Wheat domestication alters root metabolic functions to drive the assembly of endophytic bacteria

• Published in: The Plant journal : for cell and molecular biology 2024-11, Vol.120 (4), p.1263-1277
• Main Authors: Deng, Lixin, Zhang, Ali, Wang, Anze, Zhang, Hao, Wang, Tingting, Song, Weining, Yue, Hong
• Format: Article
• Language: English
• Subjects: Bacteria; Bacteria - genetics; Bacteria - metabolism; Chryseobacterium; Crops; Crops, Agricultural - microbiology; Cultivars; Domestication; Endophytes; Endophytes - metabolism; Endophytes - physiology; endophytic bacteria; Exudates; Exudation; Germplasm; Metabolites; Metabolomics; Microbiomes; Microbiota; Microorganisms; Physiological effects; Plant growth; Plant Roots - genetics; Plant Roots - metabolism; Plant Roots - microbiology; Probiotics; root exudates; Roots; Soil ecology; Soil improvement; Soil Microbiology; Sustainable development; Triticum - genetics; Triticum - metabolism; Triticum - microbiology; Tyrosine; Wheat
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.16972

SUMMARY The domestication process progressively differentiated wild relatives from modern cultivars, thus impacting plant‐associated microorganisms. Endophytic bacterial communities play vital roles in plant growth, development, and health, which contribute to the crop's sustainable development. However, how plant domestication impacts endophytic bacterial communities and relevant root exudates in wheat remains unclear. First, we have observed that the domestication process increased the root endophytic microbial community diversity of wheat while decreasing functional diversity. Second, domestication decreased the endophytic bacterial co‐occurrence network stability, and it did significantly alter the abundances of core microorganisms or potential probiotics. Third, untargeted LC–MS metabolomics revealed that domestication significantly altered the metabolite profiles, and the abundances of various root exudates released were significantly correlated with keystone taxa including the Chryseobacterium, Massilia, and Lechevalieria. Moreover, we found that root exudates, especially L‐tyrosine promote the growth of plant‐beneficial bacteria, such as Chryseobacterium. Additionally, with L‐tyrosine and Chryseobacterium colonized in the roots, the growth of wild wheat's roots was significantly promoted, while no notable effect could be found in the domesticated cultivars. Overall, this study suggested that wild wheat as a key germplasm material, and its native endophytic microbes may serve as a resource for engineering crop microbiomes to improve the morphological and physiological traits of crops in widely distributed poor soils. Significant Statement Building on previous research, our study further investigates the significant effects of long‐term domestication, which has played a crucial role in the development of human civilization, on the communities of endophytic bacteria and root exudates in wheat. Our findings indicate that wild wheat, along with its naturally occurring endophytic microbes, could be valuable resources for manipulating crop microbiomes and improving the overall characteristics of crops in nutrient‐depleted soils.