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Previous self-assembly experiments on a model icosahedral plant virus haveshown that, under physiological conditions, capsid proteins initially bind tothe genome through an en masse mechanism and form nucleoprotein complexes in adisordered state, which raises the questions as to how virions are assembledinto a highly ordered structure in the host cell. Using small-angle X-rayscattering, we find out that a disorder-order transition occurs underphysiological conditions upon an increase in capsid protein concentrations. Ourcryo-transmission electron microscopy reveals closed spherical shellscontaining in vitro transcribed viral RNA even at pH 7.5, in marked contrastwith the previous observations. We use Monte Carlo simulations to explain thisdisorder-order transition and find that, as the shell grows, the structures ofdisordered intermediates in which the distribution of pentamers does not belongto the icosahedral subgroups become energetically so unfavorable that the capscan easily dissociate and reassemble overcoming the energy barriers for theformation of perfect icosahedral shells. In addition, we monitor the growth ofcapsids under the condition that the nucleation and growth is the dominantpathway and show that the key for the disorder-order transition in both enmasse and nucleation and growth pathways lies in the strength of elastic energycompared to the other forces in the system including protein-proteininteractions and the chemical potential of free subunits. Our findings explain,at least in part, why perfect virions with icosahedral order form underdifferent conditions including physiological ones.

How a Virus Circumvents Energy Barriers to Form Symmetric Shells