Abstract
Two acidic domains of the Potato leafroll virus (PLRV) coat protein, separated by 55 amino acids and predicted to be adjacent surface features on the virion, were the focus of a mutational analysis. Eleven site-directed mutants were generated from a cloned infectious cDNA of PLRV and delivered to plants by Agrobacterium-mediated mechanical inoculation. Alanine substitutions of any of the three amino acids of the sequence EWH (amino acids 170 to 172) or of D177 disrupted the ability of the coat protein to assemble stable particles and the ability of the viral RNA to move systemically in four host plant species. Alanine substitution of E109, D173, or E176 reduced the accumulation of virus in agrobacterium-infiltrated tissues, the efficiency of systemic infection, and the efficiency of aphid transmission relative to wild-type virus, but the mutations did not affect virion stability. A structural model of the PLRV capsid predicted that the amino acids critical for virion assembly were located within a depression at the center of a coat protein trimer. The other amino acids that affected plant infection and/or aphid transmission were predicted to be located around the perimeter of the depression. PLRV virions play key roles in phloem-limited virus movement in plant hosts as well as in transport and persistence in the aphid vectors. These results identified amino acid residues in a surface-oriented loop of the coat protein that are critical for virus assembly and stability, systemic infection of plants, and movement of virus through aphid vectors.
MeSH Terms
Animals
Aphids/virology
Capsid Proteins/chemistry,physiology
Luteovirus/physiology
Solanum tuberosum/virology
Virion/physiology
Virus Assembly
Chemicals
Capsid Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Lee Lawrence
Department of Plant Pathology, 334 Plant Science, Cornell University, Ithaca, NY 14853, USA.
Kaplan Igor B
Ripoll Daniel R
Liang Delin
Palukaitis Peter
Gray Stewart M
References (28)
28 references, click to expand
-
Identification of beet western yellows luteovirus genes implicated in viral replication and particle morphogenesis.
Virology. 1993 Aug;195(2):692-9
PMID: 8337839
-
The Protein Data Bank.
Nucleic Acids Res. 2000 Jan 1;28(1):235-42
PMID: 10592235
-
Protein structure alignment by incremental combinatorial extension (CE) of the optimal path.
Protein Eng. 1998 Sep;11(9):739-47
PMID: 9796821
-
3D-Jury: a simple approach to improve protein structure predictions.
Bioinformatics. 2003 May 22;19(8):1015-8
PMID: 12761065
-
Aphid Acquisition and Cellular Transport of Potato leafroll virus-like Particles Lacking P5 Readthrough Protein.
Phytopathology. 2000 Oct;90(10):1153-61
PMID: 18944480
-
Tagging potato leafroll virus with the jellyfish green fluorescent protein gene.
J Gen Virol. 2000 Mar;81(Pt 3):617-26
PMID: 10675399
-
Effects of mutations in the beet western yellows virus readthrough protein on its expression and packaging and on virus accumulation, symptoms, and aphid transmission.
Virology. 1997 Apr 14;230(2):323-34
PMID: 9143288
-
Luteovirus-aphid interactions.
Annu Rev Phytopathol. 2003;41:539-66
PMID: 12730400
-
Analysis of epitopes on potato leafroll virus capsid protein.
Virology. 1992 Nov;191(1):485-9
PMID: 1384231
-
Effects of point mutations in the major capsid protein of beet western yellows virus on capsid formation, virus accumulation, and aphid transmission.
J Virol. 2003 Mar;77(5):3247-56
PMID: 12584348
-
Beet western yellows virus-associated RNA: an independently replicating RNA that stimulates virus accumulation.
Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10168-72
PMID: 8234272
-
Aphid transmission and systemic plant infection determinants of barley yellow dwarf luteovirus-PAV are contained in the coat protein readthrough domain and 17-kDa protein, respectively.
Virology. 1996 May 1;219(1):57-65
PMID: 8623554
-
Site-directed mutagenesis and generation of chimeric viruses by homologous recombination in yeast to facilitate analysis of plant-virus interactions.
Mol Plant Microbe Interact. 2004 Jun;17(6):571-6
PMID: 15195939
-
Enhanced genome annotation using structural profiles in the program 3D-PSSM.
J Mol Biol. 2000 Jun 2;299(2):499-520
PMID: 10860755
-
Genes and cis-acting sequences involved in replication of barley yellow dwarf virus-PAV RNA.
Virology. 1995 Sep 10;212(1):186-95
PMID: 7676628
-
Analysis of a three-dimensional structure of Potato leafroll virus coat protein obtained by homology modeling.
Virology. 2001 Jul 20;286(1):72-82
PMID: 11448160
-
Studies on the role of the minor capsid protein in transport of Beet western yellows virus through Myzus persicae.
J Gen Virol. 2001 Aug;82(Pt 8):1995-2007
PMID: 11458007
-
Comparison of sequence profiles. Strategies for structural predictions using sequence information.
Protein Sci. 2000 Feb;9(2):232-41
PMID: 10716175
-
Transformation of tobacco and potato with cDNA encoding the full-length genome of potato leafroll virus: evidence for a novel virus distribution and host effects on virus multiplication.
J Gen Virol. 1999 Nov;80 ( Pt 11):2813-22
PMID: 10580042
-
Phylogeny of capsid proteins of small icosahedral RNA plant viruses.
J Gen Virol. 1991 Jul;72 ( Pt 7):1481-6
PMID: 1856686
-
A satellite RNA of barley yellow dwarf virus contains a novel hammerhead structure in the self-cleavage domain.
Virology. 1991 Aug;183(2):711-20
PMID: 1713001
-
Local and distant sequences are required for efficient readthrough of the barley yellow dwarf virus PAV coat protein gene stop codon.
J Virol. 1996 Sep;70(9):5884-92
PMID: 8709208
-
Molecular biology of luteoviruses.
Adv Virus Res. 1996;46:413-60
PMID: 8824705
-
Tomato bushy stunt virus at 2.9 A resolution.
Nature. 1978 Nov 23;276(5686):368-73
PMID: 19711552
-
Groundnut rosette disease virus complex: biology and molecular biology.
Adv Virus Res. 2000;55:357-400
PMID: 11050947
-
Host-dependent requirement for the Potato leafroll virus 17-kda protein in virus movement.
Mol Plant Microbe Interact. 2002 Oct;15(10):1086-94
PMID: 12437307
-
Structure prediction meta server.
Bioinformatics. 2001 Aug;17(8):750-1
PMID: 11524381
-
Comparative protein modelling by satisfaction of spatial restraints.
J Mol Biol. 1993 Dec 5;234(3):779-815
PMID: 8254673