PIPS OPEN 3 ACCESS Freely available online BIOLOGY Community Page Plant Virus Biodiversity and Ecology Jonathan D. Wren, Marilyn J. Roossinck, Richard S. Nelson, Kay Scheets, Michael W. Palmer, Ulrich Melcher* The International Committee Identification Data for the Taxonomy of Viruses Exchange database [4]. IM* ac4Md from • piif« recognized a global total of Most of the available about 2,000 species of viruses as of virus information we 2005 [1]. However, data on viruses have is derived from v««a that infect terrestrial organisms, cultivated crop species, M including plants, are sparse, and recent yet these species only sequencing of samples from marine comprise a minute environments for viruses suggests fraction of all plant that 2,000 is a gross underestimate of species. And much the total number of viral species on of this information earth [2]. In addition to the paucity is derived from of data on viral diversity, little is symptomatic hosts, yet known about the level of mixed virus only a small fraction infections or temporal patterns of virus of viruses probably accumulation in native plants. For cause disease [5]. both social and scientific reasons, it is Furthermore, much important to extend our knowledge of of the data gathered 7?fc viruses and their hosts beyond those on viruses come from DOI: 10.1371/joui nal.pbio.0040080.g001 combinations currently known to monocultures, which cause disease to those that may cause favors a low diversity. Figure 1. Frequenciesof Sources of Plants from Which disease in the future (i.e., emerging Thus, the data gathered Recognized Plant Viruses Were Initially Isolated threats). In addition, we need to gain a so far have not only greater understanding of the potential been heavily skewed toward crop- later be recognized as the origins for mutualistic interactions between affecting viruses, but also toward of future crop scourges. Knowledge viruses and their hosts. That is, we standard, laboratory-strain, phenotype- now of their existence and ecology traditionally view viruses as parasites, producing viruses. The presence of will allow us to better prepare and which is not surprising given their viruses in plants seems to be relatively prevent the catastrophic outcomes prominent role as pathogens, but this common—for example, approximately often associated with such outbreaks. is not always the case. Consider, for 60% of plants surveyed in a Costa Rican example, polydnavirus-braconid wasp region containing about 7,000 plant interactions, in which the virus carries species total were positive for double- the essential genes required to suppress stranded RNA, a marker suggesting the Citation: Wren JD. Roossinck MJ. Nelson RS. Scheets K, Palmer MW. et al. (2006) Plant virus biodiversity the immune system of the lepidopteran presence of viruses (M.J. Roossinck, and ecology. PLoS Biol 4(3): e80. hosts of the wasp [3]. This is a frontier unpublished data). Taken together, that is largely unexplored. The these observations suggest a huge gap DOI: 10.1371/joui nal.pbio.0040080 Plant Virus Biodiversity and Ecology in our overall understanding of viral Copyright: © 2006 Wren et al. This is an open-access (PVBE) project has been initiated diversity, evolution, and ecology. article distributed under the terms of the Creative to survey the biodiversity of viruses Commons Attribution License, which permits Closing this gap begins with a broad unrestricted use. distribution, and reproduction in affecting vascular plants, including any medium, provided the original author and source their endophytic fungi, in The Nature cataloging and study of viruses affecting are credited. wild plants, whether symptomatic Conservancy's Tallgrass Prairie Preserve or asymptomatic, to gain a more Abbreviation: PVBE. Plant Virus Biodiversity and of Oklahoma, home to over 700 plant Ecology objective view of virus populations species. Plants are an ideal starting in nature. Ostensibly, it ends with a Jonathan D. Wren is in the Advanced Center for point for studies on virus ecology since GenomeTechnology. Stephenson Research and better understanding of the mutualistic they are immobile and can be readily Technology Center. Department of Botany and resampled. Viral screening is done interactions between viruses and their Microbiology, the University of Oklahoma. Norman. hosts. Newly discovered viruses will Oklahoma. United States of America. Marilyn J. using double-stranded RNA analysis, Roossinck and Richard S. Nelson are at the Samuel provide information for those doing cloning, sequencing, and microarray Roberts Noble Foundation. Plant Biology Division. analysis. The PVBE effort is not basic research on the mechanisms of Ardmore. Oklahoma. United States of America. Kay virus replication, translation, particle Scheets and Michael W. Palmer are In the Department directed toward studying economically of Botany. Oklahoma State University. Stillwater. assembly, and movement, as well important or symptomatic plants, Oklahoma. United States of America. Ulrich Melcher as provide tools for biotechnology is inthe Department of Biochemistry and Molecular both of which are already heavily (e.g., potential new vectors for gene Biology. Oklahoma State University. Stillwater. studied. Information in Figure 1, for Oklahoma. United States of America. knockdown studies through virus- example, summarizes the initial plant source of viruses cataloged in the Viral induced gene silencing). It is possible * To whom correspondence should be addressed. E- that some of these new viruses may mall: [email protected]; u-melcher-4@ alumnl.uchicago.edu ). PLOS Biology | www.plosbiology.org 0314 March 2006 | Volume 4 | Issue 3 | e80 Gathering information on these viruses their hosts, viruses could potentially of data from The Nature Conservancy's will also increase our ability to do be prime drivers of evolutionary Tallgrass Prairie Preserve area alone, more extensive sequence comparisons change. The degree to which viruses but the addition of other geographical between viruses, thereby allowing better have determined micro- and macro- areas will eventually provide a much predictions for active site identities evolutionary patterns in vascular plants bigger picture of continental and within viral proteins, and to identify is mostly unexplored, and the relevant global trends in plant virus biodiversity novel viral proteins and their functions. questions are not obvious. Comparing and ecology, a new and emerging field Not only will these efforts help us virus phylogenies to plant phylogenies of study that will hopefully enable us to understand virus ecology, but there is will allow us to generate hypotheses answer these important questions. • also great potential for revolutionizing about the nature of their coevolution plant ecology. The extended phenotype and to push ecology beyond the simple Acknowledgments of a virus may affect a plant's local concepts of competition, mutualism, Funding. The PVBE effort is funded adaptation to its environment. parasitism, and prédation. by NSF Grant Number EPS-0447262 and Endophytes, mycorrhizae, or other The PVBE effort faces multiple supported by the Oklahoma Agricultural symbionts could potentially mediate challenges, including creating Experiment Station whose director has such interactions. Given that many resources for an effort sustainable approved the manuscript for publication. Competing interests. The authors have plant viruses are generalists with beyond the funding period and declared that no competing interests exist. respect to host species, it is theoretically providing tools for the analysis of possible that such effects may be geographic and temporal infection References ecosystem-wide. RNA silencing [6] has patterns that can be applied to other 1. Fauquet CM, Mayo MA, Mamloff J, dramatic but unexplored ecological systems. One of our goals is to establish Desselberger U, Ball LA, editors (2005) Virus implications. As a hypothetical a community resource for information taxonomy: Vlllth Report of the International example, a bison-borne virus could on plant viruses and their relationships Committee on Taxonomy of Viruses. San Diego: Elsevier Academic Press. 1162 p. silence genes for antigrazing defenses, with noncrop plant hosts. This will 2. Breitbart M, Rohwer F (2005) Here a virus, thus facilitating its transmission. help us to better estimate the global there a virus, everywhere the same virus? Trends Microbiol 13: 278-284. Known virus-vector-host systems number of plant viruses and to address 3. Turnbull M, Webb B (2002) Perspectives on exhibit a bewildering complexity. It the following important scientific polydnavims origins and evolution. AdvVims is increasingly evident that the simple questions: what is the relationship Res 58: 203-254. 4. Brunt AA, Crabtree K, Dallwitz MJ, Gibbs AJ, view of viruses as pathogens is outdated. between virus biodiversity and host Watson L, et al., editors (1996) Plant viruses As "little pieces of genetic information" biodiversity? how often do coinfections online: Descriptions and lists from the VIDE transferred from one organism to by different viruses occur in natural database. Available: http://image.fs.uidaho. another, they have potential for systems? and what is the incidence of 5. Redouo/svsiindcek/ rMefJs .(h2t0m0.5 )A Sccyemssbeiods i1s8 v Jearnsuusa ry 2006. facilitating all sorts of interactions disease-inducing viruses compared with competition in plant virus evolution. Nat Rev among macroscopic life. Given asymptomatic or beneficial viruses in Microbiol 3: 917-924. intimate genetic interactions with natural systems? We anticipate a wealth 6. Baulcombe D (2005) RNA silencing. Trends Biochem Sei 30: 290-293. ). PLOS Biology | www.plosbiology.org 0315 March 2006 | Volume 4 | Issue 3 | e80