Introgression is the transfer of genes of one species into the gene pool of another via hybridization. As a phenomenon, it has been an important topic in animal and plant genetics research for many different reasons. For example, introgression has been implicated in the adaptation of modern humans
] and is of concern to conservation biologists due to loss of integrity of wild bird and mammal populations
]. In plants, introgression is a key concept in studies of the risks of contamination of natural populations by genetically modified (GM) crops. More commonly in crops, favorable genes from wild relatives are intentionally transferred into breeding lines for cultivar development. This has been particularly valuable in crop species that are relatively low in genetic diversity.
According to a review of crop introgression breeding
] the major functional categories of beneficial traits transferred from wild species are resistance or tolerance to abiotic stress or disease, yield, cytoplasmic male sterility or fertility restorers for hybrid production, and quality traits. Among the pioneering uses of wild crop relatives during the late 19th
to early 20th
centuries were the transfer of disease resistances into grape (Vitis vinifera
] and sugarcane (Saccarum officinarum
]. A 1986 review of 23 crops estimated that 6% of total annual economic value in the US was contributed by crop wild relatives
]. For 13 major crops of global importance, it was estimated that 46 wild species have been used in released cultivars, and that furthermore, the introgression breeding approach is increasing
]. Lack of information on pedigrees, unpublished activities within the private sector and changes in taxonomy are some of the factors that contribute to the uncertainty of the collective impacts of crop introgression breeding
Some of the earliest tomato introgression breeding in the US may have been done indirectly and unwittingly via the French variety Merville des Marchés. Recent phenotypic data collected for Merville des Marchés PI 109834 showed it to be variable in fruit size and smoothness (
); its genotype was segregating, showed population admixture, and was an outlier based on genetic distance relative to many other S. lycopersicum
]. We postulated that these were indications of S. pimpinellifolium
in its ancestry (this idea was examined in the current study). The Fusarium
wilt-resistant processing variety Marvel
] was selected from Merville des Marchés in the early 1900s, and Marvel was a parent of Marglobe released in 1925
], which in turn can be found in the pedigree of many important varieties from the 1930s through the late 1950s (H.M. Munger’s tomato pedigree chart provided by E.D. Cobb, Cornell University, 2012). Direct introgression of tomato with wild species in the US commenced in the 1930s concurrent with collection expeditions to geographic centers of origin. The first released cultivar, developed from Marglobe x S. pimpinellifolium
, was aptly named Pan American
]. Introgression breeding efforts of tomato increased globally post World War II, involving the screening of a wide range of traits and all wild tomato species
]. Such efforts continue to be of utmost priority today using sophisticated tools such as introgression libraries for gene discovery
Compellingly, of 96 introgressed traits tallied in released crop cultivars for 11 species (cassava, wheat, millet, rice, maize, sunflower, lettuce, banana, potato, groundnut, tomato), 55 of them were in tomato (Solanum lycopersicum
L.); the next highest numbers were found in rice and potato with 12 traits each
]. The emphasis and success of introgression breeding in tomato encompasses several factors including its intrinsically narrow genetic base, relative ease of crossing with several wild taxa, production demands based on growing conditions and market niche, its susceptibility to pests and pathogens, and its sensitivity to abiotic factors. In addition to resistance or tolerance to dozens of bacterial, viral, fungal, insect, and nematode pathogens, hundreds of favorable genes or quantitative trait loci (QTL) for abiotic stress resistance, flower and fruit traits, yield, and plant architecture have been mapped in wild tomato species
] and thus hold the potential to be exploited.
Introgression breeding carries a cost, namely, genetic linkage of non-targeted loci that are eliminated through repeated backcrossing. Linkage drag can persist within a genome despite backcrossing, especially if recombination is suppressed. Several examples of linkage drag in tomato and other crops have been quantified using molecular markers
]. Linkage drag can denote favorable, deleterious or neutral alleles that become inadvertently incorporated into breeding lines or cultivars.
In this study we apply the term ‘cryptic introgression’
] to describe latent genetic variation in S. lycopersicum
that originated from wild tomato species. Various scenarios can be evoked for its origins ranging from linkage drag, hybridization between feral S. lycopersicum
and wild relatives, to crossing in open-pollinated populations by wind or insect vectors with pollen of introgressed cultivars
]. Cryptic introgression is of interest in germplasm collections such as those conserved at United States Department of Agriculture, Agricultural Research Service (USDA, ARS) Plant Genetic Resources Unit (PGRU) because it can indicate novel genetic variation for exploitation by end-users, or conversely, reveal unfavorable and hence undesirable alleles with respect to crop improvement.
In previous reports we hypothesized the detection of cryptic introgression in 5% to 10% of DNA markers that were resequenced in tomato germplasm panels
]. The aim of the current study was to gather additional evidence on these alleles by resequencing and analyzing the same markers in several accessions of wild tomato species and one accession of weedy S. lycopersicum
). Although variation within wild species gene pools made it impracticable to attempt to discover the 100% identical homologous allele, the assumption was that introgressed alleles would be more closely related to the alleles of a particular wild species than to their S. lycopersicum
homologs. To identify introgressed alleles we also used evidence from mapped locations of markers, phenotypic descriptions, and historical origins of lines and accessions.
Tomato samples analyzed in this study