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Improvements in the Resistance of the Banana Species to Fusarium Wilt: A Systematic Review of Methods and Perspectives.

ABSTRACT: The fungus Fusarium oxysporum f. sp. cubense (FOC), tropical race 4 (TR4), causes Fusarium wilt of banana, a pandemic that has threatened the cultivation and export trade of this fruit. This article presents the first systematic review of studies conducted in the last 10 years on the resistance of Musa spp. to Fusarium wilt. We evaluated articles deposited in different academic databases, using a standardized search string and predefined inclusion and exclusion criteria. We note that the information on the sequencing of the Musa sp. genome is certainly a source for obtaining resistant cultivars, mainly by evaluating the banana transcriptome data after infection with FOC. We also showed that there are sources of resistance to FOC race 1 (R1) and FOC TR4 in banana germplasms and that these data are the basis for obtaining resistant cultivars, although the published data are still scarce. In contrast, the transgenics approach has been adopted frequently. We propose harmonizing methods and protocols to facilitate the comparison of information obtained in different research centers and efforts based on global cooperation to cope with the disease. Thus, we offer here a contribution that may facilitate and direct research towards the production of banana resistant to FOC.

SUBMITTER: Rocha AJ

PROVIDER: S-EPMC8066237 | biostudies-literature | 2021 Mar

REPOSITORIES: biostudies-literature

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Improvements in the Resistance of the Banana Species to Fusarium Wilt: A Systematic Review of Methods and Perspectives.

Rocha Anelita de Jesus AJ Soares Julianna Matos da Silva JMDS Nascimento Fernanda Dos Santos FDS Santos Adriadna Souza AS Amorim Vanusia Batista de Oliveira VBO Ferreira Claudia Fortes CF Haddad Fernando F Santos-Serejo Janay Almeida Dos JAD Amorim Edson Perito EP

Journal of fungi (Basel, Switzerland) 20210325 4

The fungus Fusarium oxysporum f. sp. cubense (FOC), tropical race 4 (TR4), causes Fusarium wilt of banana, a pandemic that has threatened the cultivation and export trade of this fruit. This article presents the first systematic review of studies conducted in the last 10 years on the resistance of Musa spp. to Fusarium wilt. We evaluated articles deposited in different academic databases, using a standardized search string and predefined inclusion and exclusion ...[more]

PMID: 33806239

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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.

Project description:In the last century, the banana crop and industry experienced dramatic losses due to an epidemic of Fusarium wilt of banana (FWB), caused by Fusarium oxysporum f.sp. cubense (Foc) race 1. An even more dramatic menace is now feared due to the spread of Foc tropical race 4. Plant genetic resistance is generally considered as the most plausible strategy for controlling effectively such a devastating disease, as occurred for the first round of FWB epidemic. Nevertheless, with at least 182 articles published since 1970, biological control represents a large body of knowledge on FWB. Remarkably, many studies deal with biological control agents (BCAs) that reached the field-testing stage and even refer to high effectiveness. Some selected BCAs have been repeatedly assayed in independent trials, suggesting their promising value. Overall under field conditions, FWB has been controlled up to 79% by using Pseudomonas spp. strains, and up to 70% by several endophytes and Trichoderma spp. strains. Lower biocontrol efficacy (42-55%) has been obtained with arbuscular mycorrhizal fungi, Bacillus spp., and non-pathogenic Fusarium strains. Studies on Streptomyces spp. have been mostly limited to in vitro conditions so far, with very few pot-experiments, and none conducted in the field. The BCAs have been applied with diverse procedures (e.g., spore suspension, organic amendments, bioformulations, etc.) and at different stages of plant development (i.e., in vitro, nursery, at transplanting, post-transplanting), but there has been no evidence for a protocol better than another. Nonetheless, new bioformulation technologies (e.g., nanotechnology, formulation of microbial consortia and/or their metabolites, etc.) and tailor-made consortia of microbial strains should be encouraged. In conclusion, the literature offers many examples of promising BCAs, suggesting that biocontrol can greatly contribute to limit the damage caused by FWB. More efforts should be done to further validate the currently available outcomes, to deepen the knowledge on the most valuable BCAs, and to improve their efficacy by setting up effective formulations, application protocols, and integrated strategies.

Project description:Banana (Musa spp.), a major cash and staple fruit crop in many parts of the world, is infected by Fusarium wilt, which contributes up to 100% yield loss and causes social consequences. Race 1 and race 2 of Panama wilt caused by Fusarium oxysporum f. sp. cubense (Foc) are prevalent worldwide and seriously affect many traditional varieties. The threat of Foc tropical race 4 (Foc TR4) is looming large in African counties. However, its incidence in India has been confined to Bihar (Katihar and Purnea), Uttar Pradesh (Faizabad), Madhya Pradesh (Burhanpur) and Gujarat (Surat). Management of Foc races by employing fungicides is often not a sustainable option as the disease spread is rapid and they negatively alter the biodiversity of beneficial ectophytes and endophytes. Besides, soil drenching with carbendazim/trifloxystrobin + tebuconazole is also not effective in suppressing the Fusarium wilt of banana. Improvement of resistance to Fusarium wilt in susceptible cultivars is being addressed through both conventional and advanced breeding approaches. However, engineering of banana endosphere with bacterial endophytes from resistant genotypes like Pisang lilly and YKM5 will induce the immune response against Foc, irrespective of races. The composition of the bacterial endomicrobiome in different banana cultivars is dominated by the phyla Proteobacteria, Bacteroidetes and Actinobacteria. The major bacterial endophytic genera antagonistic to Foc are Bacillus, Brevibacillus, Paenibacillus, Virgibacillus, Staphylococcus, Cellulomonas, Micrococcus, Corynebacterium, Kocuria spp., Paracoccus sp., Acinetobacter spp. Agrobacterium, Aneurinibacillus, Enterobacter, Klebsiella, Lysinibacillus, Micrococcus, Rhizobium, Sporolactobacillus, Pantoea, Pseudomonas, Serratia, Microbacterium, Rhodococcus, Stenotrophomonas, Pseudoxanthomonas, Luteimonas, Dokdonella, Rhodanobacter, Luteibacter, Steroidobacter, Nevskia, Aquicella, Rickettsiella, Legionella, Tatlockia and Streptomyces. These bacterial endophytes promote the growth of banana plantlets by solubilising phosphate, producing indole acetic acid and siderophores. Application of banana endophytes during the hardening phase of tissue-cultured clones serves as a shield against Foc. Hitherto, MAMP molecules of endophytes including flagellin, liposaccharides, peptidoglycans, elongation factor, cold shock proteins and hairpins induce microbe-associated molecular pattern (MAMP)-triggered immunity to suppress plant pathogens. The cascade of events associated with ISR and SAR is induced through MAPK and transcription factors including WRKY and MYC. Studies are underway to exploit the potential of antagonistic bacterial endophytes against Foc isolates and to develop an understanding of the MAMP-triggered immunity and metabolomics cross talk modulating resistance. This review explores the possibility of harnessing the potential bacterial endomicrobiome against Foc and developing nanoformulations with bacterial endophytes for increased efficacy against lethal pathogenic races of Foc infecting banana.Supplementary informationThe online version contains supplementary material available at 10.1007/s13205-021-02833-5.

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.

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Improvements in the Resistance of the Banana Species to Fusarium Wilt: A Systematic Review of Methods and Perspectives.

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Improvements in the Resistance of the Banana Species to Fusarium Wilt: A Systematic Review of Methods and Perspectives.

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