Laboratory of Microbiology, Ghent Universitygrid.5342.0, Ghent, Belgium.
LIPME, Université de Toulouse, INRAE, CNRS, Castanet-Tolosan, France.
mBio. 2022 Oct 26;13(5):e0103322. doi: 10.1128/mbio.01033-22. Epub 2022 Aug 30.
Hereditary symbioses have the potential to drive transgenerational effects, yet the mechanisms responsible for transmission of heritable plant symbionts are still poorly understood. The leaf symbiosis between and the bacterium offers an appealing model system to study how heritable bacteria are transmitted to the next generation. Here, we demonstrate that inoculation of apical buds with a bacterial suspension is sufficient to colonize newly formed leaves and propagules, and to ensure transmission to the next plant generation. Flagellar motility is not required for movement inside the plant but is important for the colonization of new hosts. Further, tissue-specific regulation of putative symbiotic functions highlights the presence of two distinct subpopulations of bacteria in the leaf gland and at the shoot meristem. We propose that bacteria in the leaf gland dedicate resources to symbiotic functions, while dividing bacteria in the shoot tip ensure successful colonization of meristematic tissue, glands, and propagules. Compartmentalization of intrahost populations together with tissue-specific regulation may serve as a robust mechanism for the maintenance of mutualism in leaf symbiosis. Hereditary symbioses with bacteria are common in the animal kingdom, but relatively unexplored in plants. Several plant species form associations with bacteria in their leaves, which is called leaf symbiosis. These associations are highly specific, but the mechanisms responsible for symbiont transmission are poorly understood. Using the association between the yam species and as a model leaf symbiosis, we show that bacteria are distributed to specific leaf structures via association with shoot meristems. Flagellar motility is required for initial infection but does not contribute to spread within host tissue. We also provide evidence that bacterial subpopulations at the meristem or in the symbiotic leaf gland differentially express key symbiotic genes. We argue that this separation of functional symbiont populations, coupled with tight control over bacterial infection and transmission, explain the evolutionary robustness of leaf symbiosis. These findings may provide insights into how plants may recruit and maintain beneficial symbionts at the leaf surface.
遗传共生关系有可能产生跨代效应，但负责遗传植物共生体传播的机制仍知之甚少。 和 之间的叶共生关系为研究遗传细菌如何传递给下一代提供了一个有吸引力的模型系统。在这里，我们证明，用细菌悬浮液接种顶芽足以使新形成的叶子和繁殖体定殖，并确保将其传递给下一代植物。鞭毛运动对于在植物体内的移动不是必需的，但对于新宿主的定殖很重要。此外，假定共生功能的组织特异性调节突出了在叶腺和茎尖分生组织中存在两种不同的细菌亚群。我们提出，叶腺中的细菌将资源专用于共生功能，而茎尖中的分裂细菌则确保成功定殖分生组织、腺体和繁殖体。宿主内种群的分隔以及组织特异性调节可能是维持叶共生中互利共生的稳健机制。 与细菌的遗传共生关系在动物王国中很常见，但在植物中相对较少研究。一些植物物种在其叶子中与细菌形成关联，这被称为叶共生。这些关联是高度特异的，但负责共生体传播的机制仍不清楚。我们使用薯蓣科植物 和 之间的关联作为模型叶共生关系，表明细菌通过与茎尖分生组织的关联而分布到特定的叶子结构中。鞭毛运动对于初始感染是必需的，但对宿主组织内的传播没有贡献。我们还提供了证据表明，在分生组织或共生叶腺中的细菌亚群差异表达关键共生基因。我们认为，这种功能共生体种群的分离，加上对细菌感染和传播的严格控制，解释了叶共生关系的进化稳健性。这些发现可能为植物如何在叶表面招募和维持有益共生体提供了一些见解。
