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Evolution of zucchini yellow mosaic potyvirus (ZYMV) variability on Martinique Island since its first detection

Cecile Desbie and Herve Lecoq
INRA, Station de Pathologie Végétale, Domaine Saint Maurice, BP94, 84143 Montfavet Cedex, FRANCE

Zucchini yellow mosaic potyvirus (ZYMV) is an "emerging" plant virus responsible for important damage on the yield and quality of cucurbit crops worldwide. Observed for the first time in Italy in 1973 and in France in 1979, within a few years it became one of the most damaging cucurbit viruses. Since its first description, the virus presented a high biological variability; further studies also revealed an important serological and molecular variability (Desbiez and Lecoq, 1997).

In order to understand the mechanisms of viral evolution, a 5-year study was performed on the island of Martinique. This island represents a unique ecosystem for the study of ZYMV evolution since:

• the virus was probably introduced in 1992 and subsequently spread rapidly to the whole island
• due to the insulary context, new virus introductions from independent origins are less likely to occur than on the mainland
• the tropical climate allows cucurbit growth all year round without any intercrop. Common subspontaneous Cucurbita spp. also constitute important virus reservoirs even when cucurbit crops are less abundant.

Infected samples were collected from 1992 to 1998 from different cucurbits (melon, cucumber, zucchini, squash, etc..) on the whole island. Since the first studies (1992-93), ZYMV presented an important biological variability, particularly regarding the pathotype of ZYMV isolates on melon lines or accessions possessing resistance or wilting genes (Desbiez et al., 1996). Surprisingly, the ratio of the different pathotypes remained almost constant between 1992 and 1998.

An important serological variability was also detected using a panel of 17 monoclonal antibodies which recognition sites (epitopes) in ZYMV coat protein have been identified in some cases at the level of a single amino-acid (Desbiez et al., 1997). All ZYMV isolates from Martinique presented a common serological characteristic, i.e lack of reactivity with one MAb, suggesting a close molecular relationship between them, probably related to an almost unique introduction on the island. Two serotypes were observed from 1992 to 1998, with apparent changes in their relative proportions. Six other serotypes were detected between 1992 and 1998, but were found only for one year and at one location, suggesting that the variants were eliminated shortly after their apparition by negative selection or genetic drift.

Molecular analysis of one of the most variable parts of the genome, the N-terminal part of the coat protein coding region, revealed a limited molecular variability between ZYMV isolates from Martinique. The serological differences between isolates could be correlated to single point mutations in this region of virus capsid. Sequence analysis of ZYMV isolates from Martinique and from other parts of the world revealed that Martinique isolates belonged to a ZYMV subgroup of strains present in different parts of the world but usually not very common. As a consequence of the 'bottleneck' that occurred during ZYMV introduction on the island (probably from Europe), only a fraction of ZYMV variability observed at the world level was detected on Martinique, and the most abundant group worldwide was not present on the island.

These results indicated that the origin of the virus on Martinique was probably unique, and that the molecular divergence between isolates remained very limited even after several years. After its introduction (possibly from infected fruits imported from Europe), the virus spread quickly in the new ecosystem and presented rapidly an important biological and serological variability; the lack of competition with preexisting strains may have allowed the maintenance of some of the variants that arose in the viral quasispecies due to the high mutation rate of RNA viruses. The proportion of different pathotypes on melon PI414723 possessing the Zym resistance gene to ZYMV remained almost constant during the study, although no resistant melons are theoretically grown on the island. This may be related to a low level of genetic drift and a lack of purifying selection towards the pathotype overcoming the resistance, or maybe to a frequency-dependent selection. Two major serotypes were also observed from 1992 to 1998. One of the serotypes seems te be getting predominant in the populations, what may be related to a selective advantage (this serotype is particularly abundant on subspontaneous Cucurbita moschata, maybe as an effect of host adaptation). All other serotypes were observed only transiently, and the variants were probably lost by genetic drift since they did not reach a threshold level in the populations.

The apparent evolution of ZYMV variability in Martinique may be related to the structure of the epidemics on the island: in spite of its small size, Martinique presents several different ecosystems that can be more or less compartimented. Besides, the epidemics in one crop frequently did not reach 100% infection, but were generally limited to only a few scattered plants in the field. The range of ZYMV variability was also very different from one site to the other, and on the same site, from one year to the other. The results obtained during this survey tend to indicate that the variability was very high shortly after the virus introduction, and may have reached an equilibrium after a few years. Preliminary results from other tropical islands seem to show the same rapid apparition of a variability shortly after introduction, and it will be interesting to follow virus evolution in those almost closed ecosystems. Studying the mechanisms that underlie virus evolution shortly after their introduction may provide important clues to understand the causes of plant virus emergence in general.

References
Desbiez C, Wipf-Scheibel C, Robaglia C, Delaunay T, Lecoq H. 1996. Biological and molecular variability of zucchini yellow mosaic virus on the island of Martinique. Plant Disease 80, 203-207.

Desbiez C, Gal-On A, Raccah B, Lecoq H. 1997. Characterization of epitopes of zucchini yellow mosaic potyvirus coat protein permits studies on the interactions between strains. J. Gen. Virol. 78, 2073-2076.

Desbiez C, Lecoq H. 1997. Zucchini yellow mosaic virus. Plant Pathology 46, 809-829

Abstract - Presented at the Virus Evolution Workshop
Ardmore, OK
October 21 - 24th, 1999