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Identification and characterization of miRNA169 family members in banana (Musa acuminata L.) that respond to fusarium oxysporum f. sp. cubense infection in banana cultivars.

ABSTRACT: MicroRNAs (miRNAs) play an important role in plant resistance to pathogen infections. However, little is known about the role of miRNAs in banana Fusarium wilt, which is the most economically devastating disease in banana production. In the present study, we identified and characterized a total of 18 miR169 family members in banana (Musa acuminata L.) based on small RNA sequencing. The banana miR169 family clustered into two groups based on miRNA evolutionary analysis. Multiple sequence alignment indicated a high degree of sequence conservation in miRNA169 family members across 28 plant species. Computational target prediction algorithms were used to identify 25 targets of miR169 family members in banana. These targets were enriched in various metabolic pathways that include the following molecules: glycine, serine, threonine, pentose, glycerolipids, nucleotide sugars, starch, and sucrose. Through miRNA transcriptomic analysis, we found that ma-miR169a and ma-miR169b displayed high expression levels, whereas the other 16 ma-miR169 members exhibited low expression in the HG and Baxi banana cultivars. Further experiments indicate that there were negative relationships between ma-miR169a, ma-miR169b and their targets basing on their expression levels to Foc4 (Fusarium oxysporum f. sp. cubense tropical race 4) infection in resistant cultivars. But they were low expressed in susceptive cultivars. These results suggested that the expression levels of ma-miR169a and ma-miR169b were consistent with the resistance degree of the banana cultivars to Foc4. The analysis presented here constitutes a starting point to understand ma-miR169-mediated Fusarium wilt resistance at the transcriptional level in banana and predicts possible candidate targets for the genetic improvement of banana resistance to Foc4.

SUBMITTER: Song S

PROVIDER: S-EPMC6305118 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Identification and characterization of miRNA169 family members in banana (Musa acuminata L.) that respond to fusarium oxysporum f. sp. cubense infection in banana cultivars.

Song Shun S Xu Yi Y Huang Dongmei D Ashraf Muhammad Aleem MA Li Jingyang J Hu Wei W Jin Zhiqiang Z Zeng Changying C Tang Fenling F Xu Biyu B Zeng Huicai H Li Yujia Y Xie Jianghui J

PeerJ 20181221

MicroRNAs (miRNAs) play an important role in plant resistance to pathogen infections. However, little is known about the role of miRNAs in banana Fusarium wilt, which is the most economically devastating disease in banana production. In the present study, we identified and characterized a total of 18 miR169 family members in banana (Musa acuminata L.) based on small RNA sequencing. The banana miR169 family clustered into two groups based on miRNA evolutionary analysis. Multiple sequence a ...[more]

PMID: 30595993

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Project description:BackgroundBanana wilt disease, caused by Fusarium oxysporum f. sp. cubense Tropical Race 4 (Foc TR4), is one of the most devastating diseases in banana (Musa spp.). Foc is a soil borne pathogen that causes rot of the roots or wilt of leaves by colonizing the xylem vessels. The dual RNA sequencing is used to simultaneously assess the transcriptomes of pathogen and host. This method greatly helps to understand the responses of pathogen and host to each other and discover the potential pathogenic mechanism.ResultsPlantlets of two economically important banana cultivars, Foc TR4 less susceptible cultivar NK and susceptible cultivar BX, were used to research the Foc-banana interaction mechanism. Notably, the infected NK had more significantly up-regulated genes on the respiration machinery including TCA cycle, glyoxylate, glycerol, and glycolysis compared to BX at 27 h post inoculation (hpi). In addition, genes involved in plant-pathogen interaction, starch, sucrose, linolenic acid and sphingolipid metabolisms were uniquely more greatly induced in BX than those in NK during the whole infection. Genes related to the biosynthesis and metabolism of SA and JA were greatly induced in the infected NK; while auxin and abscisic acid metabolisms related genes were strongly stimulated in the infected BX at 27 hpi. Furthermore, most of fungal genes were more highly expressed in the roots of BX than in those of NK. The fungal genes related to pathogenicity, pectin and chitin metabolism, reactive oxygen scavenging played the important roles during the infection of Foc. CCP1 (cytochrome c peroxidase 1) was verified to involve in cellulose utilization, oxidative stress response and pathogenicity of fungus.ConclusionThe transcriptome indicated that NK had much faster defense response against Foc TR4 than BX and the expression levels of fungal genes were higher in BX than those in NK. The metabolisms of carbon, nitrogen, and signal transduction molecular were differentially involved in pathogen infection in BX and NK. Additionally, the putative virulence associated fungal genes involved in colonization, nutrition acquirement and transport provided more insights into the infection process of Foc TR4 in banana roots.

Project description:The banana vascular wilt pathogen, Fusarium oxysporum f. sp. cubense, delivers a number of different secreted proteins into host plant tissues during infection. Until now, only a few of the secreted proteins from this fungus have been shown to be virulence effectors. Here, the product of fosp9, which is a gene in this pathogen, was found to be a novel virulence effector. The fosp9 gene encodes a hypothetical 185-amino-acid protein which has a functional signal peptide but contains no known motifs or domains. The fosp9 disruptants displayed a significant reduction in producing wilt symptoms on bananas, indicating that fosp9 is essential for the full virulence of this pathogen for banana. These disruptants did not exhibit a change in either saprophytic growth or conidiation on potato dextrose agar medium, but their invasive growth in the rhizomes of banana was markedly compromised, suggesting a pivotal role for fosp9 in the colonization of banana rhizome tissues by this fungus. Live-cell imaging revealed that the Fosp9-GFP fusion protein accumulated in the apoplast of the plant cells. Moreover, transcriptome profiling revealed that a number of virulence-associated genes were differentially expressed in the fosp9 disruptant relative to the wild type. Taken together, these findings suggest that Fosp9 is a genuine effector of F. oxysporum f. sp. cubense. IMPORTANCE Fusarium wilt of bananas (also known as Panama disease), caused by the fungus F. oxysporum f. sp. cubense, is one of the most devastating banana diseases worldwide. The understanding of the molecular mechanism of its pathogenicity is very limited so far. We demonstrated that the secreted protein Fosp9 from this fungus contributes to its virulence against banana hosts and is essential for colonization of banana rhizome tissues by this fungus. In particular, Fosp9 contains no known domains or motifs and has no functionally characterized homologs, implying that it is a novel secreted effector involved in F. oxysporum f. sp. cubense-banana interactions. This work provides insight into molecular mechanisms of F. oxysporum f. sp. cubense pathogenicity, and the characterization of the fosp9 gene will facilitate development of transgenic banana and plantain strains resistant to this disease by silencing this effector gene through host-induced gene silencing or other strategies.

Dataset Information

Identification and characterization of miRNA169 family members in banana (Musa acuminata L.) that respond to fusarium oxysporum f. sp. cubense infection in banana cultivars.

Publications

Identification and characterization of miRNA169 family members in banana (<i>Musa acuminata</i> L.) that respond to <i>fusarium oxysporum f.</i> sp. <i>cubense</i> infection in banana cultivars.

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