Classification of Wild Tomatoes: a Review

Torno 28 (I): 45-54. 2000 KURTZIANA ..

, Classification of wild tomatoes: a review

Iris Edith Peralta*'**& David M. Spooner*

* United States Department of Agriculture, Agricultural Research Service, Department of Horticulture, University of Wisconsin, 1575 Linden Drive, Madison, Wisconsin 53706-1590, USA.

** Facultad de Ciencias Agrarias, Universidad Nacional de Cuyo, Casilla de Correo 7, Chacras de Coria, 55/7 Mendoza, Argentina. IADIZA, Cas ilIa de Correo 507, 5500 Mendoza, Argentina. Miembro de la Carrera del Investigador. CONICET.

Resumen

Peralta, 1.E. & D. M. Spooner. 2000. Clasificacion de los tomates silvestres: una revision. Kurtziana 28 (I): 45-54. Las especies de tomates silvestres son nativas del oeste de America de Sur. Su posicion generica dentro de las Solamiceas ha sido controvertida desde el Siglo XVIII. Linneo en 1753 ubico a los tomates en Solanum mientras que Miller, un contemponineo de Linneo, los incluyo dentro del nuevo genero Lycopersicon. Posteriormente, la mayoria de los botanicos siguieron la clasificacion de Miller. Las clasificaciones basadas en morfologia 0 en estudios de cruzamientos han propuesto diferente numero de especies 0 categorias supraespecificas. Sobre la base de la cruzamientos entre especies se han identificado dos grupos; uno de ellos incluye especies autocompatibles que pueden cruzarse facilmente con el tomate cultivado, el otro comprende especies autoincompatibles que no pueden cruzase facilmente con esta especie. Recientes investigaciones moleculares, utilizando grupos ex- ternos adecuados, han mostrado que los tomates y las papas estan muy relacionados filogeneticamente y apoyan la inclusion de los tomates dentro de Solanum, clasificacion que hemos adoptado aqui. Se discute acerca del conflicto de los objetivos de las clasificiones basados en la prediccion 0 la estabilidad, una continua controversia en sistematica. Palabras clave: Lycopersicon, Solanum, tomates, clasificacion.

Abstract

Peralta, 1.E. & D. M. Spooner. 2000. Classification of wild tomatoes: a review. Kurtziana 28 (I): 45-54. Wild tomatoes are native to western South America. The generic status of wild tomatoes within the Solanaceae has been controversial since the eighteen century. Linnaeus in 1753 placed tomatoes in Solanum while Miller, a contemporary ofLinnaeus, classified tomatoes in a new genus Lycopersicon. The majority of later botanists have followed Miller. Differing numbers of species and conflicting supraspecific classifications have been proposed, based on morphology or crossing studies. Two .. major crossability groups have been identified, one that includes mainly self-compatible species that easily cross with the cultivated tomato, and another that comprises self-incompatible species not easily cross with the cultivated tomato. Recent molecular investigations using appropriate outgroups have shown that tomatoes and potatoes are close related phylogenetically, and support the inclusion . of tomatoes within Solanum, the classification advocated here. We discuss the conflicting goals of classifications based on predictivity versus stability, a continuing controversy in systematics. Key words: Lycopersicon, Solanum, tomatoes, classification. J 46 Torno 28 (I): 45-54. 2000 KURTZIANA

Wild Tomato distribution and 1). Leaves are imparipinnate, with 2-6 opposite sp~cies characters or sub-opposite, sessile or petiolate pairs of leaflets. There is great interspecific variation in Wild tomatoes (Solanum L. subsect. leaf dissection, and much intraspecific variation Lycopersicum, an autonym of Solanum section in S. peruvianum (Rick, 1963), from pinnate to Lycopersicum (Mill.) Wettst.) are entirely bipinnate with primary, secondary and tertiary American in distribution, growing in the western leaflets, and interjected leaflets. The number of South American Andes from central Ecuador, leaves per sympodium is another valuable through Peru, to northern Chile, and in the taxonomic character, either 2 or 3 (Rick et a!., Galapagos Islands, where the endemic species 1990). S. cheesmaniae grows (Table 1, Fig. 1). In The basic inflorescence is a cyme with addition, S. Iycopersicum, the wild ancestor of different kinds of branching including cultivated tomatoes, is more widespread, and monochasial, dichotomous, and polychotomous perhaps more recently distributed into Mexico, (Luckwill, 1943). The development of Colombia, Bolivia, and other South American inflorescence bracts also is considered an regions (Rick & Holle, 1990). Wild tomatoes important taxonomic character (Rick et aI., 1990). grow in a variety of habitats, from near sea level Flowers are typically yellow, and as in other to over 3,300 m.s.m. in elevation (Rick, 1973; Solanaceae, gamosepalous at the base and Taylor, 1986). These habitats include the arid gamopetalous. The self-compatible species Pacific coast to the mesic uplands in the high (Table 1) typically have smaller stellate flowers Andes. Numerous valleys, formed by rivers and the stigma is often included or flush with draining into the Pacific, characterize the western the anther. The self-incompatible species (Table side of the Andes. Wild tomato populations 1) have larger stellate-rotate or rotate flowers grow at different altitudes in these narrow and exerted stigmas. Tomatoes have a valleys, are geographically isolated, and are characteristic stamen morphology, with anthers adapted to particular microclimatic and soil connivent laterally to form a flask-shaped cone, conditions. Certainly, the diverse geography and with an elongated sterile tip at the apex (except habitats as well as different climates contributed in S. pennellii). Flowers are buzz pollinated. to wild tomato diversity (Warnock, 1988). Fruit size, color and pubescence also are Wild tomatoes are herbaceous plants, highly variable and taxonomically useful (Rick although can also undergo secondary growth. et a!., 1990; Table 1), and too are seed size, co- In their natural habitats, wild tomatoes probably lor and radial walls of the seed coat cells behave as annuals because frost or drought kill (Luckwill, 1943; Lester 1991). the plants after the first growing season (MUller, 1940). In all species the shoots are initially erect, but later, due to the weight of the branches, the Taxonomic History plants become prostrate and can root at the Ever since the cultivated tomato was nodes. Solanum Iycopersicum, S. habrochaites, introduced to Europe in the sixteenth century, S. chilense, and some races of S. peruvianum are botanists have recognized the close relationship robust and can maintain the erect habit longer of tomatoes with the genus Solanum, and until they reach 80-100 cm in height. All species commonly referred to them as S. pomiferum can produce long branches; S. peruvianum, S. during the seventeenthcentury (Luckwill, 1943). pimpinellifolium and S. Iycopersicum branches Tournefort (1694) was the first to consider can grow to more than 4 m long. Pubescence has cultivated tomatoes 'as a distinct genus, been considered an important taxonomic . Lycopersicon ("wolf peach", Greek). Tournefort character (Luckwill, 1943), distingu ishing placed species with large multilocular fruits in especially S. habrochaites and S. pennellii. the genus Lycopersicon, but kept the bilocular Wild tomato species also present species in Solanum. However, we nOWknow taxonomically significant differences in leaf, that some species have two to many locules. In inflorescence, flower and fruit characters CTable Species Plantarum, Linnaeus (1753) classified I. E. PERALTA & D. M. SPOONER. Classification of wild tomatoes: a review 47

tomatoes in the genus Solanum, and described Child. He also hypothesized that Solanum S. lycopersicum and S. peruvianum. Jussieu subsection Lycopersicoides Child and section (1789) also included tomatoes in Solanum. Miller luglandifolium (Rydb.) Child are the closest (1754), though, followed Tournefort and formally relatives of subsection Lycopersicum. described the genus Lycopersicon. Later, Miller Two most recent and complete taxonomic (1768) published diagnoses for L. esculentum treatments of tomatoes are those of MUller (the type species), L. peruvianum and L. (1940) and Luckwill (1943; Fig. 1). MUller (1940) pimpinellifolium. Miller's circumscription of the considered Lycopersicon as a distinct genus genus also included the potato, S. tuberosum, and divided it into two subgenera, and two other species of Solanum under Eulycopersicon C. H. Mull. with two species Lycopersicon (Miller, 1768), but he ultimately possessing glabrous and red- to orange-colored merged Lycopersicon and Solanum (Miller, fruits, and Eriopersicon C. H. MUll. with four 1807). Following Tournefort and Miller's early species bearing pubescent green fruits. Three work, a number of classical and modern authors years later, Luckwill (1943) adopted the same recognized Lycopersicon (e.g., Dunal, 1813; supraspecific categories but recognized different 1852; Bentham & Hooker, 1873; MUller, 1940; infraspecific taxa and five species in the Luckwill, 1943; Correll, 1958; D'Arcy, 1972, 1987, subgenus Eriopersicon (Fig. 1). These 1991; Hunziker, 1979; Rick, 1979, 1988; Ricket treatments have become outdated as the number aI., 1990; Symon, 1981, 1985; Taylor, 1986; of species and races collected from South Warnock, 1988; Hawkes, 1990). America has increased considerably (Rick, 1971, However, Wettstein (1895), in his classical 1991; Holle et aI., 1978, 1979; Taylor, 1986). revision of the Solanaceae, included Rick (1960, 1979) proposed an infrageneric Lycopersicon under Solanum, a treatment classification based on crossing relationships. followed by a minority of later authors He recognized nine wild tomato species, classified (MacBride, 1962; Seithe, 1962; Heine, 1976; into two complexes. The L. esculentum complex Fosberg, 1987). Borner (1912) also recognized included seven species, mainly self-compatible, the close affinity between tomatoes and and easily crossed with the cultivated tomato. potatoes, and proposed a new genus Within this group, three species have mostly Solanopsis to segregate them. D' Arcy (1972, glabrous, pigmented fruits, while the others have 1987) in his revision of Solanum treated pubescent, green fruits. The L. peruvianum Lycopersicon as distinct. D' Arcy (1987), later complex included the self-incompatible species recognized polymorphism in the anther S. peruvianum and S. chilense, having pubescent characters that largely separated the two gene- green fruits that seldom crossed with L. ra, and questioned if perhaps Lycopersicon esculentum (Table 1, Fig. 1). should be merged into Solanum. Different criteria used in classification, Lester (1991) studied the relationships morphology and crossability, therefore has led among domesticated pepinos, potafoes and to different numbers of species, subspecies, and tomatoes using seed coat characters and other varieties, and in conflicting hypotheses of data. He recognized that these three groups interspecific relationships (Fig. 1). In their could be included in a single genus segregated morphology-based taxonomic treatments, MUller from Solanum, but decided for practical reasons (1940) and Luckwill (1943) divided the highly to treat them in Solanum section Basarthrum, polymorphic S. peruvianum into two varieties A Solanum section Petota, and Lycopersicon, and four subspecies, respectively. In addition, respectively. MUller (1940) described a new species, L. In another taxonomic treatment, Child (1990; glandulosum C. H. MUll., and Luckwill (1943) Fig. 1) placed the tomatoes in Solanum subgenus recognized L. pissisi Phil. as a separate species Potatoe (G. Don) D'Arcy, section Lycopersicum, (Fig. 1). subsection Lycopersicum, and distributed them Based on intercrossability and morphological in three series Eriopersicon (C. H. MUll.) Child, data, Rick and Lamm (1955) recognized L. Lycopersicon, and Neolycopersicon (Correll) chilense as a separate species, and included L. Table 1 ~ 00 COMPARISON OF WILD TOMATO SPECIES (SOLANUM L. SUBSECTION LYCOPERSfCUM) (DATA COMPILED FROM MULLER, 1940; LUCKWILL, 1943; RICK, 1986; TAYLOR, 1986). THE SYNONYMS IN LYCOPERSfCON ARE LISTED ONLY WHEN THE SPECIFIC EPITHET DIFFERS BETWEEN GENERA Species Fruit color Breeding system Distribution and Habitat Comments 0, a S. Iycopersicum L. (L. esculen- Red SC', facultative allogamous Native from Ecuador and Peru, widespread Putative origin of cultivated forms 0 N tum) in America. Wide range of habitats, weed 00 in open areas ~ ~ S cheesmaniae Riley Yellow, yellow SC, exclusively autogamous Endemic of the Galapagos Archipelago. Low Closely rei ated to S. Iycopersicum v.... green, orange, purple elevations of the saline seashore , and S pimpinellifolium ...v. S pimpinellifolium B. Juss. Red SC, autogamous, facultative Low elevations in Southern Ecuador and Closely related to S. Iycopersicum N 0 allogamous Peru (coastal to usually below 1000 m), west- (some natural introgression with it) 0 0 ern end of river valleys on Pacific side. Weed in cultivated fields

S chmielewskii (Rick, Kesickii, Green SC, facultatively allogamous 1500-3000 m, Pacific side, South-Central Sympatric with S neorickii Fobes & Holle) 0. M. Spooner, Peru; moist habitats; slightly better-drained G. J Anderson & R. K. Jansen sites that S neorickii

S neorickii 0. M. Spooner, G. Pale green SC, highly autogamous 1500-3000 m, Pacific side, South Ecuador Sympatric with S chmielewskii; J Anderson, & R. K. Jansen to South-Central Peru, moist and well- evolved from S chmielewskii; yet no (L. parviflorum) drained rocky environments; more common natural introgression reported with S than S chmielewskii neorickii

S habrochaites S. Knapp & 0. Green Typically SI", 1-2 collections Typically high elevations (500-3300 m) in Insect resistant (glandular hairs), and M. Spooner (L. hirsutum) SC, but with later inbreeding moist, well drained soils; South-Western Ec- other resistances depress ion uador to South-Central Peru S. chilense (Ounal) Reiche Small green with sr, allogamous Sea level-3000 m; Southern Peru to North- Typically prostate habit; post-syngamic purple stripe ern Chile, sympatric with S peruvianum; barriers with S peruvianum, but North , grows in dry river beds, survives by deep ern most pops. of S peruvianum almos roots fully sexually compatible with S chilense " S peruvianum L. Green Typically SI, allogamous, rare pop Sea level-3000 m; Northern Peru to North- Erect habit; characterized by tremendous SC, autogamous (trend to reduced ern Chile. Wide range of environments variability, even within single accessions variability in Northern races) (many informal races recognized) ~ S pennellii Correll Green Usually SI, some SC in South- 50 m, but typically 500-1500 m; North- Covered with glandular hairs imparts in ~ ern range sect resistance; hybridizes unilaterall, ,.., Central to South-Central Peru (8-16 OS); hot N dry habitats, but subject to heavy dew; (many (as male) with many other species ex- stomata adaxially, poor root system) cept S chilense or S peruvianum ~ > "SC=self-compatible; SI= self-incompatible

.;c !. E PERALTA & D. M. SPOONER. Classification of wild tomatoes: a review 49

g/andu/osum within S. peruvianum. They also Molecular Systematics . examined a photograph of the original type collection of L. pissisi, and concluded that this 1sozymes were extensively used to examine specimen was not related to S. peruvianum (Fig. intra- and interspecific genetic variation in wild I). So/anum peruviamu11 grows throughout tomatoes (Rick, 1983, 1986a; Rick & Fobes, much of the range of the wild tomatoes. 1975a,b; Rick & Tanksley, 1981; Rick & Holle, Rick (1963) analyzed the morphological, 1990; Rick et aI., 1974, 1976, 1977). These studies ecological, and reproductive variation of S. showed that within- and between-population peruvianum, and recognized 40 informally variability was low in the self-compatible species designated races. A few of these are widespread S. cheesmaniae, S. /ycopersicum, and S. neori- coastal races, but the majority are locally ckii. Variability was greater in the facultatively distributed mountain races. Rick (1986a) allogamous S. pimpinellifo/ium, and there was identified four groups of these 40 races that a geographic component to the variability, with were isolated by reproductive barriers. Three the northern Peruvian populations, the most groups of races occur in northern Peru: a polymorphic. The self-incompatible populations of S. habrochailes from northwestern Peru Chamaya-Cuvita group, a Maraf16n group, and a Chotano-humijils/l/11 group. The races from showed more variability than the self-compati- central and southern Peru comprise the fourth ble northern and southern populations. Isozyme group of S. peruvianum races, reproductively polymorphism increased in the almost isolated ti'om the northern races. Rick (1986a) exclusively self-incompatible S. penne//ii, and also confirmed the crossing barriers between was greatest in the self-incompatible S. chi/ense the northern and southern races. The northern and S. peruvianum. races crossed to a limited degree among Not surprising, more genetic variation, themselves and with S. chi/ense, S. habrochai- examined with other molecular markers (RAPDs les and S. /ycopersicum. He also hypothesized and RFLPs), has been found for the cultivated that the Rio Maraf16n races of S. peruvianum tomato and its putative ancestor in the primary were ancestral to the wild tomatoes. center of diversity (western South America)

1\liiller, 1940 Luckwill1943 Rick,1979 Child, 1990

Subgenus Eulycopersico/l Subgenus Elilycopersico/l Esculentum complex Series Lycopersico/l L. eseulelllwn (3) - L. escillenlw/l (8)- L. eseulcnlum (2) S. lycopersicwn L. pimpinelli/cllium L. pimp;nellif;'iliwn L. pimp;nclli/cllium S. pimpinelli/cllium L. cheesllwniae S. clieesmaniae

L. pennelliihirsnlum ~eries S. pennelliiNeoZycopersicon L. elimidewskii~ Se~'ies Eriopersicoll L. panllflomm S. hahroehmles Subgenus EriopersicoJ1 Subgenus Eriopersico/l Peruvianum complex~ S. clunielewskii S. ehilmse S. chilense L. pemvianwll (3) L. pe:llvimlw~ (5)- ~ L. pl.\SLlI- . S. peruvianul11 S. peruvianum L. cheeslllaniae (2) L. clieeslllall;at: (2) S. neorickii L. liirsUlulI} (2)- L. li;rsulwil (2) L. glanduloslIIn L. giandulosllll}

~ Fig. 1.- Comparison of four major taxonomic treatments of tomatoes, showing differences in number of species. subspecies and varieties (numbers in parentheses),intrageneric classifications (under bold headings), and treatment of synonyms (connecting lines). Some new names or new combinations in Solanum were made by Spooner et al. (1993), and Knapp & Spooner (1999) but these authors make no determination regarding inlj'aseetional relationships. Child (1990) did not list S. chmielewskii and S. neorikii, but we include them within series Eriopersicon becadse they match his concept of this series. 50 Tomo 28 (1): 45-54. 2000 KURTZIANA

than in the Old World (Williams & St. Clair, Restriction fragment polymorph isms of 1993; Villand et a!., 1998). The authors mitochondrial DNA (mtDNA; McClean & concluded that more genetic diversity could be Hanson, 1986) were used to compare nine discovered at a faster rate by collecting in the species of Lycopersicon and two closely related primary center of diversity and by sampling over Solanul11 species, utilizing a phenetic approach. a wide range of environments. Molecular The mtDNA divergence is higher than that in markers are promising tools to predict genetic cpDNA, indicating that the DNA of the two variation as well as to identify beneficial genes, genomes is evolving at different rates. The especially in wild relatives of the cultivated studies of McClean and Hanson (1986) were tomato (Tanksley & McCouch, 1997). incongruent with the cpDNA results of Palmer Wild tomato species are valuable genetic and Zamir (1982) and with the morphological sources to improve important agronomic traits and crossing data. Differential organellar and to introgress resistance to diseases and introgression, lineage sorting, or possible stress tolerances in the cultivated tomato (Es- incorrect assessment of homology of the quinas Alcazar, 1981; Laterrot, 1989; Rick, 1982, mtDNA bands may be possible explanations for 1986b, 1987; Rick et al. 1987; Stevens & Rick, the incongruence. 1986). For these reasons, tomatoes have been Miller and Tanksley(1990) used single- to identified among the eight major species/gene- low-copy nuclear restriction fragment length ra for priority conservation status by the polymorph isms (RFLPs) to analyze the phenetic International Board for Plant Genetic Resources, relationships within tomatoes. They found two and presently more than 62,000 accessions are major groups, one corresponding to inbreeding conserved in genebanks (Cross, 1998). species with red fruits, and the other to Phylogenetic relationships in tomatoes have outbreeding species with green fruits. However, been studied using molecular markers. Two one accession of S. peruviamun (outbreeding, studies have been based on organellar DNA. A green fruits) was an exception in that it grouped cladistic analysis of eight species of with the inbreeding red-fruited species. They Lycopersicon and two species of Solanul11 as confirmed many isozyme results in showing a outgroups was conducted with chloroplast gradation of RFLP variation from the self-com- DNA (cpDNA) restriction site data (Palmer & patible species to the self-incompatible ones, Zamir, 1982). The DNA was cut with 2S with most found in S. peruvianul11. The RFLP restriction enzymes and 39 variable sites were diversity of the self-compatible species was observed, of which 14 bands were greater between populations than within phylogenetically informative. This analysis populations. As a matter of fact, there was more supported S. pennelli placed with tomatoes, a genetic variation in a single accession of the species that by prior treatments had been placed self-incompatible species S. peruvianul11than in Lycopersicon or Solanul11. It also supported among all 34 accessionsof the self-compatible the red fruited species as a monophyletic group. specIes. Pigmented fruit was considered a derived feature More recently, the treatment of tomatoes in within Lycopersicon (Palmer & Zamir, 1982). The Solanul11,and indeed as a monophyletic sister data were insufficient to completely resolve group to potatoes, has been supported by relationships within tomatoes as evidenced by cpDNA restriction site data, using 18 restriction two internal trichotomies and identical cpDNA endonucleases and cloned heterologous probes for S. chilense and the three accessions of S. (Spooner et a!., 1993). This study also peruvianul11. Of great interest was that cpDNA conducted a cladistic analysis of tomatoes, polymorphism was observed within the widely potatoes, and outgroups with morphological distributed and morphologically variable species data, as gleaned from the literature, that similarly S. peruvianul11 for which six accessions were supported this sister group relationship. The examined, and that these two groups of only characters shown here that separated accessions were placed in different clades. potatoes and tomatoes were presence/absence I. E. PERALTA & D. M. SPOONER. Classification of wild tomatoes: a review 51

of tubers, corolla pigmentation, anthoclade progress (Peralta, 2000). types (patterns of lateral branching and The systematic placement of tomatoes in associated inflorescences), and anther Solanum is still controversial in that it has yet morphology (free vs. connate; anthers without to gain universal acceptance, especially in the or with sterile apical appendages, anthers breeding literature. This example dramatically opening by terminal pores vs. longitudinal illustrates two main and often competing goals dehiscence). The close relationship of tomatoes in taxonomy of predictive natural classifications and potatoes is also suggested by genetic (treatment in Solanum, our taxonomic decision) linkage data (Bonierbale & aI., 1988; Gerhardt et and the maintenance of nomenclatural stability aI., 1991; Tanksley et aI., 1992). Treatments of (treatment in Lyeopersieon, the taxonomic tomatoes in Solanum are beginning to gain decision of Lester [1991] and others). In reality, acceptance in the taxonomic literature (Bohs & the overall predictive value of classifications, Olmstead, 1997; Olmstead & Palmer, 1997). based on any classification philosophy, has Intron DNA sequences of the single-copy rarely, if ever been tested empirically, and we nuclear structural gene for granule-bound starch are aware of no such tests in crops. It is not synthase (waxy) are cons idered useful to possible to resolve or even summarize these analyze phylogenetic relationships (Ballard and many issues here, and we simply state our Spooner, pel's. com.) as shown for Ipomoea hypothesis that tomatoes may be more (Miller et aI., 1999). We currently are using weny "predictivity" classified in Solanum, despite intron DNA sequences to examine relationships these tests. Classification philosophies remain of all nine species of wild tomatoes. Our under discussion in the systematic community preliminary cladistic analysis of waxy data and involve many additional questions such as supports the paraphyly of the most common reliance on nomenclatural types and and widespread species S. peruvianum. The classification ranks (Moore, 1998). The allogamous species are basal while all economic importance of tomatoes highlights autogamous and facultative allogamous species these competing goals and hypotheses of are derived (Peralta et aI., 1997). classification. It will surely stimulate discussion within the scientific community of taxonomists Conclusions and breeders to highlight the relative value of these classifications that emphasize predictivity Many of the discrepancies in taxonomic versus stability. treatments of the wild tomatoes have arisen from the application of different classification Literature Cited concepts. The classifications of MUller (1940), Luckwill (1943), and Child (1990) were based on Bentham, G. & J. D. !-looker. 1873. Solanaceae. Ge- morphology, while Rick (1979) used the nera Plantarum. 2: 882-913. Lovel Reeve & Co. Landini. biological species concept. These treatments are partly discordant with relationships as shown Bohs, L. & R. G. Olmstead. 1997. Phylogenetic by phenetic (Miller & Tanksley, 1990) or cladistic relationships in Solanum (Solanaceae) base on ndhF sequences. Syst. Bot. 22: 5-17. (Palmer & Zamir, 1982; Spooner et aI., 1993) analyses of molecular data. Bonierbale. M. W.. Steinharter, T. P. & S. D. Tanksley. 1988. RFLP maps based on a common We are attempting to resolve these set of clones reveal modes of chromosomal discrepancies by analyzing more accessions, evolution in potato flnd tomato. Genetics 120: especially from the most widely distributed and 1095-1103. , genetically variable species S. peruvianum. We Borner. C. 1912. Solanum L. und Solanopsis gen. are analyzing these accessions with explicit novo Abh. Naturwiss. Vereine Bremen, 21: 282. morphological techniques, coordinated with Child, A. 1990. A synopsis of Solanum subgenus molecular data from waxy, and using appropriate Potatoe (G. Don) D'Arcy [Tuberarium (Dun.) outgroups in Solanum. A modern revision that Bitter (s.I.)]. Feddes Repel'/. 101: 209-235. incorporates insights from different area~ is in 52 Torno 28 (1): 45-54. 2000 KURTZIANA

Correll, D. S. 1958. A new species and some & A. D. Skelding (eds.). The biology and nomenclatural changes in Solanum, section taxonomy of Solanaceae. Linnean Soc. Symp., Tuberarium. MadroFio 14: 232-236. Ser. 7, pp. 49-85. Academic Press, London. Cross, R. .r. 1998. Review paper: global genetic Jussieu, A. L. de. 1789. Genera Plantarum. Paris. resources of vegetables. PI. Val'. Seeds] ]: ], 39- 60. Laterrot, H. 1989. The tomato. Advantages and use of wild varieties for varietal creation. Rev. Hort. D'Arcy, W. G. 1972. Solanaceae studies II: 295: 13-17. typification of subdivisions of Solanum. Ann. Lester. R. N. 1991. Evolutionary relationships of /vlissouri Bol. Gard. 59: 262-278. tomato. potato and pepino, and wild species of - 1987. The circumscription ofLycopersicol1. Lycopersicon and Solanum, in J. G. Hawkes, R. Solanaceae Newslell. 2: 60-61. N. Lester, M. Nee & N. Estrada (eds.). - ] 991. The Solanaceae since 1976, with a Solanaceae Ill: taxonomy, chemistry, evolution, review of its biogeography, in J. G. Hawkes, R. pp. 283-30 I. Royal Botanic Gardens, Kew. N. Lester, M. Nee & N. Estrada (cds.). Linnaeus. C. 1753. Species Plantarum, I st cd. Solanaceae Ill: laxonomy. chemislry, evolulion, Holmiae. Stockholm. pp. 75-137. Royal Botanic Gardens, Kew. Luckwill, L. C. 1943. The genus Lycopersicon: an Dunal, M. F. 1813. Hisloire Naturelle, Medicinale historical, biological, and taxonomical survey of el £conomique des Solanum. Paris, Strasbourg, the wild and cultivated tomatoes. Aberdeen Univ. Montpellier. Stud 120: 1-44. Dunal, M. F. 1852. Solanaceae, in A.L.P.P. de MacBride, .r. F. 1962. Flora of Peru: Solanaceae. Candolle (ed.). Prodromus systematis naturalis Field Mus. Nal. Hist.. Bol. Ser. 13: 3-267. regni vegetabilis, 13: 1-690. McClean, P. E. & M. R. Hanson. 1986. Esquinas Alcazar. J. 1'. 1981. Genetic resources of Mitochondrial DNA sequence divergence among tomatoes and wild relatives. Rep. Int. Board PI. Lycopersicon and related Solanum species. Breed Resources. No.AGP: IBPGR-80-103. Genetics 112: 649-667. pp. 1-65. Rome. Miller, P. 1754. The gardeners dictionary, Abridged Fosberg, F. R. 1987. New nomenclatural combination 4th ed. London. for Galapagos plant species. Phytologia 62: 181- Miller, P. 1768. The gardeners dictionary. Abridged 183. 8th ed. London. Gerhardt c., E. Ritter, A. Barone, T. Debener, B. Miller, P. 1807. The gardener's and botanist's Walkemeier, U. Schachtchabel, H. Kaufi11ann, R. dictionary. Posth. ed. London. D. Thompson, M. W Bonierbale, M. W. Ganal, S. D. Tanksley, and F. Salamini. 1991. RFLP Miller, .r. c. & S. D. Tanksley. 1990. RFLP analysis of phylogenetic relationships and genetic maps of potato and their aligment with the variation in the genus Lycopersicol1. Theor. Appl. homoeologous tomato genome. Theor. Appl. Genet. 80: 437-448. Genel. 83 :49-57. Miller, R. E., Rausher, M. D. & P. S. Manos. 1999. Hawkes, J. G. 1990. The potato: evolution, Phylogenetic Systematics of Ipomoea biodiversity and genetic resources. Belhaven Press, London. (Convolvulaceae) based on ITS and Waxy. Syst. Bot. 24: 209-227 Heine, H. 1976. Flore de la Nouvelle Caledonie, Moore, G. 1998. A comparison of traditional and vo!.7. Musee National d'Histoire Naturelle, Paris. phylogenetic nomenclature. Taxon 47: 561-579. MUller, C. H. 1940. A revision of the genus Holle, M., Rick, C. M. & D. G. Hunt. 1978. Catalog Lycopersicon. U.S.D.A. Misc. Pub/. 382: 1-28 + of collections of green-fruited Lycopersicon lOp!. species and Solanum pennellii found in watersheds of Peru. TGC report 28:49-78. Olmstead, R. G. & J. D. Palmer. ]997. Implications for phylogeny, classification, and biogeography Holle, M., Rick, C. M. & D. G. Hunt. ]979. Catalog of Solanum from cpDNA restriction site of collections of green-fruited Lycopersicon variation. Syst. Bot. 22: 19-29. species and Solanum pennellii found in watersheds of Peru. TGC report 29:73-91. Palmer, .r. D. & D. Zamir. 1982. Chloroplast DNA Hunziker, A. 1'. 1979. South American Solanaceae: evolution and phylogenetic relationships in Lycopersicon. Proc. Natl. Acad Sci. U.SA. 79: a synoptic survey, in J. G. Hawkes, R. N. Lester 5006-50 I O. I. E. PERALTA & D. M. SPOONER. Classification of wild tomatoes: a review 53

Peralta, I. E., H. Ballard & D. M. Spooner. 1997. - 1991. Tomato resources of South America t Waxy gene intron phylogeny of tomatoes, rcveal many genetic treasures. Diversity 7: 54- Solanum subsect. Lycopersicum (Solanaceae). 56. Amer. J Bot. 84: 222. - & R. Lamm. 1955. Biosystcmatic studies ., Peralta, I. E. 2000. Phylogeny of wild tomatoes on the status of Lycopersicon chilense. Amer. J (Solanum L. section Lycopersicum [Mill.] Bot. 42: 663-675. Wettst. subsection Lycopersicum) based on - R. W. Zobel. & J. F. Fobes. 1974. Four morphology and waxy gene sequences. Ph.D. peroxidase loci in rcd-fruited tomato species: Thesis, University of Wisconsin-Madison genetics and geographic distribution. Proc. Natl. Rick, C. M. 1960. Hybridization betwecn Acad. Sci. USA 71: 835-839. Lycopersicon esculentum and Solanum pennellii. & J. F. Fobes, 1975 a. Allozymes of Phylogenetic and cytogenetic significance. Proc. Galapagos tomatoes: polymorphism, geographic Natl. Acad. Sci. USA. 46: 78-82. distribution and affinities. Evolution 29: 443-457. 1963. Barriers to interbreeding in - & J. F. Fobes, 1975 b. Allozymes variation Lycopersicon peruvianum. Evolution 17: 216- in the cultivated tomatoes and closely related 232. species. Bull. Torrey Bot. Club. 102: 376-384 - 1971. Lycopersicon, in: I. L. Wiggins & D. - E. Kesicki, J. F. Fobes & M. Holle. 1976. M. Porter (eds.). Flora of the Galapagos Islands, Genetic and biosystematic studies on two new pp. 468-471. Stanford Univ. Press, Palo Alto, sibling species of Lycopersicon from Interandean .cal i forn ia. Pcrl!. Theor. Appl. Genet. 47: 55-68. - 1973. Potential genetic resources in tomato J. F. Fobes & M. Holle. 1977. Genetic species: clues from observations in native variation in Lycopersicon pimpinellifolium: habitats, in A. M. Srb (cd.), Genes, Enzymes, evidence of evolutionary change in mating and Populations, pp. 255-269. Plenum, New systems. Pl. Syst. Evo!' 127: 139-170. York. - & S. D. Tanksley. 1981. Genetic variation 1979. Biosystcmatic studics in Lyco- in Solanum pennelli: comparison with two other persicon and closely related species of Solanum, sympatric tomato species. PI. Syst. Evol. 139: in J. G. Hawkcs, R. N. Lester & A. D. Skelding 11-45. (cds.). The biology and taxonomy of Solanaceae. ~ J. W. DeVerna, R. 1'. Chetelat & M. A. Linnean Soc. Symp., Ser.7, pp. 667-677. Stevens. 1987. Potcntial contributions of wide Academic Press, London. crosses to improvement of processing tomatoes - 1982. The potcntial of exotic germplasm Acta Hort. 200: 45-55. for tomato improvement, in I. 1<..Vasil, W. R. - & M. Holle. 1990. Andcan Lycopersicon Scowcron & 1<.. J. Frey (eds.). Plant esculentllm var. cerasiforme: genetic variation and Improvement and Somatic Cell Genetics, pp. 1- its evolutionary significance. Econ. Bot. 44 (3 28. Ncw York, Academic Press. Suppl.): 69-78. 1983. Tomato (Lycopersicon), in: S. D. - H. Laterrot & J. Philouze. 1990. A revised Tanksley & 1'. J. Orton (eds.). Isozymes, in Plant key for the Lycopersicon species. TGC report Genetics and Breeding, pp. 147-165. Elsevier 40: 3 I. Sci. Publ. Amsterdam. Seithe, A. 1962. Die Haarartcn der Gatung Solanum ] 986a. Reproductive isolation in the L. und ihre taxonomischc Verwertung. Bot. Jahrb. Lycopersicon peruvianum complex, in: W. G. Syst. 81: 261-336. D'Arcy (ed.). Solanaceae: biology and systematics, pp. 477-495. Colombia Univ. Press, Spooner, D. M., Andcrson, G.J. & R.I<.. Jansen. Ncw York. 1993. Chloroplast DNA evidence for the . interrelationships of tomatoes, potatoes, and pe- - 1986b. Germplasm resources in the wild pinos (Solanaceae). /lmer. J Bot. 80: 676-688. tomato species. Acta Hort. 190: 39-47. Stevens, M. A. & C. M. Rick. 1986. Genetics and - 1987. Genetic resources in Lycopersicon. , PI. Bioi. 4: 17-26. breeding, in J. G. Atherton & J. Rudich (eds.). The tomato crop: a scientific basis for - 1988. Tomato-like nightshades: affinities, improvement, pp. 35-109. Chapman and Hall, autoecology, and breeders opportunities. Econ. London. Bot. 42: 145-154. 54 Torno 28 (I): 45-54. 2000 KURTZIANA

Symon, D. E. 1981. The solanaceous genera Tournefort, J. P. de. 1694. Ellimens de Botanique. Browallia, Capsicum, Cestrum, Cyphomandra, Villand, .I., P. W. Skorch, T. Lai, P. Hanson, C. G. Hyoscyamus, Lycopersicon, Nierembergia, Kuo, & J. Nienhuis. 1998. Genetic variation Physalis, Petunia, Salpichroa, Withania, among tomato accessions from primary and naturalized in Australia. 1. Adelaide Bot. Gard. secondary centers of diversity. Crop Sci. 3: 133-166. (Madison) 38:1339-1347. -l - 1985. The Solanaceae of New Guinea. 1. Warnock, S. J. 1988. A review of taxonomy and Adelaide Bot. Gard. 8: 1-177. phylogeny of the genus Lycopersicon. Tanksley, S. D., M. W. Ganal, J. P. Prince, M. C. HortScience 23:.669-673. de Vicente, M. W. Bonierbale, P. Broun, T. M. Wettstein, R. von. 1895. Solanaceae, in A. Engler & Fulton, .I. J. Giovannoni, S. Grandillo, G. B. K. Prantl (eds.). Die Natiirlichen Martin, R. Messeguer, J. C. Miller, L. lVIiller, Pflanzenfamilien, 4: 4-38: Nachtrage 292-293. A. H. Paterson, O. Pineda, M. S. Roder, R. A. Williams, C. E. & D. A. St Clair. 1993. Phenetic Wing, W. Wu, & N. D. Young. 1992. High relationships and levels of variability detected density molecular linkage maps on the tomato by restriction fragment length polymorphism and and potato genomes. Genetics 132: 1141-1160. random amplified polymorphic DNA analysis Tanksley, S. D. & S. R. McCouch. 1997. Seed banks of cultivated and wild accessions of Lycopersicon and molecular maps: unlocking genetic potential esculentum. Genome 36: 619-30. from the wild. Science 277: 1063-1066. Taylor, I. B. 1986. Biosystematic of the tomato, in .I. G. Atherton & .I. Rudich (eds.). The tomato Original recibido el 3 de noviembre de 1999; crop' a scientific basis for improvement, pp. 1- aceptado el 23 de diciembre de 1999. 34. Chapman and Hall, London.

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