Abstract
Key message: This article examines the significant contributions of tomato, tobacco, petunia, potato, pepper, and eggplant to the fields of classical and molecular plant genetics and genomics from the early twentieth century to the present day.
Abstract
For millennia, species belonging to the Solanaceae Plant Family, also known as the nightshade family, have been intrinsically linked to human civilization, serving as vital sources of food, medicine, and, more recently, as captivating ornamentals. Over the past century, several members of this diverse family have become indispensable subjects in classical and molecular genetic research. The tomato plant emerged as a leading model organism in twentieth-century classical genetics, spearheading advancements in plant genome analysis, including the development of molecular linkage maps and the positional cloning of disease resistance genes and quantitative trait loci (QTL). Furthermore, tomato serves as the quintessential model for unraveling the genetic mechanisms governing fruit development and composition. Tobacco held a paramount position as the primary model for establishing the principles and methodologies of plant somatic cell genetics, encompassing in vitro cell and tissue propagation, somatic cell totipotency, doubled haploid production, and genetic transformation techniques. Petunia became instrumental in elucidating the biochemical and genetic underpinnings of flower color and development. The cultivated potato, the most economically significant member of the solanaceae plant family, ranks as the third most crucial global food crop after wheat and rice. Potato stands as the model for investigating the genetic control of tuber development. Molecular genetics and genomics research in potato, particularly association genetics, have made substantial contributions to dissecting the genetic complexity of agronomic traits and developing diagnostic markers for plant breeding applications. Pepper and eggplant, both globally relevant horticultural crops within the solanaceae plant family, have largely followed the tomato model in genetic and genomic research. Comparative genome analysis of tomato, potato, pepper, and eggplant has provided invaluable insights into the evolutionary trajectory of plant genomes within the solanaceae plant family.
Introduction
The solanaceae plant family, a remarkably diverse group, encompasses 3000–4000 species classified into approximately 90 genera. This family exhibits extraordinary adaptability, ranging from perennial trees to herbaceous annuals, thriving in diverse terrestrial habitats from arid deserts to lush rainforests (Knapp et al. 2004). Despite its vastness, only a select few members of the solanaceae plant family have attained significant importance in human societies as sources of nourishment [potato, tomato, pepper, eggplant, pepino, naranjilla, tamarillo (tree tomato)], ornamentals (petunia, Datura, certain Solanum species, Schizanthus), and medicinal compounds (tobacco, Atropa, Hyoscyamus, Mandragora). Following the rediscovery and validation of Gregor Mendel’s groundbreaking work (Mendel 1866) by Hugo de Vries and Karl Correns around the turn of the twentieth century, species from seven genera within the solanaceae plant family became focal points of genetic research, either as model organisms or due to their agricultural significance. Cultivated tomato and its wild relatives (genus Solanum, formerly Lycopersicon), tobacco (genus Nicotiana), and petunia species (genus Petunia) emerged as primary model plants in classical, cellular, and molecular genetics. Cultivated potatoes, eggplant or aubergine (genus Solanum), and pepper species (genus Capsicum) are globally important crops within the solanaceae plant family. While less suited as models for fundamental research, with the exception of tuber development in potato, classical and molecular genetic research on potato, eggplant, and pepper was predominantly directed towards addressing agricultural challenges, such as introducing disease resistance and developing improved cultivars. Datura innoxia (genus Datura), Hyoscyamus muticus (genus Hyoscyamus), and Physalis species (genus Physalis), while not extensively used in research, contributed to specific areas of genetics. Datura innoxia anthers were used in the earliest conclusive report on regenerating haploid embryos from pollen grains through in vitro culture (Guha and Maheshwari 1966). This marked the beginning of doubled haploid production, a crucial biotechnological application in breeding programs for self-fertile crops, enabling the rapid and efficient creation of homozygous plants. Leaf mesophyll protoplasts from anther culture-derived haploid Hyoscyamus muticus plants served as the source for biochemical mutant cell lines obtained through total selection (Gebhardt et al. 1981), mirroring the initial biochemical mutants selected in Neurospora crassa (Beadle and Tatum 1941). The molecular basis and potential mechanisms behind the ‘Chinese lantern’ or inflated-calyx syndrome, a distinctive sepal development after fertilization in certain solanaceae plant family genera, were investigated in Physalis species (He and Saedler 2005, 2007).
This review aims to highlight the historical roles and significant contributions of tomato, tobacco, petunia, potato, pepper, and eggplant to genetic research since the early twentieth century. Given the breadth of the subject, selectivity was necessary, potentially influenced by the author’s expertise and interests. Cytogenetics, despite its undeniable importance, and the numerous studies on gene function using transgenic plants are not covered in detail. Emphasis is placed on identifying and citing early, original literature in genetic research within the solanaceae plant family. While this may appear dated in the context of current genome sequencing, it represents the foundational knowledge that fueled the research leading to diverse biotechnological applications in plant breeding, including in vitro multiplication, doubled haploid production, genetic engineering, and marker-assisted breeding.
Tomato: A Cornerstone of Classical and Molecular Genetics in the Solanaceae Plant Family
The nine tomato species, formerly classified under the genus Lycopersicon but now integrated into the genus Solanum based on molecular taxonomy (https://solgenomics.net/about/solanum_nomenclature.pl), are indigenous to Middle and South America. The cultivated tomato (Solanum lycopersicum, previously Lycopersicon esculentum) was domesticated in pre-Columbian Mexico or Peru and introduced to Europe shortly after the Spanish conquest of Mexico in 1521. European herbals first described the ‘love apple’ around the mid-sixteenth century (Daunay et al. 2008). From Europe, tomato cultivation spread globally, becoming the second most important crop in the solanaceae plant family after potato. Alongside maize, cultivated tomato served as a primary plant model in twentieth-century classical genetics, owing to its self- and cross-compatibility, ease of cultivation, and extensive morphological diversity. The genetic linkage map of tomato began in the first decade of the twentieth century through Mendelian inheritance analysis of morphological traits like plant dwarfism and fruit and leaf color, shape, and surface structure (Craig 1907; Halsted 1905; Hedrick and Booth 1907; Price and Drinkard 1908). The discovery of genetic linkage among these traits formed the basis of the classical tomato map (Jones 1917). Seven decades later, this map encompassed nearly 320 morphological and isozyme loci (Mutschler et al. 1987). A significant portion of morphological markers originated from over 300 radiation-induced mutants, generated and characterized by Hans Stubbe and colleagues at the Institute for Genetics and Crop Plant Research in Gatersleben (former German Democratic Republic) during the 1950s and 1960s (Stubbe 1957, 1972). Positional cloning has now molecularly identified several genes underlying morphological traits described and mapped by classical geneticists, such as the transcription factors lateral suppressor (Ls) and blind (bl), which regulate axillary meristem formation (Schmitz et al. 2002; Schumacher et al. 1999), the regulatory gene ovate (o) controlling fruit shape (Liu et al. 2002), and the MYB transcription factor potato leaf (C) influencing leaf shape (Busch et al. 2011). Since the early twenty-first century, tomato mutant collections have expanded by thousands, providing new avenues for gene function discovery and analysis (Menda et al. 2004; Saito et al. 2011).
Alt Text: Ripe red tomatoes hanging on the vine, illustrating the diversity of fruit shapes and sizes within the Solanaceae plant family.
Linkage mapping using morphological and isozyme markers became less prevalent around 30 years ago with the advent of DNA-based markers, specifically restriction fragment length polymorphisms (RFLPs) (Helentjaris et al. 1985). While constructing the classical tomato map took 80 years, numerous crosses, and generations of geneticists, developing a molecular linkage map with hundreds of RFLP markers was achieved in under 10 years by a couple dozen researchers using single F2 populations derived from crosses between cultivated tomato and wild tomato species (Bernatzky and Tanksley 1986; Helentjaris et al. 1986; Tanksley et al. 1992). Tomato RFLP maps, along with maize, were among the first molecular linkage maps created in plants. These maps revolutionized plant genetics, enabling: (i) genetic dissection and mapping of quantitative trait loci (QTL), (ii) cloning genes with phenotypic effects but unknown sequences based solely on map position, and (iii) marker-assisted introgression of desirable traits like disease resistance in breeding programs. DNA-based markers for many tomato diseases and fruit quality traits have been identified through linkage mapping in interspecific hybrid progeny. Their application in commercial breeding is reviewed recently (Foolad and Panthee 2012). The use of interspecific hybrids was crucial due to limited intraspecific DNA variation in cultivated tomato, making RFLP detection challenging. Next-generation sequencing technologies, developed twenty years later, dramatically improved DNA variation detection, allowing map construction in intraspecific populations using single nucleotide polymorphism (SNP) markers (Shirasawa et al. 2010). High-density molecular linkage maps were essential for constructing a physical map, ordering and linking assembled genomic sequence fragments (scaffolds) to the 12 chromosomes of the inbred cultivar ‘Heinz 1701’, the first sequenced tomato (The Tomato Genome Consortium 2012). In addition to the cultivated tomato reference genome, genomes of wild species S. pimpinellifolium and S. pennellii, sources of valuable horticultural traits, were also sequenced (Bolger et al. 2014; The Tomato Genome Consortium 2012).
The tomato Pto gene, conferring resistance to Pseudomonas syringae pv tomato, was among the earliest examples of map-based gene cloning in plants, encoding a serine–threonine kinase (Martin et al. 1993a, b). Initial QTL mapping experiments primarily used RFLP and some isozyme markers, identifying QTL for insect resistance (Nienhuis et al. 1987) and key fruit quality traits like soluble solids concentration (mainly sugars), fruit weight, and acidity (Osborn et al. 1987; Paterson et al. 1988). Numerous QTL mapping studies have since been conducted in various interspecific populations, reviewed by (Grandillo et al. 2013), and Bernardo (2016) in this issue. QTL mapping served as a starting point for positional cloning of genes underlying QTL. The first example was a major fruit weight QTL (fw2.2) on tomato chromosome 2, identified as a gene of unknown function, possibly a cell division regulator (Frary et al. 2000; Grandillo and Tanksley 1996). Introgression lines of S. pennellii in S. lycopersicum, developed using marker-assisted selection with RFLP markers (Eshed and Zamir 1995), proved particularly valuable for QTL mapping and cloning. This resource led to identifying an invertase gene underlying a major fruit sugar content QTL (Fridman et al. 2004).
Progeny from controlled crosses between inbred parental lines dominated plant genetics in the past century. Since the early twenty-first century, population genetics principles, initially developed in human genetics, are increasingly applied to plant populations of related individuals, either in natural habitats or resulting from breeding. These populations arise from crosses among multiple parents over generations. Instead of two parental alleles per locus segregating in Mendelian ratios, multiple alleles are distributed with frequencies shaped by evolutionary forces like natural selection, random genetic drift, or human selection. Linkage disequilibrium (LD), rather than recombination frequency, is estimated as the frequency of co-inheritance of specific alleles at linked loci across meiotic generations. Phenotypic and genotypic analysis of such populations enables detecting association or LD between quantitative or qualitative traits and specific alleles of DNA-based markers. These marker–trait associations are highly beneficial for marker-assisted breeding, as they are not limited to specific genetic backgrounds. Association mapping is limited in highly inbred crops like tomato due to low genetic resolution caused by large LD. However, initial examples of QTL detection by association mapping have emerged recently (Ranc et al. 2012; Ruggieri et al. 2014; Sauvage et al. 2014). Multiparent advanced generation inter-cross (MAGIC) populations combine linkage mapping advantages, like controlled crossings, with association mapping benefits, such as multiple allele segregation and increased genetic resolution. A first MAGIC population was recently developed in tomato as a novel genetic resource for QTL mapping and cloning (Pascual et al. 2015.
Tomato naturally serves as the primary model for studying the molecular basis of fruit development and composition within the solanaceae plant family. Classical geneticists described spontaneous and induced mutations affecting fruit ripening, shape, color, and texture in the twentieth century. Many corresponding genes were cloned and functionally characterized at the end of the twentieth and early twenty-first centuries, using positional cloning or candidate gene approaches. This work revealed the importance of ethylene signaling and specific transcriptional regulators in fruit ripening (reviewed by (Giovannoni 2007; Klee and Giovannoni 2011). The FLAVR SAVR™ tomato, engineered for prolonged shelf life through antisense inhibition of polygalacturonase in fruit, became the first commercialized transgenic crop (Kramer and Redenbaugh 1994).
Tobacco: Pioneering Somatic Cell Genetics and Transformation in the Solanaceae Plant Family
In 1492, Christopher Columbus observed indigenous people smoking in Mexico and Cuba. By the mid-sixteenth century, several tobacco species, likely Nicotiana rustica initially, were introduced to Portugal and France from the New World (Daunay et al. 2008). Over subsequent centuries, tobacco spread globally as a potent drug in cigarettes, cigars, and pipes. In twentieth-century plant science, tobacco became the most widely used model for developing somatic cell genetics, including transformation technology and genetic engineering within the solanaceae plant family. In vitro plant cell and tissue multiplication, doubled haploid production, and transgenic crops, crucial components of modern green biotechnology, are largely rooted in fundamental research using tobacco cell and tissue cultures (reviewed by (Sussex 2008). The ability of dedifferentiated plant cells to grow indefinitely in vitro was conclusively demonstrated using tumor-like callus tissue from a N. glauca and N. langsdorffii hybrid (White 1939b). The subsequent regeneration of roots, shoots, and fertile plants from undifferentiated tobacco cell cultures involved discovering that plant hormones auxin and cytokinin, in correct concentrations and ratios, induce root or shoot differentiation (Skoog 1944; Skoog and Tsui 1948; White 1939a). The question then arose whether single somatic plant cells are totipotent, capable of developing into fully functional, fertile plants through cell division and organ differentiation. Tobacco single-cell cultures (Muir et al. 1954; Vasil and Hildebrandt 1965a, b) and later, leaf mesophyll protoplasts (Nagata and Takebe 1971; Nakata and Tanaka 1968) proved somatic plant cell totipotency. These advancements were enabled by improvements in culture media. The first fully defined plant tissue culture medium, ‘MS’, was developed for tobacco cell cultures and remains widely used for in vitro propagation of numerous plant species (Murashige and Skoog 1962). Another significant development was regenerating haploid plants from pollen grains through in vitro tobacco anther culture (Bourgin and Nitsch 1967; Nitsch and Nitsch 1969; Vasil and Nitsch 1975). Once in vitro plant regeneration from single cells became possible, plant cell cultures could be used like microbial cultures to isolate biochemical mutants (reviewed by (Negrutiu et al. 1984). Tobacco cells were used to obtain the first such mutants. Mutant cell lines were selected for resistance to chemicals like chlorate, 5’ bromo-deoxyuridine, and methionine sulfoximine, which kill wild-type cells while mutant cells survive (Carlson 1970, 1973; Márton et al. 1982a, b; Müller and Grafe 1978). A milestone in plant science and biotechnology was tobacco cell transformation with Agrobacterium tumefaciens-carrying T-DNA or Ti-plasmid, resulting in stable foreign gene integration and inheritance (Chilton et al. 1977; De Block et al. 1984; Hernalsteens et al. 1980; Horsch et al. 1984). Simple Agrobacterium-mediated transformation of differentiated tissues like leaf discs was demonstrated in tobacco, tomato, and petunia (Horsch et al. 1985).
Alt Text: A lush green tobacco plant growing in a field, highlighting its agricultural significance within the Solanaceae plant family.
Tobacco species also served as models to study the genetics and molecular basis of gametophytic self-incompatibility within the solanaceae plant family. Early twentieth-century studies extensively investigated self-incompatibility inheritance (then called self-sterility) in hybrids of N. alata, N. forgetiana, and N. langsdorffii (Anderson 1924; East and Mangelsdorf 1925; East and Park 1917). Seven decades later, the first gene for gametophytic self-incompatibility was cloned from N. alata, encoding a stylar glycoprotein (Anderson et al. 1986. The self-incompatibility mechanism was subsequently elucidated, showing this glycoprotein functions as an RNase degrading pollen rRNA (McClure et al. 1989, 1990. Research on the tobacco–Tobacco Mosaic Virus (TMV) host–pathogen system marks the beginning of plant virology a century ago (reviewed by (Scholthof 2008). The dominant N gene from N. glutinosa, conferring hypersensitive resistance to TMV (Holmes 1938), was finally cloned by transposon tagging in N. tabacum (Whitham et al. 1994. N was the first virus resistance gene to be sequence-characterized and is the founder of a major plant resistance gene class characterized by a Toll–interleukin receptor-like (TIR) domain, a nucleotide-binding site (NBS), and a leucine-rich repeat (LRR) domain. More recently, N. attenuata became a productive model for understanding the molecular basis of plant interactions with insect herbivores (reviewed by (Schuman and Baldwin 2016).
Nicotiana benthamiana, an Australian endemic tobacco species, has become an important experimental system for functional analysis of host–pathogen interactions, particularly virus interactions, and for protein localization and protein–protein interaction studies (reviewed by (Goodin et al. 2008). This is due to N. benthamiana‘s susceptibility to most viruses, enabling foreign gene introduction and transient expression in plant viral vectors in sense or antisense orientation (Donson et al. 1991; Kumagai et al. 1995). Another advantage of N. benthamiana is its ease of transformation via Agrobacterium tumefaciens leaf infiltration (agroinfiltration), enabling high-throughput functional screens.
Genomics arrived later in tobacco compared to other crops within the solanaceae plant family. The first linkage map was constructed using microsatellite markers (Bindler et al. 2006, 2011). Draft genome sequences are now available for three N. tabacum varieties (Sierro et al. 2014) and N. benthamiana (Bombarely et al. 2012).
Petunia: Illuminating Flower Color and Development in the Solanaceae Plant Family
Petunias are among the most popular annual bedding plants in Europe and the United States, representing the ornamental beauty of the solanaceae plant family. Native to South America, the genus Petunia, established in 1803 by French botanist Antoine-Laurant de Jussieu, includes approximately 30 known species. The first wild Petunia species were cultivated in Berlin (1823) and Glasgow (1831) botanical gardens from seeds introduced from southern South America (Gerats and Vandenbussche 2005; Krausch 2007; Sink 1984. The remarkable diversity in flower color, size, and pattern, and plant growth habit seen today results from 170 years of breeding and selection, adapting this ornamental plant to human preferences for colorful flowering decorations in windows, balconies, and gardens.
Petunia flower morphology, therefore, was likely among the earliest heritable plant characters studied through controlled crosses after Mendel’s work was rediscovered. Edith R. Saunders published a paper on ‘doubleness’ versus ‘singleness’ inheritance in petunia flowers in the very first issue of the oldest British genetics journal (Saunders 1910. In the latter half of the twentieth century, petunia, alongside snapdragon (Antirrhinum majus), became the model for classical and molecular genetics of flower pigmentation by anthocyanins, a flavonoid subclass (Gerats and Vandenbussche 2005; Holton and Cornish 1995; Winkel-Shirley 2001. This was driven by the countless flower color variations of Petunia hybrida selected by breeders from interspecific hybrid progeny or spontaneous mutations. Since early studies on petunia flower color inheritance in the context of speciation (Mather and Edwardes 1943, over thirty color mutants have been described and mapped to the seven petunia chromosomes (de Vlaming et al. 1984). Subsequently, many structural and regulatory genes in flavonoid biosynthesis were cloned and molecularly characterized from maize, snapdragon, and petunia (Dooner et al. 1991; Gerats and Vandenbussche 2005). In early plant gene cloning, the first petunia genes cloned were based on sequence homology to corresponding parsley genes, encoding chalcone synthase, the key enzyme in flavonoid biosynthesis (Reif et al. 1985. Observation and genetic analysis of unstable alleles at flower pigmentation loci (Bianchi et al. 1978; Doodeman et al. 1984; Farcy and Cornu 1979) ultimately led to discovering and cloning the non-autonomous transposable element dTph1 (Gerats et al. 1990, 2013. Transposon tagging based on dTph1 and the autonomous element Act1, combined with twenty-first-century sequencing, is now a powerful tool for forward and reverse genetics in petunia. Thousands of insertion mutants were generated using the Act1/dTph1 transposable element system, leading to novel gene identification (Van Houwelingen et al. 1998; Vandenbussche et al. 2016.
Alt Text: A vibrant display of petunia flowers in assorted colors, showcasing the ornamental diversity within the Solanaceae plant family.
Genetic engineering of petunia flower color marked a hallmark in transgenic plant history within the solanaceae plant family. The maize A1 locus, encoding dihydroquercetin 4-reductase (DQR) (O’Reilly et al. 1985; Schwarz-Sommer et al. 1987), is essential for pelargonidin biosynthesis, giving geranium flowers their brick-red color, but absent in petunia flowers. The maize A1 gene was transferred into a pale pink flowering petunia mutant accumulating DQR substrate via protoplast transformation, resulting in transgenic salmon-red flowered plants (Meyer et al. 1987. The first field experiment with transgenic plants was conducted with 30,000 plants of a transgenic petunia line at the Max Planck Institute for Plant Breeding Research in summer 1990, facing protests against transgenic plant release (witnessed by the author). This experiment showed transgene expression and flower color reduction or silencing by methylation of the 35S promoter driving transgene expression, correlated with developmental and environmental factors (Meyer et al. 1992. Genetic and molecular analysis of transgenic petunia plants with modified flower color by these and other researchers (Napoli et al. 1990; Van der Krol et al. 1990 significantly contributed to co-suppression and gene silencing discovery in plants.
Alongside Arabidopsis thaliana and Antirrhinum majus (Schwarz-Sommer et al. 1990), Petunia hybrida is a model for molecular genetics of flower development within the solanaceae plant family. Several homeotic and non-homeotic flower mutants have been described (de Vlaming et al. 1984; Saunders 1910. Identification and functional analysis of underlying genes revealed similarities and differences between transcriptional networks controlling flower development and organ identity across plant genera (Heijmans et al. 2012; Mach 2012; Van der Krol and Chua 1993.
Compared to tomato, potato, and pepper within the solanaceae plant family, genomic tools like molecular linkage maps and genome sequences are less developed in petunia, likely due to its large genome size and severely reduced recombination frequencies in Petunia hybrida progeny (Bossolini et al. 2011; Strommer et al. 2002. A draft genome sequence is currently being constructed (Vandenbussche et al. 2016.
Potato: A Staple Crop and Model for Tuber Development within the Solanaceae Plant Family
All approximately 180 tuber-bearing Solanum species are native to Latin America, inhabiting diverse habitats from Mexico to Chile, highlighting the adaptability of the solanaceae plant family. Archaeological evidence from the Peruvian coast indicates potato cultivation dates back roughly 9000 years. After the Spanish conquest of the Inca state (1532–1536), the first potatoes were introduced to Europe, likely via the Canary Islands, a common ship anchorage on routes from America to Europe (Hawkes 1990; Ríos et al. 2007. Potato cultivation slowly spread throughout Europe over the next four centuries, then globally. Today, potato is the world’s third most important food crop by production, a crucial contributor to global food security within the solanaceae plant family. Redcliffe N. Salaman’s seminal paper in the first issue of the Journal of Genetics (Salaman 1910 marked the beginning of potato genetics. Genetic analysis in potato proved initially challenging due to low fertility and difficulties in accurately scoring morphological characters as Mendelian factors. Nevertheless, Salaman reported Mendelian inheritance of pollen sterility, tuber shape, eye depth and color, and Phytophthora infestans resistance in a wild potato species (then named S. etuberosum, likely S. demissum). Years later, the tetraploid nature and tetrasomic inheritance of European cultivated potato were established (Cadman 1942; Rybin 1930; Smith 1927, leading to Mendelian segregation ratios for only two of twelve possible heterozygous parent allelic states (Aaaa x aaaa and Aaaa x Aaaa). Potato cultivars were and remain non-inbred and highly heterozygous, generated by intercrossing non-inbred parents, with heterozygous genotypes maintained through vegetative tuber propagation. Classical genetic analysis in cultivated potato remained limited and challenging. Exceptions include Aksel P. Lunden’s studies on tuber and flower color inheritance (Lunden 1960 and G. Cockerham’s work on resistance inheritance to potato viruses X and Y (Cockerham 1970. One of the seven Potato Virus X (PVX) resistance genes analyzed by Cockerham (Rx adg) was the first potato gene identified by positional cloning 30 years later (Bendahmane et al. 1999.
Alt Text: An assortment of potato tubers showcasing different skin colors and shapes, emphasizing the diversity within the Solanaceae plant family crop.
Reducing ploidy level from tetraploid to diploid greatly facilitated potato genetics within the solanaceae plant family (reviewed in (Rokka 2009). This was achieved through parthenogenetic development of 2n female gametes after pollination with certain S. phureja genotypes (Hougas et al. 1958 or anther culture of 4n cultivars and 2n plant regeneration from male gametes (Dunwell and Sunderland 1973. Diploid potatoes obtained were sexually self-incompatible, making diploid, heterozygous, self-incompatible potato genetics analogous to human genetics. The discovery of the Sli (S locus inhibitor) gene from wild potato S. chacoense, conferring self-compatibility (Hosaka and Hanneman 1998, may mark a new era in potato genetics and breeding, enabling pure diploid line generation and use in hybrid breeding (Lindhout et al. 2011. First potato linkage maps used RFLP markers and progeny of interspecific (Bonierbale et al. 1988) and intraspecific crosses (Gebhardt et al. 1989, 1991) between heterozygous, diploid parents. Twenty years later, the ultimate map, the genomic sequence corresponding to twelve potato chromosomes, was assembled from DNA sequences of an exceptional doubled monoploid, homozygous diploid genotype of S. phureja, a diploid potato species cultivated in Colombia and Peru (PGSC 2011; Sharma et al. 2013.
Closer species relatedness implies greater genome sequence similarity within the solanaceae plant family. RFLP markers, detected by DNA–DNA hybridization (Southern blot analysis) reliant on sequence similarity, allowed using RFLP markers from one species for linkage map construction in related species. Before whole genome sequences, constructing linkage maps in two species with the same RFLP marker set enabled the first genome structure comparison between sexually incompatible species, deducing genome evolution and speciation models. Genome synteny concept was first tested in plants by constructing a potato linkage map with tomato RFLP markers of known tomato linkage map position (Bonierbale et al. 1988. This showed largely conserved marker order in potato and tomato, except for five chromosome arm inversions evidenced by inverted marker order. Conserved marker order and genome structure fragments (syntenic blocks) were detectable even between distantly related species like potato and model plant Arabidopsis thaliana (Gebhardt et al. 2003. Current whole genome sequence comparisons confirm and refine syntenic relationships among solanaceae plant family species (Doganlar et al. 2002a; Hirakawa et al. 2014.
RFLP linkage maps initiated mapping major pathogen resistance genes (Barone et al. [1990](#CR5]; Leonards-Schippers et al. 1992; Ritter et al. 1991, reviewed by (Simko et al. 2007), and subsequently resistance QTL (Bonierbale et al. 1994; Leonards-Schippers et al. [1994](#CR97]; Simko et al. 2007 and complex, agronomically important tuber traits like starch content, chip color, yield, dormancy, and bruising susceptibility (Douches and Freyre 1994; Freyre et al. 1994, reviewed by (Gebhardt et al. 2014 in diploid experimental populations. Molecular cloning of first two NBS-LRR type plant resistance genes, N and RPS2 from tobacco and Arabidopsis (Bent et al. 1994; Mindrinos et al. 1994; Whitham et al. 1994, allowed identifying conserved sequence motifs, basis for PCR amplification, cloning, and RFLP mapping of ‘resistance gene like’ (RGL) sequences in potato (Leister et al. 1996. Co-segregation of one specific RGL with Gro1 locus for root cyst nematode Globodera rostochiensis resistance aided Gro1–4 nematode resistance gene cloning via candidate gene approach (Paal et al. 2004. R1, first gene for Phytophthora infestans resistance causing late blight, the most devastating potato disease, was cloned using positional cloning and candidate gene approach based on RGLs (Ballvora et al. 2002. Molecular mapping of major Potato Virus Y (PVY) and root cyst nematode Globodera pallida resistance loci enabled diagnostic marker development for breeding applications (Kasai et al. 2000; Sattarzadeh et al. 2006, reviewed by (Gebhardt 2013. Linkage mapping in tetraploid populations became feasible with labor- and time-effective methods for generating numerous markers, such as amplified fragment length polymorphism (AFLP) markers (Meyer et al. 1998 and recently, SNP arrays (Hackett et al. 2014.
Association genetics proved highly suitable and fruitful for tetraploid, non-inbred potato, especially for quantitative agronomic traits within the solanaceae plant family. Likely the first association test was performed with 383 potato varieties evaluated for field or quantitative late blight resistance and R1 gene presence (identified by infection with avirulent P. infestans races in R1 presence). Cultivars with R1 gene, overcome in the field by Phytophthora races with multiple virulence factors, were on average more late blight resistant than R1-lacking varieties (Schick et al. 1958. Nearly 50 years later, association mapping feasibility with DNA-based markers was tested in a 415 tetraploid potato cultivar gene bank collection with quantitative late blight resistance scores. Genotyping this population with PCR-based markers within or tightly linked to the cloned R1 gene, known to co-localize with a major resistance QTL (Leonards-Schippers et al. 1994, revealed that R1 gene presence was indeed associated with increased quantitative late blight resistance (Gebhardt et al. 2004. Subsequent association mapping experiments using various DNA-based marker types, including candidate gene-derived or genome-wide distributed SNPs, discovered further associations with quantitative late blight resistance and other complex traits like plant maturity, tuber starch content, yield, starch yield, chip color, and enzymatic discoloration (reviewed by (Gebhardt et al. 2014), (Mosquera et al. 2016; Schönhals et al. 2016), and Bernardo (2016) in this issue).
Potato (Solanum tuberosum), sweet potato (Ipomoea batatas), cassava (Manihot esculenta), and yam (Dioscorea species) roots and tubers are crucial for human nutrition, with potato leading research in tuber initiation and development within the solanaceae plant family, starting over 100 years ago (Bernard 1901. Tuberization is a complex trait controlled by multiple genetic and environmental factors like photoperiod, temperature, and nitrogen supply. Hormones such as gibberellins, jasmonates, and cytokinins, along with carbohydrate metabolism, are important in tuber development (reviewed by (Prat 2010). Several tuberization-functional genes have been identified, including two controlling day-length-dependent tuberization. The StSP6A gene, cloned by the candidate gene approach, encodes a protein similar to FLOWERING LOCUS T (FT), controlling day-length-dependent flowering in Arabidopsis thaliana (Navarro et al. 2011. The StCDF1 gene, cloned based on genomic position, encodes a DOF (DNA-binding with one finger) transcription factor family member (Kloosterman et al. 2013.
Pepper: From Pungency Genes to Genome Sequencing within the Solanaceae Plant Family
The genus Capsicum, with over thirty species, originates from tropical America, adding to the global diversity of the solanaceae plant family. Human Capsicum fruit consumption dates back at least 6000 years (Perry et al. 2007, and cultivation at least 2500 years. Spanish conquistadores, observing indigenous plant use, associated it with familiar and valuable black pepper, accelerating Capsicum species introduction and adoption in Europe and Asia from the sixteenth century. Today, hot and sweet peppers are cultivated globally, a significant part of human diets, particularly in Asia, enriching global cuisines with the flavors of the solanaceae plant family. Five principal cultivated hot and sweet pepper species exist: C. annuum (most widely cultivated), C. pubescens, C. chinense, C. baccatum, and C. frutescens (Daunay et al. 2008). Herbert J. Webber at Cornell University conducted the earliest study on Mendelian inheritance of C. annuum plant architecture, fruit color, shape, and flavor (Webber 1912. One finding was that pungent and sweet flavor inheritance is single-factor, with pungent dominant over sweet. Nearly 100 years later, the Pun1 gene controlling pepper pungency was identified as a putative acyltransferase catalyzing the last step in capsaicin alkaloid biosynthesis, causing pungent flavor (Stewart et al. 2005. After Erwin Baur and Carl Correns’ 1909 discovery of non-Mendelian, cytoplasmic inheritance (Hagemann 2010, C. annum was the first solanaceae plant family species where cytoplasmic inheritance was observed (Ikeno 1917. Classical genetic analysis in pepper remained relatively limited, mainly focusing on fruit characters like shape and fruit colors (yellow, orange, red, green, or brown) (Hurtado-Hernandez and Smith 1985; Peterson 1959. The first pepper linkage map was constructed in progeny of an interspecific cross between C. annuum and C. chinense using tomato RFLP markers cross-hybridizing to pepper genomic DNA. Synteny between pepper and tomato maps was used to model genome evolution (Prince et al. 1993; Tanksley et al. 1988. Subsequent 20 years saw building several molecular maps in different genetic backgrounds with various DNA markers. These maps formed the basis for linkage mapping numerous qualitative and quantitative horticultural traits like fruit characters (size, shape, weight, color, carotenoid, anthocyanin, and capsaicinoid content, pendant/erect fruit habit), disease resistance (viruses, bacteria, nematodes, and oomycete Phytophthora capsici), and male sterility (comprehensively reviewed by (Ramchiary et al. 2014). Initial fruit weight and capsaicinoid content association mapping results were also obtained (Nimmakayala et al. 2014. Map-based cloning of the Bs3 gene for Xanthomonas campestris pv. vesicatoria resistance revealed Bs3 encodes flavin monooxygenase, a novel plant resistance gene type (Römer et al. 2007. Other genes controlling important phenotypic characters were identified via candidate gene approach, e.g., pepper gene orthologous to tomato Ovate gene for fruit shape (Tsaballa et al. 2011 and recessive pvr1 gene for Potato Virus Y (PVY) resistance (Ruffel et al. 2002. Molecular mapping and cloning efforts yielded easy-to-use and cost-effective DNA-based markers suitable for breeding applications (Holdsworth and Mazourek 2015; Ramchiary et al. 2014.
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Alt Text: A colorful display of various pepper types, showcasing the diverse shapes and colors within the Solanaceae plant family crop.
An annotated, physically ordered reference genome was assembled from sequencing the Mexican landrace ‘Criollo de Morelos’ of Capsicum annuum. Cultivars ‘Perennial’ and ‘Dempsey’ and species C. chinense were re-sequenced and compared to the reference genome and tomato genome (Kim et al. 2014.
Eggplant: A Latecomer to Genomics within the Solanaceae Plant Family
Eggplant (Solanum melongena) is the only solanaceae plant family crop originating in the Old World, specifically Southeast Asia. Eggplant was known in India 2000 years ago and cultivated in China at least 1500 years ago. It was well-known in early Islamic empires in the Middle East and reached Europe probably with the Arab conquest of Spain in the eighth century, and Africa around the same time with Arab and Persian traders. Later, Europeans migrated it to America (Daunay et al. 2008. Despite being a top-five global vegetable crop, genetic research on eggplant played a less prominent role in the twentieth century within the solanaceae plant family. Byron D. Halsted compared tomato, eggplant, and pepper fruit color inheritance and noted genetic similarities, possibly the first synteny observation (Halsted 1918. Later, fruit and flower color genetics were refined (Tatebe 1939; Tigchelaar et al. 1968, and male sterility inheritance, important for hybrid breeding, was analyzed (Nuttall 1963. Eggplant entered the genomics era last among tomato, potato, and pepper within the solanaceae plant family. A linkage map was constructed in F2 progeny of an interspecific S. melongena and wild relative S. linnaeanum hybrid using 233 tomato RFLP markers (Doganlar et al. 2002a. Recently, an intraspecific map based on 415 SNP and SSR (simple sequence repeat) markers was published (Barchi et al. 2009. Linkage maps were prerequisites for QTL mapping morphological and biochemical fruit characters, including yield parameters and plant prickliness (Doganlar et al. 2002b; Portis et al. 2014; Toppino et al. 2008. Eggplant fruit is rich in chlorogenic acid, a polyphenol with high nutraceutical potential. An interspecific S. melongena and S. incanum map aided mapping genes functional in chlorogenic acid biosynthesis, and integrating tomato and other eggplant maps using common markers (Gramazio et al. 2014. Initial association mapping experiments identified SSR and SNP marker associations with fruit and plant characters. Previously linkage mapping-detected QTLs were confirmed, and novel QTLs were also found (Cericola et al. 2014; Ge et al. 2013; Portis et al. 2015. A draft genome sequence of the typical Asian eggplant cultivar ‘Nakate-Shinkuro’ was recently published (Hirakawa et al. 2014.
Alt Text: Glossy purple eggplants growing in a garden, illustrating the fruit’s distinctive color and shape within the Solanaceae plant family.
Conclusions and Perspectives: The Future of Solanaceae Plant Family Research
During the early twentieth century, as genetics emerged as a scientific discipline, tomato, potato, pepper, petunia, and eggplant were among the first plant species subjected to Mendelian studies, marking the early genetic exploration of the solanaceae plant family. Tomato gained and maintained a major plant model position in classical genetics for six decades. Tobacco became the principal model in plant somatic cell genetics, culminating in Agrobacterium tumefaciens-mediated stable transformation of tobacco cells with foreign genes and fertile transgenic plant regeneration between 1975 and 1985. This was one aspect of the plant genetics revolution in the late twentieth century. Another equally important aspect was introducing natural DNA variants as Mendelian markers, opening new approaches for genetic dissection of quantitative and qualitative phenotypic characters, positional cloning of previously intractable genes, and consequently, more efficient and precise plant breeding methods based on marker-assisted selection. Tomato played a pioneering role in this revolution within the solanaceae plant family. Population genetics adoption in the early twenty-first century proved particularly fruitful, greatly facilitating translating basic genetic research into practical breeding applications, especially in polyploid and outcrossing crop species. Tetraploid, heterozygous potato became the leading solanaceae plant family species in this genetic research area. The early twenty-first century witnessed another genetics revolution: next-generation sequencing technologies enabled whole plant genome sequencing, becoming affordable and increasingly routine. Annotated, physically ordered reference genomes of potato, tomato, and hot pepper are now available (Kim et al. 2014; PGSC 2011; Sharma et al. 2013; The Tomato Genome Consortium 2012), and draft genome sequences of tobacco and eggplant were recently published (Bombarely et al. 2012; Hirakawa et al. 2014; Sierro et al. 2014), with a petunia genome sequence under construction (Vandenbussche et al. 2016. The majority of these plants’ gene repertoire is also known thanks to large-scale cDNA sequencing and bioinformatic tools for gene annotation based on sequence homology and de novo methods. The annotated, physically ordered genome sequence is the ultimate precision genetic map, rendering molecular linkage map construction obsolete. Recombination frequency between loci pairs is replaced by physical distance in base pairs. Any DNA-based marker with minimal sequence information (~20 base pairs) can be mapped in silico to the reference genome sequence via a simple BLAST search of the corresponding genome database. This means any quantitative or qualitative trait can be anchored to the genome sequence via linked or associated DNA sequence-based markers. This enables integrating and comparing single genes and QTL mapped in different genetic backgrounds of the same species or syntenic species like tomato and potato (Mosquera et al. 2016. Genomic sequencing and hybridization of total genomic DNA to genome-wide SNP arrays will be the methods of choice for genotyping populations of individuals with known phenotypes to identify SNPs tightly linked or even identical to genes controlling natural phenotypic variation within the solanaceae plant family. This will contribute knowledge of genes and natural variants underlying complex phenotypic traits in plants, which is scarce compared to phenotypic effects of knock-out mutant alleles and over- or ectopically expressed genes. The solanaceae plant family, with its long genetic research tradition on model and non-model species, wealth of genetic and genomic resources, and relevance to human nutrition and well-being, is well-positioned to be a major player in fundamental and applied plant research in the future.
Author contribution statement
CG wrote the article.
Compliance with ethical standards
Conflict of interest
The author declares no conflict of interest.
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