Ecology and Evolution | 植物驱动的土壤微生物群落变化通过负反馈影响种子萌发

Abstract

1. Plant–soil feedbacks (PSFs) drive plant community diversity via interactions between plants and soil microbes. However, we know little about how frequently PSFs affect plants at the seed stage, and the compositional shifts in fungi that accompany PSFs on germination. 

植物-土壤反馈（PSFs）通过植物与土壤微生物的相互作用来驱动植物群落多样性。然而，我们对PSFs如何频繁地影响植物在种子阶段，以及发芽时伴随PSFs的真菌的组成变化知之甚少。

2. We conducted a pairwise PSF experiment to test whether seed germination was differentially impacted by conspecific versus heterospecific soils for seven grassland species. We used metagenomics to characterize shifts in fungal community composition in soils conditioned by each plant species. To investigate whether changes in the abundance of certain fungal taxa were associated with multiple PSFs, we assigned taxonomy to soil fungi and identified putative pathogens that were significantly more abundant in soils conditioned by plant species that experienced negative or positive PSFs. 

为了验证同种和异种土壤对7种草地植物种子萌发的影响是否存在差异，我们进行了两两PSF试验。我们使用宏基因组学来表征土壤中真菌群落组成的变化。为了研究某些真菌类群丰度的变化是否与多个PSFs相关，我们对土壤真菌进行了分类，并确定了在经历了阴性或阳性PSFs的植物条件下，土壤中显著丰富的推定病原体。

3. We observed negative, positive, and neutral PSFs on seed germination. Although conspecific and heterospecific soils for pairs with significant PSFs contained host-specialized soil fungal communities, soils with specialized microbial communities did not always lead to PSFs. The identity of host-specialized pathogens, that is, taxa uniquely present or significantly more abundant in soils conditioned by plant species experiencing negative PSFs, overlapped among plant species, while putative pathogens within a single host plant species differed depending on the identity of the heterospecific plant partner. Finally, the magnitude of feedback on germination was not related to the degree of fungal community differentiation between species pairs involved in negative PSFs. 

我们观察到阴性、阳性和中性PSFs对种子萌发的影响。尽管具有显著PSFs的同种和异种土壤都含有宿主特异性的土壤真菌群落，但具有特异性微生物群落的土壤并不一定会产生PSFs。宿主特异性病原体的特性，即在经历了负PSFs的植物条件下，在土壤中唯一存在或显著丰富的类群，在植物物种之间重叠，而在单一宿主植物物种内的假定病原体的特性取决于异源植物伙伴的特性。最后，萌发反馈的大小与涉及负性PSFs的物种对之间的真菌群落分化程度无关。

4. Synthesis. Our findings reveal the potential importance of PSFs at the seed stage. Although plant species developed specialized fungal communities in rhizosphere soil, pathogens were not strictly host-specific and varied not just between plant species, but according to the identity of plant partner. These results illustrate the complexity of microbe-mediated interactions between plants at different life stages that next-generation sequencing can begin to unravel. 

我们的发现揭示了PSFs在种子阶段的潜在重要性。尽管植物种类在根际土壤中形成了专门的真菌群落，但病原微生物并不是严格的宿主特异性的，而且不仅在植物种类之间存在差异，而且会根据植物伙伴的身份而变化。这些结果说明了在不同生命阶段的植物之间，微生物介导的相互作用的复杂性，而下一代测序可以开始解开。

Strength of PSFs on seeds germinated in conspecific versus heterospecific soil. Each panel contains results for seeds of a different plant species;x-axis labels reflect the identity of the heterospecific plant-conditioned soil. PSFs were calculated as ln(germination in conspecific soil/germination in heterospecific soil). Positive values indicate positive PSFs (higher germination in conspecific soil compared to other species' or sterile soil), and negative feedback values indicate negative PSFs (lower germination in conspecific soil compared to other species' or sterile soil). Error bars show standard error, and * indicates statistically significant PSFs (p < .05) from linear models on proportion of seeds that germinated (germination data shown in Figure S2, Tables S3–S9)

Fungal community differentiation by plant species identity. PCoAs show fungal community differences between plant species in (a) big pots, with comparison to preconditioning (Day 0) soil; (b) big pots, comparing only postconditioning fungal composition; (c) small pots with preconditioning (Day 0) soil; and (d) small pots, comparing only postconditioned soils of each plant species. Each point represents the fungal community in one pot. Colors and shapes correspond to different host plant species or a control in which fungal communities developed without a plant host; ellipses represent 95% confidence levels. Preconditioned soils differed from postconditioned soils in both big and small pots (PERMANOVA;p < .05; Tables S10 and S11). In big pots, postconditioning fungal communities were distinct among all species pairs (PERMANOVA; p < .05) but this was not the case for fungal communities in small pots (PERMANOVA; p > .05; Tables S12 and S13)

Germination success, fungal community composition, and distinguishing fungal taxa (as identified by FUNGuild) associated with four of the eight statistically significant directional PSFs. Germination trials (left column) included seeds exposed to soils previously conditioned by plants in big and small pots (see Section2.2); ordinations (middle column) include soils from both big pots (solid symbols) and small pots (hollow symbols). (a) Desmodium seeds germinated less in conspecific soil compared to Geum-conditioned soil (negative PSF); (b) Desmodium and Geum contained distinct fungal soil communities; and (c) 53 fungal ASVs, five of which are potential pathogens, were enriched in Desmodium (conspecific) soils relative to Geum (heterospecific) soils; (d) Geum seeds experienced a negative PSF compared with Poa-conditioned soil; (e) Geum and Poa soils contained distinct fungal communities; and (f) 65 ASVs, one a potential pathogen, were enriched in Geum soil relative to Poa; (g) Pycnanthemum seeds experienced greater germination success in Ageratina soil; (h) Pycnanthemum and Ageratina soils contained marginally distinct fungal communities (p = .056); and (i) relative to Ageratina soil, 83 ASVs were enriched in Pycnanthemum soil, including two potential pathogens; (j) Ageratina seeds experienced a positive PSF, which was also associated with (k) soil communities that differed in fungal composition between Ageratina and Poa, and (l) including enrichment of two potential pathogens and 28 potential mutualist ASVs in Ageratina soil relative to Poa. Ellipses reflect 95% confidence levels. Results from germination tests are contained in Tables S6–S12; PERMANOVA results for fungal communities are found in Table S14. Identities of potential pathogens are reported in Table 1. For the four additional negative PSFs, see Figure S5

Conclusion

对于一些草地物种，植物-土壤反馈影响种子发芽（植物适应性的关键组成部分），而这些PSFs与整个群落的土壤真菌变化相关。不同的微生物群落是否含有关键的宿主特异性病原体仍然是未来研究的重点。值得注意的是，我们没有检测到相互的反馈，也就是说，在任何情况下，两个物种在彼此的土壤中相对于自己的土壤中发芽更多，如果种子发芽的psf是促进共存的关键机制，这可能是预期的。在未来的PSF研究中，在不同的环境条件下测试多个物种的防御综合征，将提高我们预测种子何时以及是否会屈服于PSF，以及它们是否在维持地上植物多样性方面发挥作用的能力。最终，确定种子(尤其是田间)上的负PSF特征，并根据种子性状预测它们的大小，可能有助于最大化恢复中的多样性和预测全球变化对PSF的影响。