Bacterial Diseases of Bananas and Enset: Current State of Knowledge and Integrated Approaches Toward Sustainable Management

Bacterial diseases of bananas and enset have not received, until recently, an equal amount of attention compared to other major threats to banana production such as the fungal diseases black leaf streak (Mycosphaerella fijiensis) and Fusarium wilt (Fusarium oxysporum f. sp. cubense). However, bacteria cause significant impacts on bananas globally and management practices are not always well known or adopted by farmers. Bacterial diseases in bananas and enset can be divided into three groups: (1) Ralstonia-associated diseases (Moko/Bugtok disease caused by Ralstonia solanacearum and banana blood disease caused by R. syzygii subsp. celebesensis); (2) Xanthomonas wilt of banana and enset, caused by Xanthomonas campestris pv. musacearum and (3) Erwinia-associated diseases (bacterial head rot or tip-over disease Erwinia carotovora ssp. carotovora and E. chrysanthemi), bacterial rhizome and pseudostem wet rot (Dickeya paradisiaca formerly E. chrysanthemi pv. paradisiaca). Other bacterial diseases of less widespread importance include: bacterial wilt of abaca, Javanese vascular wilt and bacterial fingertip rot (probably caused by Ralstonia spp., unconfirmed). This review describes global distribution, symptoms, pathogenic diversity, epidemiology and the state of the art for sustainable disease management of the major bacterial wilts currently affecting banana and enset.

[1]  M. Hyakumachi,et al.  Phylogenetic relationships of Ralstonia solanacearum species complex strains from Asia and other continents based on 16S rDNA, endoglucanase, and hrpB gene sequences , 2005, Journal of General Plant Pathology.

[2]  A. Hayward,et al.  International standards for naming pathovars of phytopathogenic bacteria and a list of pathovar names and pathotype strains. , 1980 .

[3]  D. Jones.  Diseases of banana, abacá and enset. , 2000 .

[4]  R. H. Stover.  Banana, plantain and abaca diseases , 1972 .

[5]  Jaindra Nath Tripathi,et al.  Relative susceptibility of banana cultivars to Xanthomonas campestris pv. musacearum , 2009 .

[6]  C. Allen,et al.  Genomic and proteomic evidence supporting the division of the plant pathogen Ralstonia solanacearum into three species , 2016, BMC Genomics.

[7]  E. C. Teixeira,et al.  Comparison of the genomes of two Xanthomonas pathogens with differing host specificities , 2002, Nature.

[8]  T. Denny.  Plant pathogenic Ralstonia species , 2007 .

[9]  L. Sequeira,et al.  Designation of races in Pseudomonas solanacearum , 1962 .

[10]  C. Wardlaw.  Banana Diseases : Including Plantains and Abaca , 1972 .

[11]  A. Kelman,et al.  Biological and Physiological Aspects of Bacterial Wilt Caused by Pseudomonas Solanacearum , 1964 .

[12]  Richard Thwaites,et al.  Characterization of the Xanthomonas sp. causing wilt of enset and banana and its proposed reclassification as a strain of X. vasicola , 2007 .

[13]  G. Hartman,et al.  The hosts of Pseudomonas solanacearum. , 1994 .

[14]  F. Beed,et al.  Risk of banana Xanthomonas wilt spread through trade , 2013 .

[15]  G. Blomme,et al.  Rehabilitation of banana farms destroyed by Xanthomonas wilt in Uganda , 2008 .

[16]  R. H. Stover,et al.  Blood disease of bananas in Sulawesi. , 1992 .

[17]  R. Davis,et al.  Records of plant pathogenic viruses and virus-like agents from 22 Pacific island countries and territories: a review and an update , 2010, Australasian Plant Pathology.

[18]  P. Prior,et al.  Resistance to bacterial wilt (Pseudomonas solanacearum) in tomato: present status and prospects , 1994 .

[19]  I. Buddenhagen.  BLOOD BACTERIAL WILT OF BANANA: HISTORY, FIELD BIOLOGY AND SOLUTION , 2009 .

[20]  W. Ocimati,et al.  Systemicity of Xanthomonas campestris pv. musacearum and time to disease expression after inflorescence infection in East African highland and Pisang Awak bananas in Uganda , 2013 .

[21]  C. Staver,et al.  Banana in Latin America and the Caribbean: current state, challenges and perspectives , 2013 .

[22]  J. Schonfeld,et al.  Fate of Ralstonia solanacearum biovar 2 as affected by conditions and soil treatments in temperate climate zones , 2005 .

[23]  M. Doudoroff,et al.  Phenotypic Characterization and Deoxyribonucleic Acid Homologies of Pseudomonas solanacearum , 1971, Journal of bacteriology.

[24]  Jaindra Nath Tripathi,et al.  Expression of sweet pepper Hrap gene in banana enhances resistance to Xanthomonas campestris pv. musacearum. , 2010, Molecular plant pathology.

[25]  I. Buddenhagen,et al.  An Insect-Spread Bacterial Wilt Epiphytotic of Bluggoe Banana , 1962, Nature.

[26]  K. Paszkiewicz,et al.  Genome-Wide Sequencing Reveals Two Major Sub-Lineages in the Genetically Monomorphic Pathogen Xanthomonas Campestris Pathovar Musacearum , 2012, Genes.

[27]  D. Studholme,et al.  Comparative pathogenicity studies of the Xanthomonas vasicola species on maize, sugarcane and banana , 2015 .

[28]  Tunasha Banata Abayneh.  Evaluation of Biological Control Agents against Bacterial Wilt , 2010 .

[29]  Jaindra Nath Tripathi,et al.  Strategies for resistance to bacterial wilt disease of bananas through genetic engineering , 2004 .

[30]  Z. Kinyua,et al.  Identification of Xanthomonas vasicola (formerly X. campestris pv. musacearum), causative organism of banana xanthomonas wilt, in Tanzania, Kenya and Burundi , 2010 .

[31]  G. Hartman,et al.  Advances in identification and detection of Pseudomonas solanacearum. , 1994 .

[32]  I. Yano,et al.  Transfer of Two Burkholderia and An Alcaligenes Species to Ralstonia Gen. Nov. , 1995, Microbiology and immunology.

[33]  P. Prior,et al.  Diverse members of the Ralstonia solanacearum species complex cause bacterial wilts of banana , 2006, Australasian Plant Pathology.

[34]  A. Kelman.  The bacterial wilt caused by Pseudomonas solanacearum. , 1953 .

[35]  C. Allen,et al.  Comparative genomic analysis of Ralstonia solanacearum reveals candidate genes for host specificity , 2015, BMC Genomics.

[36]  C. Allen,et al.  Management of bacterial wilt disease. , 2005 .

[37]  Thierry Lescot.  World plantain and banana production systems , 2013 .

[38]  M. Schell,et al.  Inactivation of multiple virulence genes reduces the ability of Pseudomonas solanacearum to cause wilt symptoms , 1990 .

[39]  J. Smith,et al.  Outbreak of bacterial wilt on banana in Uganda , 2003 .

[40]  W. Ocimati,et al.  Incomplete systemic movement of Xanthomonas campestris pv. musacearum and the occurrence of latent infections in xanthomonas wilt‐infected banana mats , 2015 .

[41]  C. Allen,et al.  How complex is the Ralstonia solanacearum species complex , 2005 .

[42]  G. Blomme,et al.  Banana Xanthomonas wilt in Ethiopia: Occurrence and insect vector transmission , 2010 .

[43]  C. Allen,et al.  Bacterial wilt disease and the Ralstonia solanacearum species complex , 2005 .

[44]  F. Niepold,et al.  Production of monospecific antiserum against the blood disease bacterium affecting banana and plantain. , 1994 .

[45]  Jaindra Nath Tripathi,et al.  Field trial of Xanthomonas wilt disease-resistant bananas in East Africa , 2014, Nature Biotechnology.

[46]  Jonathan D. G. Jones,et al.  Genome-wide sequencing data reveals virulence factors implicated in banana Xanthomonas wilt. , 2010, FEMS microbiology letters.

[47]  P. Prior,et al.  Moko Disease-Causing Strains of Ralstonia solanacearum from Brazil Extend Known Diversity in Paraphyletic Phylotype II. , 2014, Phytopathology.

[48]  T. Feng,et al.  cDNA cloning and characterization of a plant protein that may be associated with the harpinPSS-mediated hypersensitive response , 2000, Plant Molecular Biology.

[49]  L. Tripathi,et al.  High Potassium, Calcium, and Nitrogen Application Reduce Susceptibility to Banana Xanthomonas Wilt Caused by Xanthomonas campestris pv. musacearum. , 2013, Plant disease.

[50]  S. Green.  HOW CAN THE ADVANCE OF BANANA XANTHOMONAS WILT BE HALTED , 2005 .

[51]  R. Bandyopadhyay,et al.  Role of insects in the transmission of banana bacterial wilt , 2007 .

[52]  J. W. Daniells,et al.  Combating banana wilts - what do resistant cultivars have to offer? , 2011 .

[53]  N. Nasir,et al.  Trigona minangkabau potential as bacterial spreader agent of Ralstonia solanacearum Phylotype IV cause blood disease on banana plants. , 2012 .

[54]  W. Ocimati,et al.  Effect of length of fallow period after total uprooting of a Xanthomonas wilt-infected banana field on infection of newly established planting materials: case studies from Rwanda and eastern Democratic Republic of Congo. , 2013 .

[55]  J. Mansfield,et al.  RAPD and rep PCR‐based fingerprinting of vascular bacterial pathogens of Musa spp. , 1999 .

[56]  O. Munar-Vivas,et al.  Use of field-integrated information in GIS-based maps to evaluate Moko disease (Ralstonia solanacearum) in banana growing farms in Colombia , 2010 .

[57]  P. Vandamme,et al.  Simple sequence repeats and compositional bias in the bipartite Ralstonia solanacearum GMI1000 genome , 2003, BMC Genomics.

[58]  J. Swings,et al.  Taxonomy of xanthomonads from cereals and grasses based on SDS-PAGE of proteins, fatty acid analysis and DNA hybridization , 1992 .

[59]  S. Wood,et al.  Assessing the Potential Impact of Selected Technologies on the Banana Industry in Uganda , 2008 .

[60]  G. Blomme,et al.  Garden tool transmission of Xanthomonas campestris pv. musacearum on banana (Musa spp.) and enset in Ethiopia. , 2010 .

[61]  J. A. Barnes,et al.  Worldwide Evaluation of an International Set of Resistance Sources to Bacterial Wilt in Tomato , 1998 .

[62]  R. Winkelmann,et al.  Diseases Caused by Bacteria , 1991 .

[63]  E. Kikulwe,et al.  Banana bacterial wilt incidence in Uganda , 2007 .

[64]  J. Young,et al.  Differentiation of Pseudomonas solanacearum, Pseudomonas syzygii, Pseudomonas pickettii and the Blood Disease Bacterium by partial 16S rRNA sequencing: construction of oligonucleotide primers for sensitive detection by polymerase chain reaction. , 1993, Journal of general microbiology.

[65]  J. Blackburn,et al.  Banana xanthomonas wilt continues to spread in Tanzania despite an intensive symptomatic plant removal campaign: an impending socio-economic and ecological disaster , 2016, Food Security.

[66]  T. Feng,et al.  Plant amphipathic proteins delay the hypersensitive response caused by harpinPssandPseudomonas syringaepv.syringae , 1997 .

[67]  F. Ssekiwoko,et al.  SYSTEMICITY OF Xanthomonas campestris pv. musacearum IN , 2006 .

[68]  W. Tushemereirwe,et al.  Reaction of banana germplasm to inoculation with xanthomonas campestris pv musacearum , 2007 .

[69]  T. Denny,et al.  Analysis of Genetic Variation of a Population of Banana Infecting Strains of Ralstonia solanacearum , 1998 .

[70]  T. Coutinho,et al.  Xanthomonas campestris pv. musacearum: a major constraint to banana, plantain and enset production in central and east Africa over the past decade. , 2018, Molecular plant pathology.

[71]  W. Ocimati,et al.  Systemicity and speed of movement of Xanthomonas campestris pv. musacearum in the banana plant after garden tool-mediated infection. , 2013 .

[72]  L. Sequeira.  Bacterial Wilt: the Missing Element in International Banana Improvement Programs , 1998 .

[73]  J. Swings,et al.  Reclassification of Xanthomonas , 1995 .

[74]  G. Blomme,et al.  MECHANICAL TRANSMISSION AND SURVIVAL OF BACTERIAL WILT ON ENSET , 2010 .

[75]  Y. Zhao,et al.  Ribosomal protein gene-based phylogeny for finer differentiation and classification of phytoplasmas. , 2007, International journal of systematic and evolutionary microbiology.

[76]  Nyagatare Tabagwe,et al.  Spatial and temporal diStribution of inSect VectorS of Xanthomonas campestris pv. musacearum and their actiVity acroSS banana cultiVarS Grown in rwanda , 2015 .

[77]  W. Tushemereirwe,et al.  Xanthomonas campestris pv musacearum host range in Uganda , 2007 .

[78]  M. Fegan,et al.  Analysis of the phylogenetic relationships of strains of Burkholderia solanacearum, Pseudomonas syzygii, and the blood disease bacterium of banana based on 16S rRNA gene sequences. , 1996, International journal of systematic bacteriology.

[79]  G. Blomme,et al.  The effectiveness of different herbicides in the destruction of banana Xanthomonas wilt infected plants , 2010 .

[80]  Hyungtae Kim,et al.  The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice , 2005, Nucleic acids research.

[81]  J. Bradbury,et al.  A Note on Wilt of Banana Caused by the Enset Wilt Organism Xanthomonas musacearum , 1974 .

[82]  G. Blomme,et al.  Spread of Xanthomonas campestris pv. musacearum in banana (Musa spp.) plants following infection of the male inflorescence. , 2010 .

[83]  C. Allen,et al.  The current bacterial wilt situation: a global overview. , 2005 .

[84]  A. P. Matos,et al.  Evaluation of Musa spp. for resistance to Moko disease (Ralstonia solanacearum, race 2). , 2000 .

[85]  C. Allen,et al.  Present status of blood disease in Indonesia. , 2005 .

[86]  W. Ocimati,et al.  Breaking the Cycle of Xanthomonas campestris pv. musacearum in Infected Fields through the Cultivation of Annual Crops and Disease Control in Adjacent Fields , 2016 .

[87]  B. Rodoni,et al.  A new wilt disease of banana plants associated with phytoplasmas in Papua New Guinea (PNG) , 2012, Australasian Plant Disease Notes.

[88]  L. Magnaye,et al.  Bugtok disease of banana , 1995 .

[89]  P. Prior,et al.  Recent developments in the phylogeny and classification of Ralstonia solanacearum , 2005 .

[90]  W. Ocimati,et al.  Comparative importance of infection routes for banana Xanthomonas wilt and implications on disease epidemiology and management , 2014 .

[91]  M. Osiru,et al.  Managing bacterial wilt/fruit rot disease of banana in Southeast Asia. , 2006 .

[92]  G. Tusiime,et al.  The survival of Xanthomonas Campestris PV.musacearum in soil and plant debris , 2007 .

[93]  Ranajit Bandyopadhyay,et al.  Banana Xanthomonas wilt: a review of the disease, management strategies and future research directions , 2007 .

[94]  T. Lescot.  The genetic diversity of banana , 2012 .

[95]  W. Ocimati,et al.  Does Xanthomonas campestris pv. musacearum Colonize Banana Cord Root Tissue , 2013 .

[96]  W. Ocimati,et al.  Variation in nectar volume and sugar content in male flowers of Musa cultivars grown in Rwanda and their non-effect on the numbers of visiting key diurnal insect vectors of banana Xanthomonas wilt , 2016 .

[97]  W. Ocimati,et al.  Fine-tuning banana Xanthomonas wilt control options over the past decade in East and Central Africa , 2014, European Journal of Plant Pathology.

[98]  Jean-Charles de Cambiaire,et al.  Contrasting recombination patterns and demographic histories of the plant pathogen Ralstonia solanacearum inferred from MLSA , 2011, The ISME Journal.

[99]  C. Allen,et al.  Development of bacterial wilt resistant varieties and basis of resistance in eggplant (Solanum melongena L.). , 2005 .

[100]  L. Tripathi,et al.  Nematode infection predisposes banana to soil-borne Xanthomonas campestris pv musacearum transmission. , 2010 .

[101]  I. S. Ismail,et al.  The occurrence of blood disease of banana in Selangor, Malaysia. , 2015 .

[102]  A. Molina.  Fruit rot diseases of cooking banana in Southeast Asia. , 1999 .

[103]  G. Tusiime,et al.  Role of birds & bats in long distance transmission of banana bacterial wilt in Uganda. , 2014 .

[104]  J. Bradbury,et al.  Bacterial wilt of enset (Ensete ventricosum) incited by Xanthomonas musacearum sp. n , 1968 .

[105]  R. Ploetz,et al.  Impact of diseases on export and smallholder production of banana. , 2015, Annual review of phytopathology.

[106]  P. de Vos,et al.  Polyphasic taxonomic revision of the Ralstonia solanacearum species complex: proposal to emend the descriptions of Ralstonia solanacearum and Ralstonia syzygii and reclassify current R. syzygii strains as Ralstonia syzygii subsp. syzygii subsp. nov., R. solanacearum phylotype IV strains as Ralstonia , 2014, International journal of systematic and evolutionary microbiology.

[107]  B. Liao,et al.  A broad review and perspective on breeding for resistance to bacterial wilt. , 2005 .

[108]  J. Gouzy,et al.  The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae , 2009, BMC Genomics.

[109]  Jaindra Nath Tripathi,et al.  A rapid technique for screening banana cultivars for resistance to Xanthomonas wilt , 2008, European Journal of Plant Pathology.

[110]  C. Médigue,et al.  Ralstonia syzygii, the Blood Disease Bacterium and Some Asian R. solanacearum Strains Form a Single Genomic Species Despite Divergent Lifestyles , 2011, PloS one.

[111]  W. Ocimati,et al.  Interactive effects of fertilizer and inoculum concentration on subsequent development of xanthomonas wilt in banana , 2014 .

[112]  Takayuki Ezaki,et al.  Proposal of Burkholderia gen. nov. and Transfer of Seven Species of the Genus Pseudomonas Homology Group II to the New Genus, with the Type Species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. , 1992, Microbiology and immunology.

[113]  M. S. Yepes,et al.  Identification of new hosts for Ralstonia solanacearum (Smith) race 2 from Colombia , 2012 .

[114]  G. Mahuku.  ENDOPHYTIC BACTERIA ASSOCIATED WITH BANANA AND THEIR POTENTIAL FOR CONTROLLING XANTHOMONAS WILT , 2016 .

[115]  C. Panagopoulos,et al.  A proposed nomenclature and classification for plant pathogenic bacteria , 1978 .

[116]  K. Sijam,et al.  First Report of Ralstonia solanacearum Race 2 Biovar 1 Causing Moko Disease of Banana in Malaysia. , 2014, Plant disease.

[117]  K. Smalla,et al.  Effects of compost addition and simulated solarisation on the fate of Ralstonia solanacearum biovar 2 and indigenous bacteria in soil. , 2003, FEMS microbiology ecology.

[118]  M. Gillings,et al.  Genomic fingerprinting: towards a unified view of the Pseudomonas-solanacearum species complex , 1994 .

[119]  S. Abeyasekera,et al.  Impact of awareness campaigns for banana bacterial wilt in Uganda , 2007 .

[120]  Leandro M Moreira,et al.  articleNovel insights into the genomic basis of citrus canker based on the genome sequences of two strains of Xanthomonas fuscans subsp . aurantifolii , 2010 .

[121]  V. Nakato,et al.  Status of banana Xanthomonas wilt in western Kenya and factors enhancing its spread , 2009 .

[122]  G. Blomme,et al.  Exploiting indigenous knowledge of subsistence farmers’ for the management and conservation of Enset (Ensete ventricosum (Welw.) Cheesman) (musaceae family) diversity on-farm , 2016, Journal of Ethnobiology and Ethnomedicine.

[123]  M. Fegan.  Bacterial wilt diseases of banana: evolution and ecology. , 2005 .

[124]  G. Hartman,et al.  Diversity of Pseudomonas solanacearum and related bacteria in south east Asia: new directions for moko disease. , 1994 .

[125]  G. Salmond,et al.  Top 10 plant pathogenic bacteria in molecular plant pathology. , 2012, Molecular plant pathology.

[126]  Mario Vaneechoutte,et al.  Wautersia gen. nov., a novel genus accommodating the phylogenetic lineage including Ralstonia eutropha and related species, and proposal of Ralstonia [Pseudomonas] syzygii (Roberts et al. 1990) comb. nov. , 2004, International journal of systematic and evolutionary microbiology.

[127]  C. Allen,et al.  Diversity and diagnosis of Ralstonia solanacearum. , 2005 .

[128]  A. Hayward,et al.  Characteristics of Pseudomonas solanacearum , 1964 .

[129]  P. Ewell,et al.  Integrated control of potato bacterial wilt in Eastern Africa: the experience of African highlands initiative. , 2005 .

[130]  N K Van Alfen,et al.  REASSESSMENT OF PLANT WILT TOXINS , 1989 .

[131]  S. Genin,et al.  Pathogenomics of the Ralstonia solanacearum species complex. , 2012, Annual review of phytopathology.

[132]  A. Hayward.  Biology and epidemiology of bacterial wilt caused by pseudomonas solanacearum. , 1991, Annual review of phytopathology.

[133]  J. Victoria,et al.  Taxonomy and emended description of strains of Erwinia isolated from Musa paradisiaca Linnaeus. , 1980 .

[134]  R. Davis,et al.  Blood disease and Panama disease: Two newly introduced and grave threats to banana production on the island of New Guinea , 2001 .

[135]  F. Ssekiwoko,et al.  First report of Xanthomonas campestris pv. musacearum on banana in Uganda. , 2004 .