Distribution patterns of fungal community diversity in the dominant tree species Dacrydium pectinatum and Vatica mangachapoi in tropical rainforests

Abstract

Plant microbial communities are shaped by plant compartments, but the patterns of fungal communities in aboveground and belowground compartments, and which environmental factors can affect them, remain unknown. Here, to address this research gap, high-throughput sequencing technology was performed to investigate the diversity of fungal communities in leaves' and roots' compartments of Dacrydium pectinatum and Vatica mangachapoi from Hainan Island of China. Fungal communities in leaves and roots exhibited significant differences. Eurotiomycetes (16.57%) and Dothideomycetes (45.57%) were predominantly found in leaves, while Agaricomycetes (36.53%) dominated in roots. Compared to the roots, the leaf compartments had higher α-diversity. According to the Mantel test, soil pH mainly influenced roots, while the main driving factors for leaves were rainfall and temperature. The proportion of dispersal-limited processes in rhizoplane (76.67%) and root endosphere (73.81%) were greater than that in leaf epiphytic (62.38%) and leaf endophytic (68.1%), driven by ectomycorrhizal fungi with known dispersal limitations. In summary, the compositions of the leaf and root fungal communities of both endangered tree species differed, partly driven by environmental factors unique to each compartment. Our results provide valuable theoretical and practical insights for preserving tropical tree species.

Importance: Understanding the assembly of microbial communities across different compartments is a prerequisite for harnessing them to enhance plant growth. Our findings reveal significant differences in fungal community structures between the root and leaf compartments. Compared to the roots, the leaf compartments exhibited higher α-diversity. While soil pH mainly influenced fungal communities in the roots, the primary drivers for the leaves were rainfall and temperature. The dispersal-limited processes of fungal communities in the roots were greater than those in the leaves, primarily influenced by mycorrhizal fungi. These findings demonstrate compartment-specific plant-microbe interactions and environmental responses, offering actionable insights for conserving tropical tree species through habitat optimization (e.g., soil pH management) and dispersal corridor preservation. This compartment-aware perspective enhances our ability to leverage microbial functions to improve the resilience of endangered trees in the face of climate change.

Keywords: Dacrydium pectinatum; Vatica mangachapoi; community assembly; diversity; environmental factors; fungal community.

Fig 1

Diversity of fungal community in D. pectinatum and V. mangachapoi. (A) Accumulated OTUs (γ-diversity) for all samples in five compartments. (B) Mean OTU richness (α-diversity) of fungal communities for five compartments. (C) Comparison of OTU richness of five compartments of D. pectinatum and V. mangachapoi. (D) Comparison of OTU richness of D. pectinatum across five compartments in three locations. (E) Comparison of OTU richness of V. mangachapoi across four compartments in four locations. Abbreviation: LE, leaf endophytic; PP, leaf epiphytic; RP, rhizoplane; RS, rhizosphere; RE, root endosphere; D, D. pectinatum; V, V. mangachapoi; DL, Diaoluo; JF, Jianfeng; WZ, Wuzhi; BW, Bawang; and WN, Wanning; Significance level: *P < 0.05; **P < 0.01; and ***P < 0.001.

Fig 2

The fungal community compositions and the composition of the fungal community functional groups inferred by FUNGuild for D. pectinatum and V. mangachapoi. (A) Top 10 of the phylum level. (B) Top 10 of the class level. (C) Relative abundance of fungal functions. (D) Relative abundance of fungal functions of the dominant fungal class. Abbreviation: Ag: aboveground compartment and Bg: belowground compartment. Significance level: *P < 0.05; **P < 0.01; and ***P < 0.001.

Fig 3

PCoA of taxonomic similarity based on Bray-Curtis distances for fungal community compositions at the OTU level. (A) Five compartments. (B) D. pectinatum and V. mangachapoi in five geographical locations. Abbreviation: LE, leaf endophytic; PP, leaf epiphytic; RP, rhizoplane; RS, rhizosphere; RE, root endosphere; D, D. pectinatum; V, V. mangachapoi; DL, Diaoluo; JF, Jianfeng; WZ, Wuzhi; BW, Bawang; and WN, Wanning; Significance level: *P < 0.05; **P < 0.01; and ***P < 0.001.

Fig 4

Pairwise comparisons of the environmental factors are shown. Composition (OTU level) and diversity (observed OTU richness) of the community of different compartments of D. pectinatum and V. mangachapoi were related to each environmental factor by partial Mantel tests. Edge width corresponds to Mantel’s r statistic for the corresponding distance correlation, and edge color denotes the statistical significance based on 999 permutations. Abbreviation: LE, leaf endophytic; PP, leaf epiphytic; RP, rhizoplane; RS, rhizosphere; and RE, root endosphere. Significance level: *P < 0.05; **P < 0.01; and ***P < 0.001.

Fig 5

The relationship among environmental factors, the diversity (Sobs index), and the relative abundance of Eurotiomycetes in leaf and Agaricomycetes in root in D. pectinatum and V. mangachapoi. (A) The relationship between environmental factors and Sobs index of the leaf. The light green solid circles represent samples of Bawang, and the dark green is Jianfeng. The light brown solid circles represent samples of Diaoluo, and the dark brown is Wuzhi. The dark gray solid circles represent samples of Wanning. (B) The relationship between environmental factors and the relative abundance of Eurotiomycetes in leaf. (C) The relationship between environmental factors and the relative abundance of Agaricomycetes in root. The dark green solid circles represent samples of D. pectinatum, and dark brown is V. mangachapoi. Significance level: *P < 0.05; **P < 0.01; ***P < 0.001.

Fig 6

Assembly processes of the fungal community in five compartments. (A and B) the boxplots of βNTI and Raup–Crick-based Bray–Curtis for all pairs of communities in five plant compartments. (C) the relative importance of different ecological processes in five plant compartments.Abbreviation: LE, leaf endophytic; PP, leaf epiphytic; RP, rhizoplane; RS, rhizosphere; and RE, root endosphere.