The Rice Leaf Microbiome Has a Conserved Community Structure Controlled by Complex Host-Microbe Interactions

Román-Reyna, Verónica; Pinili, Dale; Borjaa, Frances Nikki; Quibod, Ian Lorenzo; Groen, Simon C.; Mulyaningsih, Enung Sri; Rachmat, Agus; Slamet‐Loedin, Inez H.; Alexandrov, Nickolai N.; Mauleon, Ramil; Oliva, Ricardo

doi:10.2139/ssrn.3382544

Cited by 25 publications

(23 citation statements)

References 63 publications

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“…The effects of geographical locations have been reported in microbial communities residing in rhizosphere/root endosphere [5] and phyllosphere [51]. However, which factors shape seed microbial communities are controversial.…”

Section: Discussionmentioning

confidence: 99%

Domestication of Oryza species eco-evolutionarily shapes bacterial and fungal communities in rice seed

et al. 2020

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Background: Plant-associated microbiomes, which are shaped by host and environmental factors, support their hosts by providing nutrients and attenuating abiotic and biotic stresses. Although host genetic factors involved in plant growth and immunity are known to shape compositions of microbial communities, the effects of host evolution on microbial communities are not well understood. Results: We show evidence that both host speciation and domestication shape seed bacterial and fungal community structures. Genome types of rice contributed to compositional variations of both communities, showing a significant phylosymbiosis with microbial composition. Following the domestication, abundance inequality of bacterial and fungal communities also commonly increased. However, composition of bacterial community was relatively conserved, whereas fungal membership was dramatically changed. These domestication effects were further corroborated when analyzed by a random forest model. With these changes, hub taxa of inter-kingdom networks were also shifted from fungi to bacteria by domestication. Furthermore, maternal inheritance of microbiota was revealed as a major path of microbial transmission across generations. Conclusions: Our findings show that evolutionary processes stochastically affect overall composition of microbial communities, whereas dramatic changes in environments during domestication contribute to assembly of microbiotas in deterministic ways in rice seed. This study further provides new insights on host evolution and microbiome, the starting point of the holobiome of plants, microbial communities, and surrounding environments. Background The evolution of life on Earth is driven by natural selection, biased mutation, genetic drift, genetic hitchhiking, and gene flow. Regardless of plants, animals, or microorganisms, it has been ongoing for millions of years. Unlike the majority of organisms, crop plants have undergone a distinct evolutionary process called domestication. Plant domestication began~12,000 years ago and 353 food crop plants including rice, wheat, barley, potato, and tomato have undergone domestication [1]. Most crop plants have been selected and been bred for better yield and quality by anthropogenic intervention. In rice, the evolution spans about 15 million years [2]. In the genus Oryza, there are 22 wild relatives which are distributed in Asia, Africa, Australia, and America (Fig. 1). Polyploidization and other evolutionary events contribute to speciation of Oryza species [3]. With the speciation, 8000-9000 years ago, O. sativa subsp. japonica, O. sativa subsp. indica, and O. glaberrima were domesticated from the wild relatives, O. rufipogon, O. nivara, and O. barthii, respectively [2]. These domesticated rice species have been further diversified by breeding to acquire desirable agronomic traits. The phenotypes of the humans, animals, and plants are determined not only by their own genetic makeups but by their associated microbial communities. Hostassociated microbial communities show signi...

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Section: Discussionmentioning

confidence: 99%

Domestication of Oryza species eco-evolutionarily shapes bacterial and fungal communities in rice seed

et al. 2020

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“…Members belong to phyla such as Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes were found consistently on phyllosphere of both the resistant and susceptible genotypes grown Mountain and Island zones; dominance phylum -Proteobacteria on phyllosphere is reported by many workers [64][65][66]. Recently, Roman-Reyna et al [67] found region-speci c microbial hubs belonging to diverse bacterial families in rice after studying 3024 accessions. Families such as Bacillaceae, Comamonadaceae, Enterobacteriaceae, Enterococcaceae, Kineosporiaceae, Methylobacteriaceae, Microbacteriaceae, Micrococcaceae, Moraxellaceae, Nocardiaceae, Paenibacillaceae, Pseudoalteromonadaceae, Pseudomonadaceae, Rhizobiaceae, Sphingomona -daceae, and Xanthomonadaceae contributed genera such as Acinetobacter, Arthrobacter, Bacillus, Curtobacterium, Enterobacter, Exiguobacterium, Kineococcus, Methylobacterium, Microbacterium, Paenibacillus, Pantoea, Pseudoalteromonas, Pseudomonas, Rhodococcus and Sphingomonas on the phyllosphere of both the genotypes in both the contrasting agro-climatic zones indicating their speci c association with rice plant; they may represent core phyllomicrobiome of rice.…”

Section: Discussionmentioning

confidence: 86%

“…The impact of disease resistance conferring-gene (R-gene) introgression in cultivated crops on phyllomicrobiome composition and assemblage is recently reported [67]. The rice line IR24 introgressed with Xa4 gene conferring resistance to bacterial blight caused by Xanthomonas oryzae pv.…”

Section: Discussionmentioning

confidence: 99%

Deciphering Core-Phyllomicrobiome of Rice Genotypes Grown in Contrasting Mountain and Island Agroclimatic Zones: Implications for Microbiome Engineering Against Blast Disease

Sahu

Kumar

Krishnan³

et al. 2021

Preprint

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Background The fundamental role and contributions of phyllosphere habitat in shaping plant functional ecology are poorly investigated, and often underestimated. Phyllosphere -the harsh and dynamic foliar-photosynthetic-habitat is continuously exposed to vagaries of changing weather events during the entire plant life. With its adapted microbiota, the phyllosphere-niche brings microbial diversity to the plant-holobiont pool and potentially modulates a multitude of plant and agronomic traits. The phyllomicrobiome structure and the consequent ecological functions are vulnerable to a host of biotic (Genotypes) and abiotic-factors (Environment) which is further compounded by agronomic-transactions on domesticated agricultural crops. However, the ecological forces driving the phyllomicrobiome assemblage and functions are among the most under-studied aspects of plant biology. Despite the reports on the occurrence of diverse prokaryotic phyla such as Proteobacteria, Firmicutes, Bacteroides, and Actinobacteria on phyllosphere habitat, the functional characterization leading to their utilization for agricultural sustainability is not yet adequately explored.Currently, the metagenomic-Next-Generation-Sequencing (mNGS) technique scanning the conserved V3-V4 region of ribosomal RNA gene is a widely adopted strategy for microbiome-investigations. However, the structural and functional validation of mNGS annotations by microbiological methods is not integrated into the microbiome exploration-programs. In the present study, we combined the high throughput mNGS approach with conventional microbiological methods to decipher the core-functional-phyllomicrobiome of contrasting rice genotypes varying in their response to blast disease grown in contrasting agroclimatic zones in India. We, further, scanned the rice phyllosphere by electron microscopy to show the microbial communities on leaf. Magnaporthe oryzae -the phyllosphere pathogen inciting necrotic lesion on cereal crops is managed by the deployment of ‘non-durable’ blast resistance genes and ‘toxic’ fungicidal molecules. Nowadays, there is a growing consensus for devising an alternative strategy for mitigating blast owing to a recent ban on the use of most commonly used fungicidal molecule, tricyclazole. In the present work, we further identified phyllosphere- core-functional microbial groups leading to the proposal of phyllomicrobiome assisted rice blast management strategy. Multi-pronged activities of phyllomicrobiome against Magnaporthe oryzae (antifungal activity), rice innate immunity (defense elicitation), and rice blast disease (disease suppression) have been elaborated for effective management of blast by phyllomicrobiome re-engineering. ResultsRice phyllomicrobiome of tropical “Island-Zone” displayed marginally more bacterial community diversity than that of temperate ‘Mountain-Zone’. Principal coordinate analysis based on Bray Curtis and ANoSIM method indicated nearly converging-phyllomicrobiome profiles on two contrasting rice genotypes grown in the same agroclimatic zone. However, the rice genotype grown in the contrasting Mountain-zone and Island-zone displayed diverse-phyllomicrobiome profiles indicating a strong influence of environmental factors rather than the genotype on phyllomicrobiome structure and assembly. The predominance of Phyla such as Proteobacteria, Actinobacteria, and Firmicutes was observed on the rice phyllosphere irrespective of the genotypes and environmental conditions. The core-microbiome analysis showed multi-microbiota-core consisting of Acidovorax, Arthrobacter, Bacillus, Clavibacter, Clostridium, Cronobacter, Curtobacterium, Deinococcus, Erwinia, Exiguobacterium, Hymenobacter, Kineococcus, Klebsiella, Methylobacterium, Methylocella, Microbacterium, Nocardioides, Pantoea, Pedobacter, Pseudomonas, Salmonella, Serratia, Sphingomonas and Streptomyces on phyllosphere of rice genotypes grown in contrasting agroclimatic zones. The linear discriminant analysis (LDA) effect size (LEfSe) method revealed ten and two distinct bacterial genera in blast-resistant and -susceptible genotypes, respectively. The analysis further indicated 15 and 16 climate-zone specific bacterial genera for Mountain and Island zone, respectively. SparCC based network analysis of phyllomicrobiome showed hundreds of complex intra-microbial cooperative or competitive interactions on the rice genotypes and agroclimatic zones. Our microbiological validation of mNGS data further confirmed the presence of resident Acinetobacter, Aureimonas, Curtobacterium, Enterobacter, Exiguobacterium, Microbacterium, Pantoea, Pseudomonas, and Sphingomonas on the rice phyllosphere. Strikingly, the two contrasting agroclimatic zones displayed genetically identical bacterial isolates on the phyllosphere that could be attributed to the spatio-temporal transmission of core-phyllomicrobiome, perhaps, aided by rice seeds. A total of 59 distinct bacterial isolates were obtained, identified, and evaluated for their functional attributes on Magnaporthe oryzae and rice plant. The phyllomicrobiome associated core-bacterial communities showed secreted-metabolite and volatile-compound mediated antifungal activity on M. oryzae. Upon phyllobacterization (a term coined for spraying of bacterial cells on the phyllosphere), the core bacterial species such as Acinetobacter baumannii, Aureimonas sp., Pantoea ananatis, P. eucrina, and Pseudomonas putida elicited plant defense and contributed significantly to blast disease suppression. Transcriptional analysis by qPCR indicated induction of rice innate immunity associated genes such as OsPR1.1, OsNPR1, OsPDF2.2, OsFMO, OsPAD4, OsCEBiP, and OsCERK1 in phyllobacterized rice seedlings. ConclusionsThe rice genotypes growing in a particular agroclimatic zone showed a convergent phyllomicrobiome assemblage and composition. Conversely, diverging phyllomicrobiome assembly was observed on rice genotype cultivated in the contrasting agroclimatic zones. Agroclimatic zones and the associated climatic-factors rather than plant-genotypes per se appeared to drive phyllomicrobiome structure and composition on the rice genotypes. Our integrated mNGS method and microbiological validation divulged Acinetobacter, Aureimonas, Curtobacterium, Enterobacter, Exiguobacterium, Microbacterium, Pantoea, Pseudomonas, and Sphingomonas as core phyllomicrobiome of rice. Genetically identical bacterial communities belonging to Pantoea intercepted on the phyllosphere of rice grown in the two contrasting agroclimatic zones are suggestive of spatio-temporal transmission of phyllomicrobiome aided by seed. The core-microbiome mediated phyllobacterization showed potential for blast disease suppression by direct-antibiosis and defense elicitation. The identification of phyllosphere adapted functional core-bacterial communities in our study and their co-occurrence dynamics presents an opportunity to devise novel strategies for rice blast management through phyllomicrobiome reengineering in the future.

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“…In addition, secretion of endo‐1,4‐β‐ d ‐glucanase/cellulase is an important characteristic for virulence and survival in Xoo (Figure ) as it has been observed as a common feature in all plant pathogens (Sun et al , ; Rajeshwari et al , ). Substantiating this, a recent study characterizing the rice leaf microbiome indicated a major role of cellulose in facilitating plant–microbiome interactions at the leaf interface (Roman‐reyna et al , ).…”

Section: Resultsmentioning

confidence: 95%

Genome‐scale metabolic reconstruction and in silico analysis of the rice leaf blight pathogen, Xanthomonas oryzae

Koduru

Kim

Mohanty

et al. 2020

Molecular Plant Pathology

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Xanthomonas oryzae pv. oryzae (Xoo) is a vascular pathogen that causes leaf blight in rice, leading to severe yield losses. Since the usage of chemical control methods has not been very promising for the future disease management, it is of high importance to systematically gain new insights about Xoo virulence and pathogenesis, and devise effective strategies to combat the rice disease. To do this, we reconstructed a genome‐scale metabolic model of Xoo (iXOO673) and validated the model predictions using culture experiments. Comparison of the metabolic architecture of Xoo and other plant pathogens indicated that the Entner–Doudoroff pathway is a more common feature in these bacteria than previously thought, while suggesting some of the unique virulence mechanisms related to Xoo metabolism. Subsequent constraint‐based flux analysis allowed us to show that Xoo modulates fluxes through gluconeogenesis, glycogen biosynthesis, and degradation pathways, thereby exacerbating the leaf blight in rice exposed to nitrogenous fertilizers, which is remarkably consistent with published experimental literature. Moreover, model‐based interrogation of transcriptomic data revealed the metabolic components under the diffusible signal factor regulon that are crucial for virulence and survival in Xoo. Finally, we identified promising antibacterial targets for the control of leaf blight in rice by using gene essentiality analysis.

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The Rice Leaf Microbiome Has a Conserved Community Structure Controlled by Complex Host-Microbe Interactions

Cited by 25 publications

References 63 publications

Domestication of Oryza species eco-evolutionarily shapes bacterial and fungal communities in rice seed

Domestication of Oryza species eco-evolutionarily shapes bacterial and fungal communities in rice seed

Deciphering Core-Phyllomicrobiome of Rice Genotypes Grown in Contrasting Mountain and Island Agroclimatic Zones: Implications for Microbiome Engineering Against Blast Disease

Genome‐scale metabolic reconstruction and in silico analysis of the rice leaf blight pathogen, Xanthomonas oryzae

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