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      Dual species transcript profiling during the interaction between banana ( Musa acuminata) and the fungal pathogen Fusarium oxysporum f. sp. cubense

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          Abstract

          Background

          Banana 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.

          Results

          Plantlets 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.

          Conclusion

          The 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.

          Electronic supplementary material

          The online version of this article (10.1186/s12864-019-5902-z) contains supplementary material, which is available to authorized users.

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          Most cited references58

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          H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.

          Microbial elicitors or attempted infection with an avirulent pathogen strain causes the rapid production of reactive oxygen intermediates. We report here that H2O2 from this oxidative burst not only drives the cross-linking of cell wall structural proteins, but also functions as a local trigger of programmed death in challenged cells and as a diffusible signal for the induction in adjacent cells of genes encoding cellular protectants such as glutathione S-transferase and glutathione peroxidase. Thus, H2O2 from the oxidative burst plays a key role in the orchestration of a localized hypersensitive response during the expression of plant disease resistance.
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            GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis.

            Plants constantly monitor environmental fluctuations to optimize their growth and metabolism. One example is adaptive growth occurring in response to biotic and abiotic stresses. Here, we demonstrate that GH3-mediated auxin homeostasis is an essential constituent of the complex network of auxin actions that regulates stress adaptation responses in Arabidopsis. Endogenous auxin pool is regulated, at least in part, through negative feedback by a group of auxin-inducible GH3 genes encoding auxin-conjugating enzymes. An Arabidopsis mutant, wes1-D, in which a GH3 gene WES1 is activated by nearby insertion of the (35)S enhancer, exhibited auxin-deficient traits, including reduced growth and altered leaf shape. Interestingly, WES1 is also induced by various stress conditions as well as by salicylic acid and abscisic acid. Accordingly, wes1-D was resistant to both biotic and abiotic stresses, and stress-responsive genes, such as pathogenesis-related genes and CBF genes, were upregulated in this mutant. In contrast, a T-DNA insertional mutant showed reduced stress resistance. We therefore propose that GH3-mediated growth suppression directs reallocation of metabolic resources to resistance establishment and represents the fitness costs of induced resistance.
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              Fusarium Wilt of Banana.

              Banana (Musa spp.) is one of the world's most important fruits. In 2011, 145 million metric tons, worth an estimated $44 billion, were produced in over 130 countries. Fusarium wilt (also known as Panama disease) is one of the most destructive diseases of this crop. It devastated the 'Gros Michel'-based export trades before the mid-1900s, and threatens the Cavendish cultivars that were used to replace it; in total, the latter cultivars are now responsible for approximately 45% of all production. An overview of the disease and its causal agent, Fusarium oxysporum f. sp. cubense, is presented below. Despite a substantial positive literature on biological, chemical, or cultural measures, management is largely restricted to excluding F. oxysporum f. sp. cubense from noninfested areas and using resistant cultivars where the pathogen has established. Resistance to Fusarium wilt is poor in several breeding targets, including important dessert and cooking cultivars. Better resistance to this and other diseases is needed. The history and impact of Fusarium wilt is summarized with an emphasis on tropical race 4 (TR4), a 'Cavendish'-killing variant of the pathogen that has spread dramatically in the Eastern Hemisphere.
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                Author and article information

                Contributors
                liwenbin@itbb.org.cn
                375875438@qq.com
                lichunqiang@itbb.org.cn
                sunjianbo@itbb.org.cn
                lishuxia@itbb.org.cn
                pengming@itbb.org.cn
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                24 June 2019
                24 June 2019
                2019
                : 20
                : 519
                Affiliations
                ISNI 0000 0000 9835 1415, GRID grid.453499.6, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, , Chinese Academy of Tropical Agricultural Sciences, ; Haikou, 571101 Hainan China
                Author information
                http://orcid.org/0000-0001-7996-6972
                Article
                5902
                10.1186/s12864-019-5902-z
                6591919
                31234790
                c230c9f1-8005-4102-860e-c4b00b5f82e4
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 21 January 2019
                : 12 June 2019
                Funding
                Funded by: The Program of Hainan Association for Science and Technology Plans to Youth R & D Innovation
                Award ID: HAST201630
                Award Recipient :
                Funded by: Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences
                Award ID: No. 1630052016005
                Award ID: 1630052018003
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Genetics
                musa spp.,fusarium oxysporum,fusarium wilt,transcriptome,cytochrome c peroxidase
                Genetics
                musa spp., fusarium oxysporum, fusarium wilt, transcriptome, cytochrome c peroxidase

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