Solanum elaeagnifolium and S. rostratum as potential hosts of the tomato brown rugose fruit virus

PLOS ONE RESEARCH ARTICLE Solanum elaeagnifolium and S. rostratum as potential hosts of the tomato brown rugose fruit virus Maor Matzrafi ID1*, Jackline Abu-Nassar1, Chen Klap2,3, Meital Shtarkman3, Elisheva Smith3, Aviv Dombrovsky3 1 Department of Plant Pathology and Weed Research, Newe Ya’ar Research Center, Agricultural Research Organization (ARO)–Volcani Institute, Ramat Yishay, Israel, 2 The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel, 3 Department of Plant Pathology and Weed Research, Agricultural Research Organization (ARO)–Volcani Institute, Rishon LeZion, Israel a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Matzrafi M, Abu-Nassar J, Klap C, Shtarkman M, Smith E, Dombrovsky A (2023) Solanum elaeagnifolium and S. rostratum as potential hosts of the tomato brown rugose fruit virus. PLoS ONE 18(3): e0282441. https://doi.org/ 10.1371/journal.pone.0282441 Editor: Basavaprabhu L. Patil, ICAR - Indian Institute of Horticultural Research (IIHR), INDIA Received: November 11, 2022 Accepted: February 14, 2023 Published: March 1, 2023 Copyright: © 2023 Matzrafi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. * Abstract Invasive weeds cause significant crop yield and economic losses in agriculture. The highest indirect impact may be attributed to the role of invasive weeds as virus reservoirs within commercial growing areas. The new tobamovirus tomato brown rugose fruit virus (ToBRFV), first identified in the Middle East, overcame the Tm-22 resistance allele of cultivated tomato varieties and caused severe damage to crops. In this study, we determined the role of invasive weed species as potential hosts of ToBRFV and a mild strain of pepino mosaic virus (PepMV-IL). Of newly tested weed species, only the invasive species Solanum elaeagnifolium and S. rostratum, sap inoculated with ToBRFV, were susceptible to ToBRFV infection. S. rostratum was also susceptible to PepMV-IL infection. No phenotype was observed on ToBRFV-infected S. elaeagnifolium grown in the wild or following ToBRFV sap inoculation. S. rostratum plants inoculated with ToBRFV contained a high ToBRFV titer compared to ToBRFV-infected S. elaeagnifolium plants. Mixed infection with ToBRFV and PepMV-IL of S. rostratum plants, as well as S. nigrum plants (a known host of ToBRFV and PepMV), displayed synergism between the two viruses, manifested by increasing PepMVIL levels. Additionally, when inoculated with either ToBRFV or PepMV-IL, disease symptoms were apparent in S. rostratum plants and the symptoms were exacerbated upon mixed infections with both viruses. In a bioassay, ToBRFV-inoculated S. elaeagnifolium, S. rostratum and S. nigrum plants infected tomato plants harboring the Tm-22 resistant allele with ToBRFV. The distribution and abundance of these Solanaceae species increase the risks of virus transmission between species. Data Availability Statement: All relevant data are within the manuscript and its Supporting Information files. Funding: Horizon 2020, award number: 101000570, recipient: Aviv Dombrovsky. Introduction Competing interests: The authors have declared that no competing interests exist. Weeds are a source of significant agricultural crop yield and economic loss. Worldwide, the potential yield loss of major agriculture crops due to weeds (34%, on average) is higher than PLOS ONE | https://doi.org/10.1371/journal.pone.0282441 March 1, 2023 1 / 13 PLOS ONE Invasive weeds host of ToBRFV other crop pests, including insects, pathogens, viruses and animal pests [1]. Among weeds, invasive species present major economic and ecological threats to agriculture and natural areas. In recent decades, there has been a rise in reports of invasive weed species due to significant manmade global changes. Among the leading causes for this trend are import-export trade [2, 3] and climate change [4, 5]. In the United States alone, annual losses caused only by crop-related invasive weeds were estimated to be more than $27 billion dollars [6]. In Israel, several invasive species such as Parthenium hysterophorus, Solanum spp., Ambrosia confertiflora and Amaranthus spp. have been documented [7]. Apparently, the invasion route of these weeds is via imported animal feed shipments [7]. The damage due to invasive weed species is not limited to yield losses, but could be associated with the increased spread of fire-fuel [8–10] and strong allergenic effects [11–13]. Although it may be underestimated, the greatest indirect impact of invasive weeds on crop yield may be attributed to their role as virus reservoirs within commercial growing areas. Several weeds have been previously identified as potential reservoirs of plant viruses such as iris yellow spot virus, potato leafroll virus and potato virus Y (PVY) [14]. Various studies have shown that within identified weed virus hosts there was a high proportion of invasive weeds. P. hysterophorus, a prominent invasive wide spread weed species, was infected with cherry tomato leaf curl virus and tobacco curly shoot alpha satellite [15]. In Turkey, A. retroflexus appeared to be a common host of several viruses including cucumber mosaic virus, PVY and tomato spotted wilt orthotospovirus [16]. Ventenata dubia, an invasive weed species infesting grasslands, rangelands and pastures throughout the USA was susceptible to barley or cereal yellow dwarf virus infection and served as a transient agent for crop infections [17]. In Israel, we documented new invasive weed species such as A. graecizans and A. muricatus as optional hosts of tobamovirus cucumber green mottle mosaic virus [18]. The new tobamovirus tomato brown rugose fruit virus (ToBRFV), first identified in the Middle East [19, 20], overcomes the Tm-22 resistant allele of cultivated tomato varieties grown trellised in greenhouses [19]. Outbreaks of the ToBRFV disease were later reported in North America [21, 22], Germany [23], Turkey [24], Greece [25], Spain, the Netherlands and China [26]. ToBRFV causes a range of symptoms in tomato [27]. Fruit yellowing and bleaching are the most commonly occurring symptoms, accompanied by mottled mosaic leaves [19, 28]. Concomitantly, a worldwide spread of the mechanically transmitted potexvirus, pepino mosaic virus (PepMV), has also occurred [29–32]. PepMV causes fruit necrosis and plant wilting [33, 34]. ToBRFV and PepMV profoundly affect the yield and quality of tomato plants. PepMV and tobamoviruses are seed-borne, mechanically transmitted viruses [29, 35]. Plant manipulations such as planting, fruit picking, pruning and trellising, essential for tomato plant cultivation, are practices predisposing plants for disease spread of mechanically transmitted viruses. Regarding PepMV, even (...truncated)