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Published Online January 29, 2004
Science DOI: 10.1126/science.1092002

Reports

Submitted on September 29, 2003
Accepted on January 14, 2004

Molecular Evolution of the SARS Coronavirus During the Course of the SARS Epidemic in China

The Chinese SARS Molecular Epidemiology Consortium 1*

1 The complete list of authors and their affiliated institutions can be found in the supplementary text on Science Online; Correspondence to Guoping Zhao.

* To whom correspondence should be addressed. E-mail: gpzhao{at}sibs.ac.cn.

Sixty-three SARS coronavirus genomic sequences derived from the early, middle and late phases of the severe acute respiratory syndrome (SARS) epidemic were analyzed. Genotypes characteristic of each phase were discovered and the earliest genotypes were similar to animal SARS-like coronaviruses. Major deletions were observed in the Orf8 region, both at the start and the end of the epidemic. The neutral mutation rate of the viral genome was constant but the amino acid substitution rate of the coding sequences slowed during the course of the epidemic. The spike protein initially showed the strongest responses to positive selection pressures followed by subsequent purifying selection and eventual stabilization.


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   Abstract »    Full Text »    PDF »
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