SHORT COMMUNICATION Genetic Resources (2022), 3 (6), 64–73 DOI: 10.46265/genresj.PSES6766 https://www.genresj.org ISSN: 2708-3764 The role of tomato wild relatives in breeding disease-free varieties Hamid Khazaei * and Adithya Madduri World Vegetable Center, Shanhua, Taiwan Abstract: Cultivated tomato (Solanum lycopersicum) is one of the most economically important and widely grown vegetable crops worldwide. However, tomato plants are often affected by biotic and abiotic stresses that reduce yield and affect fruit quality. Phenotypic diversity is evident in cultivated tomatoes, particularly for horticultural traits, but genetic diversity is rather narrow. Major disease resistance genes for different pathogens such as viruses, fungi, bacteria and nematodes are mainly derived from wild tomato species and introgressed into cultivated tomatoes. Here, we list the major disease and insect- pest resistance genes identified in S. pimpinellifolium, S. habrochaites, S. peruvianum, S. chilense, S. pennellii, S. galapagense, S. arcanum and S. neorickii with perspective on the gap between current knowledge on tomato wild relatives and the knowledge that is needed. Keywords: Tomato, crop wild relatives, disease resistance, genomics, plant genetic resources, plant breeding Citation: Khazaei, H., Madduri, A. (2022). The role of tomato wild relatives in breeding disease-free varieties. Genetic Resources 3 (6), 64–73. doi: 10.46265/genresj.PSES6766. © Copyright 2022 the Authors. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Tomato wild relatives Crop wild relatives (CWRs) are potential sources of allelic variation useful to overcome biotic and abiotic stresses as they often grow and reproduce in marginal habitats (Ortiz, 2015; Bohra et al, 2021). Tomato wild relatives are native to South America, distributed from the coastal region of Ecuador to northern Chile, including the Galápagos Islands (Darwin et al, 2003). These regions have extremely varied environments within short distances due to differences in altitude (Andean geography) and diverse ecological habitats, which led to local adaptation and generation of large genetic diversity among (Figure 1) and within wild tomato species. Solanum section Lycopersicon (Mill.) Wettst. consists of cultivated tomato (S. lycopersicum) and 12 wild relatives (Ramı́rez-Ojeda et al, 2021). The Tomato Genetics Resource Center (C.M. Rick TGRC, University of California-Davis, USA, https:// tgrc.ucdavis.edu/) hosts the largest genetic stocks of wild tomato collections, with over 900 accessions. The largest collection belongs to accessions of ∗Corresponding author: Hamid Khazaei (hamid.khazaei@gmail.com) S. pimpinellifolium (~300) followed by S. habrochaites (~120), S. peruvianum (~100), S. chilense (~100), and S. pennellii (~50), respectively (Table 1). The World Vegetable Center (WorldVeg, Taiwan https:// genebank.worldveg.org/#/) and the United States Department of Agriculture, Agricultural Research Service (USDA-ARS, https://www.ars-grin.gov/) genebanks also maintain the second and third largest wild tomato collections, respectively (Table 1). However, the majority of their wild tomato collection was originally obtained from the TGRC collection. Furthermore, these genebanks harbour an extensive collection of introgression lines derived from different tomato wild species (Ebert and Schafleitner, 2015). Utilization of tomato wild relatives for biotic stress breeding Domestication has increased the phenotypic diversity of cultivated tomatoes but may have narrowed their resistance to biotic and abiotic constraints as selec- tion ensued (Vu et al, 2020). Tomato wild relatives germplasm harbour natural resistance to various dis- eases and insect pests. Sources of genetic resistance to many of the biotic stresses faced by cultivated toma- Received: 05.07.2022 Accepted: 08.08.2022 Published online: 22.09.2022 https://www.genresj.org https://www.dx.doi.org/10.46265/genresj.PSES6766 https://www.genresj.org https://www.dx.doi.org/10.46265/genresj.PSES6766 mailto:hamid.khazaei@gmail.com https://tgrc.ucdavis.edu/ Genetic Resources (2022), 3 (6), 64–73 CWRs role in breeding disease-free tomatoes 65 Figure 1. Diversity in fruit colour and leaf shape of some tomato wild relatives. From left to right: S. pimpinellifolium (LA1269), S. peruvianum (L00887-3), S. chilense (LA2737B) and S. galapagense (VI063177). The size of the marker is 14cm × 1cm. Photo credit: Hamid Khazaei Table 1. Genetic resources of tomato wild relatives maintained by the Tomato Genetics Resource Center (C.M. Rick TGRC), World Vegetable Center (WorldVeg), and the United States Department of Agriculture, Agricultural Research Service (USDA-ARS) genebanks (data accessed on June 23, 2022). Species No. of accessions per genebank TGRC WorldVeg USDA-ARS S. pimpinellifolium 290 342 338 S. habrochaites 120 139 49 S. peruvianum 69 116 11 S. chilense 115 46 1 S. pennellii 47 59 5 S. corneliomulleri 53 10 12 S. neorickii 47 12 8 S. galapagense 28 27 4 S. arcanum 45 4 3 S. cheesmaniae 12 17 5 S. chmielewskii 16 11 0 S. lycopersicoides 23 5 0 S. sitiens 13 5 2 S. huaylasense 16 0 0 S. ochranthum 7 0 2 S. juglandifolium 5 1 0 toes have been identified in some accessions of wild tomato species that have been historically used to intro- duce resistance (R) genes into cultivated tomato vari- eties. It should be noticed that there is genetic diversity for biotic resistance response within tomato wild species, and only a few accessions within each species have been identified as sources of resistance (Ebert and Schafleit- ner (2015) and references). We list major R genes found in and introgressed from wild tomato species into culti- vated tomatoes in Table 2, along with information about their causal pathogens as footnotes. For example, the R genes/alleles conferring resistance to the begomoviruses that cause tomato yellow leaf curl diseases (called Ty genes), were found in wild tomato species. Most tomato advanced lines grown in tropical and subtropical regions of the world carry at least one source of Ty resistance genes (Ty-1/Ty-3) or multiple Ty genes (Ty-2, ty-5, Ty-6). The pyramiding of Ty genes into one line leads to broad and probably more durable resistance to begomoviruses. Likewise, R genes for late blight (caused by Phytoph- thora infestans, Ph genes) and fusarium wilt (caused by Fusarium oxysporum, I genes) also originated from wild tomatoes (Table 2). These genes are also frequently present in the modern tomato lines worldwide. Some important major QTLs (quantitative trait locus) such as Bwr and EB, conferring bacterial wilt (caused by Ralsto- nia spp.) and early blight (caused by Alternaria linar- iae) resistance, were first introgressed to adapted culti- vated tomato cultivars from S. pimpinellifolium and later uncovered and genetically mapped. Some R genes (Rx- 1, -2 and -3) for bacterial spot resistance (caused by several species of gram-negative bacteria in the genus Xanthomonas) were also derived from S. pimpinelli- folium via cultivated tomato. Several R genes against important pathogens in tomato have mainly been intro- gressed, from the wild species S. pimpinellifolium, S. habrochaites, S. peruvianum, S. chilense and S. pennel- lii, into modern tomato varieties (Table 2). However, most tomato breeding programmes focus on S. pimpinel- lifolium due to its red fruit colour (Figure 1) and its close relationship to cultivated tomato, which allows breed- ers to easily obtain interspecific crosses. That is probably why most of the R genes have already been identified in this species. 66 Khazaei and Madduri Genetic Resources (2022), 3 (6), 64–73 Table 2. List of major biotic resistance genes incorporated into cultivated tomatoes (Solanum lycopersicum) from wild relatives of tomato and S. lycopersicum var. cerasiforme. Causative agents for the listed diseases are included in footnotes. Species R-genes’ contribution Disease/Insect pest References S. pimpinellifolium L. I and I-2 Fusarium wilt1 Stall and Walter (1965); reviewed in Chitwood-Brown et al (2021) Ph-1, Ph-2, Ph-3 and Ph-5 Late blight2 Bonde and Murphy (1952); Gallegly and Marvel (1955); AVRDC (1994); Foolad et al (2006) EB-5 and EB-9 Early blight3∗ Anderson et al (2021) Bwr-6 and Bwr-12 Bacterial wilt4∗ Wang et al (2013) Rx-1, Rx-2 and Rx-3 Bacterial spot5∗ Yu et al (1995); reviewed in Adhikari et al (2020) Rx-4 Bacterial spot Robbins et al (2009) Sm Gray leaf spot6 Parlevliet (2002) Cf genes (except Cf-4 and Cf-5) Leaf mold7 Bailey (1950); reviewed in Scott and Gardner (2007) Sw-1(a and b), Sw-2, Sw-3 and Sw-4 TSWV8 Finlay (1953); Roselló et al (1998); Zhu et al (2017); reviewed in Qi et al (2021) Pto Bacterial speck9 Pitblado and Kerr (1980) Cmm genes Bacterial canker10 Forster and Echandi (1972); Sotirova et al (1994); Sen et al (2021) S. habrochaites S. Knapp and D. M. Spooner Ph-4 Late blight Lough (2003) Cf-4 Leaf mold Stevens and Rick (1986) Ty-2 TYLCV11 Hanson et al (2006) Tm-1 ToMV12 Pelham (1966) Ol-1/Ol-3, and Ol-5 Powdery mildew13 van der Beek et al (1994); Huang et al (2000); Bai et al (2005) Cmm genes Bacterial canker Forster and Echandi (1972); Francis et al (2001); Coaker and Francis (2004); Sotirova et al (1994) Rbcq genes Gray mould14 ten Have et al (2007); Finkers et al (2007a,b) S. peruvianum L. ty-5 TYLCV Hutton et al (2012) Sw-5 and Sw-6 TSWV Giordano et al (2000); Rosello et al (2001) Mi genes Root-knot nematodes15 Smith (1944); reviewed in El-Sappah et al (2019) Tm-2, Tm-22 and Tm-2a ToMV Soost (1963); Ganal and Tanksley (1996) and Tanksley and Nelson (1996) Ve Verticillium wilt16 Diwan et al (1999) Frl Fusarium crown17 Vakalounakis et al (1997) S. chilense (Dunal) Reiche Ty-1/Ty-3a, Ty-4, and Ty-6 TYLCV Zamir et al (1994); Ji et al (2007); Ji et al (2009); Gill et al (2019) Sw-7 TSWV Stevens et al (1994) Cmm genes Bacterial canker Sotirova et al (1994) Lv Powdery mildew Yordanov et al (1975); Chunwongse et al (1997) - Gray mould ten Have et al (2007) Continued on next page Genetic Resources (2022), 3 (6), 64–73 CWRs role in breeding disease-free tomatoes 67 Table 2 continued R-genes’ contribution Disease/Insect pest References S. pennellii Correll I-3 and I-7 Fusarium wilt Catanzariti et al (2015); Gonzalez-Cendales et al (2016) Asc Alternaria stem canker18 Scott and Gardner (2007) Xv-4 Bacterial spot Astua-Monge et al (2000) Acylsugar-related genes A wide range of insects Leckie et al (2012, 2016); Schilmiller et al (2012) S. galapagense S. C. Darwin and Peralta Wf-1 and Wf-2 Whiteflies19 Firdaus et al (2013); Santegoets et al (2021) S. arcanum Peralta Ol-4 Powdery mildew Bai et al (2005) Cmm genes Bacterial canker Crinò et al (1995); Sotirova et al (1994); Sen et al (2013) S. neorickii D. M. Spooner, G. J. Anderson and R. K. Jansen V2 Verticillium wilt Kanagawa Agricultural Technology Center (1999) - Gray mould ten Have et al (2007); Finkers et al (2008) S. l. var. cerasiforme Cf-5 Leaf mold Dickinson et al (1993); Dixon et al (1998) ol-2 Powdery mildew Ciccarese et al (1998) 1Fusarium wilt caused by fungal pathogen Fusarium oxysporum (Schlecht. emend. Snyder & Hansen). 2Late blight resistance caused by the oomycete Phytophthora infestans (Mont.) de Bary. 3Early blight is caused by fungal pathogen Alternaria spp. 4Bacterial wilt caused by the group of soilborne bacteria in the Ralstonia solanacearum species complex. 5Bacterial spot caused by several species belonging to the genus Xanthomonas. It can be caused by Xanthomonas euvesicatoria ex Doidge, X. vesicatoria ex Doidge, X. perforans, and X. gardneri Šutic. ∗Early blight, bacterial wilt, and bacterial spot (Rx-1, Rx-2, and Rx-3) resistance genes are most likely derived from S. pimpinellifolium via cultivated tomato. 6Gray leaf spot caused by fungal pathogen Stemphylium lycopersici (S. lycopersici). 7Leaf mold caused by fungal pathogen Cladosporium fulvum (syn. Passalora fulva). 8TSWV, tomato spotted wilt orthotospovirus (order Bunyavirales, family Tospoviridae, genus Orthotospovirus) is transmitted by Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). 9Bacterial speck disease caused by Pseudomonas syringae pv. tomato (Pst). 10Bacterial canker caused by Clavibacter michiganensis subsp. Michiganesis. 11TYLCV, tomato yellow leaf curl virus disease. TYLCV is caused by whitefly transmitted Geminiviruses (begomoviruses). Ty-1 and Ty-3 are allelic (Verlaan et al, 2013). 12ToMV, tomato mosaic virus. ToMV is a member of the family tobamoviridae and belongs to the genus tobamovirus. 13Powdery mildew can be caused by three species of biotrophic fungal pathogens; Oidium lycopersici, Oidium neolycopersici (syn. Pseoudoidium neolycopersici), and Leveillula taurica. Ol-1 and Ol-3 are allelic (Huang et al, 2000). 14Gray mould caused by fungal pathogen Botrytis cinerea (teleomorph: Botryotinia fuckeliana). 15Root-knot nematodes can be caused by Meloidogyne incognita, M. javanica, and M. arenaria. 16Verticillium wilt caused by the biotrophic fungus Verticillium dahliae. 17Fusarium crown rot caused by F. oxysporum f. sp. radicis-lycopersici. 18Alternaria stem canker caused by fungal pathogen Alternaria alternate. 19Whitefly (Bemisia tabaci) resistance. Species 68 Khazaei and Madduri Genetic Resources (2022), 3 (6), 64–73 Challenges The utilization of wild tomatoes in breeding pro- grammes is not without a cost. CWRs generally show poor adaptation beyond their natural distribution range (Bohra et al, 2021). Furthermore, the introgressed gene from a wild relative into advanced lines may dis- rupt long-accumulated horticultural traits due to link- age drag (Tanksley and Nelson, 1996). For example, S. galapagense has been identified as a source of insect-pest resistance (Rakha et al, 2017; Vendemiatti et al, 2021). When it is crossed with cultivated tomatoes, the fruit size and setting reduce significantly, w h ich a r e unde- sirable traits. Linkage drag can be removed by con- ducting backcrosses to the recurrent parents (cultivated tomato). Applications of DNA molecular markers (MAB, marker-assisted backcrossing) allow for the monitoring of the genome around the gene/locus of interest and the genetic background, speeding up the return to the recur- rent parent genome (Tourrette et al, 2021). Genome editing can also be used to remove the undesirable gene without having extensive backcrossing. For exam- ple, CRISPR-Cas9-based gene editing was used to over- come a linkage drag in tomato by editing the jointless- 2 gene introgressed from S. cheesmaniae (Roldan et al, 2017). The World Vegetable Center is currently testing CRISPR-Cas9 to edit genes implicated with fruit size reg- ulation in interspecific c r osses b e tween S . galapagense and cultivated tomato (Schafleitner et al, 2022). Genomics-assisted breeding tools Tomato wild relatives have more to offer. Bai et al (2018) stated that about 20 pathogens could be genetically controlled by resistance genes derived from a few wild species. The genome of some tomato wild species, including S. pennellii (Bolger et al, 2014; Schmidt et al, 2017), S. chilense (Stam et al, 2019), S. pimpinellifolium (Razali et al, 2018; Wang et al, 2020; Gramazio et al, 2020) and S. lycopersicoides (Powell et al, 2022) along with the pan-genome (Gao et al, 2019) have been assembled. These efforts have bolstered our knowledge and understanding of tomato wild species along with the genetics of resistance genes. Recent improvements in genomic resources have enabled us to track and genetically map the wild tomato genes in commercially adapted varieties (Anderson et al, 2021). The tomato community largely benefits from advanced, rich genomic resources (https:// solgenomics.net/) and phenotyping tools; however, rapid generation technology (speed breeding) has not yet been developed. Robust DNA markers for major genes derived from wild relatives have been developed and widely applied in private and public breeding programmes worldwide (Foolad and Panthee, 2012; Hanson et al, 2016). In the past, sources of important disease resistance genes in wild tomato relatives have been intensively investigated. However, the majority of R genes were discovered only in a few species (listed in Table 1). The other wild species that either are not easy to cross with cultivated tomatoes or are self-incompatible or allogamous have not contributed much to this journey (e.g. S. chmielewskii, S. corneliomulleri, S. huaylalloasense, S. juglandifolium, S. ochranthum, S. lycopersicoides and S. sitiens). Regarding these species, the literature only represents a few accessions of S. lycopersicoides being resistant to grey mould (caused by Botrytis cinerea) (Davis et al, 2009) or a few accessions of S. corneliomulleri being resistant to the TYLCV (Yan et al, 2018), but major genes/alleles from these species are yet to be reported. For some of these species, only a few accessions have been collected or are available in genebanks (Table 1). Among these species, some genomic studies were performed on S. sitiens (Chetelat et al, 2019) and S. lycopersicoides (Powell et al, 2022), which are potential sources of genes for adaptation to abiotic stresses (i.e. drought and heat stresses). Introgression lines were also developed from S. chmielewskii to study the accumulation of secondary metabolites in tomato fruit (Ballester et al, 2016). Conclusions Now that the scientific community has access to advanced tissue culture techniques, double haploidy protocols, modern phenotyping facilities, and genomic and bioinformatic tools, tomato wild relatives could be explored even more. This may provide new sources of genetic resources and R genes that could be used to pyramid new genes into one variety leading to broad and probably more durable resistance. Furthermore, ongoing advances in sequencing technology can be used to develop reference genome sequences for undiscovered tomato wild relatives, and the development of tomato pan-genomes will be a valuable strategy in harnessing the genetic diversity of these species. Additionally, genome editing enables de novo domestication strategies for the targeted use of tomato relatives (Zsögön et al, 2018). Thus, exploring the variation in tomato wild species could be an interesting topic for future studies. Conflict of interest statement The authors declare that they have no conflict of interest. Author contributions Original draft: Hamid Khazaei; review and editing: Hamid Khazaei and Adithya Madduri. All authors read and agreed to the published version of the manuscript. Funding Financial support was provided by the Foreign, Com- monwealth and Development Office (UK) and by the long-term strategic donors to the World Vegetable Cen- ter, Taiwan: UK aid from the UK Government, the United States Agency for International Development (USAID), the Australian Centre for International Agricul- tural Research (ACIAR), Germany, Thailand, Philippines, Genetic Resources (2022), 3 (6), 64–73 CWRs role in breeding disease-free tomatoes 69 Korea, and Japan. The authors thank Roland Schafleit- ner, Peter Hanson and Ya-ping Lin for their kind sugges- tions on the manuscript. 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Biotechnol 36, 1211–1216. doi: https://doi.org/10.1038/nbt.4272 https://doi.org/10.1038/s41467-020-19682-0 https://doi.org/10.1038/s41467-020-19682-0 https://doi.org/10.3389/fpls.2018.01198 https://doi.org/10.1093/genetics/141.2.675 https://doi.org/10.1093/genetics/141.2.675 https://doi.org/10.1007/BF00225889 https://doi.org/10.1007/BF00225889 https://doi.org/10.1105/tpc.17.00180 https://doi.org/10.1105/tpc.17.00180 https://doi.org/10.1038/nbt.4272 Tomato wild relatives Utilization of tomato wild relatives for biotic stress breeding Challenges Genomics-assisted breeding tools Conclusions Conflict of interest statement Author contributions Funding