Evaluating the hologenome concept by analyzing the root-endosphere microbiota of chimeric plants

Marine Biget; Tingting Wang; Cendrine Mony; Qicheng Xu; Lucie Lecoq; Véronique Chable; Kevin R Theis; Ning Ling; Philippe Vandenkoornhuyse

doi:10.1016/j.isci.2023.106031

Evaluating the hologenome concept by analyzing the root-endosphere microbiota of chimeric plants

iScience. 2023 Jan 23;26(2):106031. doi: 10.1016/j.isci.2023.106031. eCollection 2023 Feb 17.

Authors

Marine Biget¹, Tingting Wang^{1

2}, Cendrine Mony¹, Qicheng Xu², Lucie Lecoq¹, Véronique Chable³, Kevin R Theis⁴, Ning Ling², Philippe Vandenkoornhuyse¹

Affiliations

¹ Université de Rennes 1, CNRS, UMR 6553 ECOBIO (écosystèmes, biodiversité, évolution), 35000 Rennes, France.
² Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Nanjing 210095, China.
³ UMR BAGAP INRAE, Centre Bretagne-Normandie, Domaine de la Motte, BP35327, 35653 Le Rheu Cedex, France.
⁴ Department of Biochemistry, Microbiology and Immunology, Wayne State University School of Medicine, Detroit, MI, USA.

Abstract

The hologenome concept considers the entity formed by a host and its microbiota, the holobiont, as new level of hierarchical organization subject to neutral and selective forces. We used grafted plants to formally evaluate the hologenome concept. We analyzed the root-endosphere microbiota of two independent watermelon and grapevine plant systems, including ungrafted and reciprocal-grafting combinations. Grafted and ungrafted hosts harbor markedly different microbiota compositions. Furthermore, the results indicate a non-random assembly of bacterial communities inhabiting the root endosphere of chimeric plants with interactive effect of both the rootstock and scion on the recruitment of microorganisms. Because chimeric plants did not have a random microbiota, the null hypothesis that holobionts assemble randomly and hologenome concept is an intellectual construction only can be rejected. The study supports the relevance of hologenome as biological level of organization and opens new avenues for a better fundamental understanding of plants as holobionts.

Keywords: Bioinformatics; Interaction of plants with organisms; Microbiome.