Abstract
Background
Plants can retain atmospheric particulate matter (PM) through their unique foliar microstructures, which has a profound impact on the phyllosphere microbial communities. Yet, the underlying mechanisms linking atmospheric particulate matter (PM) retention by foliar microstructures to variations in the phyllosphere microbial communities remain a mystery. In this study, we conducted a field experiment with ten Ulmus lines. A series of analytical techniques, including scanning electron microscopy, atomic force microscopy, and high-throughput amplicon sequencing, were applied to examine the relationship between foliar surface microstructures, PM retention, and phyllosphere microbial diversity of Ulmus L.
Results
We characterized the leaf microstructures across the ten Ulmus lines. Chun exhibited a highly undulated abaxial surface and dense stomatal distribution. Langya and **ngshan possessed dense abaxial trichomes, while Lieye, Zuiweng, and Daguo had sparsely distributed, short abaxial trichomes. Duomai, Qingyun, and Lang were characterized by sparse stomata and flat abaxial surfaces, whereas **ye had sparsely distributed but extensive stomata. The mean leaf retention values for total suspended particulate (TSP), PM2.5, PM2.5-10, PM10-100, and PM> 100 were 135.76, 6.60, 20.10, 90.98, and 13.08 µg·cm− 2, respectively. Trichomes substantially contributed to PM2.5 retention, while larger undulations enhanced PM2.5-10 retention, as evidenced by positive correlations between PM2.5 and abaxial trichome density and between PM2.5-10 and the adaxial raw microroughness values. Phyllosphere microbial diversity patterns varied among lines, with bacteria dominated by Sediminibacterium and fungi by Mycosphaerella, Alternaria, and Cladosporium. Redundancy analysis confirmed that dense leaf trichomes facilitated the capture of PM2.5-associated fungi, while bacteria were less impacted by PM and struggled to adhere to leaf microstructures. Long and dense trichomes provided ideal microhabitats for retaining PM-borne microbes, as evidenced by positive feedback loops between PM2.5, trichome characteristics, and the relative abundances of microorganisms like Trichoderma and Aspergillus.
Conclusions
Based on our findings, a three-factor network profile was constructed, which provides a foundation for further exploration into how different plants retain PM through foliar microstructures, thereby impacting phyllosphere microbial communities.
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Background
Rapid industrial development and urbanization have led to the emission of large amounts of harmful gases and particulate matter (PM) into the atmosphere [1], which has been particularly pronounced in develo** countries [2]. Atmospheric PM, especially PM2.5 (diameter ≤ 2.5 μm) and PM10 (diameter ≤ 10 μm), often contains heavy metals and can lead to urban haze, which has become the most serious air pollution issue in China in recent decades [3, 4]. Numerous studies have shown that plants can improve air quality in polluted areas by filtering PM from the air and retaining it on their unique leaf surface microstructures [22,23,24].
In this study, to elucidate the underlying relationship between the PM, foliar microstructures, and phyllosphere microbial diversity, we used ten asexual lines (to ensure a consistent genetic background) of eight distinct species, one variety, and one cultivar of Ulmus as study materials. Sanning electron microscopy (SEM) and atomic force microscopy (AFM) were applied to characterize the foliar microstructures. Using the laser particle size, we further characterized the particle size distribution of the PM retained on the foliar surface. Furthermore, we used 16 S rRNA gene and ITS high-throughput amplicon sequencing to analyze the phyllosphere microbial diversity among the lines (consist of bacteria and fungi). Based on the unique foliar microstructures of plants and their known role in retaining PM, we hypothesize that specific variations in leaf microstructures would influence the phyllosphere microbial community by providing distinct microhabitats for PM-borne microorganisms. To address this hypothesis, our study was designed to investigate: (1) how foliar surface microstructures influence PM retention capacity, and (2) how variations in PM retention shape the diversity and composition of phyllosphere microorganisms across the ten Ulmus lines.
Materials and methods
Study site and plant materials
The study site (38.1517°N, 114.4843°E) was a nursery at Hebei Academy of Forestry and Grassland Science located in ** and as shelterbelts that can effectively retain atmospheric PM, although this ability varies among species [70]. The TSP index reflects the total amount of PM retained on the leaf surface, which can be used as an indicator to evaluate the PM retention capacity of plant species [71]. In this study, the average TSP values of the ten Ulmus lines (135.76 µg·cm− 2; Fig. 1) were much higher (by 59.62–231.44%) than most common woody plants under similar climatic conditions, including Buxus megistophylla, Fraxinus pennsylvanica, and Sophora japonica [81]. Notably, we also found that, unlike the bacterial communities, certain fungal functional classes, particularly “Symbiotroph”, varied among the ten lines, with significantly higher relative abundance observed in **ye. This may be attributed to the ecological traits of the “Symbiotroph” class of fungi, potentially establishing a mutually beneficial symbiotic relationship with the plant [82]. For instance, similar to endophytes [83], phyllosphere microorganisms might provide the plant with antimicrobial substances or other beneficial compounds for defending pathogens, and in return, the plant provides the necessary resources for the fungi to thrive [84]. This may also indirectly reflect the potential higher tolerance of **ye to biotic stress than the other lines, but it needs to be further verified.
Atmospheric PM conditions significantly impact the phyllosphere microbial community of many species [19, 85, 86]. Based on the RDA analysis (Fig. 5a and b), our results suggest that fungal microorganisms could be carried by the PM2.5 attached to the dense leaf trichomes. In contrast, bacteria were not easily carried by PM and were also difficult to capture by or attach to the leaf microstructures of the Ulmus lines. Based on a correlation profile (Fig. 5c and d), we found that several microorganisms (consisting of both bacteria and fungi) were correlated (p < 0.05) with PM factors and/or leaf microstructures, suggesting that the microstructures of the leaf surfaces of the ten Ulmus lines enable them to capture PM-borne microorganisms. For example, PM2.5 carried microorganisms, such as Trichoderma and Aspergillus; the microstructures of the leaf surface, especially the dense and long trichomes, provided an ideal microhabitat for the PM2.5-microorganism complexes (Fig. 5d). The two positive feedback loops (i.e., PM2.5 -abaxial trichome lengh-Aspergillus and PM2.5-abaxial trichome density- Trichoderma) within the correlation network profile also provides evidence to support this (Fig. 6). In contrast, within the profile, we also found two negative feedback loops (PM2.5−10/PM> 100-adaxial RMS values-Cladosporium), suggesting that PM in these size ranges is difficult to be retained by the microrough leaf adaxial surface, or even if captured, it is unable to promote/even inhibit the proliferation of specific microorganisms (Fig. 6). We further assessed the significance of the aforementioned four feedback loops through multiple regression analysis and confirmed their validity (p < 0.05) (Table S9). Overall, our data prove that plant foliar microstructures can create an ideal microhabitat for PM-borne microorganisms. On the other hand, whether and how these PM-borne microorganisms subsequently affect plant growth and development remains to be further explored.
Conclusions
We demonstrate that the ten Ulmus lines investigated exhibited considerable PM retention capacities, with a mean TSP value of 135.76 µg·cm− 2. Variations in leaf surface microstructures, particularly the length and density of the trichome and the surface roughness, were the primary determinants of differential PM retention capacities among the lines. Long and dense trichomes substantially contributed to the retention of PM2.5, while larger undulations on the leaf surface enhanced the capture of PM10. Notably, these leaf microstructures provided ideal microhabitats for retaining PM-borne microorganisms, as evidenced by positive feedback loops between PM2.5, trichome characteristics, and the relative abundances of phyllosphere fungi like Trichoderma and Aspergillus. In contrast, bacterial communities were less impacted by PM. Our findings establish a three-factor network profile linking PM, leaf microstructures, and phyllosphere microbial communities, providing insights for further exploration into how different plants retain PM through foliar microstructures, thereby influencing their associated microbiomes.
Data availability
The raw sequencing data reported in this article have been publicly available under Genome Sequence Archivein in National Center for Bioinformation, China (https://ngdc.cncb.ac.cn/gsa; No. CRA016188 and CRA016189).
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We gratefully acknowledge the handling editors and the two anonymous reviewers for their valuable comments on this work.
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This work was financially supported by the Science and Technology Development Fund of Central Guidance on Local (216Z6301G), China; and the Key Research and Development Program of Hebei Province (21326301D), China.
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MSY and YRH conceived and designed the research. LRX and YCL conducted all experiments, analyzed the data, interpreted the results, and wrote the manuscript. LRX, SXF, CL, XYZ, and YCR performed the statistical analysis. YJL provided critical revisions. The authors all approved of publication, and there is no conflict of interest.
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Xu, L., Liu, Y., Feng, S. et al. The relationship between atmospheric particulate matter, leaf surface microstructure, and the phyllosphere microbial diversity of Ulmus L.. BMC Plant Biol 24, 566 (2024). https://doi.org/10.1186/s12870-024-05232-z
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DOI: https://doi.org/10.1186/s12870-024-05232-z