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

• Published in: Plant molecular biology 2012-10, Vol.80 (3), p.273-287
• Main Authors: Sade, Dagan, Eybishtz, Assaf, Gorovits, Rena, Sobol, Iris, Czosnek, Henryk
• Format: Article
• Language: English
• Subjects: Animals; Base Sequence; Begomovirus - immunology; Begomovirus - pathogenicity; Bemisia tabaci; Biochemistry; Biomedical and Life Sciences; Disease resistance; Disease Resistance - genetics; Feeding; Gene expression; Gene Expression Regulation, Developmental - genetics; Gene Expression Regulation, Plant - genetics; Gene Silencing; Genomics; Genotype; Heat; Hemiptera - virology; hexose transporter; Infection; Inoculation; Leaves; Life Sciences; Lipocalin; Lipocalins - genetics; Lipocalins - metabolism; Lycopersicon esculentum; Lycopersicon esculentum - genetics; Lycopersicon esculentum - immunology; Lycopersicon esculentum - physiology; Lycopersicon esculentum - virology; Molecular Sequence Data; Monosaccharide Transport Proteins - genetics; Monosaccharide Transport Proteins - metabolism; permease; Plant biology; Plant diseases; Plant Diseases - immunology; Plant Diseases - virology; Plant Leaves - genetics; Plant Leaves - immunology; Plant Leaves - physiology; Plant Leaves - virology; Plant Pathology; Plant Proteins - genetics; Plant Proteins - metabolism; Plant resistance; Plant Sciences; Plant Stems - genetics; Plant Stems - immunology; Plant Stems - physiology; Plant Stems - virology; Plant viruses; Planting; Plants; Reactive oxygen species; Reactive Oxygen Species - metabolism; Salts; Sequence Alignment; Sequence Analysis, DNA; Solanum; Stress, Physiological; Tomato yellow leaf curl virus; Tomatoes; yellow leaf
• ISSN: 0167-4412; 1573-5028
• DOI: 10.1007/s11103-012-9946-6

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.