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.
{"title":"Differential 'resuscitation' from the seed microbiota: a plant-holobiont ecological strategy for buffering stresses.","authors":"Ying Xu,Ning Ling,Cendrine Mony,Philippe Vandenkoornhuyse","doi":"10.1111/nph.70920","DOIUrl":"https://doi.org/10.1111/nph.70920","url":null,"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.","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"64 1","pages":""},"PeriodicalIF":9.4,"publicationDate":"2026-01-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146015274","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Guillaume Charrier,Al P Kovaleski,Bénédicte Wenden,Heikki Hänninen
Cold hardiness models are useful tools to predict cold damage in plants, such as those produced by unseasonal temperature cycles or by increased cold exposure. Although development of these models started about five decades ago, their applications remain limited. We describe the main paradigms driving the different types of cold hardiness models (empirical to process-based), their similarities and differences. Among the existing paradigms, process-based models are built to translate physiological mechanisms into mathematical functions over a broad range of climatic conditions, thus making them more accurate for studying the effect of climate change. Different approaches have been developed in predicting cold hardiness: (1) empirical relationships between temperature and cold hardiness; (2) phenological processes controlling acclimation and deacclimation rates; (3) phenological and physiological processes predicting cold hardiness through the osmo-hydric approach; and (4) molecular regulation driving the metabolic drivers of cold hardiness. For the first three approaches, we describe the context, the experimental and field observations that defined their frameworks as well as their limitations. To increase the realism of cold hardiness models, we describe the potential of a fourth approach, based on the perception of environmental signals, how it translates into cold acclimation/deacclimation and provide recommendations to develop this framework.
{"title":"Cold hardiness mechanisms and modeling: existing approaches and future avenues.","authors":"Guillaume Charrier,Al P Kovaleski,Bénédicte Wenden,Heikki Hänninen","doi":"10.1111/nph.70863","DOIUrl":"https://doi.org/10.1111/nph.70863","url":null,"abstract":"Cold hardiness models are useful tools to predict cold damage in plants, such as those produced by unseasonal temperature cycles or by increased cold exposure. Although development of these models started about five decades ago, their applications remain limited. We describe the main paradigms driving the different types of cold hardiness models (empirical to process-based), their similarities and differences. Among the existing paradigms, process-based models are built to translate physiological mechanisms into mathematical functions over a broad range of climatic conditions, thus making them more accurate for studying the effect of climate change. Different approaches have been developed in predicting cold hardiness: (1) empirical relationships between temperature and cold hardiness; (2) phenological processes controlling acclimation and deacclimation rates; (3) phenological and physiological processes predicting cold hardiness through the osmo-hydric approach; and (4) molecular regulation driving the metabolic drivers of cold hardiness. For the first three approaches, we describe the context, the experimental and field observations that defined their frameworks as well as their limitations. To increase the realism of cold hardiness models, we describe the potential of a fourth approach, based on the perception of environmental signals, how it translates into cold acclimation/deacclimation and provide recommendations to develop this framework.","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"65 1","pages":""},"PeriodicalIF":9.4,"publicationDate":"2026-01-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"146005103","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}