Narrow Bottlenecks Affect Pea Seedborne Mosaic Virus Populations during Vertical Seed Transmission but not during Leaf Colonization

Abstract

The effective size of populations (Ne) determines whether selection or genetic drift is the predominant force shaping their genetic structure and evolution. Populations having high Ne adapt faster, as selection acts more intensely, than populations having low Ne, where random effects of genetic drift dominate. Estimating Ne for various steps of plant virus life cycle has been the focus of several studies in the last decade, but no estimates are available for the vertical transmission of plant viruses, although virus seed transmission is economically significant in at least 18% of plant viruses in at least one plant species. Here we study the co-dynamics of two variants of Pea seedborne mosaic virus (PSbMV) colonizing leaves of pea plants (Pisum sativum L.) during the whole flowering period, and their subsequent transmission to plant progeny through seeds. Whereas classical estimators of Ne could be used for leaf infection at the systemic level, as virus variants were equally competitive, dedicated stochastic models were needed to estimate Ne during vertical transmission. Very little genetic drift was observed during the infection of apical leaves, with Ne values ranging from 59 to 216. In contrast, a very drastic genetic drift was observed during vertical transmission, with an average number of infectious virus particles contributing to the infection of a seedling from an infected mother plant close to one. A simple model of vertical transmission, assuming a cumulative action of virus infectious particles and a virus density threshold required for vertical transmission to occur fitted the experimental data very satisfactorily. This study reveals that vertically-transmitted viruses endure bottlenecks as narrow as those imposed by horizontal transmission. These bottlenecks are likely to slow down virus adaptation and could decrease virus fitness and virulence.

Analysis of viral (zucchini yellow mosaic virus) genetic diversity during systemic movement through a Cucurbita pepo vine

“…In addition, work with PPV in Prunus suggests that although the viral population within a host may harbour extensive genetic diversity, this diversity will be differentiated into sub-populations that reflect the physical structure of the tree (Jridi et al, 2006), and which will in turn influence the impact of any population bottleneck. The existence of relatively wide population bottlenecks, as noted here, has been reported in the case of some other plant viruses, (Fabre et al, 2014; Gutierrez et al, 2012) and may be of sufficient size to allow natural selection to proceed efficiently (Bergstrom et al, 1999). …”

Demographics of Natural Oral Infection of Mosquitos by Venezuelan Equine Encephalitis Virus

“…Again, comparisons of values between the two VEEV pairs should be made cautiously due to differences in the experimental design potentially influencing bottleneck sizes. Severe bottlenecks, on the order of single digits, are the rule during primary infection in the few virus models analyzed so far, despite involving unrelated viruses and different transmission modes (15)(16)(17)(18)(19)(20). Here, VEEV population sizes were between 1 and 2 orders of magnitude higher.…”

Interaction of virus populations with their hosts

“…Severe population bottlenecks occur during plant leave inoculation, and seed or aphid transmission of plant viruses, such as cucumber mosaic virus, tobacco mosaic virus, pea seedborne mosaic virus, and potato virus Y variants, among others (Li and Roossinck, 2004;Ali et al, 2006;Moury et al, 2007;Betancourt et al, 2008;Sacristan et al, 2011;Fabre et al, 2014;reviewed in Roossinck, 2008;Gutierrez et al, 2012). Aphids transmit an average of 0.5-5 virus particles into the recipient plant host, a range of values that is very similar to that estimated for HIV-1, with evidence that in about 75% of HIV-1-infected patients a single founder genome initiated the infection while in the others a minimum of two to five viruses was involved (Keele et al, 2008).…”