Intra-specific variability and biological relevance of P3N-PIPO protein length in potyviruses

BMC Evolutionary Biology

José M Cuevas²  Santiago F Elena³  Julia Hillung¹ 

[1] Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, València 46022, Spain;Present address: Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, València 46980, Spain;The Santa Fe Institute, 87501, Santa Fe, NM, USA

关键词: Virus fitness components;    Virus evolution;    Potyvirus;    Molecular evolution;    Host-range determinants;    Bayesian phylogenetic methods;   

Others  :  1085156
DOI  :  10.1186/1471-2148-13-249

 received in 2013-08-29, accepted in 2013-11-06,  发布年份 2013

【 摘 要 】

Background

Pipo was recently described as a new ORF encoded within the genome of the Potyviridae family members (PNAS 105:5897–5902, 2008). It is embedded within the P3 cistron and is translated in the +2 reading frame relative to the potyviral long ORF as the P3N-PIPO fusion protein. In this work, we first collected pipo nucleotide sequences available for different isolates of 48 Potyvirus species. Second, to determine the biological implications of variation in pipo length, we measured infectivity, viral accumulation, cell-to-cell and systemic movements for two Turnip mosaic virus (TuMV) variants with pipo alleles of different length in three different susceptible host species, and tested for differences between the two variants.

Results

In addition to inter-specific variation, there was high variation in the length of the PIPO protein among isolates within species (ranging from 1 to 89 amino acids). Furthermore, selection analyses on the P3 cistron did not account for the existence of stop codons in the pipo ORF, but showed that positive selection was significant in the overlapping region for Potato virus Y (PVY) and TuMV. In some cases, variability in length was associated with host species, geographic provenance and/or other strain features. We found significant empirical differences among the phenotypes associated with TuMV pipo alleles, though the magnitude and sign of the effects were host-dependent.

Conclusions

The combination of computational molecular evolution analyses and experiments stemming from these analyses provide clues about the selective pressures acting upon the different-length pipo alleles and show that variation in length may be maintained by host-driven selection.

【 授权许可】

   
2013 Hillung et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Riechmann JL, Lain S, García JA: Highlights and prospects of potyvirus molecular biology. J Gen Virol 1992, 73:1-16.
• [2]Ward CW, Shukla DD: Taxonomy of potyviruses: current problems and some solutions. Intervirology 1991, 32:269-296.
• [3]Kong WP, Roos RP: Alternative translation initiation site in the DA strain of Theiler's murine encephalomyelitis virus. J Virol 1991, 65:3395-3399.
• [4]Green KY, Ando T, Balayan MS, Berke T, Clarke IN, Estes MK, Matson DO, Nakata S, Neill JD, Studdert MJ, et al.: Taxonomy of the caliciviruses. J Infect Dis 2000, 181:S322-S330.
• [5]van der Wilk F, Dullemans AM, Verbeek M, van den Heuvel JF: Nucleotide sequence and genomic organization of Acyrthosiphon pisum virus. Virology 1997, 238:353-362.
• [6]Urcuqui-Inchima S, Haenni AL, Bernardi F: Potyvirus proteins: a wealth of functions. Virus Res 2001, 74:157-175.
• [7]Chung BY, Miller WA, Atkins JF, Firth AE: An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci U S A 2008, 105:5897-5902.
• [8]Wei T, Zhang C, Hong J, Xiong R, Kasschau KD, Zhou X, Carrington JC, Wang A: Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Pathog 2010, 6:e1000962.
• [9]Wen RH, Hajimorad MR: Mutational analysis of the putative PIPO of Soybean mosaic virus suggests disruption of PIPO protein impedes movement. Virology 2010, 400:1-7.
• [10]Vijayapalani P, Maeshima M, Nagasaki-Takekuchi N, Miller WA: Interaction of the trans-frame Potyvirus protein P3N-PIPO with host protein PCaP1 facilitates potyvirus movement. PLoS Pathog 2012, 8:e1002639.
• [11]Lin L, Luo Z, Yan F, Lu Y, Zheng H, Chen J: Interaction between potyvirus P3 and ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) of host plants. Virus Genes 2011, 43:90-92.
• [12]Choi SH, Hagiwara-Komoda Y, Nakahara KS, Atsumi G, Shimada R, Hisa Y, Naito S, Uyeda I: Quantitative and qualitative involvement of P3N-PIPO in overcoming recessive resistance against Clover yellow vein virus in pea carrying the cyv1 gene. J Virol 2013, 87:7326-7337.
• [13]Cuevas JM, Delaunay A, Visser JC, Bellstedt DU, Jacquot E, Elena SF: Phylogeography and molecular evolution of Potato virus Y. PLoS ONE 2012, 7:e37853.
• [14]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
• [15]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.
• [16]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.
• [17]Ilardi V, Nicola-Negri ED: Genetically engineered resistance to Plum pox virus infection in herbaceous and stone fruit hosts. GM Crops 2011, 2:24-33.
• [18]Schubert J, Fomitcheva V, Sztangret-Wisniewska J: Differentiation of Potato virus Y strains using improved sets of diagnostic PCR-primers. J Virol Methods 2007, 140:66-74.
• [19]Ohshima K, Tomitaka Y, Wood JT, Minematsu Y, Kajiyama H, Tomimura K, Gibbs AJ: Patterns of recombination in Turnip mosaic virus genomic sequences indicate hotspots of recombination. J Gen Virol 2007, 88:298-315.
• [20]Pond SL, Frost SD, Grossman Z, Gravenor MB, Richman DD, Brown AJ: Adaptation to different human populations by HIV-1 revealed by codon-based analyses. PLoS Comput Biol 2006, 2:e62.
• [21]Kosakovsky Pond SL, Frost SD: Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 2005, 22:1208-1222.
• [22]Delport W, Poon AF, Kosakovsky , Pond SL: Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010, 26:2455-2457.
• [23]Drummond AJ, Rambaut A: BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214. BioMed Central Full Text
• [24]Parker J, Rambaut A, Pybus OG: Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect Genet Evol 2008, 8:239-246.
• [25]Slatkin M, Maddison WP: A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics 1989, 123:603-613.
• [26]Wang TH, Donaldson YK, Brettle RP, Bell JE, Simmonds P: Identification of shared populations of Human immunodeficiency virus type 1 infecting microglia and tissue macrophages outside the central nervous system. J Virol 2001, 75:11686-11699.
• [27]Chen CC, Chao CH, Chen CC, Yeh SD, Tsai HT, Chang CA: Identification of Turnip mosaic virus isolates causing yellow stripe and spot on calla lily. Plant Dis 2003, 87:901-905.
• [28]Lafforgue G, Tromas N, Elena SF, Zwart MP: Dynamics of the establishment of systemic Potyvirus infection: independent yet cumulative action of primary infection sites. J Virol 2012, 86:12912-12922.
• [29]Gibbs AJ, Ohshima K, Phillips MJ, Gibbs MJ: The prehistory of potyviruses: their initial radiation was during the dawn of agriculture. PLoS ONE 2008, 3:e2523.
• [30]Glasa M, Malinowski T, Predajna L, Pupola N, Dekena D, Michalczuk L, Candresse T: Sequence variability, recombination analysis, and specific detection of the W strain of Plum pox virus. Phytopathology 2011, 101:980-985.
• [31]Felsenstein J: Phylogenies and the comparative method. Am Nat 1985, 125:1-15.
• [32]Zwart MP, Daròs JA, Elena SF: One is enough: In vivo effective population size is dose-dependent for a plant RNA virus. PLoS Pathog 2011, 7:e1002122.
• [33]Zwart MP, Daròs JA, Elena SF: Effect of potyvirus effective population size in inoculated leaves on viral accumulation and the onset of symptoms. J Virol 2012, 86:9737-9747.
• [34]Agudelo-Romero P, Carbonell P, Pérez-Amador MA, Elena SF: Virus adaptation by manipulation of host's gene expression. PLoS ONE 2008, 3:e2397.
• [35]Jenner CE, Wang X, Tomimura K, Ohshima K, Ponz F, Walsh JA: The dual role of the potyvirus P3 protein of Turnip mosaic virus as a symptom and avirulence determinant in brassicas. Mol Plant Microbe Interact 2003, 16:777-784.
• [36]Suehiro N, Natsuaki T, Watanabe T, Okuda S: An important determinant of the ability of Turnip mosaic virus to infect Brassica spp. and/or Raphanus sativus is in its P3 protein. J Gen Virol 2004, 85:2087-2098.
• [37]Kim BM, Suehiro N, Natsuaki T, Inukai T, Masuta C: The P3 protein of Turnip mosaic virus can alone induce hypersensitive response-like cell death in Arabidopsis thaliana carrying TuNI. Mol Plant Microbe Interact 2010, 23:144-152.
• [38]Hjulsager CK, Olsen BS, Jensen DM, Cordea MI, Krath BN, Johansen IE, Lund OS: Multiple determinants in the coding region of Pea seed-borne mosaic virus P3 are involved in virulence against sbm-2 resistance. Virology 2006, 355:52-61.
• [39]Desbiez C, Gal-On A, Girard M, Wipf-Scheibel C, Lecoq H: Increase in Zucchini yellow mosaic virus symptom severity in tolerant zucchini cultivars is related to a point mutation in P3 protein and is associated with a loss of relative fitness on susceptible plants. Phytopathology 2003, 93:1478-1484.
• [40]Glasa M, Svoboda J, Novakova S: Analysis of the molecular and biological variability of Zucchini yellow mosaic virus isolates from Slovakia and Czech Republic. Virus Genes 2007, 35:415-421.
• [41]Eggenberger AL, Hajimorad MR, Hill JH: Gain of virulence on Rsv1-genotype soybean by an avirulent Soybean mosaic virus requires concurrent mutations in both P3 and HC-Pro. Mol Plant Microbe Interact 2008, 21:931-936.
• [42]Wen RH, Maroof MA, Hajimorad MR: Amino acid changes in P3, and not the overlapping PIPO-encoded protein, determine virulence of Soybean mosaic virus on functionally immune Rsv1-genotype soybean. Mol Plant Pathol 2011, 12:799-807.
• [43]Tan Z, Gibbs AJ, Tomitaka Y, Sánchez F, Ponz F, Ohshima K: Mutations in Turnip mosaic virus genomes that have adapted to Raphanus sativus. J Gen Virol 2005, 86:501-510.
• [44]Choi IR, Horken KM, Stenger DC, French R: An internal RNA element in the P3 cistron of Wheat streak mosaic virus revealed by synonymous mutations that affect both movement and replication. J Gen Virol 2005, 86:2605-2614.