Mayer Teresa, Teutloff Erik, Unger Kerstin, Lehenberger Pamela, Agler Matthew T
Plant Microbiosis Lab, Institute of Microbiology, Friedrich Schiller University, Jena, Germany.
Cluster of Excellence, Balance of the Microverse, Friedrich Schiller University, Jena, Germany.
Microbiome. 2025 Apr 22;13(1):102. doi: 10.1186/s40168-025-02090-1.
Upon seed germination, soil bacteria are activated to transition to the plant and eventually colonize mature tissues like leaves. These bacteria are poised to significantly influence plant health, but we know little about their colonization routes. We studied the mechanisms of the transition of soil bacteria to germinating plants and leaves using an in-planta isolation approach and by experimentally manipulating inoculation times. We then tested how plant-microbe-microbe interactions shape assembly mechanisms in natural soil communities by amending soil with a trackable, labeled strain of the opportunistic pathogen Pseudomonas viridiflava (Pv3D9).
We identified 27 diverse genera of leaf-associated bacteria that could transition alone from a few cells near a germinating plant to mature leaves, suggesting that the soil-to-leaf transition is probably important for them in nature. Indeed, when plants were only inoculated by soil after the emergence of true leaves, less diverse bacteria transitioned to mature leaves via different colonization mechanisms than when plants germinated in the presence of soil microorganisms. In particular, deterministic processes drove the colonization of phylogenetic bins dominated by Pedobacter, Enterobacter, Stenotrophomonas, Janthinobacterium, Pseudomonas, and Chryseobacterium only in the natural soil-to-leaf transition. Host genotype and soil amendments with Pv3D9, both of which affect host physiology, had strong effects on mainly deterministic colonization.
Diverse bacteria transition from soil to leaves during natural colonization, resulting in characteristic diversity in healthy leaf microbiomes. The mechanisms of colonization are a mix of stochastic processes, which will be largely shaped by competition, and deterministic processes which are more responsive to factors that shape host physiology. In the chase toward targeted manipulation of microbiomes, identifying these mechanisms for a given host and environment provides important information. Developing targeted treatments, however, will require further dissection of the pathways by which host factors drive stochastic and deterministic transitions from soil to leaves. Video Abstract.
种子萌发时，土壤细菌被激活，向植物转移并最终定殖于叶片等成熟组织。这些细菌对植物健康有重大影响，但我们对其定殖途径知之甚少。我们采用植物体内分离方法并通过实验控制接种时间，研究了土壤细菌向萌发植物和叶片转移的机制。然后，我们通过用可追踪、标记的机会致病菌绿黄假单胞菌（Pv3D9）菌株改良土壤，测试了植物 - 微生物 - 微生物相互作用如何塑造天然土壤群落中的组装机制。
我们鉴定出27个不同的与叶片相关的细菌属，它们能够从萌发植物附近的少数细胞单独转移到成熟叶片，这表明从土壤到叶片的转移在自然环境中对它们可能很重要。事实上，当真叶出现后才用土壤接种植物时，与在土壤微生物存在下萌发的植物相比，通过不同定殖机制转移到成熟叶片的细菌种类更少。特别是，只有在自然的土壤到叶片的转移过程中，确定性过程驱动了以Pedobacter、Enterobacter、Stenotrophomonas、Janthinobacterium、Pseudomonas和Chryseobacterium为主的系统发育类群的定殖。宿主基因型和用Pv3D9进行的土壤改良，这两者都会影响宿主生理，对主要是确定性定殖有强烈影响。
在自然定殖过程中，多种细菌从土壤转移到叶片，导致健康叶片微生物群落具有特征性的多样性。定殖机制是随机过程（主要受竞争影响）和确定性过程的混合，确定性过程对影响宿主生理的因素更敏感。在追求对微生物群落进行靶向操纵的过程中，确定给定宿主和环境的这些机制提供了重要信息。然而，开发靶向治疗方法将需要进一步剖析宿主因素驱动从土壤到叶片的随机和确定性转移的途径。视频摘要。
