Functional plasticity of the crinivirus minor coat protein (CPm): two regions in a foregut-binding chimeric CPm mediate virus transmission by whitefly vectors

The transmission of lettuce infectious yellows virus (LIYV) is determined by a minor coat protein (CPm)-mediated virion retention process located in the foregut of its whitefly (Bemisia tabaci New World [NW]) vector.  However, the molecular mechanism underlying foregut-binding and transmission remains unknown.  Using chimeric CPm mutants engineered with different lengths of the LIYV CPm coding sequence and that of another NW vector transmitted crinivirus, lettuce chlorosis virus (LCV), we have obtained CPmP-1, a foregut-binding competent and whitefly transmissible CPm mutant.  In immuno-gold labeling transmission electron microscopy analysis, the virions of CPmP-1 are distinctly labeled by antibodies directed against the CPm of LCV but not LIYV.  This unique antibody recognition pattern is also displayed in the foreguts of NW vectors that have fed on CPmP-1 virions.  The transmission of CPmP-1 was consistently inhibited when NW vectors fed on a mixture of CPmP-1 virions and anti-LCV CPm antibody.  The inhibition of CPm-P1 transmission by the LCV CPm-specific antibody correlated with a significant reduction in the number of vectors that retained the virus in their foreguts.  In contrast, with NW vectors that fed on a mixture of CPmP-1 virions and an anti-LIYV CPm antibody, virus transmission was consistently observed and correlated with a significant number of NW vectors that retained the virus in their foreguts.  Together, these results are consistent with the hypothesis that the two LCV CPm regions in CPmP-1 are exposed on the surface of the virion and play an important role in mediating its binding to the vector’s foregut.