Tomato Yellow Leaf Curl Virus-Resistant and -Susceptible Tomato Genotypes Similarly Impact the Virus Population Genetics.

Wendy G Marchant,Saurabh Gautam,Samuel F Hutton,Rajagopalbabu Srinivasan

doi:10.3389/fpls.2020.599697

Abstract

Tomato yellow leaf curl virus is a species in the genus Begomovirus and family Geminiviridae. Tomato yellow leaf curl virus (TYLCV) infection induces severe symptoms on tomato plants and causes serious yield losses worldwide. TYLCV is persistently transmitted by the sweetpotato whitefly, Bemisia tabaci (Gennadius). Cultivars and hybrids with a single or few genes conferring resistance against TYLCV are often planted to mitigate TYLCV-induced losses. These resistant genotypes (cultivars or hybrids) are not immune to TYLCV. They typically develop systemic infection, display mild symptoms, and produce more marketable tomatoes than susceptible genotypes under TYLCV pressure. In several pathosystems, extensive use of resistant cultivars with single dominant resistance-conferring gene has led to intense selection pressure on the virus, development of highly virulent strains, and resistance breakdown. This study assessed differences in TYLCV genomes isolated from susceptible and resistant genotypes in Florida and Georgia. Phylogenetic analyses indicated that Florida and Georgia isolates were distinct from each other. Population genetics analyses with genomes field-collected from resistant and susceptible genotypes from Florida and/or Georgia provided no evidence of a genetic structure between the resistant and susceptible genotypes. No codons in TYLCV genomes from TYLCV-resistant or susceptible genotypes were under positive selection, suggesting that highly virulent or resistance-breaking TYLCV strains might not be common in tomato farmscapes in Florida and Georgia. With TYLCV-resistant genotypes usage increasing recently and multiple tomato crops being planted during a calendar year, host resistance-induced selection pressure on the virus remains a critical issue. To address the same, a greenhouse selection experiment with one TYLCV-resistant and susceptible genotype was conducted. Each genotype was challenged with TYLCV through whitefly-mediated transmission serially 10 times (T1-T10). Population genetics parameters at the genome level were assessed at T1, T5, and T10. Results indicated that genomes from resistant and susceptible genotypes did not differentiate with increasing transmission number, no specific mutations were repeatedly observed, and no positive selection was detected. These results reiterate that resistance in tomato might not be exerting selection pressure against TYLCV to facilitate development of resistance-breaking strains. TYLCV populations rather seem to be shaped by purifying selection and/or population expansion.

Highlights

Tomato yellow leaf curl virus (TYLCV) infects tomato and causes substantial yield losses in the southeastern United States and in many parts of the world (Czosnek and Laterrot, 1997; Momol et al, 1999; Polston et al, 1999; Moriones and NavasCastillo, 2000; Pappu et al, 2000; Varma and Malathi, 2003)
The number of haplotypes was slightly higher in TYLCV genomes isolated from resistant genotypes than susceptible genotypes in Georgia
The number of substitutions and indels were slightly higher in TYLCV genomes isolated from resistant genotypes than susceptible genotypes in Georgia (Table 2)

Summary

Introduction

Tomato yellow leaf curl virus (TYLCV) infects tomato and causes substantial yield losses in the southeastern United States and in many parts of the world (Czosnek and Laterrot, 1997; Momol et al, 1999; Polston et al, 1999; Moriones and NavasCastillo, 2000; Pappu et al, 2000; Varma and Malathi, 2003). Symptoms of TYLCV infection in tomato plants include stunted growth, chlorosis, curling of leaves, and reduced fruit yield (Cohen and Nitzany, 1966; Cohen and Antignus, 1994; Picó et al, 1996). Resistance to TYLCV has been incorporated from wild solanum species into tetraploid cultivated tomato (Lapidot et al, 1997; Lapidot and Friedmann, 2002; Yan et al, 2018). TYLCV-resistant genotypes are systemically infected, often exhibit milder symptoms, and suffer reduced yield loss than susceptible genotypes (Figure 1). Whiteflies acquire reduced amounts of virus from TYLCV-infected resistant genotypes than susceptible genotypes, suggesting that resistant genotypes might not function as effective inoculum sources in comparison with susceptible genotypes (Lapidot et al, 2001; Legarrea et al, 2015). Ty-6 has been characterized as the incomplete dominance gene (Gill et al, 2019)

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Conclusion