Linkage Analysis and a QTL Study of Sexual Compatibility Factors and Floral Traits
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Copyright 0 1997 by the Genetics Society of America An Interspecific Backcross of Lycopersicon esculentum X L. hirsutum: Linkage Analysis and a QTL Study of Sexual Compatibility Factors and Floral Traits Dario Bernacchi and Steven D. Tanksley Department of Plant Breeding and Biometry, Cornell University, Ithaca, New York, 14850 Manuscript received February 7, 1997 Accepted for publication July 10, 1997 ABSTRACT A BC, population of the self-compatible tomato Lycopersicon escuhtum and its wild self-incompatible relative L. hirsutum f. typicum was used for restriction fragment length polymorphism linkage analysis and quantitative trait loci (QTL) mappingof reproductive behavior and floral traits. The self-incompati- bility locus, S, on chromosome 1 harbored the only QTL for self-incompatibility indicating that the transition to self-compatibility in the lineage leading to the cultivated tomato was primarily the result of mutations at the S locus. Moreover, the major QTL controlling unilateral incongruityalso mapped to the S locus, supporting the hypothesis that self-incompatibility and unilateral incongruity are not independent mechanisms. The mating behaviorof near-isogenic lines carrying the L. hirsutum allele for the S locus on chromosome 1 in an otherwise L. esculentum background support these conclusions. The S locus region of chromosome 1 also harbors most major QTL for several floral traits important to pollination biology (e.g., number and sizeof flowers), suggesting a gene complex controlling both genetic and morphological mechanisms of reproduction control. Similar associationsin other flowering plants suggest~- that such complex may have been conserved since early periods of plant evolution or else reflect a convergent evolutionary process. N angiosperms numerous mechanisms are known to and FRANKLIN1992). For SSI, as in Brassica, the S locus I determinewhether a population reproduces by contains genes coding for a secreted glycoprotein as cross-pollination (SI), self-pollination (SC) or a combi- well as a transmembrane proteinkinase (TANTIKANJANA nation of the two. Genetic self-incompatibility encom- et al. 1993), butit is still unclear how these two compo- passes a group of mechanisms that prevent self-pollina- nents interact to mediate the S locus response. Less tion in plants via pollen-pistil interactions (DE NETTAN- known are thepollen-specific components of either GSI COURT 1977; THOMPSONand KIRCH 1992; SIMS1993). or SSI systems. It is proposed that selectivity in GSI may Genetic self-incompatibility can be controlled by a sin- be based on the expression of pollen-specific kinases gle multiallelic locus (S locus) or by several loci and that would interact with the style-specific proteins may be determined sporophytically (SSI) or gameto- (KUNZet al. 1996). phytically (GSI) (CORRENS1913; PRELL1921; DE NET- Plants not only displayintraspecific self-incompatibil- TANCOURT 1977). ity, but also interspecific incompatibility. Unlike the sit- Genetic self-incompatibility in plants, in particular uation with self-incompatibility,the genetic basis of in- that controlled by a single locus, is well characterized compatibility between plant species is not well under- and displays an extraordinary degree of polymorphism stood. A common phenomenon observed in crosses comparable to the major histocompatibility complex between related species is unidirectional crosscompati- (MHC) in mammals (RIVERS et al. 1993). For example, bility,also known as unilateral incongruity (UI), in in Tnyolium repens over 200 alleles have been identified which only one species can serve as the female parent (DE NETTANCOURT1977). Genes from the S locus have (LEWISand CROW 1958). A series of models, often been cloned and characterized in several species. In contradictory, have been proposed for the control of most families with GSI, an S locus gene product is a UI. LEWISand CROW (1958) observed that UI is most glycoprotein with ribonuclease activity (SRNAse) ex- commonly manifested when pollen from a SC species pressed in the stigma and style and involved in the is rejected by the style of a SI species. Most exceptions to this rule would involve SC species that only recently determination of pollen rejection (ANDERSON et al. 1989; MCCLURE1989, 1990). Ribonuclease activity has diverged from SI progenitors and thus have imperfect compatibility systems (LEWISand CROWE1958). This is notbeen detected in Papaveraceae (FRANKLIN-TONG an important point since it implies a common genetic basis for SI and UI (LEWISand CROWE1958). Working Corresponding author: Steven D. Tanksley, Department of Plant Breeding and Biometry, 252 Emerson Hall, Cornel1 University with Nicotiana, PANDEY(1968, 1969, 1970) extended Ithaca, NY 14853-1902. E-mail: [email protected] this model and provided genetical evidence that Genetics 147: 861-877 (October, 1997) 862 D. Bernacchi and S. D. Tanksley pointed to the S locus in the control of UI. He also be relatedto mating behavior. The study was performed suggested that different genes within the S locus com- on a BCI population producedfrom a cross between the plex were controlling interspecific compatibility and in- self-compatible tomato inbred L. esculentum cv. E6203 traspecific compatibility. A similar model connecting (recurrent parent) and the self-incompatible wild to- SI and UI has recently been proposed in Brassicaceae mato L. hirsutum f. typicum accession LA1777. L. hirsu- (HISCOCKand DICKSON 1993) and Solanaceae (TROG tum and L. esculentum are highly differentiated with re- NITZ and SCHMIEDICHE 1993). Othershave either re- spect to flower morphology. L. hirsutum flowers are jected the involvement of the S locus in UI (ABDALLA characteristic of an insect-pollinated obligate outcross- 1974; HOGENBOOM1975) or proposed a multigenic ing species, producing many large showy flowers, with model for the control of UI (MARTIN 1963, 1964,1967; broad petals forming a minimally indented corolla of- HARDON1967). ten folding over backward. Its sepals reach midway up In addition to genetic barriers, there are physiologi- the anther cone and also fold over backward at the tip. cal, morphological and ecological factors that influence Its stigmas are always well exserted beyond the anther the balance between self-pollination and cross-pollina- cone and provide easy access to insect pollination. In tion in plant populations (GRANT 1971).Cross-pollina- contrast, the cultivated tomato has fewer, lessconspicu- tion can be promoted by asynchrony of pollen shedding ous, flowerswith smaller corollas and well indented and stigma receptivity (protogyny and protandry), or petals. Its sepals fully embrace the flower bud and its by spatial separation as in flower heteromorphy, dioecy stigmas are typically flush or recessed with respect to or stigma exsertion. In turn, selfing may be promoted theanther coneinsuring self-pollination. Several of by cleistogamy, non-shedding pollen and proximity of these traits are believed to be associated with the fre- female and male parts. Reproduction may also be af- quency of insect visitation: corolla diameter, total num- fected by factors affecting plant-pollinator interaction, ber of flowers, length of the inflorescence and bud such as flower display, color cues, chemical attractants type (RICK 1988). Crosses between these two species are and flower shape and size (GRANT 1971). possible only if L. hirsutum acts as the staminate parent, Several studies have investigated the relationship be- thus falling under the (SI X SC) categorization of UI tween genetic incompatibility and morphological fea- (LEWISand CROW 1958). The goals of this study were tures affecting reproductive behavior. A classic example to determine the genetic basis of the following: (1) SC comes from some families withSSI (Primulaceae, Oxali- in L. esculentum us. SI in L. hirsutum, (2) the UI response daceae, Linaceae, Rubiaceae, Apocynaceae) that also observed in crosses between the two species, (3) floral show flower heteromorphism (distyly and tristyly). Ge- traits that differentiate the species and that are likely netic studies have shown that floral heteromorphy con- to be involved in pollination. To conduct this experi- trol is closely linked to genetic self-incompatibility in ment we constructed a molecular linkage map, the first many instances (for a review see DE NETTANCOURT reported from a cross between these two species. 1977). In contrast,studies in the insect-pollinated genus Layia and Potentilla failed to show any genetic linkage MATERIALS AND METHODS between genetic self-incompatibility and floral traits. The tomato genus, Lycopersicon, is ideal for genetic Plant material and population structure: Half-sib seed of studies of self-incompatibility, unilateral incongruity L. hirsutum f. typicum LA1777, hereafter referred to as H, was provided by C. M. RICK, University of California, Davis. H seed and floral variation associated with pollination behav- was grown at lo", 8 hr photoperiod, in a growth chamber. ior. All species in this genus are interfertileand encom- The seven most vigorous seedlings were saved and a single pass the full range of mating behaviors from small- individual was selected to serve as the staminate parent in a flowered self-pollinators (e.g., L. paruijlomm, L. chees- cross to L. esculentum cv. E6203, hereafter referred to as E. Approximately 70% of the F, seeds germinated andwere con- manii) to large-flowered SI obligate outcrossers (e.g., L. firmed to be hybrids based on intermediate leaf morphology pennellii,