Abstract Various fungi have been identified in seagrass compartments; however, the exact nature of their interactions with these marine flowering plants remains largely uncharacterized. The partnership between seagrasses and Lulworthiaceae fungi represents a typical and compelling example of such an underwater association. Here, we combine UHPLC-MS/MS, transcriptomics, and plant growth assays to validate the putative symbiosis between the seagrass Halophila ovalis and the Lulworthiaceae fungus Halophilomyces hongkongensis , and elucidate the underlying mechanism of this relationship. We confirmed that H. hongkongensis produces the phytohormone indole-3-acetic acid (IAA). Through transcriptomic analysis, we proposed its IAA biosynthesis pathways. All identified IAA biosynthesis genes were upregulated in seagrass roots/rhizomes compared to rhizosphere sediments, with the tryptophan aminotransferase gene (indole-3-pyruvic acid pathway) exhibiting a significant increase. Furthermore, H. hongkongensis was confirmed as a plant growth-promoting fungus; its culture filtrates promoted Arabidopsis thaliana shoot and lateral root/root hair growth, an effect strongly correlated with IAA production and highly likely in seagrass. Beyond IAA-specific analyses, its upregulated genes were significantly enriched in pathways such as tryptophan metabolism, starch/sucrose metabolism, and DNA replication. Collectively, these results indicate that H. hongkongensis establishes a growth-promoting symbiosis with H. ovalis by upregulating its IAA biosynthesis genes and secreting IAA; in return, the host provides carbohydrates that sustain fungal metabolism and support active DNA replication. This study provides the first mechanistic verification of a seagrass-Lulworthiaceae symbiosis, significantly advancing our understanding of marine plant-fungal interactions. It also demonstrates the first IAA-linked plant growth-promoting capacity of a member from the cryptic marine fungal family Lulworthiaceae.
Wang et al. (Fri,) studied this question.