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Putative Gene Promoter Sequences in the Chlorella Viruses

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Putative Gene Promoter Sequences in the Chlorella Viruses View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by DigitalCommons@University of Nebraska University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Papers in Plant Pathology Plant Pathology Department 10-25-2008 Putative Gene Promoter Sequences in the Chlorella Viruses Lisa A. Fitzgerald University of Nebraska-Lincoln, [email protected] Philip Boucher University of Nebraska-Lincoln Giane Yanai-Balser University of Nebraska-Lincoln Karsten Suhre German Research Center for Environmental Health, 85764 Neuherberg, Germany Michael Graves University of Massachusetts-Lowell, Lowell, MA See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/plantpathpapers Part of the Plant Pathology Commons Fitzgerald, Lisa A.; Boucher, Philip; Yanai-Balser, Giane; Suhre, Karsten; Graves, Michael; and Van Etten, James L., "Putative Gene Promoter Sequences in the Chlorella Viruses" (2008). Papers in Plant Pathology. 128. https://digitalcommons.unl.edu/plantpathpapers/128 This Article is brought to you for free and open access by the Plant Pathology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in Plant Pathology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Lisa A. Fitzgerald, Philip Boucher, Giane Yanai-Balser, Karsten Suhre, Michael Graves, and James L. Van Etten This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/ plantpathpapers/128 Published in Virology 380:2 (October 25, 2008), pp. 388-393; doi 10.1016/j.virol.2008.07.025 Copyright © 2008 Elsevier Inc. Used by permission. http://www.sciencedirect.com/science/journal/00426822 Submitted June 23, 2008; revised July 8, 2008; accepted July 18, 2008; published online September 2, 2008. Putative gene promoter sequences in the chlorella viruses Lisa A. Fitzgerald,1,6 Philip T. Boucher,1 Giane M. Yanai-Balser,1 Karsten Suhre,2,3 Michael V. Graves,4 and James L. Van Etten,1,5 1 Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA 2 Institute of Bioinformatics and Systems Biology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Neuherberg, Germany 3 Department of Biology, Ludwig-Maximilians-Universität, 82152 Planegg-Martinsried, Germany 4 Department of Biological Sciences, University of Massachusetts-Lowell, Lowell, MA 01854, USA 5 Nebraska Center for Virology, University of Nebraska-Lincoln, Lincoln, NE 68583-0900, USA 6 Current address — National Institute of Standards and Technology, Gaithersburg, MD 20899, USA Corresponding author — James L. Van Etten, Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583-0722, USA. Fax 402 472-2853. Abstract Three short (7 to 9 nucleotides) highly conserved nucleotide sequences were identified in the putative promoter regions (150 bp upstream and 50 bp downstream of the ATG translation start site) of three members of the genus Chlorovirus, family Phycodnaviridae. Most of these sequences oc- curred in similar locations within the defined promoter regions. The sequence and location of the motifs were often conserved among homolo- gous ORFs within the Chlorovirus family. One of these conserved sequences (AATGACA) is predominately associated with genes expressed early in virus replication. Keywords: Chlorella viruses, Phycodnaviridae, Chlorovirus, Virus PBCV-1, Virus NY-2A, Virus MT325, Promoters Introduction PBCV-1 infects its host by attaching rapidly to the external sur- face of the algal cell wall (Meints et al., 1984). Attachment occurs Chlorella viruses (family Phycodnaviridae, genus Chlorovirus) at a unique virus vertex (Onimatsu et al., 2006) and is followed by are large, icosahedral, plaque-forming, dsDNA-containing vi- digestion of the cell wall at the attachment point. Following host ruses that infect and replicate in certain isolates of chlorella-like wall degradation, the PBCV-1 internal membrane presumably green algae. The 330-kb genome of the prototype virus, Parame- fuses with the host membrane, which leads to the entry of virus cium bursaria chlorella virus 1 (PBCV-1), was sequenced and an- DNA and probably associated proteins into the host. An empty notated more than 10 years ago (Li et al., 1997). The virus contains capsid remains on the host surface. Circumstantial evidence sug- 366 putative protein-encoding genes and a polycistronic gene that gests that the infecting PBCV-1 DNA, and DNA associated pro- encodes 11 tRNAs ([Li et al., 1997] and [Van Etten, 2003]). Approx- teins, rapidly move to the nucleus to initiate virus transcription imately 40% of its predicted gene products resemble proteins of (Van Etten, 2003). Support for this hypothesis includes the fact known function and many are unexpected for a virus. Currently, that neither PBCV-1 nor any of the chlorella viruses encode a rec- three species are included in the genus Chlorovirus: i) viruses that ognizable RNA polymerase or RNA polymerase subunit. Fur- infect Chlorella NC64A (NC64A viruses), ii) viruses that infect Chlo- thermore, RNA polymerase activity was not detected in PBCV-1 rella Pbi (Pbi viruses) and iii) viruses that infect symbiotic zooch- virions (Rohozinski and Van Etten, unpublished results). Conse- lorella in the coelenterate Hydra viridis (Yamada et al., 2006). Chlo- quently, assuming that the infecting viral DNA moves to the nu- rella NC64A and Chlorella Pbi are normally endosymbionts of the cleus, it must commandeer one of the host’s RNA polymerases protozoan Paramecium bursaria, but they can be cultured indepen- (probably RNA polymerase II) to initiate viral transcription (Van dently of the protozoan. The current study involves three chlorella Etten, 2003). Therefore, the host polymerase(s), possibly in com- viruses whose genomes have been sequenced: viruses PBCV-1 bination with a virus protein(s), must recognize some virus DNA and NY-2A (Fitzgerald et al., 2007b) are NC64A viruses with 330- promoter sequence(s) to initiate transcription. This process occurs kb and 369-kb genomes, respectively, and virus MT325, a Pbi vi- rapidly because early PBCV-1 transcripts can be detected within rus with a 314-kb genome (Fitzgerald et al., 2007a). 5 to 10 min post-infection (p.i.) (Schuster et al., 1986). Virus DNA 388 P UTATIVE GENE P ROMOTER SEQUENCES IN THE CHLORELLA VIRUSES 389 Figure 1. Genomic locations of homologous genes between NY-2A and either PBCV-1 or MT325. When a homologous gene is detected between NY-2A and another genome a line is drawn. If the gene is transcribed in the same direction the line is blue. If the gene is transcribed in the opposite direction the line is red. replication starts 60 to 90 min p.i., followed by transcription of late (Fitzgerald et al., 2007b), whereas the average amino acid iden- virus genes. Nascent virus capsids begin to assemble in localized tity between PBCV-1 and MT325 is ~ 50% (Fitzgerald et al., 2007a). regions of the cytoplasm, called virus assembly centers, at 2 to 4 h Most PBCV-1 and NY-2A gene homologs are located co-linearly; p.i. By 5 to 6 h p.i. the cytoplasm contains many progeny viruses in contrast, homologous genes in PBCV-1 and MT325 have almost and by 6 to 8 h p.i. the cell lyses and releases progeny viruses (~ no co-linearity with each other (Figure 1). Thus, the promoter el- 1000 particles/cell). ements of the two NC64A viruses might be expected to be more Thus, PBCV-1 transcription is temporally programmed. Genes similar to each other than between NC64A and Pbi viruses. defined as “early” are transcribed within 5–60 min p.i.; some of The following criteria were originally used to define genes in the earliest transcripts form in the absence of de novo protein syn- the three viruses: i) a minimal size of 65 codons initiated by an thesis (Schuster et al., 1986, Yanai-Balser et al., unpublished re- ATG codon, ii) when genes overlapped, the largest gene was cho- sults). Transcripts of genes defined as “late” begin to appear 60– sen and iii) genes typically contain A + T-rich (> 70%) regions in 90 min p.i.; their appearance probably requires translation of early the 50 nucleotides upstream of the ATG translation start codon (Li viral genes. However, some early gene transcripts can also be de- et al., 1997). For this study, promoter regions were defined as en- tected in later stages of infection. The PBCV-1 genes are not spa- compassing a 200-bp region (150 bp upstream and 50 bp down- tially clustered on the genome by either temporal or functional stream of the ATG translation start site) of each viral encoded class. Therefore, temporal regulation of transcription must occur gene. However, the intergenic regions between PBCV-1 genes via cis- and possibly trans-acting regulatory elements. have an average size of 81 nucleotides with a standard deviation The purpose of the current study is to identify conserved DNA of 83 nucleotides (excluding the two-tailed 5% most extreme data sequences that might be involved in activation and regulation of points). In fact, 260 of the 366 PBCV-1 genes have less than 100 nu- viral transcription by using bioinformatic procedures. We iden- cleotides between them. Using this definition, many of the puta- tified three conserved nucleotide sequences that appear within tive viral promoter regions are located in an adjacent gene. 150 nucleotides of the ATG translation start codon of many vi- rus genes. One of these motifs is associated predominately with Three conserved sequences occur in the chlorella virus promoter regions early viral gene transcription and is likely to serve as a promoter for early genes. Using AlignAce software, three highly conserved nucleotide sequences were identified in the PBCV-1 promoter regions (Fig- Results and discussion ure 2). These sequences were optimized as described in the Mate- rials and methods section to generate three sequences that range Viruses analyzed and criteria used to define genes and promoter regions in size from 7 to 9 nucleotides (Table 1); one or more degenerate in this study positions occur in two of the three sequences.
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