Host and viral factors determine the dispensability of coat protein for bipartite geminivirus systemic movement

Geminiviruses have unique, twinned icosahedral particles which encapsidate circular single-stranded DNA. Their genomes are composed of either one or two DNA segments. Monopartite geminiviruses absolutely require a functional coat protein (CP) for infectivity, whereas bipartite geminivirus CP null mutants can infect plants systemically. However, we show here that a CP mutant of the bipartite tomato golden mosaic virus (TGMV), which can infect Nicotiana benthamiana systemically, is confined to the inoculated leaves of Nicotiana tabacum or Datura stramonium. We also show that a CP mutant of the related bean golden mosaic virus (BGMV), which can infect beans systemically, is confined to the inoculated leaves of N. benthamiana. In each case, the extent of viral DNA accumulation in inoculated leaves was unaffected by the absence of CP, which suggests that CP is required specifically for systemic movement. The dispensability of CP is correlated with the degree of virus-host adaptation. TGMV is well adapted to N. benthamiana and does not require CP to infect this host systemically, whereas BGMV is poorly adapted to N. benthamiana and requires CP. Analysis of TGMV-BGMV hybrid viruses revealed that the viral genetic background can also affect the dispensability of CP for systemic movement in N. benthamiana. Thus, bipartite geminivirus movement in planta can be resolved genetically into three components: (i) local, cell-to-cell movement, which does not require CP; (ii) CP-dependent systemic movement, which occurs in all hosts tested; and (iii) CP-independent systemic movement, which occurs in hosts to which a given virus is well adapted.