Bacterial endophytome-mediated resistance in banana for the management of Fusarium wilt

Abstract

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 information: The online version contains supplementary material available at 10.1007/s13205-021-02833-5.

Keywords: Bacterial endophytes; Banana; Foc; Fusarium wilt; Growth promotion; Plant immunity.

Fig. 1

Proportions of bacterial endophytes in banana conferring resistance against Fusarium wilt of banana. Where 19—Bacilli are B. pumilus, B. thuringiensis, B. subtillis, B. cereus, B. amyloliquefaciens, B. flexus, B. megaterium, B. methylotrophicus, B. axarquienses, B. licheniformis, B. tequlensis, B. safensis, B. okhensis, Panibacillus sp., Staphylococcus pasteuri, Staphylococcus epidermidis, Sporalactobacillus sp. and Aneurinibacillus sp., Lysinibacillus sp.; 15—Actinobacteria are Micrococcus luteus, M. terreus, M. yunnanensis, M. endophyticus, Kytococcus sedentarius, Brevibacterium pityocampae, Arthrobacter chlorophenolicus, Curtobacterium oceanosedimentum, Corynebacterium lipophiloflavum, Kocuria rhizophila, Jatrophihabitans endophyticus, Tessaracoccus flavescens, Kocuria palustris, Rothia terrae and Naumannella halotolerans; 7—γ-Proteobacteria are Klebsiella pneumoniae, K. variicola, Pseudomonas aeruginosa, P. putida, Enterobacter cloacae, Serratia marcescens and S. nematodiphila; 5—α-Proteobacteria are Agrobacterium tumefaciens, Rhizobium sp., Sphingomonas mucosissima, S. panni and Brevundimonas vesicularis; 1—β-Proteobacteria is Pseudoacedovorax intermedius

Fig. 2

Plant growth promotional activities of bacterial endophytes. The endophytic bacteria balance the hormones through biosynthesis of salicylic acid, jasmonic acid which are essential in development, metabolism, and stress responses. Where SAM S-adenosyl methionine; FLS2 flagellin sensitive 2; BIK BAK1 like; BAK1 brassinosteroid insensitive1-associated kinase1; IAA indole acetic acid; OA organic acid; ACC 1-aminocyclopropane carboxylic acid; GA gibberellic acid; ROS reactive oxygen species; Sid siderophore, SMs secondary metabolites; CK cytokinin

Fig. 3

MAMP-triggered immunity by bacterial endophytes. The MAMP molecules from endophytic bacteria are recognized by the pattern recognition receptor (PRR) present in the plasma membrane. This results in calcium and hydrogen ion influx and K+ efflux occurs. This redox and pH changes in the cell leads to long distance transport of signal. The mitogen-activated protein kinase (MAPK) gene gets activated first and the activated MAPKKK phosphorylate to MPKK and MPK which leads into transcriptional reprogramming. The transcriptional factors like WRKY, ACS2/6, ERF 6/104, TGA, MYB/MYC gets activated to regulate the defence genes expression. This complex interaction results in production of pathogenesis-related genes, phytoalexin, callose deposition, ROS, defensin. Where, MAMP microbe-associated molecular pattern; FLS2 flagellin sensitive 2; BAK1 brassinosteroid insensitive1-associated kinase1; BIK BAK1 like; MTI MAMP-triggered immunity; TGA transcription factor; NPR1 non-pathogenesis-related 1; ETI effector-triggered immunity; NO nitric oxide; ROS reactive oxygen species