The NLR Protein Encoded by the Resistance Gene Ty-2 Is Triggered by the Replication-Associated Protein Rep/C1 of Tomato Yellow Leaf Curl Virus.

Xuexue Shen,Zhe Yan,Marjon Arens,Xiaoxuan Wang,Anne-Marie A Wolters,Richard Kormelink,Yinlei Wang,Yuling Bai,Richard G F Visser,Yongchen Du

doi:10.3389/fpls.2020.545306

Abstract

The whitefly-transmitted tomato yellow leaf curl virus (TYLCV) is one of the most destructive viral pathogens of cultivated tomato. To combat TYLCV, resistance gene Ty-2 has been introduced into cultivated tomato (Solanum lycopersicum) from wild tomato species Solanum habrochaites by interspecific crossing. Introgression lines with Ty-2 contain a large inversion compared with S. lycopersicum, which causes severe suppression of recombination and has hampered the cloning of Ty-2 so far. Here, we report the fine-mapping and cloning of Ty-2 using crosses between a Ty-2 introgression line and several susceptible S. habrochaites accessions. Ty-2 was shown to encode a nucleotide-binding leucine-rich repeat (NLR) protein. For breeding purposes, a highly specific DNA marker tightly linked to the Ty-2 gene was developed permitting marker-assisted selection. The resistance mediated by Ty-2 was effective against the Israel strain of TYLCV (TYLCV-IL) and tomato yellow leaf curl virus-[China : Shanghai2] (TYLCV-[CN : SH2]), but not against tomato yellow leaf curl Sardinia virus (TYLCSV) and leafhopper-transmitted beet curly top virus (BCTV). By co-infiltration experiments we showed that transient expression of the Rep/C1 protein of TYLCV, but not of TYLCSV triggered a hypersensitive response (HR) in Nicotiana benthamiana plants co-expressing the Ty-2 gene. Our results indicate that the Rep/C1 gene of TYLCV-IL presents the avirulence determinant of Ty-2-mediated resistance.

Highlights

Tomato yellow leaf curl disease (TYLCD) is a viral disease caused by a complex of virus species
We showed that the Ty-2 gene from S. habrochaites is located in a region with suppressed recombination caused by a 200-kb inversion when compared with cultivated tomato S. lycopersicum (Wolters et al, 2015)
F2 recombinant A5 was susceptible to tomato yellow leaf curl virus (TYLCV), indicating that Ty-2 is located below marker AW910upF2R3 (Table 1)

Summary

Introduction

Tomato yellow leaf curl disease (TYLCD) is a viral disease caused by a complex of virus species. Tomato yellow leaf curl virus (TYLCV) is one of the causing agents and the most wide-spread one (Navas-Castillo et al, 2011). Its genome consists of one circular single-stranded DNA molecule containing six open reading frames (ORFs) (Gronenborn, 2007) Based on their functions, the proteins encoded by the six ORFs have been named coat protein (CP/ V1), virus movement protein (MP/V2), replication-associated protein (Rep/C1), transcriptional activation protein (TrAP/C2), replication enhancer protein (REn/C3), and a protein determining symptom expression and virus spreading (C4). Preventing viruses from infecting the host mainly requires the control of virus vectors by the use of appropriate physical barriers (traps and screens) and chemical agents (insecticides). Lossof-function allele ty-5 hinders viral translation, leading to resistance (Lapidot et al, 2015), indicating that the Pelota gene is a susceptibility gene for TYLCV

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