Diversity and phylogeography of begomovirus-associated beta satellites of okra in India

Virology Journal

M Krishna Reddy⁴  Rob W Briddon⁵  Salil Jalali¹  P Swaranalatha¹  CN Lakshminarayana Reddy³  V Venkataravanappa² 

[1] Indian Institute of Horticultural Research, Hessaraghatta Lake PO, Bangalore, India;Indian Vegetable Research Institute, Varanasi 221305, Uttar Pradesh, India;Department of Plant Pathology, College of Sericulture, University of Agricultural Sciences, Chintamani, Karnataka, India;Division of Plant Pathology, Plant Virology Laboratory, Indian Institute of Horticultural Research, Hessaraghatta Lake PO, Bangalore 560 089, India;Agricultural Biotechnology Division, National Institute for Biotechnology and Genetic Engineering, P.O. Box 577, Jhang Road, Faisalabad, Pakistan

关键词: Recombination;    Okra;    Diversity;    Betasatellites;    Begomovirus;    Geminivirus;   

Others  :  1155374
DOI  :  10.1186/1743-422X-8-555

 received in 2011-04-24, accepted in 2011-12-21,  发布年份 2011

【 摘 要 】

Background

Okra (Abelmoschus esculentus; family Malvaceae) is grown in temperate as well as subtropical regions of the world, both for human consumption as a vegetable and for industrial uses. Okra yields are affected by the diseases caused by phyopathogenic viruses. India is the largest producer of okra and in this region a major biotic constraint to production are viruses of the genus Begomovirus. Begomoviruses affecting okra across the Old World are associated with specific, symptom modulating satellites (beta satellites). We describe a comprehensive analysis of the diversity of beta satellites associated with okra in India.

Results

The full-length sequences of 36 beta satellites, isolated from okra exhibiting typical begomovirus symptoms (leaf curl and yellow vein), were determined. The sequences segregated in to four groups. Two groups correspond to the beta satellites Okra leaf curl beta satellite (OLCuB) and Bhendi yellow vein beta satellite (BYVB) that have previously been identified in okra from the sub-continent. One sequence was distinct from all other, previously isolated beta satellites and represents a new species for which we propose the name Bhendi yellow vein India beta satellite (BYVIB). This new beta satellite was nevertheless closely related to BYVB and OLCuB. Most surprising was the identification of Croton yellow vein mosaic beta satellite (CroYVMB) in okra; a beta satellite not previously identified in a malvaceous plant species. The okra beta satellites were shown to have distinct geographic host ranges with BYVB occurring across India whereas OLCuB was only identified in northwestern India. Okra infections with CroYVMB were only identified across the northern and eastern central regions of India. A more detailed analysis of the sequences showed that OLCuB, BYVB and BYVIB share highest identity with respect βC1 gene. βC1 is the only gene encoded by beta satellites, the product of which is the major pathogenicity determinant of begomovirus-beta satellite complexes and is involved in overcoming host defenses based on RNAi.

Conclusion

The diversity of beta satellites in okra across the sub-continent is higher than previously realized and is higher than for any other malvaceous plant species so far analyzed. The beta satellites identified in okra show geographic segregation, which has implications for the development and introduction of resistant okra varieties. However, the finding that the βC1 gene of the major okra beta satellites (OLCuB, BYVB and BYVIB) share high sequence identity and provides a possible avenue to achieve a broad spectrum resistance.

【 授权许可】

   
2011 Venkataravanappa et al; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Stanley J, Bisaro DM, Briddon RW, Brown JK, Fauquet CM, Harrison BD, Rybicki EP, Stenger DC: Geminiviridae. In Virus Taxonomy, VIIIth Report of the ICTV. Edited by Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA. London: Elsevier/Academic Press; 2005:301-326.
• [2]Rojas MR, Hagen C, Lucas WJ, Gilbertson RL: Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Ann Rev Phytopathol 2005, 43:361-394.
• [3]Navot N, Pichersky E, Zeidan M, Zamir D, Czosnek H: Tomato yellow leaf curl virus: a whitefly-transmitted geminivirus with a single genomic component. Virology 1991, 185:151-161.
• [4]Lefeuvre P, Martin DP, Harkins G, Lemey P, Gray AJA, Meredith S, Lakay F, Monjane A, Lett J-M, Varsani A, Heydarnejad J: The spread of Tomato yellow leaf curl virus from the Middle East to the world. PLoS Pathogens 2010, 6:e1001164.
• [5]Briddon RW, Stanley J: Sub-viral agents associated with plant single-stranded DNA viruses. Virology 2006, 344:198-210.
• [6]Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X, Fauquet CM: Recommendations for the classification and nomenclature of the DNA-β satellites of begomoviruses. Arch Virol 2008, 153:763-781.
• [7]Briddon RW, Bull SE, Amin I, Idris AM, Mansoor S, Bedford ID, Dhawan P, Rishi N, Siwatch SS, Abdel-Salam AM, et al.: Diversity of DNA β: a satellite molecule associated with some monopartite begomoviruses. Virology 2003, 312:106-121.
• [8]Li ZH, Xie Y, Zhou XP: Tobacco curly shoot virus DNA β is not necessary for infection but intensifies symptoms in a host-dependent manner. Phytopathology 2005, 95:902-908.
• [9]Saunders K, Norman A, Gucciardo S, Stanley J: The DNA β satellite component associated with ageratum yellow vein disease encodes an essential pathogenicity protein (βC1). Virology 2004, 324:37-47.
• [10]Cui X, Tao X, Xie Y, Fauquet CM, Zhou X: A DNA β associated with Tomato yellow leaf curl China virus is required for symptom induction. J Virol 2004, 78:13966-13974.
• [11]Saeed S, Y Zafar Y, Randles JW, Rezaian MA: A monopartite begomovirus-associated DNA β satellite substitutes for the DNA B of a bipartite begomovirus to permit systemic infection. J Gen Virol 2007, 88:2881-2889.
• [12]Cui X, Li G, Wang D, Hu D, Zhou X: A begomovirus DNAβ-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol 2005, 79:10764-10775.
• [13]Kon T, Sharma P, Ikegami M: Suppressor of RNA silencing encoded by the monopartite tomato leaf curl Java begomovirus. Arch Virol 2007, 152:1273-1282.
• [14]Cheng X, Wang X, Wu J, Briddon RW, Zhou X: βC1 encoded by tomato yellow leaf curl China betasatellite forms multimeric complexes in vitro and in vivo. Virology 2011, 409:156-162.
• [15]Andleeb S, Amin I, Bashir A, Briddon Rob W, Mansoor S: Transient expression of βC1 protein differentially regulates host genes related to stress response, chloroplast and mitochondrial functions. Virol J 2010, 7:373.
• [16]Yang J-Y, Iwasaki M, Machida C, Machida Y, Zhou X, Chua N-H: βC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 2008, 22:2564-2577.
• [17]Eini O, Dogra S, Selth LA, Dry IB, Randles JW, Rezaian MA: Interaction with a host ubiquitin-conjugating enzyme is required for the pathogenicity of a geminiviral DNA β satellite. Mol Plant Microbe Interact 2009, 22:737-746.
• [18]Briddon RW, Bull SE, Amin I, Mansoor S, Bedford ID, Rishi N, Siwatch SS, Zafar MY, Abdel-Salam AM, Markham PG: Diversity of DNA 1; a satellite-like molecule associated with monopartite begomovirus-DNA β complexes. Virology 2004, 324:462-474.
• [19]Mansoor S, Khan SH, Bashir A, Saeed M, Zafar Y, Malik KA, Briddon RW, Stanley J, Markham PG: Identification of a novel circular single-stranded DNA associated with cotton leaf curl disease in Pakistan. Virology 1999, 259:190-199.
• [20]Saunders K, Stanley J: A nanovirus-like component associated with yellow vein disease of Ageratum conyzoides: evidence for interfamilial recombination between plant DNA viruses. Virology 1999, 264:142-152.
• [21]Nawaz-ul-Rehman MS, Nahid N, Mansoor S, Briddon RW, Fauquet CM: Post-transcriptional gene silencing suppressor activity of the alpha-Rep of non-pathogenic alphasatellites associated with begomoviruses. Virology 2010, 405:300-308.
• [22]Laufs J, Traut W, Heyraud F, Matzeit V, Rogers SG, Schell J, Gronenborn B: In vitro cleavage and joining at the viral origin of replication by the replication initiator protein of tomato yellow leaf curl virus. Proc Natl Acad Sci USA 1995, 92:3879-3883.
• [23]Hussain K, Hussain M, Mansoor S, Briddon RW: Complete nucleotide sequence of a begomovirus and associated betasatellite infecting croton (Croton bonplandianus) in Pakistan. Arch Virol 2011, 156:1101-1105.
• [24]Amin I, Mansoor S, Amrao L, Hussain M, Irum S, Zafar Y, Bull SE, Briddon RW: Mobilization into cotton and spread of a recombinant cotton leaf curl disease satellite. Arch Virol 2006, 151:2055-2065.
• [25]Saeed M, Behjatnia SAA, Mansoor S, Zafar Y, Hasnain S, Rezaian MA: A single complementary-sense transcript of a geminiviral DNA β satellite is determinant of pathogenicity. Mol Plant Microbe Interact 2005, 18:7-14.
• [26]Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P: RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 2010, 26:2462-2463.
• [27]De La Torre-Almaraz R, Monsalvo-Reyes A, Romero-Rodriguez A, Argüello-Astorga GR, Ambriz-Granados S: A new begomovirus inducing yellow mottle in okra crops in Mexico is related to Sida yellow vein virus. Plant Dis 2006, 90:378.
• [28]Paprotka T, Metzler V, Jeske H: The complete nucleotide sequence of a new bipartite begomovirus from Brazil infecting Abutilon. Arch Virol 2010, 155:813-816.
• [29]Hernandez-Zepeda C, Idris AM, Carnevali G, Brown JK, Moreno-Valenzuela OA: Molecular characterization and phylogenetic relationships of two new bipartite begomovirus infecting plants in Yucatan, Mexico. Virus Genes 2007, 35:369-377.
• [30]Kon T, Rojas MR, Abdourhamane IK, Gilbertson RL: The role and interactions of begomoviruses and satellite DNAs associated with okra leaf curl disease in Mali, West Africa. J Gen Virol 2009, 90:1001-1013.
• [31]Shih S, Kumar S, Tsai W, Lee L, Green S: Complete nucleotide sequences of okra isolates of Cotton leaf curl Gezira virus and their associated DNA-β from Niger. Arch Virol 2009, 154:369-372.
• [32]Tiendrébéogo F, Lefeuvre P, Hoareau M, Villemot J, Konate G, Traore A, Barro N, Traore V, Reynaud B, Traore O, Lett J-M: Molecular diversity of Cotton leaf curl Gezira virus isolates and their satellite DNAs associated with okra leaf curl disease in Burkina Faso. Virol J 2010, 7:48. BioMed Central Full Text
• [33]Idris AM, Briddon RW, Bull SE, Brown JK: Cotton leaf curl Gezira virus-satellite DNAs represent a divergent, geographically isolated Nile Basin lineage: predictive identification of a satDNA REP-binding motif. Virus Res 2005, 109:19-32.
• [34]Idris AM, Hussein MH, Abdel-Salam AM, Brown JK: Genetic variability of satellite DNA associated with monopartite begomoviruses of okra and hollyhock exhibiting vein thickening symptoms. Arab J Biotechnol 2002, 5:67-82.
• [35]Chen L-F, Rojas M, Kon T, Gamby K, Xoconostle-Cázares B, Gilbertson RL: A severe symptom phenotype in tomato in Mali is caused by a reassortant between a novel recombinant begomovirus (Tomato yellow leaf curl Mali virus) and a betasatellite. Mol Plant Pathol 2009, 10:415-430.
• [36]Hamon S, van Sloten DH: Malvaceae; Abelmoschus; Okra. In Evolution of crop plants. Second edition. Edited by Smartt J, Simmonds NW. Hrlow, UK: Longman Scientific and Technical; 1995:350-357.
• [37]Nawaz-ul-Rehman MS, Fauquet CM: Evolution of geminiviruses and their satellites. FEBS Lett 2009, 583:1825-1832.
• [38]Amin I, Mansoor S, Iram S, Khan MA, Hussain M, Zafar Y, Bull SE, Briddon RW, Markham PG: Association of monopartite begomovirus producing subgenomic DNA and a distinct DNA β on Croton bonplandianus showing yellow vein symptoms in Pakistan. Plant Dis 2002, 86:444.
• [39]Qazi J, Amin I, Mansoor S, Iqbal J, Briddon RW: Contribution of the satellite encoded gene βC1 to cotton leaf curl disease symptoms. Virus Res 2007, 128:135-139.
• [40]Idris AM, Shahid MS, Briddon RW, Khan AJ, Zhu J-K, Brown JK: An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation. J Gen Virol 2011, 92:706-717.
• [41]Xie K, Cai JH, Hu DM, Wei X, Jia Q, Qin BX, Chen BS, Meng JR, Liu YL: First report of okra leaf curl disease in China. J Plant Pathol, in press.
• [42]Lopez-Ochoa L, Ramirez-Prado J, Hanley-Bowdoin L: Peptide aptamers that bind to a geminivirus replication protein interfere with viral replication in plant cells. J Virol 2006, 80:5841-5853.
• [43]Rudolph C, Schreier PH, Uhrig JF: Peptide-mediated broad-spectrum plant resistance to tospoviruses. Proc Natl Acad Sci USA 2003, 100:4429-4434.
• [44]Jose J, Usha R: Bhendi yellow vein mosaic disease in India is caused by association of a DNA β satellite with a begomovirus. Virology 2003, 305:310-317.
• [45]Lodhi MA, Ye GN, Weeden NF, Reisch B: A simple and efficient method for DNA extraction from grapevine cultivars and Vitis species. Plant Mol Biol Rep 1994, 12:6-13.
• [46]Briddon RW, Bull SE, Mansoor S, Amin I, Markham PG: Universal primers for the PCR-mediated amplification of DNA β; a molecule associated with some monopartite begomoviruses. Mol Biotechnol 2002, 20:315-318.
• [47]Briddon RW, Mansoor S, Bedford ID, Pinner MS, Saunders K, Stanley J, Zafar Y, Malik KA, Markham PG: Identification of DNA components required for induction of cotton leaf curl disease. Virology 2001, 285:234-243.
• [48]Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ: Multiple sequence alignment with Clustal X. Trends Biochem Sci 1998, 23:403-405.
• [49]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5:Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [50]Padidam M, Sawyer S, Fauquet CM: Possible emergence of new geminiviruses by frequent recombination. Virology 1999, 265:218-225.
• [51]Smith JM: Analyzing the mosaic structure of genes. J Mol Evol 1992, 34:126-129.
• [52]Posada D, Crandall KA: The effect of recombination on the accuracy of phylogenetic estimation. J Mol Evol 2002, 54:396-402.
• [53]Gibbs MJ, Armstrong JS, Gibbs AJ: Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 2000, 16:573-582.
• [54]Boni MF, Posada D, Feldman MW: An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 2007, 176:1035-1047.