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Studies of tomato plants in response to infections with PVX and different PVY isolates reveal a remarkable PVX-PVYNTN synergism and diverse expression profiles of genes involved in different pathways

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Abstract

Potato virus Y (PVY) undergoes continuous nucleotide mutation and genome recombination, leading to novel strains with varying pathogenicity on host plants. Little is known about how tomato plants respond to infections with different PVY strains, especially the emerging strains such as PVYNTN and PVYN:O, and in combination with other viral species such as Potato virus X (PVX). In this study, the response of tomato (cultivar Rutgers) plants to single and mixed infections with PVY and PVX was investigated. Plants infected singly with PVYO, PVYN:O, PVYN or PVYNTN developed mosaic symptoms and leaf deformation; whereas plants infected with PVX developed mild local lesion and varying degrees of mosaic and leaf deformation symptoms. Mixed PVX+PVY infections induced more severe symptoms, which include severe local and systemic leaf necrosis, leaf drop and severe leaf deformation, compared to single infections with PVX or PVY, indicating PVX-PVY synergism. The level of PVX-PVY synergism was affected significantly by PVY strains, with PVYNTN being the greatest effector. Quantitative analysis of viral titre indicated that mixed PVX+PVY infections elevated PVX level and reduced PVY level. A comparative transcriptional analysis of 46 key genes involved in signal molecule synthesis and signal transduction using NanoString technology revealed diverse gene expression profiles in both single and mixed infections. Two hierarchical expression clusters, one up-regulated and the other down-regulated, were observed during the infections. In general, mixed infections led to more genes being differentially regulated than single infections. The expression alteration of genes involved in oxidative stress and salicylic acid (SA)-pathways is particularly noteworthy, as the mixed infections, especially PVX+PVYNTN infections, led to a further elevation of reactive oxygen species (ROS) and SA producing abilities and a reduction of ROS scavenging ability over single infections.

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Acknowledgments

The authors thank the greenhouse staff at the Potato Research Centre for horticultural assistance. This research was funded by Agriculture and Agri-Food Canada under the Project #1110. Z Liang was a receipt of the Ministry of Education of China-AAFC Ph.D. Student Internship Program.

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Author notes

  1. Zengenni Liang

    Present address: Hunan Agricultural Product Processing Institute, Hunan Academy of Agricultural Sciences, Changsha, Hunan, China, 410125

Authors and Affiliations

  1. Potato Research Centre, Agriculture and Agri-Food Canada, P.O. Box 20280, 850 Lincoln Road, Fredericton, NB, Canada, E3B 4Z7

    Zengenni Liang, Virginia Dickison & Xianzhou Nie

  2. College of Horticulture and Landscape, Hunan Agricultural University, Changsha, Hunan, China, 410128

    Zengenni Liang & Xingyao Xiong

  3. Agricultural Certification Services, 1030 Lincoln Road, Fredericton, NB, Canada, E3B 8B7

    Mathuresh Singh

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Correspondence to Xianzhou Nie.

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Figure S1

Symptoms induced by PVX and PVY strains on inoculated leaflets in tomato (cv. Rutgers). (A), PVX; (B): PVYO-FL; (C), PVYO-RB; (D) PVYN:O-Mb58; (E) PVYNTN-Sl; (F) PVYN-Jg; (G) PVX+PVYO-FL; (H) PVX+PVYO-RB; (I) PVX+PVYN:O-Mb58; (J) PVX+PVYNTN-Sl; (K) PVX+PVYN-Jg; (L) Mock. Local lesions (necrotic spots) can be seen in (A) and (G)-(F). The photographs were taken at 6 days post-inoculation (dpi). Experiments were repeated three times and similar results were obtained. (GIF 40 kb)

High Resolution Image (TIFF 9417 kb)

Figure S2

Symptoms on the third leaves from the top in PVX and PVY infected plants. (A) PVX; (B) PVYO-FL; (C) PVYO-RB; (D) PVYN:O-Mb58; (E) PVYNTN-Sl; (F) PVYN-Jg; (G) PVX+PVYO-FL; (H) PVX+PVYO-RB; (I) PVX+PVYN:O-Mb58; (J) PVX+PVYNTN-Sl; (K) PVX+PVYN-Jg; (L) Mock. The photographs were taken at 39 days post-inoculation (dpi). The experiment was repeated three times with similar results. Symptom types and severities in (A), intermediate chlorosis and leaf rugosity/deformation; (B)-(D) and (F), mild mosaic and leaf rugosity/deformation; (E), mild mosaic and intermediate leaf rugosity/deformation; (G)-(I) and (K), severe chlorosis and leaf rugosity/deformation; (J), extremely severe chlorosis and leaf rugosity/deformation. (GIF 3334 kb)

High Resolution Image (TIFF 9261 kb)

Table S1

Enzyme-linked-immunosorbent assay (ELISA) for detection of viruses in inocula using various PVX and PVY antibodies. (DOC 32 kb)

Table S2

PVX and PVY levels measured by RT-PCR. (DOC 32 kb)

Table S3

Probe sequences used for NanoString nCounter analysis of gene expression. (DOC 69 kb)

Table S4

Effect of single and mixed infections with PVX and PVY on gene expression in tomato. (XLSX 30 kb)

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Liang, Z., Dickison, V., Singh, M. et al. Studies of tomato plants in response to infections with PVX and different PVY isolates reveal a remarkable PVX-PVYNTN synergism and diverse expression profiles of genes involved in different pathways. Eur J Plant Pathol 144, 55–71 (2016). https://doi.org/10.1007/s10658-015-0750-4

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