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Identification and characterization of early Fusarium wilt responsive mRNAs and long non-coding RNAs in banana root using high-throughput sequencing.

ABSTRACT: Fusarium wilt disease, caused by Fusarium oxysporum f.sp. cubense (Foc), has been recognized as the most devastating disease to banana. The regulatory role of long non-coding RNAs (lncRNAs) in plant defense has been verified in many plant species. However, the understanding of their role during early FocTR4 (Foc tropical race 4) infection stage is very limited. In this study, lncRNA sequencing was used to reveal banana root transcriptome profile changes during early FocTR4 infection stages. Quantitative real time PCR (qRT-PCR) was performed to confirm the expression of eight differentially expressed (DE) lncRNAs (DELs) and their predicted target genes (DETs), and three DE genes (DEGs). Totally, 12,109 lncRNAs, 36,519 mRNAs and 2642 novel genes were obtained, of which 1398 (including 78 DELs, 1220 DE known genes and 100 DE novel genes) were identified as FocTR4 responsive DE transcripts. Gene function analysis revealed that most DEGs were involved in biosynthesis of secondary metabolites, plant-pathogen interaction, plant hormone signal transduction, phenylalanine metabolism, phenylpropanoid biosynthesis, alpha-linolenic acid metabolism and so on. Coincidently, many DETs have been identified as DEGs in previous transcriptome studies. Moreover, many DETs were found to be involved in ribosome, oxidative phosphorylation, lipoic acid metabolism, ubiquitin mediated proteolysis, N-glycan biosynthesis, protein processing in endoplasmic reticulum and DNA damage response pathways. QRT-PCR result showed the expression patterns of the selected transcripts were mostly consistent with our lncRNA sequencing data. Our present study showed the regulatory role of lncRNAs on known biotic and abiotic stress responsive genes and some new-found FocTR4 responsive genes, which can provide new insights into FocTR4-induced changes in the banana root transcriptome during the early pathogen infection stage.

SUBMITTER: Cheng C

PROVIDER: S-EPMC8358008 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Members of the microbiotas colonizing the plant endophytic compartments and the surrounding bulk and rhizosphere soil play an important role in determining plant health. However, the relative contributions of the soil and endophytic microbiomes and their mechanistic roles in achieving disease suppression remain elusive. To disentangle the relative importance of the different microbiomes in the various plant compartments in inhibiting pathogen infection, we conducted a field experiment to track changes in the composition of microbial communities in bulk and rhizosphere soil and of root endophytes and leaf endosphere collected from bananas planted on Fusarium-infested orchards in disease-suppressive and disease-conducive soils. We found that the rhizosphere and roots were the two dominant plant parts whose bacterial communities contributed to pathogen suppression. We further observed that Pseudomonas was potentially a key organism acting as a pathogen antagonist, as illustrated by microbial community composition and network analysis. Subsequently, culturable pathogen-antagonistic Pseudomonas strains were isolated, and their potential suppressive functions or possible antibiosis in terms of auxin or siderophore synthesis and phosphate solubilization were screened to analyze the mode of action of candidate disease-suppressive Pseudomonas strains. In a follow-up in vivo and greenhouse experiment, we revealed that microbial consortia of culturable Pseudomonas strains P8 and S25 (or S36), isolated from banana plantlet rhizosphere and roots, respectively, significantly suppressed the survival of pathogens in the soil, manipulated the soil microbiome, and stimulated indigenous beneficial microbes. Overall, our study demonstrated that root-associated microbiomes, especially the antagonistic Pseudomonas sp. components, contribute markedly to soil suppression of banana Fusarium wilt. IMPORTANCE Soil suppression of Fusarium wilt disease has been proven to be linked with the local microbial community. However, the contribution of endophytic microbes to disease suppression in wilt-suppressive soils remains unclear. Moreover, the key microbes involving in Fusarium wilt-suppressive soils and in the endophytic populations have not been fully characterized. In this study, we demonstrate that root-associated microbes play vitally important roles in disease suppression. Root-associated Pseudomonas consortia were recognized as a key component in inhibiting pathogen abundance associated with the host banana plants. This finding is crucial to developing alternate strategies for soilborne disease management by harnessing the plant microbiome.

Project description:BackgroundPlant microbiome highlights the importance of endosphere microbiome for growth and health of the host plant. Microbial community analysis represents an elegant way to identify keystone microbial species that have a more central position in the community. The aim of this study was to access the interactions between the keystone bacterial species and plants during banana Fusarium wilt process, by comparing the endophytic bacterial and fungal community in banana roots and shoot tips during growth and wilting processes. The keystone bacterial species were isolated and further engineered to improve banana wilt resistance.ResultsBanana endosphere microbiome structure varied during plant growth and wilting processes. Bacterial and fungal diversity in the shoot tips and roots increased with the development of the banana plantlets. The bacterial groups belonging to the Enterobacteriaceae family with different relative abundances were detected in all the samples. The Klebsiella spp. might be the keystone bacteria during the growth of banana plantlets. The relative abundance of Fusarium associated with the wilt disease did not increase during the wilting process. The endophytic Enterobacteriaceae strains Enterobacter sp. E5, Kosakonia sp. S1, and Klebsiella sp. Kb were isolated on Enterobacteriaceae selective medium and further engineered by expressing 1-aminocyclopropane-1-carboxylate (ACC) deaminase on the bacterial cell walls (designated as E5P, S1P, and KbP, respectively). Pot experiments suggested that plants inoculated with strains E5, E5P, S1, and S1P increased resistance to the Fusarium wilt disease compared with the controls without inoculation, whereas the Klebsiella inoculation (Kb and KbP) did not increase the wilt resistance. Compared with the inoculation with the wild strains E5 and S1, the inoculation with engineered strains E5P and S1P significantly increased wilt resistance and promoted plant growth, respectively. The results illustrated that the keystone species in the banana microbiome may not be dominant in numbers and the functional role of keystone species should be involved in the wilt resistance.ConclusionThe ACC deaminase activity of engineered bacteria was essential to the Fusarium wilt resistance and growth promotion of banana plants. Engineering keystone bacteria in plant microbiome with ACC deaminase on the cell walls should be a promising method to improve plant growth and disease resistance.

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Project description:Fusarium is one of the most important fungal genera of plant pathogens that affect the cultivation of a wide range of crops. Agricultural losses caused by Fusariumoxysporumf.sp.cubense (Foc) directly affect the income, subsistence, and nourishment of thousands of farmers worldwide. For Viet Nam, predictions on the impact of Foc for the future are dramatic, with an estimated loss in the banana production area of 8% within the next five years and up to 71% within the next 25 years. In the current study, we applied a combined morphological-molecular approach to assess the taxonomic identity and phylogenetic position of the different Foc isolates collected in northern Viet Nam. In addition, we aimed to estimate the proportion of the different Fusarium races infecting bananas in northern Viet Nam. The morphology of the isolates was investigated by growing the collected Fusarium isolates on four distinct nutritious media (PDA, SNA, CLA, and OMA). Molecular phylogenetic relationships were inferred by sequencing partial rpb1, rpb2, and tef1a genes and adding the obtained sequences into a phylogenetic framework. Molecular characterization shows that c. 74% of the Fusarium isolates obtained from infected banana pseudostem tissue belong to F.tardichlamydosporum. Compared to F.tardichlamydosporum, F.odoratissimum accounts for c.10% of the Fusarium wilt in northern Viet Nam, demonstrating that Foc TR4 is not yet a dominant strain in the region. Fusariumcugenangense - considered to cause Race 2 infections among bananas - is only found in c. 10% of the tissue material that was obtained from infected Vietnamese bananas. Additionally, one of the isolates cultured from diseased bananas was phylogenetically not positioned within the F.oxysporum species complex (FOSC), but in contrast, fell within the Fusariumfujikuroi species complex (FFSC). As a result, a possible new pathogen for bananas may have been found. Besides being present on several ABB 'Tay banana', F.tardichlamydosporum was also derived from infected tissue of a wild Musalutea, showing the importance of wild bananas as a possible sink for Foc.

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Identification and characterization of early Fusarium wilt responsive mRNAs and long non-coding RNAs in banana root using high-throughput sequencing.

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