Conventional and new genetic resources for an eggplant breeding revolution

Copyedited by: OUP Journal of Experimental Botany, Vol. 74, No. 20 pp. 6285–6305, 2023 https://doi.org/10.1093/jxb/erad260 Advance Access Publication 8 July 2023 © The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: [email protected] REVIEW PAPER Conventional and new genetic resources for an eggplant breeding revolution PietroGramazio1,†,, DavidAlonso1,†,, AndreaArrones1,, GloriaVillanueva1,, MariolaPlazas1, LauraToppino2,, LorenzoBarchi3,, EzioPortis3,, PaolaFerrante4,, SergioLanteri3,, Giuseppe LeonardoRotino2,, GiovanniGiuliano4,, SantiagoVilanova1, and JaimeProhens1,*, 1 Instituto de Conservación y Mejora de la Agrodiversidad Valenciana, Universitat Politècnica de València, Camino de Vera 14, 46022 Valencia, Spain 2 CREA Research Centre for Genomics and Bioinformatics, Via Paullese 28, 26836 Montanaso Lombardo, LO, Italy 3 Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), Plant Genetics, University of Turin, Largo P. Braccini 2, 10095 Grugliasco, TO, Italy 4 Agenzia Nazionale Per Le Nuove Tecnologie, L’energia e Lo Sviluppo Economico Sostenibile (ENEA), Casaccia Research Centre, Rome, Italy † These authors contributed equally to this work. * Correspondence: jpr[email protected].es Received 16 March 2023; Editorial decision 4 July 2023; Accepted 5 July 2023 Editor: JohnLunn, MPI of Molecular Plant Physiology, Germany Abstract Eggplant (Solanum melongena) is a major vegetable crop with great potential for genetic improvement owing to its large and mostly untapped genetic diversity. It is closely related to over 500 species of Solanum subgenus Leptostemonum that belong to its primary, secondary, and tertiary genepools and exhibit a wide range of characteristics useful for eggplant breeding, including traits adaptive to climate change. Germplasm banks worldwide hold more than 19000 accessions of eggplant and related species, most of which have yet to be evaluated. Nonetheless, eggplant breeding using the cultivated S. melongena genepool has yielded significantly improved varieties. To overcome current breeding challenges and for adaptation to climate change, a qualitative leap forward in eggplant breeding is necessary. The initial findings from introgression breeding in eggplant indicate that unleashing the diversity present in its relatives can greatly contribute to eggplant breeding. The recent creation of new genetic resources such as mutant libraries, core collections, recombinant inbred lines, and sets of introgression lines will be another crucial element and will require the support of new genomics tools and biotechnological developments. The systematic utilization of eggplant genetic resources supported by international initiatives will be critical for a much-needed eggplant breeding revolution to address the challenges posed by climate change. Keywords: Eggplant, genepools, genetic resources, genomics, germplasm banks, introgression breeding, Solanum melongena, wild relatives. Downloaded from https://academic.oup.com/jxb/article/74/20/6285/7221360 by Instituto Ingenio (CSIC-UPV) user on 06 November 2023 Copyedited by: OUP 6286 | Gramazio et al. Introduction Eggplant (Solanum melongena L.), also known as common eggplant, brinjal, and aubergine, was domesticated 9000–10000 years ago from its wild ancestor, S. insanum L., in the Indian subcontinent and Southeast Asia (Page et al., 2019a). Apart from the intra-specific diversity of eggplant, over 500 species of Solanum subgenus Leptostemonum (Vorontsova and Knapp, 2016; Knapp et al., 2019), belonging to its primary, secondary and tertiary genepools, provide a formidable source of additional diversity (Syfert et al., 2016). As the sixth most important vegetable crop globally in terms of production, following tomato, onion, watermelon, cucumber, and cabbage (FAOSTAT, 2023), eggplant holds significant agricultural value. Its global production has increased by 24% over the past decade, from 47.3×106 t in 2012 to 58.6×106 t in 2021 (FAOSTAT, 2023). As a warm-climate crop, it is mostly cultivated in tropical, subtropical, and temperate regions of the world, and is an important part of the cuisine from East Asia, the Indian subcontinent, Southern Asia, the Middle East, and the Mediterranean basin. Eggplant contributes to alleviating ‘hidden hunger’ by providing significant dietary amounts of K, P, Mn, Cu, and folate, but also high concentrations of bioactive phenolics beneficial for human health (Plazas et al., 2013; Rosa-Martínez et al., 2021). In recent years, the impact of climate change on agricultural production has become a significant concern, and eggplant cultivation is expected to be strongly affected (del Pozo et al., 2019; Habib-ur-Rahman et al., 2022). Increased spells of extreme events such as intense drought periods may have a dramatic impact on crops sensitive to water stress, including eggplant (Plazas et al., 2022). Although significant advances have occurred in eggplant breeding (Daunay and Hazra, 2012; Chapman, 2020; Toppino et al., 2021; Arafa et al., 2022), they have not kept pace with those for other major vegetable crops, such as tomato. Tomato breeding programs have made extensive use of genetic resources, including the introgression of multiple genes from crop wild relatives (CWRs) that have been incorporated into modern cultivars (Díez and Nuez, 2008; Schouten et al., 2019). While eggplant breeding programs have been successful in developing new improved cultivars, until now only a few of them have involved the introgression of useful traits. For example, resistance to the fungal wilts Fusarium oxysporum f. sp. melongenae (Fom) and Verticillium dahliae from S. aethiopicum (Toppino et al., 2007, 2008b, 2009) and S. linnaeanum (Liu et al., 2015) has been exploited with considerable success, and new eggplant materials resistant to these diseases have been obtained (Toppino et al., 2021). In addition to brinjal eggplant, two other related minor crops, namely the scarlet eggplant (S. aethiopicum L.) and the gboma eggplant (S. macrocarpon L.), were domesticated in Africa (Page et al., 2019b) and are mostly grown in the sub-Saharan region (Schippers, 2000). Although they have mostly local importance, they are relevant crops, particularly S. aethiopicum, in some parts of the world such as Brazil and the Caribbean as well as in southern Italy, where a Protected Denomination of Origin exists for the S. aethiopicum landrace ‘Melanzana Rossa di Rotonda’ (Schippers, 2000; Sunseri et al., 2010). The fact that both species are cross-compatible with common eggplant (Bletsos et al., 2004; Oyelana and Ugborogho, 2008; Rotino et al., 2014) is of great relevance for the breeding of the latter crop, as they share many domestication traits, facilitating the introduction of resistance to some pests and diseases from these species to common eggplant without dragging in undesirable traits present in wild species (Toppino et al., 2021; Arafa et al., 2022). Eggplant displays a wide morphological diversity, even within a single varietal group, particularly for fruit traits such as size, color, and shape (Fig. 1), as well as for agronomic traits and adaptation to different environments (Cericola et al., 2013; Taher et al., 2017; Chapman, 2020; Kouassi et al., 2020; Ro et al., 2022; Salinier et al., 2022; Toppino et al., 2022). The diversity present within the cultivated eggplant is of great interest for eggplant breeding and has allowed the development of significantly improved modern cultivars (Daunay and Hazra, 2012). However, as occurs with many other vegetables, this high morphological diversity is mostly the consequence of genetic variation in a few major genes, particularly those related to fruit traits (Daunay et al., 2004; Portis et al., 2015; Toppino et al., 2016; Mangino et al., 2021; Arrones et al., 2022; Guan et al., 2022), and the overall genetic variation of the crop is narrow (Acquadro et al., 2017; Barchi et al., 2019a; Liu et al., 2019). Therefore, the exploitation of the genetic diversity present in other cultivated eggplants (S. aethiopicum and S. macrocarpon) and wild relatives represents a promising avenue for developing improved eggplant materials by incorporating their unique traits (Oyelana and Ugborogho, 2008; Prohens et al., 2012; Toppino et al., 2021). Eggplant breeding challenges for the present and the future: the need for a breeding revolution Eggplant yield has increased dramatically from a global average of 10.2 t/ha in the decade 1961–1970 to 28.0 t/ha in 2012– 2021 (FAOSTAT, 2023). There is not much information on the genetic versus agronomic factors that have driven this dramatic yield increase, although Muñoz-Falcón et al. (2009) found that modern varieties of black eggplants yielded on average 29.8% more than landraces, suggesting that improvement of cultivation techniques such as protected cultivation, irrigation, improved fertilization, and pest and pathogen management may have had a major role in yield increase in the last decade. This suggests that major genetic advances that have already Downloaded from https://academic.oup.com/jxb/article/74/20/6285/7221360 by Instituto Ingenio (CSIC-UPV) user on 06 November 2023 Copyedited by: OUP Conventional and new genetic resources in eggplant | 6287 taken place in other major staple and vegetable crops (Hedden, 2003; Díez and Nuez, 2008) may still need to occur in the coming decades for eggplant breeding to produce dramatically improved varieties adapted to the new conditions posed by climate change. So far, breeding advances and actual exploitation of genetic resources in eggplant, particularly those from related species, have not been comparable to those obtained in other major vegetable crops such as tomato (Schouten et al., 2019). Although tomato has a narrow genetic diversity and exhibits limited crossability with only a few CWRs, considerable broadening of the genetic base and genetic advances have been achieved in this species through introgression breeding using wild relatives as donors. Among these achievements, the introgression of multiple genes for tolerance to diseases and fruit quality traits, the development of heterotic hybrids, the improvement of shelf-life, the diversification of varietal types, and the adaptation to multiple environments (Díez and Nuez, 2008) have enabled the production of a large number of highly productive tomato varieties of many different typologies, resistant to the major diseases and suited to different environments. The success obtained in the extensive use of genetic resources in tomato breeding suggests that in eggplant, which exhibits an even greater diversity of cross-compatible relatives, the advances in breeding for adaptation to climate change and other traits, achievable with a systematic use of its genetic resources, may be extraordinary. Like tomato, eggplant is self-compatible and mostly autogamous (Daunay and Hazra, 2012). Indeed, in a study involving eggplant and tomato accessions genotyped by single primer enrichment technology (SPET)—a genotyping technique that employs targeted amplification of specific genomic regions using a single specific primer (Scaglione et al., 2019)—the heterozygosity of eggplant and tomato was reported to be 0.67% and 0.65%, respectively (Barchi et al., 2019a), confirming the mostly autogamous reproduction of both species, which in turn impacts the applicable breeding methods. However, high levels of cross-pollination can occur when the circumstances are favorable, such as in open field conditions with the presence of pollinators (Quamruzzaman, 2021). Avoiding cross-pollination is highly relevant for maintaining purity in the case of reproduction of landraces or germplasm accessions. Breeding in eggplant traditionally relies on selection from both within and among landraces as well as in the development of F1 hybrids, which are predominant in high-value markets (EU Plant Variety Database, 2022). It has long been known that F1 hybrids in eggplant generally display heterosis (i.e. the hybrid displays superior quantitative traits, such as yield, with respect to the standard parent) (Kakizaki, 1931; Sambandam, 1964), and heterobeltiosis (i.e. the hybrid displays superior quantitative traits with respect to the best parent) is also common (Rodríguez-Burruezo et al., 2008; Kumar et al., 2020). Selection of parents for heterotic hybrids is possible by evaluating the parents’ combining ability, as well as by selecting parents with high genetic distance using molecular markers (RodríguezBurruezo et al., 2008). It is worth remembering that landraces and pure line selections of eggplant with excellent yields are also available and extensively cultivated (Muñoz-Falcón et al., 2009; Taher et al., 2017). However, further improvement of the yield potential is a significant challenge in eggplant breeding, Fig. 1. Diversity of fruit morphology in the cultivated (S. melongena) gene pool (A), within a particular cultivar type (striped eggplant) (B), and in wild relatives from the primary (GP1), secondary (GP2), and tertiary (GP3) genepools (C). Downloaded from https://academic.oup.com/jxb/article/74/20/6285/7221360 by Instituto Ingenio (CSIC-UPV) user on 06 November 2023 Copyedited by: OUP 6288 | Gramazio et al. and will undoubtedly benefit from the incorporation of new genetic diversity to allow additional genetic advances (MuñozFalcón et al., 2009; Daunay and Hazra, 2012). One of the major current challenges in eggplant breeding is the development of breeding lines with an improved tolerance or resistance to major pests and diseases (Toppino et al., 2021), which may cause crop losses of up to 100% (Daunay and Hazra, 2012; Arafa et al., 2022). Eggplant is affected by numerous diseases, although the most relevant in terms of economic impact is the bacterial wilt caused by Ralstonia solanacearum, which is highly prevalent in tropical regions (Lebeau et al., 2013; Barik et al., 2020). In many cases, bacterial wilt prevents eggplant cultivation unless plants are grafted onto resistant rootstocks (Namisy et al., 2019). Verticillium and Fusarium wilts, as well as nematodes, are also important eggplant pathogens in many regions of the world (Arafa et al., 2022). So far, most modern commercial varieties of eggplant do not carry genes for disease resistance (Srinivasan, 2009). Introgression breeding from the multiple sources of resistance found in eggplant-related species can result in the development of a new generation of materials with resistance to the main eggplant pathogens, mimicking the process that occurred in tomato breeding, where the incorporation of disease-resistance genes introgressed from wild relatives was a crucial technical innovation for the success of modern commercial varieties (Díez and Nuez, 2008; Schouten et al., 2019). The eggplant fruit and shoot borer (Leucinodes orbonalis) is the most damaging and difficult pest to control in the Indian subcontinent, Southern and East Asia, where multiple insecticide sprays are used to partially control it (Srinivasan, 2008). This pest is such a damaging and limiting factor in eggplant cultivation that two countries (Bangladesh and the Philippines) have authorized the use of genetically modified Bt eggplants expressing the cry1Ac gene from Bacillus thuringiensis to control the eggplant fruit and shoot borer (Shelton et al., 2018; Gonzalvo et al., 2022). Additional pests attacking S. melongena are spider mites, whiteflies, and aphids, which also affect other solanaceous crops (Srinivasan, 2009). To this purpose, the development of eggplant hairless material such as CleanLeaf® (Rijk Zwaan, De Lier, The Netherlands) has improved biological pest control in greenhouse cultivation, as the pests are more accessible to their predators and parasites. The development of new resistant or tolerant varieties can benefit from the use of eggplant genetic resources, as sources of variation to the main diseases are available in these materials (Arafa et al., 2022). Abiotic stresses are expected to increase in the areas where eggplant is cultivated due to climate change (Toppino et al., 2022; Khalid et al., 2023). Eggplant is mildly tolerant to water and salinity stresses (Heuer et al., 1986; Díaz-Pérez and Eaton, 2015; Kouassi et al., 2020; Toppino et al., 2022); however, developing new varieties with better resilience is needed, particularly in drought-prone areas or where water and soil salinity is a problem for eggplant cultivation. Tolerances to extreme temperatures and soil flooding are also important breeding objectives. Despite being a warm-climate plant, high temperatures affect pollen viability and fruit set (Toppino et al., 2022), and heat-tolerant varieties are needed for production in the warm seasons. Tolerance to cold is also important in off-season production in temperate areas, as growth and development are arrested, and fruit set is impaired by low temperatures (Toppino et al., 2022). To this purpose, parthenocarpic materials have been developed that can set fruit even under cold conditions affecting pollen viability (Kikuchi et al., 2008). Improving water and nutrient use efficiencies is also necessary for a more sustainable agriculture. In this context, breeding for better root systems could lead to more sustainable production (Chapman, 2020). Diversification and improvement of fruit quality (Daunay and Hazra, 2012) represent other important challenges in breeding. Eggplant displays a large diversity of fruit sizes, shapes, and colors, facilitating breeding for outer fruit quality and appearance traits. Quantitative trait loci (QTL) have been identified for fruit morphological traits (Portis et al., 2015; Toppino et al., 2016, 2020; Barchi et al., 2019c; Mangino et al., 2021), although few causative genes have been identified. One exception is the APRR2 gene (Arrones et al., 2022), which controls the synthesis of fruit peel chlorophyll, as well as several genes involved in anthocyanin synthesis (Florio et al., 2021; He et al., 2022; Li et al., 2022). The identification of causative genes underlying other important traits for fruit appearance, such as the presence of fruit stripes, fruit netting, or prickliness, will provide additional tools for eggplant breeding. Eggplant is one of the vegetables with the highest antioxidant and bioactive properties, resulting from its high content of phenolic acids (Kaushik et al., 2015), which are also associated with increased browning of the fruit flesh (Mishra et al., 2013; Docimo et al., 2016; Kaushik et al., 2017), a non-desirable trait. Breeders, by directly selecting genotypes with low fruit browning indirectly selected for low content in phenolic acids (Prohens et al., 2007). Selection for low polyphenol oxidase (PPO) activity has been proposed to improve the phenolic acid content while limiting the effects of browning (Plazas et al., 2013). Indeed, CRISPR/ CAS9 editing of PPO genes expressed in the fruit has been shown to reduce fruit flesh browning without affecting phenolic acid content (Maioli et al., 2020; Kodackattumannil et al., 2023). Parthenocarpic fruit set is also of interest for reducing fruit browning, as browning is more intense in the tissues surrounding the seeds (Sarengaowa et al., 2022). Finally, saponins present in the fruit flesh tissues contribute to the bitterness of some accessions, which is also an undesirable trait (Aubert et al., 1989). In summary, research on the above traits will provide a more efficient development of improved eggplant cultivars. Eggplant CWRs often exhibit concentrations of glycoalkaloids above those considered safe for human consumption (Aubert et al., 1989; Rosa-Martínez et al., 2022a). This represents a challenge in introgression breeding of eggplant, although several works showed that most introgression lines display glycoalkaloid concentrations similar to those of the cultivated Downloaded from https://academic.oup.com/jxb/article/74/20/6285/7221360 by Instituto Ingenio (CSIC-UPV) user on 06 November 2023 Copyedited by: OUP Conventional and new genetic resources in eggplant | 6289 recurrent parent (Mennella et al., 2010; Rosa-Martínez et al., 2022a). This indicates that, although levels of glycoalkaloids have to be monitored in the introgressed breeding lines, most of these lines will be safe for consumption. Rootstock development is another important field in eggplant breeding. Rootstocks with robust root systems have been shown to improve yield and confer tolerance to soil diseases and abiotic stresses in eggplant (Gisbert et al., 2011; Barik et al., 2020). In this way, wild eggplant relatives, as well as interspecific hybrids, have demonstrated high potential as rootstocks for improving eggplant production (Sabatino et al., 2018; Toppino et al., 2021). For example, the eggplant wild relative S. torvum, which is resistant to most soil diseases and nematodes, and hybrids between eggplant and scarlet eggplant, which provide vigor and good performance under cold conditions, are used as rootstocks at the commercial level (King et al., 2010; Schwarz et al., 2010; Calvo-Asensio et al., 2014; Ranil et al., 2015). The systematic exploitation of genetic diversity and the use of modern technologies, such as molecular markers, for introgression breeding in eggplant will facilitate the development of highly productive and resilient varieties with traits such as disease and pest resistance, yield heterosis through genetic diversity, tolerance to abiotic stresses, including improved rootstocks, removal of undesirable traits such as prickliness, and the development of long shelf-life or seedless materials (Daunay and Hazra, 2012; Chapman, 2020; Arafa et al., 2022; Toppino et al., 2022). To achieve a successful breeding revolution, systematic efforts must be made to efficiently and rapidly utilize the high genetic diversity present in eggplant and its CWRs. In particular, so far, the large genetic diversity present in CWRs has been barely exploited and used in eggplant breeding. Moreover, speed breeding techniques, such as cold priming at the expanded cotyledon stage, K fertilization supplementation, and embryo rescue, which have proven to be efficient tools for reducing generation cycles in tomato and pepper (Manzur et al., 2014; Ayenan et al., 2019; Gimeno-Páez et al., 2023, Preprint), need to be developed for a faster and more efficient eggplant breeding revolution. The eggplant genepools and their potential for eggplant breeding enhancement The large diversity present for morphological and agronomic traits of interest in cultivated eggplant (Fig. 1) has facilitated the development of new varieties with improved performance and new combinations of traits (Taher et al., 2017). However, intra-specific variation is reduced for some traits, particularly tolerance to some biotic and abiotic stresses (Arafa et al., 2022), and improving such traits will require accessing interspecific diversity. In addition, the vast number of eggplant relatives, with their diverse phenotypic (Fig. 1) and physiological characteristics and environmental adaptation greatly expands the access to exotic and wild genetic diversity for eggplant breeding. Indeed, eggplant can be hybridized with many wild relatives from the subgenus Leptostemonum, which are adapted to a wide range of environments of all tropical and subtropical regions of the world (Vorontsova and Knapp, 2016; Knapp et al., 2019). Many of these wild relatives can be crossed with eggplant (Daunay and Hazra, 2012; Rotino et al., 2014; Plazas et al., 2016), facilitating conventional breeding methods to introgress the traits of interest in eggplant from allied species. Interspecific hybrids between eggplant and wild relatives as well as backcrosses with eggplant have been obtained through sexual crosses using several wild and allied species (Daunay and Hazra, 2012; Rotino et al., 2014; Premabati Devi et al., 2015; Plazas et al., 2016; Daunay et al., 2019). This has included many species from the Old World (Rotino et al., 2014; Plazas et al., 2016; Toppino et al., 2021), as well as American species such as S. elaeagnifolium, S. torvum, S. viarum, and S. sisymbriifolium (Daunay and Hazra, 2012; Rotino et al., 2014; Kouassi et al., 2016; Plazas et al., 2016), which diverged from eggplant approximately 6.7, 7.7, 8.3, and 8.9 million years ago, respectively (Särkinen et al., 2013). The accessibility for breeding of the available genetic diversity of eggplant-related species depends mainly on the genepool (primary, secondary, or tertiary) they belong to (Prohens et al., 2017), although there are significant differences within the secondary and tertiary genepools in the crossability and ease of hybridization and subsequent introgression breeding (Kouassi et al., 2016; Plazas et al., 2016). The primary genepool (GP1) of eggplant consists of the cultivated eggplant S. melongena and its ancestor S. insanum L. (Syfert et al., 2016), which was previously considered a botanical variety of S. melongena (S. melongena var. insanum) (Knapp et al., 2013; Ranil et al., 2017). Although two genetic groups, named Occidental (predominantly grown in the Middle East, Europe, and Africa) and Oriental (mostly grown in the Indian subcontinent, Southeast and Eastern Asia), have been recognized within S. melongena (Vilanova et al., 2012; Cericola et al., 2013), no genetic barriers exist between them or with S. insanum, and hybridization within and between S. melongena groups or between S. melongena and S. insanum is equally successful (Plazas et al., 2016; Daunay et al., 2019). Solanum insanum grows as a wild or weedy species in a wide range of environments in its natural distribution (Indian subcontinent, Southeast and Eastern Asia, Madagascar, and some Indian Ocean islands) (Ranil et al., 2017). In these areas, S. melongena and S. insanum form a genetic continuum with intermediate forms resulting from hybridization, and genetic flow between both species has been documented (Knapp et al., 2013; Davidar et al., 2015; Mutegi et al., 2015; Page et al., 2019a). Solanum insanum has a high potential for the development of improved cultivars (Ranil et al., 2017). Nonetheless, due to the natural genetic flow between S. insanum and S. melongena, it is plausible that some unknown introgressions from the former have been already inadvertently incorporated and utilized in eggplant breeding. This species, therefore, represents a reservoir Downloaded from https://academic.oup.com/jxb/article/74/20/6285/7221360 by Instituto Ingenio (CSIC-UPV) user on 06 November 2023 Copyedited by: OUP 6290 | Gramazio et al. of potential superior untapped alleles for traits of interest, including those related to climate change, which could be easily transferred to the S. melongena genepool. The secondary genepool (GP2) is very broad in terms of number of species (Eggplant clade, Anguivi grade, and Climbing clade), geographic distribution (Africa, Indian subcontinent, Southeast and Eastern Asia), and environmental adaptation (from desertic areas to wet forests; from sea level to 3300 m) (Vorontsova and Knapp, 2016; Syfert et al., 2016; Knapp et al., 2017). The wild ancestor of eggplant (S. insanum) diverged from all GP2 species between 1.5 and 4.6 million years ago (Särkinen et al., 2013). Within GP2, eggplant hybridization and introgression are easier with Eggplant clade species, showing a higher hybridization success, hybrid seed viability and pollen fertility than in the Anguivi grade and Climbing clade (Rotino et al., 2014; Plazas et al., 2016). Generally, embryo rescue is unnecessary to obtain hybrids and backcrosses with S. melongena, although hybridization with GP2 species is more challenging than with GP1 materials (Kouassi et al., 2016; Plazas et al., 2016; Daunay et al., 2019) and sometimes alternative breeding strategies such as somatic hybridization have been necessary to obtain fertile hybrids (Rotino et al., 1998; Särkinen et al., 2013). Several species belonging to GP2 such as S. anguivi, S. dasyphyllum, S. incanum, S. linnaeanum, and S. tomentosum (Table 1) have been identified as of great interest for eggplant breeding due to their tolerance to biotic and abiotic stresses and high contents of bioactive compounds beneficial for human health (Syfert et al., 2016; Kaushik et al., 2017; Arafa et al., 2022; Toppino et al., 2022). For some of them, introgressed and backcrossed populations have been obtained, while many other interesting GP2 species still unexploited in breeding hold great potential. Moreover, the other two cultivated eggplants, S. aethiopicum and S. macrocarpon, are also valuable for eggplant breeding, since aside from presenting characteristics of interest for breeding, they display the typical traits associated to the domestication syndrome, which facilitates their use in breeding (Särkinen et al., 2013; Plazas et al., 2014). Table 1. Solanum species from the primary (GP1), secondary (GP2), and tertiary (GP3) genepools (according to Syfert et al., 2016) for which introgression breeding with eggplant has been reported. Species Main traits of interest for eggplant breeding Most advanced type of generations obtained with S. melongena References Primary genepool (GP1) S. insanum Drought and salinity tolerance, phytochemical composition Advanced backcrosses Ranil et al. (2017), Brenes et al. (2020); Plazas et al. (2020), Nadeeshani et al. (2021); González-Orenga et al. (2023) Secondary genepool (GP2) S. aethiopicum Resistance or tolerance to Fusarium and bacterial wilts and nematodes, vigor of F1 hybrids as rootstocks, spider mite resistance Lines with introgressed resistance to Fusarium and Verticillium wilt Collonnier et al. (2001); Toppino et al. (2008b); Prohens et al. (2012); Calvo-Asensio et al. (2014); Barbierato et al. (2016); Barchi et al. (2018); Taher et al. (2019), Zhuang and Wang (2011) S. anguivi Drought tolerance, high content of phenolics Second backcross generation Kaushik (2019); Plazas et al. (2020); Kouassi et al. (2020) S. dasyphyllum Drought tolerance, two-spotted spider mite and silverleaf whitefly tolerance Advanced backcrosses Plazas et al. (2020); Kouassi et al. (2020); Taher et al. (2020); Villanueva et al. (2023) S. incanum Drought tolerance, bacterial wilt resistance, fruit and shoot borer resistance, silverleaf whitefly tolerance, high content of phenolics Introgression lines Bletsos and Olympios (2008); Prohens et al. (2013); Gramazio et al. (2017); Namisy et al. (2019); Mangino et al. (2020); Taher et al. (2020) S. lichtensteinii Drought tolerance, silverleaf whitefly tolerance Second backcross generation Vorontsova and Knapp (2016); Plazas et al. (2020); Taher et al. (2020) S. lidii Unexplored so far Second backcross generation Plazas et al. (2020) S. linnaeanum Salinity tolerance, Verticillium wilt resistance Lines with introgressed resistance to Verticillium wilt Mennella et al. (2010); Acciarri et al. (2004); Zhuang et al. (2014); Liu et al. (2015) S. tomentosum Fusarium and Verticillium wilts and nematodes resistance, silverleaf whitefly tolerance Introgression lines Toppino et al. (2018); Taher et al. (2020); Caliskan et al. (2023) Tertiary genepool (GP3) S. elaeagnifolium Drought tolerance, high content of phenolics Advanced backcrosses García-Fortea et al. (2019); Plazas et al. (2020); Villanueva et al. (2021) Downloaded from https://academic.oup.com/jxb/article/74/20/6285/7221360 by Instituto Ingenio (CSIC-UPV) user on 06 November 2023 Copyedited by: OUP Conventional and new genetic resources in eggplant | 6291 Hybridization of eggplant with around 20 GP2 species has been achieved, including the Anguivi grade cultivated species S. aethiopicum and S. macrocarpon, as well as S. linnaeanum, S. incanum, and S. tomentosum (Daunay and Hazra, 2012; Särkinen et al., 2013; Rotino et al., 2014; Plazas et al., 2016; Daunay et al., 2019; Toppino et al., 2021). Different kinds of introgression materials were obtained with eggplant relatives from GP2, mostly aimed at exploiting resistance traits to pathogens and adverse environmental conditions. The tertiary genepool (GP3) is genetically very diverse, including species found in Africa and Madagascar, as well as in Australia, Pacific Islands, Asia and in distant American species of subgenus Leptostemonum (Fig. 2) (Knapp et al., 2013; Syfert et al., 2016). As expected, the success of hybridization of eggplant with GP3 species is very low, although attempts to obtain interspecific hybrids with eggplant have been successful in several cases, including the Madagascar species S. pyracanthos and the American S. elaeagnifolium, S. sisymbriifolium, S. torvum, and S. viarum (Rotino et al., 2014; Kouassi et al., 2016; Plazas et al., 2016; Daunay et al., 2019). In many cases, embryo rescue was necessary, especially in crosses with American species. Although interspecific hybrids between eggplant and American species are highly sterile, some backcrosses to eggplant were obtained when the interspecific hybrid with S. elaeagnifolium was used as maternal parent, suggesting the possibility to exploit previously untapped GP3 genetic material for introgression breeding (Plazas et al., 2016; García-Fortea et al., 2019). Overall, the large genetic, phenotypic, and physiological diversity present in the three genepools represents an enormous potential for eggplant breeding, which has been barely explored, particularly in the case of wild species (Daunay and Hazra, 2012; Rotino et al., 2014; Taher et al., 2017; Toppino et al., 2021, 2022; Arafa et al., 2022; Salinier et al., 2022). Unlocking this high diversity will be essential for developing new materials with adaptation to climate change and for meeting the urgent need for an eggplant breeding revolution. Eggplant germplasm collections Based on the recent Global Strategy for the Conservation and Use of Eggplants (Solberg et al., 2022), 19020 accessions of cultivated eggplants and relatives are conserved in 110 germplasm Fig. 2. Dendrogram representing relationships of the most relevant groups of the primary (GP1), secondary (GP2), and tertiary (GP3) genepools of S. melongena. Based on Whalen (1984), Vorontsova et al. (2013), Aubriot et al. (2016), Knapp and Vorontsova (2016), and Knapp et al. (2019). Downloaded from https://academic.oup.com/jxb/article/74/20/6285/7221360 by Instituto Ingenio (CSIC-UPV) user on 06 November 2023 Copyedited by: OUP 6292 | Gramazio et al. banks and collections around the world (Fig. 3) (FAO, 2010). The largest genebank collections of eggplant are conserved at the National Bureau of Plant Genetic Resources (India; 4236 accessions), the World Vegetable Center (an international organization with eggplant germplasm collections headquartered in Taiwan; 3036 accessions), the INRAE Genebank of France (2388 accessions), the National Genebank for Vegetable Germplasm Resources of China (1601 accessions) and the NARO Genebank of Japan (1501 accessions) (Taher et al., 2017; Salinier et al., 2022; Solberg et al., 2022). When considering the Genesys (https://www.genesys-pgr. org/) and WIEWS (World Information and Early Warning System on Plant Genetic Resources for Food and Agriculture; https://www.fao.org/wiews/en/) global germplasm databases, most of the conserved materials of the eggplant genepools correspond to cultivated S. melongena (12665 accessions), S. aethiopicum (1004), and S. macrocarpon (208), while the wild species of GP1, GP2, and GP3 genepools are much less represented (2351 accessions in total) (Solberg et al., 2022). Among the wild species, S. incanum is the most abundant (GP2; 423 accessions), followed by S. torvum (GP3; 358 accessions), S. aculeatissimum (GP3; 210 accessions), S. virginianum (GP2; 187 accessions), and S. grandiflorum (GP3; 184 accessions). However, apart from these five wild species, the number of remaining wild species accessions from GP2 and GP3 of eggplant is dramatically low, with just 14 species having more than 10 accessions conserved, while for many others no accessions are conserved at all (Solberg et al., 2022). This is particularly evident for the 14 eggplant CWRs classified as at risk of extinction (one critically endangered, nine threatened, three near threatened, and one extinct in the wild); for six of them (including S. ruvu, which is considered extinct in the wild) no accessions are conserved in germplasm banks and for the remaining, up to just four accessions are conserved ex situ (Syfert et al., 2016). Relevant information for the in situ conservation, i.e. the on-site management of genetic resources, is available thanks to Syfert et al. (2016). The study identified hotspots of diversity of eggplant crop wild relatives in southern and eastern Africa and the Indian subcontinent. These hotspots, found in protected areas of Kenya, Tanzania, and Uganda, are potential areas of interest for establishing in situ conservation policies and collecting genetic resources to fill germplasm gaps in ex situ collections. However, few in situ programs are ongoing. A total of five eggplant wild relatives (S. lidii, S. linnaeanum, S. marginatum, S. sisymbriifolium, and S. torvum) are included in the European priority CWR taxa (Rubio Teso et al., 2021), although none of them is native to continental Europe (Vorontsova et al., 2013; Vorontsova and Knapp, 2016), and two (S. sisymbriifolium and S. torvum) are invasive (Alaniz et al., 2020; Musarella, 2020). Two of these species (S. lidii and S. marginatum) are found only in one European country, and specific conservation sites exist only for S. lidii, which is an endangered endemism of the Canary Islands (Gramazio et al., 2020; Rubio Teso et al., 2021). The level of exploration of the cultivated eggplant germplasm is variable, depending on the traits. While passport data are available for most accessions conserved in germplasm banks, the availability of characterization data, generally obtained using standardized descriptors such as those of Bioversity (IBPGR, 1990), UPOV (2011), or EGGNET (van der Weerden and Barendse, 2007), is much more limited. On Fig. 3. Map of global distribution of cultivated eggplant and its wild relatives in genebank holdings. Map elaborated according to data from FAO et al. (2010), Taher et al. (2017), Salinier et al. (2022), and Solberg et al. (2022). Downloaded from https://academic.oup.com/jxb/article/74/20/6285/7221360 by Instituto Ingenio (CSIC-UPV) user on 06 November 2023 Copyedited by: OUP Conventional and new genetic resources in eggplant | 6293 the one hand, some phenotypic studies were performed using a large number of accessions (>150) and aiming at evaluating the morphological diversity of cultivated eggplant (Cericola et al., 2013; Kumar et al., 2013; Liu et al., 2018; Oladosu et al., 2021; Ro et al., 2022). These studies revealed a large diversity of morpho-agronomic characteristics in the cultivated eggplant genepool and provided relevant information for their utilization in breeding. Large screening for evaluation traits in germplasm collections of eggplant relatives is more limited. Seventy S. aethiopicum accessions, mostly belonging to the Gilo group, were assessed for morpho-physiological traits, amplified fragment length polymorphism (AFLP) and simple sequence repeat (SSR) molecular markers and chlorogenic acid content, revealing a wide genetic diversity (Sunseri et al., 2010). A total of 125 accessions of S. aethiopicum and S. macrocarpon were evaluated by Taher et al. (2019) for resistance to the two-spotted spider mite (Tetranychus urticae), resulting in the identification of high levels of resistance in two accessions of S. macrocarpon. In another large evaluation, Stommel and Whitaker (2003) studied the phenolic acid profiles of 115 accessions, mostly of cultivated S. melongena, but also including some accessions of S. aethiopicum, S. anguivi, S. incanum, and S. macrocarpon. Another study on 73 accessions, most of which were of S. melongena but also included S. aethiopicum and S. macrocarpon, also found large variations in total phenolics content (8.4fold) and fruit flesh browning (7.3-fold), but less in ascorbic acid (2.3-fold) (Prohens et al., 2007). Overall, given the large number of species in GP2 and GP3 of eggplant, the focused identification of germplasm strategy (FIGS), which is based on the assumption that wild accessions growing in specific environments must have adaptive genes to these conditions (Street et al., 2016), might help in identifying putative species or accessions of interest for tolerance to a certain biotic or abiotic stress (Prohens et al., 2017). However, the exploration of eggplant and relatives germplasm collections for traits relevant to adaptation to climate change has been very scarce until now. To achieve a breakthrough in eggplant breeding, it is essential to systematically evaluate the available variation and identify sources of variation for adaptation to climate change. Use of genetic resources in breeding: achievements and challenges Selection of eggplants started more than a century ago, with accessions having improved characteristics already present in seed catalogues in the late 19th and early 20th centuries (Daunay and Janick, 2007). In addition, heterosis for yield was already reported in 1931 (Kakizaki, 1931), which opened the door for the development of hybrid varieties with improved features. Genetic improvements in eggplant have relied on the use of germplasm, and breeders have been using the eggplant germplasm (mostly of cultivated S. melongena) for breeding and developing new selections, lines, and hybrids. According to a survey of germplasm banks (Solberg et al., 2022), the number of eggplant accessions distributed per year ranged between 0 and 503, revealing that some germplasm banks make a significant distribution to users, many of whom are breeders. The genetic improvements of eggplant are evident in the characteristics of modern cultivars, which are considerably better in yield and overall quality than landraces. For example, the modern F1 hybrid cultivars found in western markets have no prickles, greater earliness, intense black color and epidermal shininess, lower fruit flesh browning (Prohens et al., 2007; Muñoz-Falcón et al., 2009), and increased yield (Sambandam, 1964; Rodríguez-Burruezo et al., 2008; Daunay and Hazra, 2012; Kaushik et al., 2018; Kumar et al., 2020). The development of modern eggplant cultivars has been mainly carried out employing the cultivated genepool. This resulted in a reduction of the genetic base of eggplant elite breeding lines and materials used for developing modern F1 hybrids. For instance, Muñoz-Falcón et al. (2009) evaluated the genetic diversity of black eggplants of different groups and found that modern F1 hybrids have a narrow genetic base and share a common genepool. This situation is in contrast to tomato, where the widespread use of CWRs, especially for introgressions of biotic resistance traits, increased the genetic diversity of modern varieties (Díez and Nuez, 2008; Schouten et al., 2019). The exploitation of cultivated eggplant germplasm allowed the development of new cultivars and elite materials with improved resistance or tolerance to pests and diseases. Indeed, sources of resistance to the most significant pests, including the eggplant fruit and shoot borer, leafhopper, aphids, spider mites, and whiteflies, as well as to the primary diseases such as bacterial wilt, Fusarium, and Verticillium wilts, have been identified (Taher et al., 2017; Arafa et al., 2022; Salinier et al., 2022). Many of these cultivated accessions have been transferred to researchers and breeders for incorporation into their breeding pipelines (Taher et al., 2017). However, while some quantitative improvements have been achieved, resulting in cultivars with improved tolerance, the genetic diversity for resistance to these biotic stresses present in the primary genepool of eggplant seems to be limited (Taher et al., 2017). Accessions of wild eggplant GP2 and GP3 species, as well as from the cultivated S. aethiopicum, have been employed for introgression breeding (Mennella et al., 2010; Liu et al., 2015; Gramazio et al., 2017; Plazas et al., 2020; Villanueva et al., 2021). Eggplant lines fully resistant to F. oxysporum f. sp. melongenae (Fom) have been obtained by introgressing the Rfo-sa1 resistance locus from S. aethiopicum (Toppino et al., 2008b). Interestingly, the response mechanism to Fom inoculation triggered by this locus is also able to protect the plant from Verticillium wilt (Barbierato et al., 2016; Barchi et al., 2018) when the two fungi are used in a combined artificial inoculation. These elite Fom-resistant lines introgressed from S. aethiopicum, along with Downloaded from https://academic.oup.com/jxb/article/74/20/6285/7221360 by Instituto Ingenio (CSIC-UPV) user on 06 November 2023 Copyedited by: OUP 6300 | Gramazio et al. for a pre-doctoral (FPU18/01742) contract. 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