Comparing patterns and scales of plant virus phylogeography: Rice yellow mottle virus in Madagascar and in continental Africa

Abstract

Rice yellow mottle virus (RYMV) in Madagascar Island provides an opportunity to study the spread of a plant virus disease after a relatively recent introduction in a large and isolated country with a heterogeneous host landscape ecology. Here, we take advantage of field survey data on the occurrence of RYMV disease throughout Madagascar dating back to the 1970s, and of virus genetic data from ninety-four isolates collected since 1989 in most regions of the country to reconstruct the epidemic history. We find that the Malagasy isolates belong to a unique recombinant strain that most likely entered Madagascar through a long-distance introduction from the most eastern part of mainland Africa. We infer the spread of RYMV as a continuous process using a Bayesian statistical framework. In order to calibrate the time scale in calendar time units in this analysis, we pool the information about the RYMV evolutionary rate from several geographical partitions. Whereas the field surveys and the phylogeographic reconstructions both point to a rapid southward invasion across hundreds of kilometers throughout Madagascar within three to four decades, they differ on the inferred origin location and time of the epidemic. The phylogeographic reconstructions suggest a lineage displacement and unveil a re-invasion of the northern regions that may have remained unnoticed otherwise. Despite ecological differences that could affect the transmission potential of RYMV in Madagascar and in mainland Africa, we estimate similar invasion and dispersal rates. We could not identify environmental factors that have a relevant impact on the lineage dispersal velocity of RYMV in Madagascar. This study highlights the value and complementarity of (historical) nongenetic and (more contemporaneous) genetic surveillance data for reconstructing the history of spread of plant viruses.

Emerging strains of watermelon mosaic virus in Southeastern France: model-based estimation of the dates and places of introduction

“…9 to 14 years after the estimated introduction dates. Such a lapse between the introduction of a plant pathogen and its first detection is consistent with estimations obtained for other plant viruses [38,39,40,19]. ESs strains have been detected in several European and Mediterranean countries ( [14]), and in the USA [41], in the few years following their description in France, and their prevalence in these countries seems to increase even if few time series data are available.…”

“…As plant viruses are rapidly-evolving pathogens with small genomes and high mutation rates [15], they may present measurably evolving populations [16] over the time scale of decades. Thus, the spatio-temporal histories of invading species can sometimes be reconstructed from georeferenced and dated genomic data, with phylogeographic methodologies [17,18,19] or population dynamic models embedding evolutionary processes. Over shorter time-scales, or when only abundance data are available, recent mechanistic modelling approaches have been proposed to infer the date and place of introduction of a single species along with other demographic parameters [20].…”

An original structural fold underlies the multitask P1, a silencing suppressor encoded by the Rice yellow mottle virus

“…We have also initiated a deep search of rice proteins as potential P1 interactors. Our work opens huge perspectives towards the understanding on how P1 structural properties sustain P1 sequence diversity among the numerous RYMV isolates identified so far in the African continent and neighboring islands (Rakotomalala et al, 2019) and much beyond among the sobemovirus gender.…”

Disease Pandemics and Major Epidemics Arising from New Encounters between Indigenous Viruses and Introduced Crops

“…Since the mid-1990s, it has caused a disease epidemic of major economic significance in rice-growing regions and become a major deterrent to rice cultivation in SSA. Both irrigated and rainfed rice develop RYMD but its incidences are higher in irrigated crops [1,55,75,[78][79][80][81]. However, it has not yet spread elsewhere in the world.…”

“…Although spread by vectors from infected alternative hosts or via contaminated irrigation water, soil containing plant debris or agricultural machinery could account for local spread, but they would not account for its rapid long-distance dissemination. Rakotomalala et al [81] suggested that the rice trade might have been responsible for spreading RYMV from continental Africa to Madagascar. Thus, unknowingly transporting RYMV-infected live rice seedlings, stubble or ratoons to Madagascar, and planting them there, would have introduced the virus.…”