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Title: The C-terminus of the Polerovirus P5 readthrough domain limits virus infection to the phloem

Author
item PETER, KARI - CORNELL UNIVERSITY
item GILDOW, FRED - PENNSYLVANIA STATE UNIV
item PALUKAITIS, PETER - SCOTTISH CROP INST
item Gray, Stewart

Submitted to: Journal of Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/10/2009
Publication Date: 6/1/2009
Citation: Peter, K., Gildow, F., Palukaitis, P., Gray, S.M. 2009. The C-terminus of the Polerovirus P5 readthrough domain limits virus infection to the phloem. Journal of Virology. 83(11):5419-5429.

Interpretive Summary: The polerovirus genera includes many economically important viruses including Potato leafroll virus, Cereal yellow dwarf viruses and Beet western yellows virus. These viruses are all restricted to the vascular tissues of their plant hosts and are dependent upon vascular feeding insects to be transmitted between plant hosts. It was hypothesized that the vascular limitation was because these viruses lacked a movement protein that would transport the virus out of the vascular tissue into other tissues. The work reported in this paper provides evidence for a complete paradigm shift in this thinking. We show that one of the structural proteins of Potato leafroll virus actually functions as a nonstructural movement protein to facilitate the spread of virus in the vascular tissues. However, one portion of this protein is actually responsible for limiting the virus to the vascular tissue and prevents the virus from moving into other tissues. When we genetically altered the virus so it did not produce this portion of the protein the virus was able to invade other tissues. Remarkably, over time the virus mutated on its own to restore production of this protein and to re-locate the virus back to the vascular tissues. This is the first report of a virus movement protein that is positively selected to limit the virus to a specific tissue type. Restriction of the virus to the vascular tissue is critical for successful transmission by insect vectors and continued propagation of the virus.

Technical Abstract: Unlike most plant viruses, poleroviruses are restricted to vascular phloem tissues, from which they are transmitted by their aphid vectors. Phloem limitation has been attributed to the absence of virus proteins facilitating movement or counteracting plant defense. The polerovirus capsid is composed of a total of 180 copies of two forms of coat protein, the major P3 protein and a few copies of P3/P5, a translational readthrough of P3. P3/P5 is required for insect transmission, and acts in trans to facilitate long-distance virus movement in phloem tissue. Specific polerovirus mutants lacking part, or all, of the P5 domain moved into and infected nonvascular mesophyll tissue when the source-sink relationship of the plant was altered by pruning. However, in a period of months a phloem-specific distribution of the virus was re-established, in the absence of aphid transmission. Virus from the new phloem-limited infection showed compensatory mutations that restored production of full length P3/P5. Results support our hypothesis that phloem limitation in poleroviruses presumably does not result from a deficiency in the repertoire of virus genes but rather from P3/P5 accumulation under selection in the infected plant, with the co-lateral effect of facilitating transmission by phloem-feeding aphid vectors.