Abstract
Luteoviruses avoid degradation in the hemolymph of their aphid vector by interacting with a GroEL homolog from the aphid's primary endosymbiotic bacterium (Buchnera sp.). Mutational analysis of GroEL from the primary endosymbiont of Myzus persicae (MpB GroEL) revealed that the amino acids mediating binding of Potato leafroll virus (PLRV; Luteoviridae) are located within residues 9 to 19 and 427 to 457 of the N-terminal and C-terminal regions, respectively, of the discontinuous equatorial domain. Virus overlay assays with a series of overlapping synthetic decameric peptides and their derivatives demonstrated that R13, K15, L17, and R18 of the N-terminal region and R441 and R445 of the C-terminal region of the equatorial domain of GroEL are critical for PLRV binding. Replacement of R441 and R445 by alanine in full-length MpB GroEL and in MpB GroEL deletion mutants reduced but did not abolish PLRV binding. Alanine substitution of either R13 or K15 eliminated the PLRV-binding capacity of the other and those of L17 and R18. In the predicted tertiary structure of GroEL, the determinants mediating virus binding are juxtaposed in the equatorial plain.
MeSH Terms
Alanine/chemistry,metabolism
Amino Acid Sequence
Amino Acid Substitution
Amino Acids/chemistry
Animals
Aphids/microbiology
Binding Sites
Buchnera/genetics,metabolism
Chaperonin 60/chemistry,genetics,metabolism
Gene Deletion
Luteovirus/metabolism
Models, Molecular
Molecular Sequence Data
Mutation
Protein Structure, Tertiary
Sequence Alignment
Solanum tuberosum/virology
Chemicals
Amino Acids
Chaperonin 60
Alanine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Hogenhout S A
Plant Research International, 6700 AA Wageningen, 6709 PD Wageningen, The Netherlands.
van der Wilk F
Verbeek M
Goldbach R W
van den Heuvel J F
References (30)
30 references, click to expand
-
A comprehensive set of sequence analysis programs for the VAX.
Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95
PMID: 6546423
-
A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of tomato yellow leaf curl virus.
Virology. 1999 Mar 30;256(1):75-84
PMID: 10087228
-
Nucleotide sequence and organization of potato leafroll virus genomic RNA.
FEBS Lett. 1989 Mar 13;245(1-2):51-6
PMID: 2466700
-
A novel ubiquitous protein 'chaperonin' supports the endosymbiotic origin of mitochondrion and plant chloroplast.
Biochem Biophys Res Commun. 1989 Sep 15;163(2):780-7
PMID: 2571331
-
Molecular chaperones.
Annu Rev Biochem. 1991;60:321-47
PMID: 1679318
-
Nucleotide sequence of mouse Tcp-1a cDNA.
Gene. 1991 Sep 15;105(2):269-73
PMID: 1937024
-
A molecular chaperone from a thermophilic archaebacterium is related to the eukaryotic protein t-complex polypeptide-1.
Nature. 1991 Dec 12;354(6353):490-3
PMID: 1836250
-
Structures of chaperonins from an intracellular symbiont and their functional expression in Escherichia coli groE mutants.
J Bacteriol. 1992 Mar;174(6):1869-74
PMID: 1347769
-
Mutation Ala2-->Ser destabilizes intersubunit interactions in the molecular chaperone GroEL.
J Mol Biol. 1993 May 5;231(1):58-64
PMID: 8098773
-
A TCP1-related molecular chaperone from plants refolds phytochrome to its photoreversible form.
Nature. 1993 Jun 17;363(6430):644-8
PMID: 8099715
-
Facilitated folding of actins and tubulins occurs via a nucleotide-dependent interaction between cytoplasmic chaperonin and distinctive folding intermediates.
Mol Cell Biol. 1994 May;14(5):2895-904
PMID: 7909354
-
Reversible interaction of beta-actin along the channel of the TCP-1 cytoplasmic chaperonin.
Biophys J. 1994 Jul;67(1):364-8
PMID: 7919008
-
Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae.
J Gen Virol. 1994 Oct;75 ( Pt 10):2559-65
PMID: 7931143
-
The crystal structure of the bacterial chaperonin GroEL at 2.8 A.
Nature. 1994 Oct 13;371(6498):578-86
PMID: 7935790
-
Residues in chaperonin GroEL required for polypeptide binding and release.
Nature. 1994 Oct 13;371(6498):614-9
PMID: 7935796
-
A carboxy-terminal deletion impairs the assembly of GroEL and confers a pleiotropic phenotype in Escherichia coli K-12.
J Bacteriol. 1994 Nov;176(22):6980-5
PMID: 7961461
-
Identification of the major chromaffin granule-binding protein, chromobindin A, as the cytosolic chaperonin CCT (chaperonin containing TCP-1).
J Biol Chem. 1994 Dec 23;269(51):32035-8
PMID: 7798195
-
The stability of the molecular chaperonin cpn60 is affected by site-directed replacement of cysteine 518.
J Biol Chem. 1994 Dec 23;269(51):32151-4
PMID: 7798211
-
Cystosolic chaperonin subunits have a conserved ATPase domain but diverged polypeptide-binding domains.
Trends Biochem Sci. 1994 Dec;19(12):543-8
PMID: 7846767
-
Aphid transmission of beet western yellows luteovirus requires the minor capsid read-through protein P74.
EMBO J. 1995 Feb 15;14(4):650-9
PMID: 7882968
-
Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells.
Mol Microbiol. 1995 Jan;15(1):1-11
PMID: 7752884
-
The 2.4 A crystal structure of the bacterial chaperonin GroEL complexed with ATP gamma S.
Nat Struct Biol. 1996 Feb;3(2):170-7
PMID: 8564544
-
In vitro interactions of the aphid endosymbiotic SymL chaperonin with barley yellow dwarf virus.
J Virol. 1997 Jan;71(1):569-77
PMID: 8985385
-
The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid.
J Virol. 1997 Oct;71(10):7258-65
PMID: 9311800
-
Potato leafroll virus binds to the equatorial domain of the aphid endosymbiotic GroEL homolog.
J Virol. 1998 Jan;72(1):358-65
PMID: 9420234
-
SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling.
Electrophoresis. 1997 Dec;18(15):2714-23
PMID: 9504803
-
The role of polar interactions in the molecular recognition of CD40L with its receptor CD40.
Protein Sci. 1998 May;7(5):1124-35
PMID: 9605317
-
Anatomy of hot spots in protein interfaces.
J Mol Biol. 1998 Jul 3;280(1):1-9
PMID: 9653027
-
CD2 and the nature of protein interactions mediating cell-cell recognition.
Immunol Rev. 1998 Jun;163:217-36
PMID: 9700513
-
Homologous plant and bacterial proteins chaperone oligomeric protein assembly.
Nature. 1988 May 26;333(6171):330-4
PMID: 2897629