Contrasting Patterns of Phyllosphere Fungal Diversity Between Angiosperms and Gymnosperms Along a Subalpine-Elevation Gradient

Xiaocheng Yu , Yuxuan Mo , Yuehua Hu , Zhaoqiao Wu , Qiang Luo , Liang Song , Zhenghong Tan , Hua-Zheng Lu

Integrative Conservation ›› 2025, Vol. 4 ›› Issue (3) : 476 -490.

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Integrative Conservation ›› 2025, Vol. 4 ›› Issue (3) : 476 -490. DOI: 10.1002/inc3.70028
RESEARCH ARTICLE

Contrasting Patterns of Phyllosphere Fungal Diversity Between Angiosperms and Gymnosperms Along a Subalpine-Elevation Gradient

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Abstract

Leaf functional traits play a fundamental role in shaping phyllosphere microbial diversity; however, their influence across evolutionary lineages and elevational gradients remains insufficiently understood. This study investigates the α-diversity, β-diversity, community assembly processes, and co-occurrence networks of phyllosphere fungi in Angiosperms and Gymnosperms along an elevational gradient (2900–4100 m) on Bai Ma Snow Mountain, southwestern China. By analyzing leaf functional traits and environmental factors, we evaluated their effects on fungal diversity, community assembly, and network stability under varying environmental conditions. Fungal α-diversity in Angiosperms followed a cosine-like pattern, peaking at mid-elevations, whereas Gymnosperms exhibited a consistent decline with increasing elevation. β-Diversity patterns revealed more pronounced structural shifts in Angiosperms, indicating stronger sensitivity to environmental gradients. Deterministic processes dominated community assembly at higher elevations, while stochastic processes were more influential at low-to-mid elevations, particularly in Angiosperms. Key leaf functional traits, including specific leaf area (SLA), leaf vein angle (LVA), and roughness (RS), were strongly correlated with fungal α-diversity in Angiosperms, with SLA and LVA showing negative correlations and RS a positive correlation. In contrast, Gymnosperms exhibited weaker associations with these traits. Co-occurrence network analyses revealed dynamic shifts in microbial connectivity in Angiosperms, where positive and negative interactions initially decreased but increased again at higher elevations. In contrast, Gymnosperms exhibited a steady decline in positive and negative interaction ratios along the gradient. These findings provide a foundation for integrating plant functional traits and microbial interactions into conservation strategies, prioritizing core fungal taxa, rare Angiosperms at higher elevations, and fragile alpine ecosystems, to enhance specific functional-taxa conservation and ecosystem resilience.

Keywords

angiosperms / elevational gradients / gymnosperms / leaf functional traits / microbial diversity / phyllosphere fungi

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Xiaocheng Yu, Yuxuan Mo, Yuehua Hu, Zhaoqiao Wu, Qiang Luo, Liang Song, Zhenghong Tan, Hua-Zheng Lu. Contrasting Patterns of Phyllosphere Fungal Diversity Between Angiosperms and Gymnosperms Along a Subalpine-Elevation Gradient. Integrative Conservation, 2025, 4(3): 476-490 DOI:10.1002/inc3.70028

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References

[1]

Le Bagousse-Pinguet, Y., P. Liancourt, L. Götzenberger, et al. 2018. “A Multi-Scale Approach Reveals Random Phylogenetic Patterns at the Edge of Vascular Plant Life.” Perspectives in Plant Ecology, Evolution and Systematics 30: 22–30.

[2]

Bahram, M., F. Hildebrand, S. K. Forslund, et al. 2018. “Structure and Function of the Global Topsoil Microbiome.” Nature 560: 233–237.

[3]

Barberán, A., S. T. Bates, E. O. Casamayor, and N. Fierer. 2014. “Erratum: Using Network Analysis to Explore Co-Occurrence Patterns in Soil Microbial Communities.” ISME Journal 8: 952.

[4]

Bar-On, Y. M., and R. Milo. 2019. “The Global Mass and Average Rate of Rubisco.” Proceedings of the National Academy of Sciences of the United States of America 116: 4738–4743.

[5]

Bashir, I., A. F. War, I. Rafiq, Z. A. Reshi, I. Rashid, and Y. S. Shouche. 2022. “Phyllosphere Microbiome: Diversity and Functions.” Microbiological Research 254: 126888.

[6]

Beattie, G. A.2011. “Water Relations in the Interaction of Foliar Bacterial Pathogens With Plants.” Annual Review of Phytopathology 49: 533–555.

[7]

Bodenhausen, N., M. W. Horton, and J. Bergelson. 2013. “Bacterial Communities Associated With the Leaves and the Roots of Arabidopsis thaliana.” PLoS One 8: e56329.

[8]

Bolyen, E., J. R. Rideout, M. R. Dillon, et al. 2019. “Author Correction: Reproducible, Interactive, Scalable and Extensible Microbiome Data Science Using QIIME 2.” Nature Biotechnology 37: 1091.

[9]

Bond, W. J.1989. “The Tortoise and the Hare - Ecology of Angiosperm Dominance and Gymnosperm Persistence.” Biological Journal of the Linnean Society 36: 227–249.

[10]

Brodribb, T. J., and T. S. Feild. 2010. “Leaf Hydraulic Evolution Led a Surge in Leaf Photosynthetic Capacity During Early Angiosperm Diversification.” Ecology Letters 13: 175–183.

[11]

Callahan, B. J., P. J. McMurdie, M. J. Rosen, A. W. Han, A. J. Johnson, and S. P. Holmes. 2016. “DADA2: High-Resolution Sample Inference From Illumina Amplicon Data.” Nature Methods 13: 581–583.

[12]

Chaudhry, R., G. Dranitsaris, T. Mubashir, J. Bartoszko, and S. Riazi. 2020. “A Country Level Analysis Measuring the Impact of Government Actions, Country Preparedness and Socioeconomic Factors on COVID-19 Mortality and Related Health Outcomes.” Eclinicalmedicine 25: 100464.

[13]

Choat, B., S. Jansen, T. J. Brodribb, et al. 2012. “Global Convergence in the Vulnerability of Forests to Drought.” Nature 491: 752–755.

[14]

Cohu, C. M., O. Muller, W. W. Adams, 3rd, and B. Demmig-Adams. 2014. “Leaf Anatomical and Photosynthetic Acclimation to Cool Temperature and High Light in Two Winter Versus Two Summer Annuals.” Physiologia Plantarum 152: 164–173.

[15]

Couturier, E., S. Courrech du Pont, and S. Douady. 2009. “A Global Regulation Inducing the Shape of Growing Folded Leaves.” PLoS One 4: e7968.

[16]

Deng, Y., P. Zhang, Y. Qin, et al. 2016. “Network Succession Reveals the Importance of Competition in Response to Emulsified Vegetable Oil Amendment for Uranium Bioremediation.” Environmental Microbiology 18: 205–218.

[17]

Díaz, S., J. Kattge, J. H. Cornelissen, et al. 2016. “The Global Spectrum of Plant Form and Function.” Nature 529: 167–171.

[18]

Dixon, P.2003. “VEGAN, a Package of R Functions for Community Ecology.” Journal of Vegetation Science 14: 927–930.

[19]

Doan, H. K., V. N. Ngassam, S. F. Gilmore, R. Tecon, A. N. Parikh, and J. H. J. Leveau. 2020. “Topography-Driven Shape, Spread, and Retention of Leaf Surface Water Impacts Microbial Dispersion and Activity in the Phyllosphere.” Phytobiomes Journal 4: 268–280.

[20]

Duclos, T. R., W. DeLuca, and D. King. 2019. “Direct and Indirect Effects of Climate on Bird Abundance Along Elevation Gradients in the Northern Appalachian Mountains.” Diversity and Distributions 25: 1670–1683.

[21]

Duncan, W. G.1971. “Leaf Angles, Leaf Area, and Canopy Photosynthesis.” Crop Science 11: 482.

[22]

Faticov, M., A. Abdelfattah, T. Roslin, et al. 2021. “Climate Warming Dominates Over Plant Genotype in Shaping the Seasonal Trajectory of Foliar Fungal Communities on Oak.” New Phytologist 231: 1770–1783.

[23]

Gao, X. N., H. Sun, R. Liu, Z. L. Wu, and Y. W. Qi. 2022. “The Impact of Sugarcane Brown Rust and Host Resistance on the Phyllosphere Bacterial Community.” Sugar Tech 24: 1420–1429.

[24]

Guo, X., J. J. Feng, Z. Shi, et al. 2018. “Climate Warming Leads to Divergent Succession of Grassland Microbial Communities.” Nature Climate Change 8: 813.

[25]

He, H. S., Z. Q. Hao, D. J. Mladenoff, G. F. Shao, Y. M. Hu, and Y. Chang. 2005. “Simulating Forest Ecosystem Response to Climate Warming Incorporating Spatial Effects in North-Eastern China.” Journal of Biogeography 32: 2043–2056.

[26]

Herrmann, M., P. Geesink, R. Richter, and K. Küsel. 2021. “Canopy Position Has a Stronger Effect Than Tree Species Identity on Phyllosphere Bacterial Diversity in a Floodplain Hardwood Forest.” Microbial Ecology 81: 157–168.

[27]

Izuno, A., M. Kanzaki, T. Artchawakom, C. Wachrinrat, and Y. Isagi. 2016. “Vertical Structure of Phyllosphere Fungal Communities in a Tropical Forest in Thailand Uncovered by High-Throughput Sequencing.” PLoS One 11: e0166669.

[28]

Kembel, S. W., and R. C. Mueller. 2014. “Plant Traits and Taxonomy Drive Host Associations in Tropical Phyllosphere Fungal Communities.” Botany 92: 303–311.

[29]

Kembel, S. W., T. K. O'connor, H. K. Arnold, S. P. Hubbell, S. J. Wright, and J. L. Green. 2014. “Relationships Between Phyllosphere Bacterial Communities and Plant Functional Traits in a Neotropical Forest.” Proceedings of the National Academy of Sciences of the United States of America 111: 13715–13720.

[30]

Koike, F., and M. Hotta. 1996. “Foliage-Canopy Structure and Height Distribution of Woody Species in Climax Forests.” Journal of Plant Research 109: 53–60.

[31]

Kou, Y., C. Li, B. Tu, J. Li, and X. Li. 2023. “The Responses of Ammonia-Oxidizing Microorganisms to Different Environmental Factors Determine Their Elevational Distribution and Assembly Patterns.” Microbial Ecology 86: 485–496.

[32]

Leveau, J. H.2019. “A Brief From the Leaf: Latest Research to Inform Our Understanding of the Phyllosphere Microbiome.” Current Opinion in Microbiology 49: 41–49.

[33]

Li, C. N., B. Tu, Y. P. Kou, et al. 2021. “The Assembly of Methanotrophic Communities Regulated by Soil pH in a Mountain Ecosystem.” Catena 196: 104883.

[34]

Lindow, S. E., and M. T. Brandl. 2003. “Microbiology of the Phyllosphere.” Applied and Environmental Microbiology 69: 1875–1883.

[35]

Liu, J., W. Zhang, Y. Liu, et al. 2023. “Differences in Phyllosphere Microbiomes Among Different Populus Spp. in the Same Habitat.” Frontiers in Plant Science 14: 1143878.

[36]

Lu, H. Z., R. Brooker, L. Song, et al. 2020. “When Facilitation Meets Clonal Integration in Forest Canopies.” New Phytologist 225: 135–142.

[37]

Luo, L., Z. Zhang, P. Wang, et al. 2019. “Variations in Phyllosphere Microbial Community Along With the Development of Angular Leaf-Spot of Cucumber.” AMB Express 9: 76.

[38]

Ma, J., Z. L. Zhao, S. Lin, and Y. M. Xie. 2021. “Topology of Leaf Veins: Experimental Observation and Computational Morphogenesis.” Journal of the Mechanical Behavior of Biomedical Materials 123: 104788.

[39]

Mahnert, A., R. A. Ortega, C. Berg, M. Grube, and G. Berg. 2018. “Leaves of Indoor Ornamentals Are Biodiversity and Functional Hotspots for Fungi.” Frontiers in Microbiology 9: 2343.

[40]

McElwain, J. C., C. Yiotis, and T. Lawson. 2016. “Using Modern Plant Trait Relationships Between Observed and Theoretical Maximum Stomatal Conductance and Vein Density to Examine Patterns of Plant Macroevolution.” New Phytologist 209: 94–103.

[41]

Mechaber, W. L., D. B. Marshall, R. A. Mechaber, R. T. Jobe, and F. S. Chew. 1996. “Mapping Leaf Surface Landscapes.” Proceedings of the National Academy of Sciences of the United States of America 93: 4600–4603.

[42]

Nestler, S.2022. “An Extension of the Mixed-Effects Growth Model That Considers Between-Person Differences in the Within-Subject Variance and the Autocorrelation.” Statistics in Medicine 41: 471–482.

[43]

Nilsen, E. T., R. Arora, and M. Upmanyu. 2014. “Thermonastic Leaf Movements in During Freeze-Thaw Events: Patterns, Functional Significances, and Causes.” Environmental and Experimental Botany 106: 34–43.

[44]

Ning, D., M. Yuan, L. Wu, et al. 2020. “A Quantitative Framework Reveals Ecological Drivers of Grassland Microbial Community Assembly in Response to Warming.” Nature Communications 11: 4717.

[45]

Osono, T.2006. “Role of Phyllosphere Fungi of Forest Trees in the Development of Decomposer Fungal Communities and Decomposition Processes of Leaf Litter.” Canadian Journal of Microbiology 52: 701–716.

[46]

Pandey, B., K. W. Pan, M. A. Dakhil, et al. 2021. “Contrasting Gymnosperm Diversity Across an Elevation Gradient in the Ecoregion of China: The Role of Temperature and Productivity.” Frontiers in Ecology and Evolution 9: 679439.

[47]

Peay, K. G., C. von Sperber, E. Cardarelli, et al. 2017. “Convergence and Contrast in the Community Structure of Bacteria, Fungi and Archaea Along a Tropical Elevation-Climate Gradient.” FEMS Microbiology Ecology 93: fix045.

[48]

Perreault, R., and I. Laforest-Lapointe. 2022. “Plant-Microbe Interactions in the Phyllosphere: Facing Challenges of the Anthropocene.” ISME Journal 16: 339–345.

[49]

Rahbek, C.1995. “The Elevational Gradient of Species Richness: A Uniform Pattern?” Ecography 18: 200–205.

[50]

Sack, L., and C. Scoffoni. 2013. “Leaf Venation: Structure, Function, Development, Evolution, Ecology and Applications in the Past, Present and Future.” New Phytologist 198: 983–1000.

[51]

Sanders, N. J.2002. “Elevational Gradients in Ant Species Richness: Area, Geometry, and Rapoport's Rule.” Ecography 25: 25–32.

[52]

Shigyo, N., K. Umeki, and T. Hirao. 2019. “Plant Functional Diversity and Soil Properties Control Elevational Diversity Gradients of Soil Bacteria.” FEMS Microbiology Ecology 95: fiz025.

[53]

Siles, J. A., and R. Margesin. 2016. “Abundance and Diversity of Bacterial, Archaeal, and Fungal Communities Along an Altitudinal Gradient in Alpine Forest Soils: What Are the Driving Factors?” Microbial Ecology 72: 207–220.

[54]

da Silva, P. G., J. M. Lobo, M. C. Hensen, F. Z. Vaz-de-Mello, M. I. M. Hernández, and K. Feeley. 2018. “Turnover and Nestedness in Subtropical Dung Beetle Assemblages Along an Elevational Gradient.” Diversity and Distributions 24: 1277–1290.

[55]

Sohrabi, R., B. C. Paasch, J. A. Liber, and S. Y. He. 2023. “Phyllosphere Microbiome.” Annual Review of Plant Biology 74: 539–568.

[56]

Spooren, J., S. van Bentum, L. S. Thomashow, C. Pieterse, D. M. Weller, and R. L. Berendsen. 2024. “Plant-Driven Assembly of Disease-Suppressive Soil Microbiomes.” Annual Review of Phytopathology 62: 1–30.

[57]

De La Torre, A. R., Z. Li, Y. Van de Peer, and P. K. Ingvarsson. 2017. “Contrasting Rates of Molecular Evolution and Patterns of Selection Among Gymnosperms and Flowering Plants.” Molecular Biology and Evolution 34: 1363–1377.

[58]

Vacher, C., A. Hampe, A. J. Porté, U. Sauer, S. Compant, and C. E. Morris. 2016. “The Phyllosphere: Microbial Jungle at the Plant-Climate Interface.” Annual Review of Ecology, Evolution, and Systematics 47: 1–24.

[59]

Vorholt, J. A.2012. “Microbial Life in the Phyllosphere.” Nature Reviews Microbiology 10: 828–840.

[60]

van der Wal, A., and J. H. Leveau. 2011. “Modelling Sugar Diffusion Across Plant Leaf Cuticles: The Effect of Free Water on Substrate Availability to Phyllosphere Bacteria.” Environmental Microbiology 13: 792–797.

[61]

Wang, L., H. Gong, W. Liao, and Z. Wang. 2015. “Accumulation of Particles on the Surface of Leaves During Leaf Expansion.” Science of the Total Environment 532: 420–434.

[62]

Wang, X., Z. Q. Yuan, A. Ali, et al. 2023. “Leaf Traits and Temperature Shape the Elevational Patterns of Phyllosphere Microbiome.” Journal of Biogeography 50: 2135–2147.

[63]

Wang, Y. S., Y. P. Kou, C. N. Li, et al. 2019. “Contrasting Responses of Diazotrophic Specialists, Opportunists, and Generalists to Steppe Types in Inner Mongolia.” Catena 182: 104168.

[64]

Wu, X., W. J. Shi, and F. L. Tao. 2021. “Estimations of Forest Water Retention Across China From an Observation Site-Scale to a National-Scale.” Ecological Indicators 132: 108274.

[65]

Yan, K., W. Han, Q. Zhu, C. Li, Z. Dong, and Y. Wang. 2022. “Leaf Surface Microtopography Shaping the Bacterial Community in the Phyllosphere: Evidence From 11 Tree Species.” Microbiological Research 254: 126897.

[66]

Yang, T., P. Weisenhorn, J. A. Gilbert, et al. 2016. “Carbon Constrains Fungal Endophyte Assemblages Along the Timberline.” Environmental Microbiology 18: 2455–2469.

[67]

Yang, Y., Z. H. Shen, J. Han, and Z. Y. Ciren. 2016. “Plant Diversity Along the Eastern and Western Slopes of Baima Snow Mountain, China.” Forests 7: 89.

[68]

Yao, H., X. Sun, C. He, X. C. Li, and L. D. Guo. 2020. “Host Identity Is More Important in Structuring Bacterial Epiphytes Than Endophytes in a Tropical Mangrove Forest.” FEMS Microbiology Ecology 96: fiaa038.

[69]

Yuan, M. M., X. Guo, L. W. Wu, et al. 2021. “Climate Warming Enhances Microbial Network Complexity and Stability.” Nature Climate Change 11: 343–U100.

[70]

Zhou, H. L., G. S. Zhou, Q. J. He, L. Zhou, Y. H. Ji, and M. Z. Zhou. 2020. “Environmental Explanation of Maize Specific Leaf Area Under Varying Water Stress Regimes.” Environmental and Experimental Botany 171: 103932.

[71]

Zhou, J., and D. Ning. 2017. “Stochastic Community Assembly: Does It Matter in Microbial Ecology?” Microbiology and Molecular Biology Reviews: MMBR 81: e00002-00017.

[72]

Zhu, L. W., T. Y. Fu, J. Du, et al. 2023. “Hydraulic Role in Differential Stomatal Behaviors at Two Contrasting Elevations in Three Dominant Tree Species of a Mixed Coniferous and Broad-Leaved Forest in Low Subtropical China.” Forest Ecosystems 10: 100095.

[73]

Zhu, Y. G., C. Xiong, Z. Wei, et al. 2022. “Impacts of Global Change on the Phyllosphere Microbiome.” New Phytologist 234: 1977–1986.

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2025 The Author(s). Integrative Conservation published by John Wiley & Sons Australia, Ltd on behalf of Xishuangbanna Tropical Botanical Garden (XTBG).

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