Linking rhizosphere bacterial succession to metabolite dynamics unravels the underlying survival strategies of desert ephemeral plants

Abstract Desert ephemerals complete rapid life cycles to survive aridity, yet the ontogenetic coordination of below‐ground rhizosphere interactions with above‐ground resource allocation remains unclear. This study examined six dominant ephemeral species ( Eremurus inderiensis , Eremopyrum orientale , Erodium oxyrrhynchum , Allium mongolicum , Alyssum linifolium and Nepeta micrantha ) in the Gurbantünggüt Desert across seedling and flowering stages, integrating plant biomass, rhizosphere metabolites and bacterial communities. This study detected consistent ontogenetic shifts at the overall level: a 44.4% decrease in root: shoot ratio shifting biomass from below‐ground to above‐ground with interspecific variations. Concurrently, rhizosphere metabolic space contracted by 86.4%, with species‐specific metabolic plasticity strongly correlated with biomass reallocation magnitude. Bacterial communities exhibited reduced α‐diversity, simplified co‐occurrence networks and a predicted functional transition from carbon to nitrogen metabolism. Keystone microbe–metabolite associations shifted from carbon‐based linkages at the seedling stage to nitrogen‐centric correlations at flowering, accompanied by stage‐specific turnover of keystone taxa and reconfiguration of microbe–metabolite networks. At the species level, however, the key taxa, metabolites and network dynamics underlying these shifts were highly specific, with divergent niche‐width dynamics and stage‐specific interactions corresponding to host metabolic plasticity. Path modelling revealed a universal, stage‐dependent reversal in biomass drivers: below‐ground biomass was initially supported by broad bacterial niche width, whereas flowering‐stage above‐ground biomass was directly driven by rhizosphere metabolites. These findings demonstrate that host developmental stage orchestrates a phased rhizosphere strategy in desert ephemerals. This strategy synchronizes keystone taxa succession and microbe–metabolite network reconfiguration with plant ontogenetic goals, enabling a conserved shift from microbial‐assisted establishment to metabolite‐driven reproduction despite species‐specific pathways. This study provides novel insights for plant–microbe co‐adaptation in resource‐limited desert ecosystems. Read the free Plain Language Summary for this article on the Journal blog.