Five RNA species, which are identified by the size and the results of hybridization to two different probes, are depicted below the construct. Four RNA species are schematically drawn below the construct. The FHV sequences are indicated in thick lines. TY-eGFP was included as a control. The proteins were transferred to a nitrocellulose membrane. Plant material Agroinfiltration of the Agrobacterium tumefaciens harboring various TYMV constructs into Nicotiana benthamiana was carried out as previously described Western analysis of eGFP expression Leaf samples 0.
References 1. Dreher T. Turnip yellow mosaic virus: transfer RNA mimicry, chloroplasts and a C-rich genome. Plant Pathol. Targeting of the Turnip Yellow Mosaic Virus 66K replication protein to the chloroplast envelope is mediated by the K protein.
Chen J. Viral virulence protein suppresses RNA silencing-mediated defense but upregulates the role of microRNA in host gene expression. Plant Cell. Yildiz I. Applications of viral nanoparticles in medicine. Shin H. Replication and encapsidation of recombinant Turnip yellow mosaic virus RNA. Ball L. Requirements for the self-directed replication of Flock house virus RNA1.
Induction and suppression of RNA silencing by an animal virus. Selling B. Genomic RNA of an insect virus directs synthesis of infectious virions in plants. Price B. Indeed, when a virus is first described on a specific plant, plants from the same genus or family are frequently over-represented in subsequent host range studies, and very distant species e.
Third, the host change inference is largely based on parsimony principles which minimize the numbers of host changes per branch length i. The inferred host gains, host losses, and total host changes were fairly distributed among the main potyvirus clades and among the main plant families examined. However, it should be emphasized that most plant species belonged to only six families corresponding to important groups of crop species, what may introduce a bias.
This high relative frequency of host gains in terminal branches is compatible with a role of host jumps on the specialization and isolation of virus populations in new plant species environments and subsequently on potyvirus speciation [ 28 ].
Host gains inferred on internal branches of the potyvirus phylogenetic tree were scarcer and concentrated on a few branches. While the global radiation of potyviruses took place circa years ago, the diversification of some clades into species was estimated around years ago [ 28 , 29 ], and intraspecific diversification probably took place only a few centuries ago [ 30 , 31 ].
Indeed, many host—virus encounters that could lead to host jumps took place less than years ago with the intensification of intercontinental exchanges of plants [ 30 , 32 ]. Given the small number of plant species analyzed in the present study and the bias in favor of crop species, it is unlikely to help identifying the plant species or families from which the genus Potyvirus originated.
Five of the remaining species are laboratory plants chosen in many studies because of their susceptibility to many viruses, inducing either local lesions or systemic infections Chenopodium amaranticolor , C.
The three other plant species Lathyrus odoratus , Lupinus albus, and Trigonella foenum-graecum belong to the same family Fabaceae and originate from the Near East or the Mediterranean Basin. However, the accuracy of their inference as hosts of the potyvirus MRCA should be taken with care because relatively few viruses of our dataset have been tested on these plants 13 or Gibbs and Ohshima [ 18 ] assumed that the Potyvirus genus emerged from wild monocotyledonous plants around the Fertile Crescent of the Middle East.
This assumption was based on the topology of the potyvirus phylogenetic tree. However, early-branching lineages do not necessarily signify ancestral traits as emphasized by Crisp and Cook [ 33 ] and intuitive assertion of ancestry from phylogenetic trees may be misleading. In our analyses, the five monocots Allium cepa and four species of the Poaceae were inferred to be non-hosts for the potyvirus MRCA but were only tested against a small subset of viruses 12 to 15, except Zea mays , a New World Poaceae, which was tested against 25 viruses.
It remains also possible that, after jumping to crop plants, the ancestor of potyviruses had lost the capacity to infect plants belonging to its original species or family. Molecular determinants of host jumps are largely unknown for plant viruses but see [ 3 ] and references therein , in contrast with molecular determinants involved in the breakdown of resistance genes, i.
Perhaps the most striking result of this study is the large number of repeated correlated host gains in the potyvirus phylogenetic tree, i. It is questionable whether the molecular events involved in these different host changes are independent or not.
Many of these correlated host gains occurred several times in the potyvirus phylogenetic tree and the frequency of such recurrent events largely outweighs the expectations of chance. Hence, it is probable that several of these host gains were not independent and that the acquired capacity to infect a first plant species increased the probability that the virus also acquired the capacity to infect a second plant species.
Underlying molecular mechanisms could be either pleiotropy, i. Recombination is also widespread in potyviruses and may alter their genome in such a drastic way that multiple traits could be affected simultaneously by a single recombination event.
In that case, we would expect that recurrent co-occurrences of host gains would preferentially affect plant species from the same geographical origin. Both the molecular and bridgehead hypotheses are supported by the fact that plant species corresponding to repeated host gain co-occurrences belong more frequently to the same botanical family or share more frequently the same continent of origin than expected under random.
This study shows that the potyvirus host range followed a dynamic pattern, with frequent gains or losses during evolution and, surprisingly, frequent and repeated co-occurrences of host gains in different potyvirus clades. It also confirms the potentially important role of agriculture and crop plants on the diversification of potyviruses. Consequently, potyvirus evolution and speciation in the future could be strongly affected by future agricultural changes, such as the choice of new crop species or of growing crop species in new geographical areas.
Indeed, agricultural environments are favorable for virus adaptation, specialization, and speciation, given the large number and genetic homogeneity of hosts in crops [ 27 , 28 , 36 ]. The molecular determinants involved in potyvirus host jumps, either from the virus or the plant side, are largely unknown but see [ 6 , 14 , 16 ].
Given the multiple virus and host factors interacting during virus infection [ 37 , 38 , 39 ], it would be interesting to test formally the hypothesis of common genetic determinants involved in multiple host gains in potyviruses by reverse genetics approaches.
Our study suggests candidate potyviruses and plant species for these approaches Table 3. We thank Emmanuel Szadkowski and Loup Rimbaud for insightful comments on a previous version of the manuscript. Branches with no changes and changes for which alternative scenarios exist are omitted; Table S3: Branches in the potyvirus phylogenetic tree where the number of inferred host gains significantly exceeded expectations of random distributions; Table S4.
Co-occurrence of host losses i. For each batch of 10, simulations, an identical number N of host and non-host statuses corresponding to a fictitious plant species was fixed. Then, each simulation involved the two following steps. This allowed obtaining the probability P 64 that the plant species was host of the potyvirus MRCA corresponding to branch 64 Figure 1.
Table A1 indicates that between 0. Conceptualization: B. All authors have read and agreed to the published version of the manuscript. National Center for Biotechnology Information , U. Journal List Viruses v. Published online Jan Author information Article notes Copyright and License information Disclaimer. Received Dec 12; Accepted Jan This article has been cited by other articles in PMC.
Associated Data Supplementary Materials virusess Abstract Virus host range, i. Keywords: potyvirus, potyviridae, ancestral reconstruction, discrete character, host jump, host shift, host range expansion.
Introduction Host range of a parasite is defined as the set of organisms where the parasite can perform, at least partly, its infection cycle.
Materials and Methods 2. Collating Host Range Data Host range data of potyvirus species were obtained from two bibliographic sources, which have established quite exhaustive lists of host and non-host plant species for each potyvirus species [ 18 , 20 ]. Phylogenetic Analyses For each potyvirus species for which we could obtain host range data, we checked whether full genome or near full genome sequences were available in databanks. Results 3. Building a Potyvirus and Rymovirus Phylogenetic Tree To identify host range changes during the evolution of potyviruses, we first established the phylogenetic relationships between 62 virus species for which genome and host range data were available: 59 Potyvirus species and three Rymovirus species used as outgroups.
Open in a separate window. Figure 1. Both the striped flea beetle Phyllotreta striolata F. Cruciferae Goeze , reported vectors of the virus 1 , were present at each site. Infected plants exhibited bright yellow to yellow-green mosaic mottling and often showed chlorotic lesions on the lower leaves.
Strains or suspected strains of turnip mosaic virus include: Anemone mosaic virus syn: Anemone latent virus ; Brassica nigra mosaic virus; cabbage black ringspot virus syn: cabbage black spot, Brassica virus 1 ; cabbage black ring virus; cabbage ring necrosis virus syn: brassicavirus annulolaedens ; cabbage virus A.
It is carried by 40 to 50 species of aphids but especially by the cabbage aphid and green peach aphid Myzus persicae Sulzer. It also can be transmitted by diseased leaves being rubbed against healthy ones" Chupp and Sherf, The virus is "transmitted in a nonpersistent manner" Pink and Walkey, , which means that the virus reproduces in the plant and that aphids simply aid in transporting the virus.
Because turnip mosaic virus is nonpersistant, controlling for aphids is futile. To control internal necrosis, only cabbage heads that are symptomless in the field should be stored for any length of time Walkey and Webb, Resistant cultivars: Pink and Walkey examined the resistance of sixteen cauliflower cultivars to turnip mosaic virus. There was no correlation between symptoms of glasshouse-grown plants and field-grown plants. Thus, resistant cultivar studies should be conducted on field-grown plants.
Overall none of the cultivars was very resistant to the virus. Lim et al. Two Korean cultivars were resistant in all three plantings: Nabyeng 60 days and Kongng 3, with an average infection of 1. Neither cultivar is heat tolerant. Two other cultivars, Tip Top Japan and Ta Feng Taiwan were found to be resistant in fall field plantings and moderately resistant in spring plantings
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