripathy,
  • Vinesh Banoth,
  • Y. R. Aruna,
  • Udaya Bhaskar Kethineni,
  • A. Anandan,
  • B. Kumar,
  • Sanjay Kumar

摘要

The interaction between maize (Zea mays) and Aspergillus species poses a huge threat to global food safety due to the production of aflatoxins, the toxic secondary metabolites that contaminate maize and pose health risks to humans and animals. The molecular basis of maize defense to Aspergillus flavus infection was studied through the integration of transcriptome-wide differential expression, functional enrichment, network analysis and DNA methylation profiling combined with machine learning, and finally, these patterns were compared with normal seed germination. Aspergillus infection triggered a rapid reprogramming of maize gene expression, replacing germination-associated pathways—most notably starch hydrolysis via α-amylase—with the massive induction of seed storage protein genes. Concurrently, Aspergillus manipulates maize metabolism, degrades tissues, and exploits nutrient reserves, including zein proteins, to support its proliferation and aflatoxin production. Major down-regulated genes under fungal infection compared to normal germination that led to the weakening of maize defenses include acidic endochitinase, CRRSP and AFP1. Up-regulation of rRNA N-glycosylases and ricin-like lectin genes, key ribosome-inactivating proteins (RIPs), highlights their critical role in maize defense against Aspergillus infection, offering potential for crop protection through advanced strategies like transgenic expression and CRISPR/Cas9 editing. Metabolic changes were reflected in the altered expression of hydrolytic enzymes (e.g., alpha-amylase, phytase) and stress response proteins with a huge impact on seed germination and resistance. DNA methylation plays a significant role in regulating maize responses to fungal invasion, including zein metabolism, with hypomethylation activating defense genes and epigenetic stress memory priming plants for future challenges. Differential gene expression was correlated with promoter methylation in pathogenesis-related (PR) genes as well as zein and alpha-amylase genes. ML algorithms identified Zm00001eb115030, Zm00001eb078730, Zm00001eb089460, Zm00001eb375640 and Zm00001eb201830 as the most methylation-sensitive defense genes affecting maize reactions. This study identifies key players in the maize-Aspergillus crosstalk, focusing on the molecular and epigenetic mechanisms that underpin this interaction, with implications for developing resistant maize varieties.