Differential ‘resuscitation’ from the seed microbiota: a plant-holobiont ecological strategy for buffering stresses

Abstract

The plant and its associated microbiota constitute a holobiont. Within this framework, the seed endophyte reservoir, shaped through multigenerational selection, exhibits pronounced host specificity, mutualistic potential, and signatures of co-evolution. We hypothesise that this reservoir operates as a ‘symbiotic toolbox’ forming an ‘Anticipated Utility Microbiota’ within the holobiont. Upon germination, specific microbes from this toolbox may undergo resuscitation to buffer environmental stresses, thereby influencing plant fitness. Using axenic Vicia sativa seeds, we simulated cold, salinity, and drought stresses and applied 16S rRNA sequencing to track seed symbiont resuscitation. Taxa showing resuscitation across stresses were classified as generalists, whilst those resuscitating under specific stresses were specialists. Microbial inoculants from these taxa were then tested in pots for host growth effects. As expected, distinct resuscitation patterns under different stresses supported the hypothesised seed ‘symbiotic toolbox’. We identified 115 generalist amplicon sequence variants (e.g. Methylobacterium, Pantoea, and Sphingomonas) and stress-specific specialists: 60 cold specialists (e.g. Stenotrophomonas and Geobacter), 79 salt specialists (e.g. Leptotrichia), and 13 drought specialists (e.g. Proteobacteria). Strikingly, generalist microbial inoculants consistently promoted seedling growth across stresses, whilst specialist inoculants showed stress-specific efficacy. This study elucidates a holobiont mechanism whereby vertically transmitted seed microbes constitute a ‘symbiotic toolbox’ that differentially resuscitates under stress, thereby enhancing seedling fitness.