A developmentally regulated lipocalin-like gene is overexpressed in Tomato yellow leaf curl virus-resistant tomato plants upon virus inoculation, and its silencing abolishes resistance

Dagan Sade, Assaf Eybishtz, Rena Gorovits, Iris Sobol, Henryk Czosnek*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

27 Scopus citations

Abstract

To discover genes involved in tomato resistance to Tomato yellow leaf curl virus (TYLCV), we previously compared cDNA libraries from susceptible (S) and resistant (R) tomato lines. Among the genes preferentially expressed in R plants and upregulated by TYLCV infection was a gene encoding a lipocalin-like protein. This gene was termed Solanum lycopersicum virus resistant/susceptible lipocalin (SlVRSLip). The SlVRSLip structural gene sequence of R and S plants was identical. SlVRSLip was expressed in leaves during a 15-day window starting about 40 days after sowing (20 days after planting). SlVRSLip was upregulated by Bemisia tabaci (the TYLCV vector) feeding on R plant leaves, and even more strongly upregulated following whitefly-mediated TYLCV inoculation. Silencing of SlVRSLip in R plants led to the collapse of resistance upon TYLCV inoculation and to a necrotic response along the stem and petioles accompanied by ROS production. Contrary to previously identified tomato lipocalin gene DQ222981, SlVRSLip was not regulated by cold, nor was it regulated by heat or salt. The expression of SlVRSLip was inhibited in R plants in which the hexose transporter gene LeHT1 was silenced. In contrast, the expression of LeHT1 was not inhibited in SlVRSLip-silenced R plants. Hence, in the hierarchy of the gene network conferring TYLCV resistance, SlVRSLip is downstream of LeHT1. Silencing of another gene involved in resistance, a Permease-I like protein, did not affect the expression of SlVRSLip and LeHT1; expression of the Permease was not affected by silencing SlVRSLip or LeHT1, suggesting that it does not belong to the same network. The triple co-silencing of SlVRSLip, LeHT1 and Permease provoked an immediate cessation of growth of R plants upon infection and the accumulation of large amounts of virus. SlVRSLip is the first lipocalin-like gene shown to be involved in resistance to a plant virus.

Original languageAmerican English
Pages (from-to)273-287
Number of pages15
JournalPlant Molecular Biology
Volume80
Issue number3
DOIs
StatePublished - Oct 2012

Bibliographical note

Funding Information:
Acknowledgments This research was supported by a grant from the U.S. Agency for International Development, Middle East Research and Cooperation (MERC) program to H.C. (GEG-G-00-02-00003-00), Project M21-037. Dr. Favi Vidavski and Hila Beeri (Tomatech Ltd, Rehovot, Israel) provided the R and S tomato seeds. The authors thank Prof. David Baulcombe and the Gatsby Charitable Foundation, The Sainsbury Laboratory, for providing the TRV vectors.

Keywords

  • Gene silencing
  • Lipocalin
  • Resistance
  • Tomato
  • Virus

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