Association of 'Candidatus Liberibacter solanacearum' with Zebra Chip Disease of Potato Established by Graft and Psyllid Transmission, Electron Microscopy, and PCR.

A new disease of potatoes, tentatively named zebra chip (ZC) because of the intermittent dark and light symptom pattern in affected tubers which is enhanced by frying, was first found in Mexico in 1994 and in the southwestern United States in 2000. The disease can cause severe economic losses in all market classes of potatoes. The cause of ZC has been elusive, and only recently has been associated with 'Candidatus Liberibacter' sp. Field samples of potato plants were collected from several locations in the United States, Mexico, and Guatemala to determine transmission to potato and tomato by grafting of ZC-infected scions and psyllid feeding. The disease was successfully transmitted, through up to three generations, by sequential top- and side-grafting ZC-infection scions to several potato cultivars and to tomato. The disease was also successfully transmitted to potato and tomato plants in greenhouse experiments by potato psyllids collected from potato plants naturally affected with ZC. Transmission electron microscopic observation of ZC-affected tissues revealed the presence of bacteria-like organisms (BLOs) in the phloem of potato and tomato plants inoculated by grafting and psyllid feeding. The BLOs were morphologically similar in appearance to BLOs associated with other plant diseases. Polymerase chain reaction (PCR) amplified 16S rDNA sequences from samples representing different geographic areas, including the United States, Mexico, and Guatemala, were almost identical to the 16S rDNA of 'Ca. L. solanacearum' previously reported from solanaceous plants in New Zealand and the United States. Two subclades were identified that differed in two single base-pair substitutions. New specific primers along with an innovative rapid PCR were developed. This test allows the detection of the bacteria in less than 90 min. These data confirm the association of 'Ca. L. solanacearum' with potatoes affected by ZC in the United States, Mexico, and Guatemala.

[1]  B. Schneider,et al.  Classification of plant-pathogenic mycoplasma-like organisms using restriction-site analysis of PCR-amplified 16S rDNA , 1993 .

[2]  J. Munyaneza,et al.  Clover Proliferation Group (16SrVI) Subgroup A (16SrVI-A) Phytoplasma is a Probable Causal Agent of Potato Purple Top Disease in Washington and Oregon. , 2004, Plant disease.

[3]  Ing-Ming Lee,et al.  "Candidatus Phytoplasma americanum", a phytoplasma associated with a potato purple top wilt disease complex. , 2006, International journal of systematic and evolutionary microbiology.

[4]  W. Carter Injuries to plants caused by insect toxins , 2008, The Botanical Review.

[5]  S. Vautrin,et al.  Association with the Syndrome "Basses Richesses" of Sugar Beet of a Phytoplasma and a Bacterium-Like Organism Transmitted by a Pentastiridius sp. , 2002, Phytopathology.

[6]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..

[7]  K. Matsuda,et al.  Physiological effects of psyllid (Paratrioza cockerelli) on potato , 2008, American Potato Journal.

[8]  L. Ward,et al.  A New 'Candidatus Liberibacter' Species Associated with Diseases of Solanaceous Crops. , 2009, Plant disease.

[9]  George Karypis,et al.  Introduction to Parallel Computing , 1994 .

[10]  J. Bové,et al.  Huanglongbing: a destructive, newly-emerging, century-old disease of citrus [Asia; South Africa; Brazil; Florida] , 2006 .

[11]  D. Gundersen-Rindal,et al.  Revised Classification Scheme of Phytoplasmas based on RFLP Analyses of 16S rRNA and Ribosomal Protein Gene Sequences , 1998 .

[12]  P. I. da Costa,et al.  'Candidatus Liberibacter americanus', associated with citrus huanglongbing (greening disease) in São Paulo State, Brazil. , 2005, International journal of systematic and evolutionary microbiology.

[13]  E. Brown,et al.  Is 16S rDNA a Reliable Phylogenetic Marker to Characterize Relationships Below the Family Level in the Enterobacteriaceae? , 2008, Journal of Molecular Evolution.

[14]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[15]  J. Fletcher,et al.  Identification, Phylogenetic Analysis, and Biological Characterization of Serratia marcescens Strains Causing Cucurbit Yellow Vine Disease. , 2003, Phytopathology.

[16]  M. Armando,et al.  Potato purple top in Mexico: III. Effects of plant spacing and insecticide application , 1999 .

[17]  A. Hilton,et al.  New and old pathogens of potato in changing climate , 2007 .

[18]  J. Shiller,et al.  A New 'Candidatus Liberibacter' Species in Solanum betaceum (Tamarillo) and Physalis peruviana (Cape Gooseberry) in New Zealand. , 2008, Plant disease.

[19]  J. Abad,et al.  First Report of the Detection of 'Candidatus Liberibacter' Species in Zebra Chip Disease-Infected Potato Plants in the United States. , 2009, Plant disease.

[20]  F. Rodríguez-Valera,et al.  Intragenomic 16S rDNA Divergence in Haloarcula marismortui Is an Adaptation to Different Temperatures , 2007, Journal of Molecular Evolution.

[21]  T. Paine,et al.  Frequency of Secondary Symbiont Infection in an Invasive Psyllid Relates to Parasitism Pressure on a Geographic Scale in California , 2007, Applied and Environmental Microbiology.

[22]  A. Jensen,et al.  Association of Beet Leafhopper (Hemiptera: Cicadellidae) with a Clover Proliferation Group Phytoplasma in Columbia Basin of Washington and Oregon , 2005, Journal of economic entomology.

[23]  J. Anderson,et al.  A New 'Candidatus Liberibacter' Species in Solanum tuberosum in New Zealand. , 2008, Plant disease.

[24]  J. Crosslin,et al.  Further Evidence that Zebra Chip Potato Disease in the Lower Rio Grande Valley of Texas is Associated with Bactericera cockerelli , 2007 .

[25]  B. L. Richards A new and destructive Disease of the Potato in Utah and its Relation to the Potato Psylla. (Abstract). , 2022 .

[26]  P. Miklas,et al.  Clover Proliferation Group (16SrVI) Subgroup A (16SrVI-A) Phytoplasma is a Probable Causal Agent of Dry Bean Phyllody Disease in Washington. , 2004, Plant disease.

[27]  T. Paine,et al.  A New Huanglongbing Species, “Candidatus Liberibacter psyllaurous,” Found To Infect Tomato and Potato, Is Vectored by the Psyllid Bactericera cockerelli (Sulc) , 2008, Applied and Environmental Microbiology.

[28]  R. F. Carvalho,et al.  Grafting of tomato mutants onto potato rootstocks: An approach to study leaf-derived signaling on tuberization , 2005 .

[29]  D. S. Leal-Klevezas,et al.  Multiple phytoplasmas associated with potato diseases in Mexico. , 2002, Canadian journal of microbiology.

[30]  M. Klein Association of Bacterialike Organisms With a New Potato Disease , 1976 .

[31]  J. Bové,et al.  The phloem-limited bacterium of greening disease of citrus is a member of the alpha subdivision of the Proteobacteria. , 1994, International journal of systematic bacteriology.

[32]  N. Gudmestad,et al.  First Report of a Defect of Processing Potatoes in Texas and Nebraska Associated with a New Phytoplasma. , 2006, Plant disease.

[33]  A. Bressan,et al.  Characterization of a gamma-3 Proteobacteria Responsible for the Syndrome "Basses Richesses" of Sugar Beet Transmitted by Pentastiridius sp. (Hemiptera, Cixiidae). , 2007, Phytopathology.

[34]  J. Bové,et al.  Phylogenetic characterization of the bacterium-like organism associated with marginal chlorosis of strawberry and proposition of a Candidatus taxon for the organism, 'Candidatus phlomobacter fragariae'. , 1998, International journal of systematic bacteriology.

[35]  S. Pennycook,et al.  'Candidatus Liberibacter solanacearum', associated with plants in the family Solanaceae. , 2009, International journal of systematic and evolutionary microbiology.