Diversity and functional traits of the flower stigma microbiome in heterotrophic and autotrophic plants: Phelipanche ramosa vs. its host Nicotiana tabacum

Abstract

Phelipanche ramosa is a widespread parasitic weed of significant economic importance, particularly affecting tomatoes and tobacco. Despite its well-documented impact on agriculture, its microbial associations remain poorly understood. For the first time, we used Next-Generation Sequencing (NGS) to determine the composition of microorganisms (bacteria and fungi) on the flower stigma of P. ramosa and its host, Nicotiana tabacum, as well as to explore their potential functions. The stigma is a nutrient-rich environment that fosters a varied microbial community, encompassing both beneficial and pathogenic organisms affecting plant health and reproductive success. Unique bacterial populations were identified in P. ramosa stigmas, which were absent or less abundant in N. tabacum stigmas. We identified 49 bacterial OTUs in P. ramosa stigmas, primarily Proteobacteria (87.5%) with dominant genera like Pantoea and Pseudomonas. In contrast, N. tabacum stigmas (18 OTUs) were also rich in Proteobacteria (69.6%) but showed higher levels of Leuconostoc and Enterobacteriaceae. Phelipanche ramosa stigmas exhibited a higher abundance of Actinobacteria, while N. tabacum stigmas had a greater proportion of Firmicutes. Fungal communities differed significantly: P. ramosa stigmas (109 OTUs) were dominated by Basidiomycota, while N. tabacum (69 OTUs) was primarily colonised by Ascomycota, with the genus Candida common in the host but absent in the parasite. Specific genera such as Chalastospora, Ustilaginaceae, and Bensingtonia were more abundant or exclusive to P. ramosa stigmas. Nicotiana tabacum stigmas hosted a potentially functionally rich bacterial microbiome, while P. ramosa harbored a more limited one. In contrast, both the structural diversity and functional (metabolic) potential of the fungal communities were higher in P. ramosa compared to N. tabacum. Microbiome network analysis highlighted distinct physiological functions associated with autotrophic and heterotrophic lifestyles. Some identified microorganisms may play key roles in nutrient availability and pathogenicity, including potentially beneficial ones that could provide new opportunities for biological control. This study highlights the significant relationships between microbial diversity and functional traits, underscoring the importance of these dynamics in the structure and functioning of the stigma microbiome.