Rice Blast Lesions: an Unexplored Phyllosphere Microhabitat for Novel Antagonistic Bacterial Species Against Magnaporthe oryzae

Sahu, Kuleshwar Prasad; Kumar, Aundy; Patel, Asharani; Kumar, Mukesh; Krishnan, Subbaiyan Gopala; Prakash, Ganesan; Rathour, Rajeev; Gogoi, Robin

doi:10.1007/s00248-020-01617-3

Cited by 38 publications

(27 citation statements)

References 50 publications

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“…Similarly, Arabidopsis thaliana genes governing SA-mediated defense and growth promotion were found up-regulated by P. putida BP25 [99] and Bacillus megaterium BP17 [100]{Vibhuti, 2017 #61; Akamatsu, 2013 #44}. Species belonging to Microbacterium and Stenotrophomonas have also been recently reported to elicit defense against rice blast disease [101]. Patel et al [102] recently reported the antifungal and defense elicitation activity by BVC belongs to pyrazine against the rice blast disease.…”

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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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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“…It was found that S. maltophilia lowered the mycelial growth of Colletotrichum nymphaeae by 60% [ 55 ]. For the antagonist Sphingobacterium multivorum , few studies have demonstrated its capabilities as BCAs [ 56 ]. Surprisingly, our study found that S. multivorum inhibited the mycelial growth of N. solani and reduced the DRR severity.…”

Section: Discussionmentioning

confidence: 99%

“…Surprisingly, our study found that S. multivorum inhibited the mycelial growth of N. solani and reduced the DRR severity. This bacterium was previously reported to have important antifungal effect against Magnaporthe oryzae , the causal agent of rice blast [ 56 ]. This bacterial species was also found effective in degrading hexaconazole, thereby presenting a sustainable microbial bioremediation of persistent organic pollutants [ 57 ].…”

Section: Discussionmentioning

confidence: 99%

Potential Role of Rhizobacteria Isolated from Citrus Rhizosphere for Biological Control of Citrus Dry Root Rot

Ezrari

Mhidra

Radouane

et al. 2021

Plants

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Citrus trees face threats from several diseases that affect its production, in particular dry root rot (DRR). DRR is a multifactorial disease mainly attributed to Neocosmospora (Fusarium) solani and other several species of Neocosmospora and Fusarium spp. Nowadays, biological control holds a promising control strategy that showed its great potential as a reliable eco-friendly method for managing DRR disease. In the present study, antagonist rhizobacteria isolates were screened based on in vitro dual culture bioassay with N. solani. Out of 210 bacterial isolates collected from citrus rhizosphere, twenty isolates were selected and identified to the species level based on the 16S rRNA gene. Molecular identification based on 16S rRNA gene revealed nine species belonging to Bacillus, Stenotrophomonas, and Sphingobacterium genus. In addition, their possible mechanisms involved in biocontrol and plant growth promoting traits were also investigated. Results showed that pectinase, cellulose, and chitinase were produced by eighteen, sixteen, and eight bacterial isolates, respectively. All twenty isolates were able to produce amylase and protease, only four isolates produced hydrogen cyanide, fourteen isolates have solubilized tricalcium phosphate, and ten had the ability to produce indole-3-acetic acid (IAA). Surprisingly, antagonist bacteria differed substantially in their ability to produce antimicrobial substances such as bacillomycin (five isolates), iturin (ten isolates), fengycin (six isolates), surfactin (fourteen isolates), and bacteriocin (subtilosin A (six isolates)). Regarding the PGPR capabilities, an increase in the growth of the bacterial treated canola plants, used as a model plant, was observed. Interestingly, both bacterial isolates Bacillus subtilis K4-4 and GH3-8 appear to be more promising as biocontrol agents, since they completely suppressed the disease in greenhouse trials. Moreover, these antagonist bacteria could be used as bio-fertilizer for sustainable agriculture.

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“…Microbiomes can reinforce the defensive capabilities of plants by interrupting the plant-pathogen interactions, which subsequently improve the disease resilience in plants [89]. Bacterial antagonists belonging to Achromobacter, Comamonas, Curtobacterium, Enterobacter, Leclercia, Microbacterium, Pantoea, Sphingobacterium, and Stenotrophomonas genera showed tremendous biocontrol potential against M. oryzae and triggered the expression of defense genes, such as OsCEBiP, OsCERK1, OsEDS1, and OsPAD4, in rice seedlings against rice blast disease [162]. Similarly, root-associated Pseudomonas sp.…”

Section: Roles In Activation Of Plant Immune Responsementioning

confidence: 99%

Plant–Microbiome Crosstalk: Dawning from Composition and Assembly of Microbial Community to Improvement of Disease Resilience in Plants

Noman

Ahmed

Ijaz

et al. 2021

IJMS

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Plants host diverse but taxonomically structured communities of microorganisms, called microbiome, which colonize various parts of host plants. Plant-associated microbial communities have been shown to confer multiple beneficial advantages to their host plants, such as nutrient acquisition, growth promotion, pathogen resistance, and environmental stress tolerance. Systematic studies have provided new insights into the economically and ecologically important microbial communities as hubs of core microbiota and revealed their beneficial impacts on the host plants. Microbiome engineering, which can improve the functional capabilities of native microbial species under challenging agricultural ambiance, is an emerging biotechnological strategy to improve crop yield and resilience against variety of environmental constraints of both biotic and abiotic nature. This review highlights the importance of indigenous microbial communities in improving plant health under pathogen-induced stress. Moreover, the potential solutions leading towards commercialization of proficient bioformulations for sustainable and improved crop production are also described.

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Rice Blast Lesions: an Unexplored Phyllosphere Microhabitat for Novel Antagonistic Bacterial Species Against Magnaporthe oryzae

Cited by 38 publications

References 50 publications

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

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

Potential Role of Rhizobacteria Isolated from Citrus Rhizosphere for Biological Control of Citrus Dry Root Rot

Plant–Microbiome Crosstalk: Dawning from Composition and Assembly of Microbial Community to Improvement of Disease Resilience in Plants

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