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Title: Characterization of Local and Systemic Impact of Whitefly (Bemisia tabaci) Feeding and Whitefly-Transmitted Tomato Mottle Virus Infection on Tomato Leaves by Comprehensive Proteomics

Abstract

Tomato mottle virus (ToMoV) is a ssDNA plant begomovirus transmitted to solanaceous crops by the whitefly species complex (Bemisia tabaci), causing stunted growth, leaf mottling, and reduced fruit yield. Using a genetic repertoire of 7 genes, ToMoV pathogenesis includes manipulation of multiple plant biological processes to circumvent antiviral defenses. To further understand the effects of whitefly feeding and whitefly-transmitted ToMoV infection on tomato plants (Solanum lycopersicum ‘Florida Lanai’), we generated comprehensive protein profiles of leaves subjected to feeding by either (1) viruliferous whiteflies harboring ToMoV, or (2) non-viruliferous whiteflies, or (3) a no-feeding control. In each condition (1-3), whiteflies were confined to clip cages on a mature leaf for 3 days. The effects of whitefly feeding and ToMoV infection were measured both locally and systemically by sampling either a mature leaf directly from the site of whitefly feeding, or from a newly formed leaf 10 days post feeding (dpf). At 3 dpf, relatively few biological processes were affected specifically by ToMoV at the site of feeding, and include proteins associated with translation initiation and elongation, and plasmodesmata dynamics. In contrast, the systemic impacts of ToMoV on younger leaves at 10 dpf were more pronounced and included a virus-specific change inmore » plant proteins associated with mRNA maturation and export, RNA-dependent DNA methylation, and other plant anti-viral transcriptional gene silencing systems. Our analysis supports previous findings and provides novel insight into biological processes in tomato altered locally and systemically by whitefly feeding and ToMoV infection.« less

Authors:
ORCiD logo [1];  [2];  [3];  [3];  [3];  [4]; ORCiD logo [1];  [2]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  2. Univ. of Florida, Gainesville, FL (United States)
  3. Univ. of Texas at San Antonio, TX (United States)
  4. Pennsylvania State Univ., University Park, PA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Defense Advanced Research Projects Agency (DARPA); USDOD
OSTI Identifier:
1674962
Report Number(s):
PNNL-SA-153927
Journal ID: 1422-0067
Grant/Contract Number:  
AC05-76RL01830; HR0011-17-2-0055
Resource Type:
Accepted Manuscript
Journal Name:
International Journal of Molecular Sciences (Online)
Additional Journal Information:
Journal Name: International Journal of Molecular Sciences (Online); Journal Volume: 21; Journal Issue: 19
Publisher:
MDPI
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; tomato; tomato mottle virus; RNA directed DNA methylation; transcriptional gene silencing; Begomovirus; Geminivirus; Bemisia tabaci; whitefly; pathogenesis; proteomics

Citation Formats

Ogden, Aaron J., Boukari, Wardatou, Nava, Alba, Lucinda, Natalia, Sunter, Garry, Curtis, Wayne R., Adkins, Joshua N., and Polston, Jane E. Characterization of Local and Systemic Impact of Whitefly (Bemisia tabaci) Feeding and Whitefly-Transmitted Tomato Mottle Virus Infection on Tomato Leaves by Comprehensive Proteomics. United States: N. p., 2020. Web. doi:10.3390/ijms21197241.
Ogden, Aaron J., Boukari, Wardatou, Nava, Alba, Lucinda, Natalia, Sunter, Garry, Curtis, Wayne R., Adkins, Joshua N., & Polston, Jane E. Characterization of Local and Systemic Impact of Whitefly (Bemisia tabaci) Feeding and Whitefly-Transmitted Tomato Mottle Virus Infection on Tomato Leaves by Comprehensive Proteomics. United States. https://doi.org/10.3390/ijms21197241
Ogden, Aaron J., Boukari, Wardatou, Nava, Alba, Lucinda, Natalia, Sunter, Garry, Curtis, Wayne R., Adkins, Joshua N., and Polston, Jane E. Wed . "Characterization of Local and Systemic Impact of Whitefly (Bemisia tabaci) Feeding and Whitefly-Transmitted Tomato Mottle Virus Infection on Tomato Leaves by Comprehensive Proteomics". United States. https://doi.org/10.3390/ijms21197241. https://www.osti.gov/servlets/purl/1674962.
@article{osti_1674962,
title = {Characterization of Local and Systemic Impact of Whitefly (Bemisia tabaci) Feeding and Whitefly-Transmitted Tomato Mottle Virus Infection on Tomato Leaves by Comprehensive Proteomics},
author = {Ogden, Aaron J. and Boukari, Wardatou and Nava, Alba and Lucinda, Natalia and Sunter, Garry and Curtis, Wayne R. and Adkins, Joshua N. and Polston, Jane E.},
abstractNote = {Tomato mottle virus (ToMoV) is a ssDNA plant begomovirus transmitted to solanaceous crops by the whitefly species complex (Bemisia tabaci), causing stunted growth, leaf mottling, and reduced fruit yield. Using a genetic repertoire of 7 genes, ToMoV pathogenesis includes manipulation of multiple plant biological processes to circumvent antiviral defenses. To further understand the effects of whitefly feeding and whitefly-transmitted ToMoV infection on tomato plants (Solanum lycopersicum ‘Florida Lanai’), we generated comprehensive protein profiles of leaves subjected to feeding by either (1) viruliferous whiteflies harboring ToMoV, or (2) non-viruliferous whiteflies, or (3) a no-feeding control. In each condition (1-3), whiteflies were confined to clip cages on a mature leaf for 3 days. The effects of whitefly feeding and ToMoV infection were measured both locally and systemically by sampling either a mature leaf directly from the site of whitefly feeding, or from a newly formed leaf 10 days post feeding (dpf). At 3 dpf, relatively few biological processes were affected specifically by ToMoV at the site of feeding, and include proteins associated with translation initiation and elongation, and plasmodesmata dynamics. In contrast, the systemic impacts of ToMoV on younger leaves at 10 dpf were more pronounced and included a virus-specific change in plant proteins associated with mRNA maturation and export, RNA-dependent DNA methylation, and other plant anti-viral transcriptional gene silencing systems. Our analysis supports previous findings and provides novel insight into biological processes in tomato altered locally and systemically by whitefly feeding and ToMoV infection.},
doi = {10.3390/ijms21197241},
journal = {International Journal of Molecular Sciences (Online)},
number = 19,
volume = 21,
place = {United States},
year = {Wed Sep 30 00:00:00 EDT 2020},
month = {Wed Sep 30 00:00:00 EDT 2020}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

Figure 1 Figure 1: (A) The experimental design involved subjecting tomato plants to infection by whiteflies (+WF), viruliferous whiteflies loaded with tomato mottle virus (+WFV), and a no-feeding control (NFC). Leaf samples were collected from the whitefly site of feeding (SOF) at 3 days post feeding (dpf) and systemically from younger leavesmore » at 10 dpf. Separate plants were used to sample leaves from the SOF at 3 dpf and leaves distal to the SOF at 10 dpf (plant 1/plant 2). (B) Representative plants at 10 dpf. Only the plants subjected to feeding by viruliferous whiteflies exhibited stunted growth and mottled leaves, which are characteristic of ToMoV infection. (C–G) All leaves, including the NFC, received clip cages. Additional sample handling included the removal of clip cages, whitefly termination by insecticidal soap, excision of the leaf, and isolation of the leaf area at the SOF within the clip cages.« less

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