Chronic sublethal aluminum exposure and wild oat caryopsis decay influence gene expression of Fusarium avenaceum F.a.1

Authors: LEWIS, RICKY - Washington State University; Okubara, Patricia; FUERST, PATRICK - Washington State University; HE, RUIFENG - Washington State University; GANG, DAVID - Washington State University; SULLIVAN, TARAH - Washington State University

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/10/2020
Publication Date: 2/4/2020
Citation: Lewis, R.W., Okubara, P.A., Fuerst, P.E., He, R., Gang, D., Sullivan, T. 2020. Chronic sublethal aluminum exposure and wild oat caryopsis decay influence gene expression of Fusarium avenaceum F.a.1. Frontiers in Microbiology. 11:51. https://doi.org/10.3389/fmicb.2020.00051.
DOI: https://doi.org/10.3389/fmicb.2020.00051

Interpretive Summary: Accumulation of wild oat weed seeds in soils of wheat agroecosystems has been associated with yield reduction. Wild oat also competes with wheat for nutrients and water in soils undergoing acidification. Aluminum and other heavy metals become solubilized in acid soils, contributing to heavy metal toxicity. The soilborne fungal pathogen causing Fusarium root and crown of small-grain cereals preferentially caused seed decay in wild oat compared to wheat. This manuscript discusses how gene expression in this fungus is affected by the presence of wild oat seeds, aluminum or both. The findings indicate that aluminum triggers expression of defense-related genes in the fungus, whereas the presence of wild oat seeds stimulates both defense-related and metabolic genes in the fungus.

Technical Abstract: Global weed pressure represents a major hurdle to crop production. Fusarium avenaceum F.a.1 is a novel strain of a fungal pathogen shown to potentially preferentially decay wild oat (Avena fatua) caryopses compared with those of wheat (Triticum aestivum). Understanding the molecular mechanisms involved in weed seed-pathogen interactions is crucial to developing novel weed seed suppression technologies. Additionally, wild oat often competes with wheat in regions undergoing soil acidification, which leads to increases in soluble concentrations of many metals, including aluminum (Al). A transcriptomic approach was used to investigate molecular responses of F.a.1 during wild oat caryopsis colonization in the presence and absence of chronic, sublethal concentrations of Al (400 µM). Gene expression in F.a.1 was influenced by both caryopsis colonization and aluminum exposure. For instance, caryopsis colonization was associated with upregulation of genes related to stress/defense, organic acid metabolism, basic metabolism, amino acid/peptide/protein metabolism, and phosphate-related metabolism, and downregulation of genes associated with siderophore and iron transport, iron metabolism, stress/defense, organic acid metabolism, metal-related metabolism, basic metabolism, phosphate-related metabolism. Aluminum exposure was associated with upregulation of genes involved in siderophore biosynthesis, secretion, uptake, and utilization, along with several other “iron metabolism-related” genes. Colonization of caryopses was associated with upregulation of genes associated with the citrate cycle and carbon metabolism pathways, while downregulation of genes associated with the N-glycan metabolism pathway was observed. Al exposure led to upregulation of genes associated with biosynthesis of amino acids, 2-oxocarboxylic acid metabolism, biosynthesis of secondary metabolites, carbon metabolism, lysine biosynthesis, valine, leucine and isoleucine degradation, cysteine and methionine metabolism, and propanoate metabolism pathways. Siderophore-related responses were associated with aluminum toxicity and occurred concurrently with differential regulation of genes indicating disruption of iron homeostasis. These findings suggest aluminum toxicity is attenuated by siderophore metabolism in F.a.1. In summary, both caryopsis colonization and aluminum toxicity uniquely influence transcriptomic responses of F.a.1.