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DNA Polymorphism, Haplotype Structure and Balancing Selection in the Leavenworthia Pgic Locus

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DNA Polymorphism, Haplotype Structure and Balancing Selection in the Leavenworthia Pgic Locus Copyright 1999 by the Genetics Society of America DNA Polymorphism, Haplotype Structure and Balancing Selection in the Leavenworthia PgiC Locus Dmitry A. Filatov and Deborah Charlesworth Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom Manuscript received April 2, 1999 Accepted for publication July 6, 1999 ABSTRACT A study of DNA polymorphism and divergence was conducted for the cytosolic phosphoglucose isomerase (PGI:E.C.5.3.1.9) gene of ®ve species of the mustard genus Leavenworthia: Leavenworthia stylosa, L. alabam- ica, L. crassa, L. uni¯ora, and L. torulosa. Sequences of an internal 2.3-kb PgiC gene region spanning exons 6±16 were obtained from 14 L. stylosa plants from two natural populations and from one to several plants for each of the other species. The level of nucleotide polymorphism in L. stylosa PgiC gene was quite high (p50.051, u50.052). Although recombination is estimated to be high in this locus, extensive haplotype structure was observed for the entire 2.3-kb region. The L. stylosa sequences fall into at least two groups, distinguished by the presence of several indels and nucleotide substitutions, and one of the three charge change nucleotide replacements within the region sequenced correlates with the haplotypes. The differ- ences between the haplotypes are older than between the species, and the haplotypes are still segregating in at least two of ®ve species studied. There is no evidence of recent or ancient population subdivision that could maintain distinct haplotypes. The age of the haplotypes and the results of Kelly's ZnS and Wall's B and Q tests with recombination suggest that the haplotypes are maintained due to balancing selection at or near this locus. N a previous study of the single cytosolic phosphoglu- diversity is expected to be elevated at very closely linked I cose isomerase (PgiC) gene of Leavenworthia stylosa, sites (Strobeck 1983; Hudson and Kaplan 1988). Only Liu et al. (1999) found unexpectedly high levels of DNA a few de®nitive cases of balancing selection have been sequence polymorphism. In the part of the gene stud- described at the DNA level, including the major histo- ied, around intron 12, this was found to be accompanied compatibility complex (Mhc) polymorphism (Klein by distinct haplotype structure and a high level of link- 1986), studied mostly in humans (reviewed in Klein et age disequilibrium between haplotypes. On the basis of al. 1990) and self-incompatibility loci in plants (re- the sequence data, the recombination rate was esti- viewed in Sims 1993 and Charlesworth and Awa- mated to be high in the region studied, and data from dalla 1998). A peak of polymorphism has been attrib- other loci (Liu et al. 1998) did not support the hypothe- uted to the effect of balancing selection in the Drosophila sis of population subdivision. It therefore seemed likely melanogaster Adh locus (Hudson et al. 1987), although that the high nucleotide polymorphism and haplotype as this peak is not entirely attributable to the F/S amino structure could be the results of the long-term action acid difference, but also occurs in the S alleles, the of balancing selection in or near intron 12. On the situation at this locus is not entirely clear. Studies of other hand, the data exhibited no deviations from the other loci with allozyme polymorphisms have failed to neutral model. Thus the cause of the high polymor- ®nd such peaks (Takano et al. 1993). Here we present phism remained unclear. further DNA polymorphism data from the cytosolic A neutral polymorphic site is expected to be main- phosphoglucose isomerase (PgiC) locus of L. stylosa, tained in a population for less than 4N generations. which strengthen the evidence that this gene is another Advantageous or deleterious alleles will be ®xed or elim- example of a gene under balancing selection. inated much faster than this (Kimura and Ohta 1969). The goal of the present work is to examine the level However, polymorphisms can be maintained for very of nucleotide polymorphism and haplotype structure in long times if balancing selection acts in or near the a much larger PgiC region than previously sequenced, locus. In the presence of a polymorphic variant, such to determine the extent of the region of high polymor- as an amino acid involved in an allozyme polymorphism, phism in L. stylosa, and to obtain a larger number of allele sequences in order to test for deviations from the neutral model in this locus. For these purposes we obtained DNA sequences of PgiC alleles for a region Corresponding author: D. A. Filatov, Institute of Cell, Animal, and spanning exons 6±16. Very surprisingly, this demon- Population Biology, King's Bldgs., West Mains Rd., University of Edin- burgh, Edinburgh EH9 3JT, United Kingdom. strated that the observed haplotype structure extends E-mail: dmitry.®[email protected] much further than the intron 12 region, despite evi- Genetics 153: 1423±1434 (November 1999) 1424 D. A. Filatov and D. Charlesworth dence of multiple recombination events. Interestingly, 112 and 24 primers were used to amplify a 1.3-kb region one of the amino acid replacements associated with a referred to below as region B (Figure 1). Primers 18 and 24 were used to amplify the entire 2.3-kb PgiC region of the four charge change correlates with the haplotypes. Compari- other Leavenworthia species and of C. hirsuta. The ampli®ca- son of the sequences from different Leavenworthia spe- tion products were cloned into the pCR2.1 vector using the cies shows that the split between haplotypes preceded TA cloning kit (Invitrogen, San Diego) and both strands were the split between the species in the genus. This is even sequenced on an ABI Prism 377 automatic sequencer (Perkin clearer now that we have included sequences from a Elmer, Norwalk, CT). Sequence alignment and analysis: The sequences obtained further species in the genus that also has high allozyme were aligned using ClustalX v.1.64 software (Thomson et al. diversity (L. alabamica populations; see Charlesworth 1997) followed by additional hand alignment using the and Yang 1998). Despite the ancient origin of the haplo- PROSEQ v.2.3, multiwindow sequence processor for Windows types, they are thus still segregating in at least two Leav- 95 developed by D. Filatov (unpublished results). Sequence enworthia species. Furthermore, several tests potentially data analyses (estimators of DNA diversity, the estimators of recombination rate C and g, the estimator of silent site diver- able to detect deviations from the neutral model, partic- gence Dxy, and Tajima's, Fu and Li's, McDonald and Kreitman ularly tests including the possibility of recombination, (MK), and Hudson, Kreitman, and Aguade (HKA) tests of Kelly's ZnS (Kelly 1997) and Wall's B and Q statistics neutrality) were performed using DNAsp v.2.93 (Rozas and (Wall 1999), detect signi®cant deviation from neutral Rozas 1997), SITES v.1.1 (Hey and Wakeley 1997), PROSEQ expectations. v.2.3, and an unpublished Fortran program written by D. Charlesworth. Wall's B and Q tests (Wall 1999), Kelly's test (Kelly 1997), sliding windows for linkage disequilibrium anal- yses, permutation tests for geographic subdivision (Hudson MATERIALS AND METHODS et al. 1992), and coalescent simulations with recombination Species and populations: A detailed description of the genus were performed by PROSEQ v.2.3. For all phylogenetic analy- Leavenworthia, including most of the populations studied ses we used MEGA v.1.01 (Kumar et al. 1993). here, is in Liu et al. (1999). In this study we used 14 plants A permutation approach (Hudson et al. 1992) was used to of an outcrossing species L. stylosa from populations 95007 (6 estimate the signi®cance of sequence differences between the plants) and Hem1 (8 plants). Four alleles were obtained from two L. stylosa populations studied and between the L and S 3 plants from two L. alabamica populations (see Charles- haplotypes of L. stylosa. The value of the Kst* statistic was worth and Yang 1998), two alleles from a partially self-incom- calculated for two groups of sequences (either for the two patible population (95006) and two from a highly self-fertile geographic populations or for L and S haplotypes). The criti- population (95009). One allele was sequenced from a L. crassa cal value for this statistic was obtained by 1000 random permu- plant from the partially self-incompatible population 95005, tations of the sequences between the two groups in the sample. and one was sequenced from each of two highly inbreeding Coalescent simulations: For the coalescent simulations (see species, L. torulosa (population 95008) and L. uni¯ora (popula- below) we used program routines in Pascal code kindly pro- tion 95011). Since the genus Leavenworthia is thought to be vided by J. Hey. These routines implement the standard algo- closely related to Cardamine (Rollins 1963), we also isolated rithm of the coalescent process with recombination (Hudson DNA from one Cardamine hirsuta plant collected at the Univer- 1983, 1990, 1993). The routines were rewritten in Object Pas- sity of Edinburgh King's Buildings campus for use as an out- cal and built into the PROSEQ v.2.3 (D. Filatov, unpublished group. data). The program generates random samples of a given Molecular methods: Genomic DNA was isolated from Leav- size with a given number of segregating sites and speci®ed enworthia leaves of individual plants by a standard hexa- recombination rates. These simulated samples were used to decyltrimethylammonium bromide (CTAB) plant miniprep estimate critical values of Kelly's (1997) and Wall's (1999) method with several modi®cations. Leaves (z100 mg) were tests with recombination. In our simulations (see below), we thoroughly ground in liquid nitrogen and then in 1 ml of used several values of the recombination rate, chosen to be extraction buffer (0.35 m sorbitol, 5 mm EDTA, 0.1 m Tris- close to the values estimated from the L.
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