Host selection shapes crop microbiome assembly and network complexity

Xiong, Chao; Zhu, Yan; Wang, Juntao; Singh, Brajesh K.; Han, Li‐Li; Shen, Ju-Pei; Li, Peipei; Wang, Guibao; Wu, Chuanfa; Ge, An‐Hui; Zhang, Limei; He, Ji‐Zheng

doi:10.1111/nph.16890

Cited by 416 publications

(446 citation statements)

References 91 publications

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“…The most dominant taxa as hub microbes belong to bacterial phyla Proteobacteria (21 OTUs), Actinobacteria (12 OTUs) and fugal phyla Ascomycota (20 OTUs). This is consistent with the finding that Proteobacteria, Actinobacteria and Ascomycota are the most abundant phyla in plants and soil (24,64).…”

Section: Hub Microbessupporting

confidence: 92%

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Network mapping of root-microbe interactions inArabidopsis thaliana

Zhang

Jin

et al. 2020

Preprint

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Understanding how plants interact with their colonizing microbiota to determine plant phenotypes is a fundamental question in modern plant science. Existing approaches for genome-wide association studies (GWAS) are based on the association analysis between host genes and the abundance of individual microbes, failing to characterize the genetic architecture of microbial interactions that are thought to a determinant of microbiota structure, organization, and function. Here, we implement a behavioral model to quantify various patterns of microbe-microbe interactions, i.e., mutualism, antagonism, aggression, and altruism, and map host genes that modulate microbial networks constituted by these interaction types. We reanalyze a root-microbiome data involving 179 accessions of Arabidopsis thaliana and find that the four networks differ structurally in the pattern of bacterial-fungal interactions and microbiome complexity. We identify several fungus and bacterial hubs that play a central role in mediating microbial community assembly surrounding A. thaliana root systems. We detect 1142 significant host genetic variants throughout the plant genome and then implement Bayesian networks (BN) to reconstruct epistatic networks involving all significant SNPs and find 91 hub QTLs. Gene annotation shows that a number of the hub genes detected are biologically relevant, playing roles in plant growth and development, resilience against pathogens, root development, and improving resistance against abiotic stress conditions. The new model allows us to better understand the underlying mechanisms that govern the relationships between plants and their entire microbiota and harness soil microbes for plant production.

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Section: Hub Microbessupporting

confidence: 92%

“…It has been commonly recognized that the microbiota and their hosts form complex but well-orchestrated interaction networks (22,23). For example, the crop microbiome assembly is shaped by the host, even to a greater extent environmental factors (24).…”

Section: Introductionmentioning

confidence: 99%

Network mapping of root-microbe interactions inArabidopsis thaliana

Zhang

Jin

et al. 2020

Preprint

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“…Total DNA was extracted from the aforementioned samples using the FastDNA SPIN Kit for Soil (MP Biomedicals, Solon, USA) following manufacturer's instructions. The V5-V6 region of bacterial 16S rRNA gene (799F-1115R) [14,51], and the ITS2 region (fITS7-ITS4) of fungal ITS [16,52,53] were ampli ed ( Table S1). The primers sequence and PCR ampli cations were shown in Table S1.…”

Section: Dna Extraction and Ampli Cation Sequencingmentioning

confidence: 99%

Disease-induced Changes in Plant Microbiome Assembly and Functional Adaptation

Gao

Xiong

Gao

et al. 2020

Preprint

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Background: Plant microbiome is an integral part of the host influencing its growth and health. The increasing evidence indicates that plant rhizosphere may recruit beneficial microbes to suppress soil-borne pathogen, but the ecological mechanisms that govern plant microbiome assembly and functions under disease in both below and aboveground compartments are not fully understood. Here we examined both bacterial and fungal communities from soils (rhizosphere and bulk soil) and multiple plant compartments (e.g. root, stem, and fruit) of chili pepper (Capsicum annuum L.) at two pepper production sites, and explored how Fusarium wilt disease (FWD) affect the assembly, co-occurrence patterns, and ecological functions of plant-associated microbiomes. Results: Our data demonstrated that FWD had less impact on reproductive organ (fruit) than on vegetative organs (root and stem), with the strongest impact in the stem upper epidermis. Fungal intra-kingdom networks presented lower stabilities and their communities were more sensitive to FWD than the bacterial communities. Moreover, the diseased pepper was more susceptible to colonization by other pathogenic fungi, but they may recruit potential beneficial bacteria to facilitate host or offspring survival, and FWD may enhance the ecological importance of fungal taxa in the interkingdom network. Further, metagenomic analysis revealed that several potential protective functional genes encoding detoxify and biofilm formation were significantly enriched in the diseased pepper.Conclusion: Together, these results significantly advance our understanding of pepper microbiome assembly and functions under biotic stress. Our work highlights the diseased plant and the aboveground compartments harbor a potential of beneficial microbiomes and functions that, in concert, can provide potential critical data for harnessing the plant microbiome for sustainable agriculture.

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“…Moreover, we also found that members of Sordariomycetes (18.27-46.34%) were distributed mainly in root tissues, while Tremellomycetes (1.21-30.59%) were distributed mainly in leaves and stems. This differentiation of the fungi in above-and belowground tissues could possibly be the result of resource utilization, which drives the rapid evolutionary radiation of microbes competing for resources, causing them to diverge and adapt to different niches to reduce competition [18,65].…”

Section: Discussionmentioning

confidence: 99%

“…Several studies have documented the signi cant effects and selective pressure of host plants on endophytic fungal species and community composition [18][19][20][21][22]. For example, Yao et al [19] found that plant identity had a greater effect on endophytic fungal community composition than epiphytic fungi in the leaves of six mangrove species in South China, and Martínez-García et al [20] showed differences in the arbuscular mycorrhizal fungal communities under different shrubs in a semiarid environment.…”

Section: Introductionmentioning

confidence: 99%

Niche Differentiation and Co-Occurrence Network of Fungal Communities Associated with Host Affiliations in an Extremely Arid Desert Ecosystem

Zuo¹,

Li²,

Yang³

et al. 2020

Preprint

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Background: Desert shrubs represent high productivity and play essential roles in maintaining the biodiversity and stability of ecosystem functioning in arid desert ecosystems. These xerophytic plants provide specific biotic and abiotic conditions for the resident specialist microorganisms. However, a robust understanding of the structural composition of the fungal microbiome associated with desert plants and especially the relationship between above- and belowground communities is currently lacking. In this study, we examined the endophytic fungal communities associated with the root, stem, and leaf tissues of five desert shrubs using Illumina MiSeq sequencing of internal transcribed spacer 2 (ITS2) sequences.Results: A total of 337 operational taxonomic units (OTUs) of endophytic fungi were identified at a 97% sequence similarity level. Pleosporales were dominant and played an irreplaceable role as keystone species in maintaining the connectivity and complexity of the fungal networks. Desert shrub identity significantly affected the community composition of the endophytic fungi in different tissues. Compared with the fungi in the aboveground tissues, root-associated fungi represented the most abundant reservoir of biodiversity in the desert habitat and displayed significantly high tissue specificity. Interestingly, the aboveground stems and leaves showed higher taxonomic overlap with underground root tissues than with each other. The root fungal network revealed the highest connectivity, and the interspecies relationships between desert fungal OTUs revealed a high percentage of co-presence rather than mutual exclusion. In addition, members of Hypocreales played a central role in connecting the above- and belowground fungal networks.Conclusions: This study represents the first example of research revealing plant-fungus endophytic associations in an extremely arid desert ecosystem with the simultaneous consideration and comparison of above- and belowground niches. Understanding the complex host-microbe interactions associated with desert plants could provide a basis for the exploitation of plant-fungus associations in the manipulation of the shrub microbiome for ecological restoration purposes.

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Host selection shapes crop microbiome assembly and network complexity

Cited by 416 publications

References 91 publications

Network mapping of root-microbe interactions inArabidopsis thaliana

Network mapping of root-microbe interactions inArabidopsis thaliana

Disease-induced Changes in Plant Microbiome Assembly and Functional Adaptation

Niche Differentiation and Co-Occurrence Network of Fungal Communities Associated with Host Affiliations in an Extremely Arid Desert Ecosystem

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