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Cultivated and wild pearl millet display contrasting patterns of abundance and co-occurrence in their root mycobiome.

ABSTRACT: Fungal communities associated with roots play a key role in nutrient uptake and in mitigating the abiotic and biotic stress of their host. In this study, we characterized the roots mycobiome of wild and cultivated pearl millet [Pennisetum glaucum (L.) R. Br., synonym: Cenchrus americanus (L.) Morrone] in three agro-ecological areas of Senegal following a rainfall gradient. We hypothesized that wild pearl millet could serve as a reservoir of endophytes for cultivated pearl millet. We therefore analyzed the soil factors influencing fungal community structure and whether cultivated and wild millet shared the same fungal communities. The fungal communities associated with pearl millet were significantly structured according to sites and plant type (wild vs cultivated). Besides, soil pH and phosphorus were the main factors influencing the fungal community structure. We observed a higher fungal diversity in cultivated compared to wild pearl millet. Interestingly, we detected higher relative abundance of putative pathotrophs, especially plant pathogen, in cultivated than in wild millet in semi-arid and semi-humid zones, and higher relative abundance of saprotrophs in wild millet in arid and semi-humid zones. A network analysis based on taxa co-occurrence patterns in the core mycobiome revealed that cultivated millet and wild relatives had dissimilar groups of hub taxa. The identification of the core mycobiome and hub taxa of cultivated and wild pearl millet could be an important step in developing microbiome engineering approaches for more sustainable management practices in pearl millet agroecosystems.

SUBMITTER: Mofini MT

PROVIDER: S-EPMC8741948 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe rhizosheath, a cohesive soil layer firmly adhering to plant roots, plays a vital role in facilitating water and mineral uptake. In pearl millet, rhizosheath formation is genetically controlled and influenced by root exudates. Here, we investigated the impact of root exudates on the microbiota composition, interactions, and assembly processes, and rhizosheath structure in pearl millet using four distinct lines with contrasting soil aggregation abilities.ResultsUtilizing 16S rRNA gene and ITS metabarcoding for microbiota profiling, coupled with FTICR-MS metabonomic analysis of metabolite composition in distinct plant compartments and root exudates, we revealed substantial disparities in microbial diversity and interaction networks. The ß-NTI analysis highlighted bacterial rhizosphere turnover driven primarily by deterministic processes, showcasing prevalent homogeneous selection in root tissue (RT) and root-adhering soil (RAS). Conversely, fungal communities were more influenced by stochastic processes. In bulk soil assembly, a combination of deterministic and stochastic mechanisms shapes composition, with deterministic factors exerting a more pronounced role. Metabolic profiles across shoots, RT, and RAS in different pearl millet lines mirrored their soil aggregation levels, emphasizing the impact of inherent plant traits on microbiota composition and unique metabolic profiles in RT and exudates. Notably, exclusive presence of antimicrobial compounds, including DIMBOA and H-DIMBOA, emerged in root exudates and RT of low aggregation lines.ConclusionsThis research underscores the pivotal influence of root exudates in shaping the root-associated microbiota composition across pearl millet lines, entwined with their soil aggregation capacities. These findings underscore the interconnectedness of root exudates and microbiota, which jointly shape rhizosheath structure, deepening insights into soil-plant-microbe interactions and ecological processes shaping rhizosphere microbial communities. Deciphering plant-microbe interactions and their contribution to soil aggregation and microbiota dynamics holds promise for the advancement of sustainable agricultural strategies. Video Abstract.

Project description:Under conditions of high vapor pressure deficit (VPD) and soil drying, restricting transpiration is an important avenue to gain efficiency in water use. The question we raise in this article is whether breeding for agro-ecological environments that differ for the rainfall have selected for traits that control plant water use. These are measured in pearl millet materials bred for zones varying in rainfall (8 combinations of parent and F1-hybrids, 18 F1-hybrids and then 40 F1-hybrids). In all cases, we found an agro-ecological variation in the slope of the transpiration response to increasing VPD, and parental line variation in the transpiration response to soil drying within hybrids/parent combinations. The hybrids adapted to lower rainfall had higher transpiration response curves than those from the highest rainfall zones, but showed no variation in how transpiration responded to soil drying. The genotypes bred for lower rainfall zones showed lower leaf area, dry matter, thicker leaves, root development, and exudation, than the ones bred for high rainfall zone when grown in the low VPD environment of the greenhouse, but there was no difference in their root length neither on the root/shoot index in these genotypes. By contrast, when grown under high VPD conditions outdoors, the lower rainfall hybrids had the highest leaf, tiller, and biomass development. Finally, under soil drying the genotypes from the lower rainfall accumulated less biomass than the ones from higher rainfall zone, and so did the parental lines compared to the hybrids. These differences in the transpiration response and growth clearly showed that breeding for different agro-ecological zones also bred for different genotype strategies in relation to traits related to plant water use. Highlights: • Variation in transpiration response reflected breeding for agro-ecological zones • Different growth strategies depended on the environmental conditions • Different ideotypes reflected rainfall levels in specific agro-ecological zones.

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Cultivated and wild pearl millet display contrasting patterns of abundance and co-occurrence in their root mycobiome.

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