A plant genetic network for preventing dysbiosis in the phyllosphere

Chen, Tao; Nomura, Kinya; Wang, Xiaolin; Sohrabi, Reza; Xu, Jin; Yao, Lishuang; Paasch, Bradley C.; Ma, Li; Kremer, James M.; Cheng, Yuti; Zhang, Li; Wang, Nian; Wang, Ertao; Xin, Xiu-Fang; He, Sheng Yang

doi:10.1038/s41586-020-2185-0

Cited by 326 publications

(286 citation statements)

References 51 publications

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“…2, 8). This result is similar to recent studies indicating that dysbiosis of endophytic microbiome in the phyllosphere caused the leaves to exhibit non-pathogenic symptoms of the disease [28], suggesting that the structure of the endophytic microbiome could play a key role in maintaining plant health. However, how diseases mediated by pathogenic invasions are related to dysbiosis of the endophytic microbiome remains to be further studied.…”

Section: Discussionsupporting

confidence: 91%

Phyllosphere Microbiome in Response to Citrus Melanose

Li¹,

Xu²,

Wang³

et al. 2020

Preprint

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Background: Like microbiomes in the rhizosphere, phyllosphere microbiomes can have an important role in plant growth and health. However, whether and how the phyllosphere microbiomes respond to the invasion of pathogens is not well understood. In this study, we address this question using the citrus phyllosphere-associated microbiome as a model.Results: Through DNA metabarcoding (16S for bacteria and ITS for fungi) and shotgun metagenomic sequencing, we found that phyllosphere microbiomes in different ecological habitats (epiphytes and endophytes) responded differently to melanose disease caused by the fungal pathogen Diaporthe citri on citrus (Citrus unshiu) leaves. We observed that citrus phyllosphere-associated microbiome responded to the melanose disease in five ways: (1) increasing microbial richness; (2) reducing community evenness; (3) enriching selected microbes; (4) enhancing microbial interactions; and (5) enriching functional features involved in metabolism and fungal cell wall degrading.Conclusions: Our study revealed how phyllosphere microbiomes in the epiphytic and endophytic habitats differ between diseased and healthy leaves. Based on the differences at both the taxonomic and functional levels, we propose a general conceptual paradigm to describe the different microbial community assembly processes for the phyllosphere microbiome in response to leaf disease and how such processes impact plant health. Our results provide novel insights for understanding the contributions of the phyllosphere microbial community response during pathogen invasion.

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Section: Discussionsupporting

confidence: 91%

Phyllosphere Microbiome in Response to Citrus Melanose

Li¹,

Xu²,

Wang³

et al. 2020

Preprint

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“…Plant adapt to drought by manipulating aboveground-belowground feedbacks between plants and soil microbiota [19]. The aboveground tissue is functionally distinct from the belowground tissue [47]. Plant tness responses to drought were governed by rapid changes in belowground microbial communities [19].…”

Section: Microbiota Communities Resident In Above-and Belowground Tismentioning

confidence: 99%

Microbiota community assembly in wild rice (Oryza longistaminata) in response to drought stress shows phylogenetic conservation, stochasticity, and aboveground-belowground patterns

Ding

Peng

Chen

et al. 2020

Preprint

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Abstract Background Drought is a global environmental stress that limits crop yields. Microbial communities control many biogeochemical processes, and a predictive understanding of how crop microbial communities assemble in response to drought stress is central to addressing the challenges caused by drought. Little is known about the microbiome assembly processes in rice-ecosystems, particularly with regard to their environmental adaptation. Wild rice may serve as a source of superior drought tolerance candidate for rice breeding. There is an urgent need to explore wild rice resistance mechanisms to drought stress. Here, we evaluated the effect of drought stress on the microbial community recruitment and assembly in the endosphere (leaf, stem, and root) and rhizosphere of Oryza longistaminata. Results Species replacement was the dominant process shaping microbial community composition under drought stress. O. longistaminata recruited the phyla Actinobacteria and Fusobacteria, the genus Streptomyces, and phototrophic prokaryotes to improve its fitness. The host exerted strong effects on microbiome assembly, and the responses of the microbial community structure to the drought environment showed above- and belowground patterns. Drought reduced taxonomic α-diversity and destabilized co-occurrence network properties in the leaves and stems, but not in the roots and rhizosphere. Drought promoted the restructuring and strengthening of belowground network links to more strongly interconnect network properties. The drought response of the microbiome was phylogenetically conserved. Stochastic (neutral) processes acted on microbial community reassembly in response to drought stress across all four compartments. Conclusions Our results provide new insight into the mechanisms through which drought alters microbial community assembly in drought-tolerant wild rice and reveal a potential strategy for manipulating plant microbiomes to improve crop fitness.

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“…To design PCR primers that speci cally amplify the bacterial 16S, sequence alignment was performed using plant Mt18S and Ct16S and bacterial 16S. Because plant bacterial microbiota is mainly composed of Proteobacteria, Actinobacteria, Bacteroidetes and Firmicutes [19,29,39,40], we selected 33 species from these four phyla ( Fig. S1A) and aligned the corresponding 16S with Mt18S and Ct16S of several plants, including O. sativa, A. thaliana, and Zea mays.…”

Section: Primer Design and In Silico Evaluation Of Primer Coveragementioning

confidence: 99%

“…However, this non-culture method is still not suitable for analyses of the plant endo-bacteriome because of the high sequence identity among bacterial 16S, plant Mt18S and Ct16S sequences. In a few previous studies, bacterial cells have been enriched from plant tissues by washing and vortexing [16,17] or the host DNA has been ltered out from the sequencing results [12,[18][19][20][21]. However, the former approach inevitably leads to an incomplete collection of endophytes, and the latter results in limited sequencing depth and low coverage of bacterial communities.…”

Section: Introductionmentioning

confidence: 99%

“…As a result, PCR ampli cation with these primers resulted in co-ampli cation of high-proportion plant DNAs. The most commonly used primer pair for plant-associated microbiota is 799F/1193R that ampli es the 16S V 5 -V 7 regions [15,19,28,29]. This primer pair is e cient in producing Ct16S-free amplicons and excludes Mt18S via removal of the ~ 350 bp-longer amplicons produced from most plants [15,28,30].…”

Section: Introductionmentioning

confidence: 99%

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Quantitative and Qualitative Characterization of Plant Endo-bacteriome by Plant Dna-free Sequencing Method

Zhang¹,

Chen²,

Zhang³

et al. 2020

Preprint

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Background: Plant endophytic bacteria colonize plants’ internal tissues and interact with plants more closely than do epiphytic or environmental bacteria. However, the community structure of such endophytic bacteria could not be efficiently deciphered, and the microbiota abundance could not be quantified through absolute quantification. Application of 16S rRNA gene sequencing to characterize the plant endophytic community is greatly hindered by the high sequence identities among bacterial 16S rRNA, plant mitochondrial 18S rRNA and chloroplast 16S rRNA genes. This makes it difficult to identify bacterial sequences among total DNAs extracted from plant material.Results: We designed PCR primer sets that are able to specifically amplify bacterial DNAs, even when there are very few bacteria colonizing the plant material. We computationally and experimentally evaluated the specificity, coverage, and accuracy of the newly designed primer sets (322F/796R and 799F/1107R) and two widely used primer sets (338F/806R and 799F/1193R). When applied to a same planting-soil community through next generation sequencing (NGS), the four different primer sets revealed similar high-abundant taxa composition with variation in taxa abundance. Primer sets amplifying the same 16S variable regions generated more comparable sequencing results. When applied to a rice endo-bacteriome, both 799F/1107R and modified 322F-Dr/796Rs (Primer pair 322F/796R with a penultimate-base substitution in 322F) produced plant DNA-free bacterial amplicon libraries. Primer 322F-A/796R was then used through NGS to decipher the rice endo-bacteriomes. The rice root and leaf endo-bacteriomes shared 66.36% OTU identity but enriched different bacterial species. Within the same host genotype and soil type, the root endo-bacteriome was more stable than the leaf endo-bacteriome across individual plants. 322F-A/796R was used through absolute quantitative PCR to quantitate the population size of leaf or root endophytes, which revealed 106–107 and 109–1010 bacteria per gram fresh weight, respectively.Conclusions: This is the first study to develop plant DNA-free bacterial 16S amplification methods. The newly designed primer sets combined with NGS deciphered the rice endo-bacteriome structure, and absolute quantitative PCR quantitated the size of the endobacterial population. The protocols developed here are suitable for various plants, will significantly advance studies on plant endo-bacteriomes.

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A plant genetic network for preventing dysbiosis in the phyllosphere

Cited by 326 publications

References 51 publications

Phyllosphere Microbiome in Response to Citrus Melanose

Phyllosphere Microbiome in Response to Citrus Melanose

Microbiota community assembly in wild rice (Oryza longistaminata) in response to drought stress shows phylogenetic conservation, stochasticity, and aboveground-belowground patterns

Quantitative and Qualitative Characterization of Plant Endo-bacteriome by Plant Dna-free Sequencing Method

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