Molecular mapping of the viral determinants of systemic wilting induced by a Lettuce mosaic virus (LMV) isolate in some lettuce cultivars

doi:10.1016/j.virusres.2004.12.001

Virus Research

Volume 109, Issue 2, May 2005, Pages 175-180

https://doi.org/10.1016/j.virusres.2004.12.001 Get rights and content

Abstract

The isolate AF199 of Lettuce mosaic virus (LMV, genus Potyvirus) causes local lesions followed by systemic wilting and plant death in the lettuce cultivars Ithaca and Vanguard 75. Analysis of the phenotype of virus chimeras revealed that a region within the P1 protein coding region (nucleotides 112–386 in the viral genome) and/or another one within the CI protein coding region (nucleotides 5496–5855) are sufficient together to cause the lethal wilting in Ithaca, but not in Vanguard 75. This indicates that the determinants of this particular symptom are different in these two lettuce cultivars. The wilting phenotype was not directly correlated with differences in the deduced amino acid sequence of these two regions. Furthermore, transient expression of the LMV-AF199 proteins, separately or in combination, did not induce local necrosis or any other visible reaction in the plants. Together, these results suggest that the systemic wilting reaction might be due to RNA rather than protein sequences.

Section snippets

Acknowledgements

We thank Thierry Mauduit for taking care of the plants used in this study, Frédéric Revers for helpful discussions and occasional technical help and Kathryn Mayo-Candresse for her help with the English of the manuscript. This work was performed in the frame of a French–Brazilian bilateral agreement (CAPES-COFECUB project nos. 255/98 and 342/01), and was partially supported by the Conseil Régional d’Aquitaine and FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo). RKS was financially

References (32)

F. Garcia-Arenal et al.
Nucleotide sequence analysis of six satellite RNAs of cucumber mosaic virus: primary sequence and secondary structure alterations do not correlate with differences in pathogenicity
Virology
(1987)
A. Merits et al.
Biochemical and genetic evidence for interactions between potato A potyvirus-encoded proteins P1 and P3 and proteins of the putative replication complex
Virology
(1999)
F. Revers et al.
Comparison of the complete nucleotide sequences of two isolates of lettuce mosaic virus differing in their biological properties
Virus Res.
(1997)
L. Simón-Buela et al.
Long sequence in the 5′ noncoding region of plum pox virus is not necessary for viral infectivity but contribute to viral competitiveness and pathogenesis
Virology
(1997)
L. Bos et al.
Further observations on variation of lettuce mosaic virus in relation to lettuce (Lactuca sativa L.), and a discussion of resistance terminology
Eur. J. Plant Pathol.
(1994)
M. Chu et al.
Two separate regions in the genome of the tobacco etch virus contain determinants of the wilting response of Tabasco pepper
Mol. Plant-Microbe Interactions
(1997)
C.W. Collmer et al.
The I gene of bean: a dosage-dependent allele conferring extreme resistance, hypersensitive resistance, or spreading vascular necrosis in response to the potyvirus Bean common mosaic virus
Mol. Plant-Microbe Interactions
(2000)
S. Dinant et al.
Lettuce mosaic virus: a review
Plant Pathol.
(1992)
C. Dogimont et al.
Genetic analysis of broad spectrum resistance to potyvirus using doubled haploid lines of pepper (Capsicum annum L.)
Euphytica
(1996)
J.J. English et al.
Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation.
Plant J.
(1997)

I. Fernandez et al.

The 5′ noncoding region of Grapevine chrome mosaic virus RNA-2 triggers a necrotic response on three Nicotiana spp

Mol. Plant-Microbe Interactions

(1999)

R.P. Hellens et al.

pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation

Plant Mol. Biol.

(2000)

R. Krause-Sakate et al.

Systemic necrosis caused by two isolates of Lettuce mosaic virus (LMV) in lettuce (Lactuca sativa) cultivars possessing the Mo2 gene

Virus Rev. Res. Suppl.

(1999)

R. Krause-Sakate et al.

Molecular characterization of Lettuce mosaic virus field isolates reveals a distinct and widespread type of resistance-breaking isolate: LMV-Most

Phytopathology

(2002)

M.M. Kyle et al.

Inheritance of resistance to potyviruses in Phaseolus vulgaris L. II. Linkage relations and utility of a dominant gene for lethal systemic necrosis to soybean mosaic virus

Theor. Appl. Genet.

(1993)

P.E. Kyriakopoulou

A lethal strain of lettuce mosaic virus in Greece

Phytoparasitica

(1985)

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Molecular mapping of the viral determinants of systemic wilting induced by a Lettuce mosaic virus (LMV) isolate in some lettuce cultivars

Abstract

Section snippets

Acknowledgements

Virology

Virology

Virus Res.

Virology

Further observations on variation of lettuce mosaic virus in relation to lettuce (Lactuca sativa L.), and a discussion of resistance terminology

Eur. J. Plant Pathol.

Two separate regions in the genome of the tobacco etch virus contain determinants of the wilting response of Tabasco pepper

Mol. Plant-Microbe Interactions

The I gene of bean: a dosage-dependent allele conferring extreme resistance, hypersensitive resistance, or spreading vascular necrosis in response to the potyvirus Bean common mosaic virus

Mol. Plant-Microbe Interactions

Lettuce mosaic virus: a review

Plant Pathol.

Genetic analysis of broad spectrum resistance to potyvirus using doubled haploid lines of pepper (Capsicum annum L.)

Euphytica

Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation.

Plant J.

The 5′ noncoding region of Grapevine chrome mosaic virus RNA-2 triggers a necrotic response on three Nicotiana spp

Mol. Plant-Microbe Interactions

pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation

Plant Mol. Biol.

Systemic necrosis caused by two isolates of Lettuce mosaic virus (LMV) in lettuce (Lactuca sativa) cultivars possessing the Mo2 gene

Virus Rev. Res. Suppl.

Molecular characterization of Lettuce mosaic virus field isolates reveals a distinct and widespread type of resistance-breaking isolate: LMV-Most

Phytopathology

Inheritance of resistance to potyviruses in Phaseolus vulgaris L. II. Linkage relations and utility of a dominant gene for lethal systemic necrosis to soybean mosaic virus

Theor. Appl. Genet.

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Phytoparasitica