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Population Biology |
Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee 37235 USA
Received for publication January 11, 2007. Accepted for publication June 20, 2007.
ABSTRACT
Chloroplast DNA (cpDNA) is maternally inherited in the majority, but not all, of angiosperm species. The mode of inheritance of cpDNA is a critical determinant of its molecular evolution and of its population genetic structure. Here, we present the results of investigations of the inheritance of cpDNA in Silene vulgaris, a plant used in a variety of studies in which cpDNA is an important component. PCR/RFLP markers were used to compare mother and offspring cpDNA genotypes sampled from two natural populations, and mother, father, and offspring genotypes obtained from controlled greenhouse crosses. Ten of 215 offspring cpDNA genotypes studied in the controlled crosses and three of 156 offspring from natural populations did not match that of the mother, demonstrating rare nonmaternal inheritance. That the chloroplast genome is occasionally transmitted through pollen is discussed in the context of using S. vulgaris cpDNA as a marker in studies of seed dispersal and when considering the joint evolution of the chloroplast and mitochondrial genomes.
Key Words: Caryophyllaceae • chloroplast DNA • maternal inheritance • paternal leakage • Silene vulgaris
In angiosperms the chloroplast genome is maternally inherited, or largely maternally inherited, in the majority of the species that have been studied. In many species, however, at least occasional paternal transmission results in either paternal or biparental inheritance in some individuals (Sears, 1980
; Corriveau and Coleman, 1988
; Reboud and Zeyl, 1994
; Birky, 1995
, 2001
; Mogensen, 1996
; Röhr et al., 1998
). Such occurrences are more often documented from experimental crosses than in open-pollinated, natural populations, so the impact of rare paternal leakage on the population biology of the chloroplast genome is not well known. Chloroplast DNA (cpDNA) is widely used by plant evolutionary biologists for a variety of reasons, including as a marker of seed movement in studies of population structure and phylogeography (Ennos, 1994
; McCauley, 1995
; Ouborg et al., 1999
; Provan et al., 2001
; Hamilton and Miller, 2002
; Petit et al., 2005
), and as a tool in studies of plant systematics (Olmstead and Palmer, 1994
; Kelchner, 2000
; Wolfe and Randle, 2004
). Many of these applications assume maternal inheritance as a chief determinate of both the magnitude of gene flow and the mode of molecular evolution of the genome. Further, the tendency for angiosperm chloroplast genomes to be maternally inherited has led to the suggestion that they be considered as useful sites for insertion of engineered genes in genetically manipulated species because the lack of transmission through pollen would greatly reduce the probability of "escape" (Gressel, 1999
; Grevich and Danielle, 2005
; but see Smith, 1989
and Haygood et al., 2004
). Thus, understanding the frequency and circumstances of paternal leakage of the chloroplast genomes of angiosperms is useful to plant biologists who study a variety of topics.
Silene vulgaris (Moench) Garcke (bladder campion, Caryophyllaceae) is a weedy species widely studied for a variety of reasons, including its gynodioecious mating system (e.g., Jolls and Chenier, 1989
; Petterson, 1992
; Charlesworth and Laporte, 1998
; McCauley et al., 2000
; Glaettli and Goudet, 2006
), its occurrence as a weedy exotic in North America (McCauley et al., 2003
; Bailey and McCauley, 2006
), its ecological interactions with pathogens and insects (Antonovics et al., 2002
; Kephart et al., 2006
), and its ability to tolerate heavy metals (Schat et al., 1996
; Bringezu et al., 1999
; Bratteler et al., 2006
). Chloroplast DNA markers have been used in studies of population structure of S. vulgaris (McCauley, 1998
; McCauley et al., 2003
), its mating system (Ingvarsson and Taylor, 2002
; McCauley and Olson, 2003
), and the molecular evolution of its organellar genomes (Ingvarsson et al., 2003
; Ingvarsson, 2004
; Houliston and Olson, 2006
).
Recent studies of the inheritance of the mitochondrial genome of S. vulgaris have shown that it is at least occasionally subject to paternal leakage and that this results in fairly widespread heteroplasmy (McCauley et al., 2005
; Welch et al., 2006
). The inheritance of the chloroplast genome in S. vulgaris has not been studied previously, though maternal inheritance of cpDNA was found in a limited study of the closely related S. alba (Mill.) Krause (McCauley, 1994
). Here, we present a PCR/RFLP-based study of the inheritance of cpDNA in S. vulgaris and provide evidence of occasional paternal leakage derived from both formal crosses and studies of natural populations.
MATERIALS AND METHODS
Information on the inheritance of cpDNA was obtained from two classes of individuals. The first consisted of a set of parents and their offspring obtained from controlled crosses described in Bailey and McCauley (2005)
. Briefly, seeds were collected from 12 natural populations of S. vulgaris in Virginia and New York and grown to flowering in the Vanderbilt greenhouse. Crosses were made between unrelated hermaphrodite individuals originating from the same, or different, local population. Seeds resulting from these crosses were also grown to flowering in the greenhouse. The second set of individuals was obtained by collecting seed capsules and corresponding maternal leaf tissue from one natural population of S. vulgaris in Virginia and one in New York. Seeds collected from these natural populations were grown to flowering in the Vanderbilt greenhouse. Nonmaternal inheritance was inferred in the first data set when offspring resembled the pollen donor rather than the pollen recipient. Nonmaternal inheritance was inferred in the second data set when the haplotype of an offspring did not match that of its mother but rather that of another cpDNA haplotype known to occur in the study population, though the specific pollen donor haplotype was not known in the open-pollinated natural populations.
The PCR/RFLP cpDNA haplotype of each individual reported in the present study was determined using one or more of the primer pairs and methods outlined in McCauley et al. (2003)
and Bailey and McCauley (2005)
. Briefly, DNA extracted from each of the parents in the cross study was used as a template for four separate PCR reactions utilizing either the c&d (trnL intron) and e&f (trnL–trnF spacer region) cpDNA primer pairs described by Taberlet et al. (1991)
or the S&G (trnS–trnG spacer region) and the H&PSBA (trnH–psbA spacer region) cpDNA primer pairs described by Hamilton (1999)
. Ten microliters of the PCR product obtained from a given primer pair was digested with the restriction enzyme MseI and the resulting fragments electrophoresed on a 4% Metaphor (Cambrex, Rockland, Maine, USA) agarose gel stained with ethidium bromide. A haplotype was defined as the combination of restriction fragment patterns obtained by considering the products of each of the four primer pairs. This method identified 19 different PCR/RFLP haplotypes in a survey of North American populations (McCauley et al., 2003
), of which eight were represented in the crosses (Bailey and McCauley, 2005
). Haplotype differences include differences in the number of MseI restriction sites and fragment length variation due to small indels in one or more PCR products. Because those crosses were designed for other purposes (Bailey and McCauley, 2005
), not all included detectable cpDNA haplotype differences between parents. Those families in which the pollen donor and recipient PCR/RFLP cpDNA haplotypes differed according to the product generated by at least one primer pair were selected for further study. The haplotypes of the 215 offspring produced by the 15 crosses meeting this criterion were determined using the product obtained from the reaction involving the specific primer pairs that amplified the regions of cpDNA at which that set of parents were known to differ. Offspring cpDNA haplotypes were compared to those of both parents.
Detection of nonmaternal inheritance in natural populations requires the identification of polymorphic cpDNA markers within populations so that there is at least the chance that the pollen recipient and the unknown pollen donor could contribute different cpDNA haplotypes to the offspring, according to the mode of inheritance. Otherwise, nonmaternal inheritance would be undetectable. Natural populations in Delaware County, New York and Rockingham County, Virginia were selected for study because these populations were known to contain restriction fragment length polymorphism in the amplification products obtained using the H&PSBA primers (McCauley et al., 2003
). The H/PSBA haplotypes were determined using DNA extracted from leaf material obtained from mothers and from offspring collected as seed and grown to the seedling stage in the greenhouse. Thus, an offspring whose cpDNA haplotype does not resemble the maternal haplotype is inferred to represent a case of paternal leakage, although it is possible for some cases of paternal leakage to go undetected when the unknown cpDNA haplotype of the pollen donor matches that of the pollen recipient. Forty-eight offspring individuals, distributed among seven maternal lines, were genotyped from the Virginia population, and 108 offspring, distributed among 11 lines, were genotyped in the New York population study.
The PCR/RFLP genotyping protocol was repeated for all offspring whose cpDNA haplotype did not match the maternal haplotype, including samples from both the cross and natural populations, to verify the results.
RESULTS
Sample size and diagnostic cpDNA primer information used to compare cpDNA haplotypes of parents and offspring obtained from the cross study are provided in Table 1. Of the 215 offspring individuals assayed, 205 (95.3%) had a cpDNA haplotype that matched that of the mother, whereas 10 had a cpDNA haplotype that matched that of the father. Inheritance was strictly maternal in 13 of 15 families. One of 15 offspring showed paternal inheritance in one family, as evidenced by maternal/paternal haplotype differences in restriction fragment patterns obtained when either the e&f or H&PSBA PCR products were digested with MseI (see Fig. 1 for a gel image representative of the parent–offspring comparisons used in this study). In a second family the inheritance of nine of 10 offspring was paternal, while the inheritance of the tenth offspring was maternal. In this case maternal/paternal haplotype differences were evident in the restriction fragment patterns produced by MseI digestion of PCR products obtained from either the S&G, c&d, or H&PSBA primers.
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Paternal leakage of cpDNA was detected in 4.7% of the offspring individuals in the greenhouse crosses and 1.9% of offspring individuals collected from the field. It is important to recall that in all greenhouse crosses the paternal and maternal cpDNA haploytpes were known to differ, whereas the paternal haploytpes of the field-collected individuals were unknown. Given that many fertilizations in the natural populations undoubtedly involved pollen from a donor that happened to carry a cpDNA marker haplotype identical to that of the mother (including cases of self-fertilizations), the leakage rate estimated from natural populations is surely an underestimate of the true rate, which is perhaps closer to the rate estimated by the controlled crosses.
These results have implications for two types of ongoing studies of S. vulgaris. A potentially important implication for the population biology of S. vulgaris concerns the use of cpDNA in studies of the population structure. In angiosperms, population structure, as measured by statistics such as Fst, is almost always much greater when estimated by cpDNA or mtDNA markers than by nuclear markers (Petit et al., 2005
). This is predicted by theory, in part because with strict maternal inheritance cytoplasmic genes should disperse only by seed (Birky et al., 1983
, 1989
; Petit et al., 1993
). This nuclear/organellar gene difference has been seen in S. vulgaris as well, using both cpDNA and mtDNA markers, which give similar results (McCauley, 1998
; Olson and McCauley, 2002
). Fst is often used to gage the amount of gene flow, and with maternal inheritance of cpDNA, Fst differences between nuclear and cpDNA markers have been used to estimate the relative contributions of seed and pollen movement to total gene flow (McCauley, 1995
). One theoretical consequence of transmission of either organellar genome through pollen at even a low level is a reduction in the expected magnitude of Fst and in the difference between the Fst value estimated using organellar vs. nuclear markers (Petit et al., 1993
). Whatever the impact of transmission through pollen might be on estimates of Fst based on mtDNA and cpDNA in S. vulgaris, the results presented here suggest that the impact is about the same for each genome, given that there is now evidence for paternal leakage of each at approximately the same rate. The rate of paternal transmission of cpDNA documented here falls well within the range shown by Haygood et al. (2004)
to allow for the potential escape of chloroplast transgenes through pollen, and such escape would be undesirable had S. vulgaris been a genetically modified crop species and able to hybridize with wild relatives.
One empirical observation that has been made of the joint distribution of cpDNA and mtDNA genotypes in natural populations of S. vulgaris is that the two genomes seem to be in gametic disequilibrium (Olson and McCauley, 2000
; Storchova and Olson, 2004
). In no cases in these studies were all four possible combinations found between a pair of cpDNA and a pair of mtDNA haplotypes. Olson and McCauley (2000)
attributed this strict association to the co-transmission of the two cytoplasmic genomes expected if each was always maternally inherited. This association has also been found in other plant species (e.g., Desplanque et al., 2000
). Dissociation of the two genomes would be permitted by paternal leakage of one or the other genome, though the potential for dissociation might be diminished if they tend to leak together. Recent studies of the transmission of the mitochondrial DNA in S. vulgaris have indicated occasional paternal leakage of that genome (McCauley et al., 2005
; Welch et al., 2006
). When combined with the evidence for paternal leakage of the chloroplast genome presented here, it is not clear why these strong mtDNA/cpDNA haplotype associations are found in natural populations of S. vulgaris. In fact, a recent joint analysis of chloroplast and mitochondrial gene sequence data also suggests that co-transmission is not universal in S. vulgaris (Houliston and Olson, 2006
). Given that paternal leakage has now been demonstrated for each genome, it would be interesting to investigate the independence of the leakage events using experimental crosses. Given the cpDNA/mtDNA gametic disequilibrium in natural populations (Olson and McCauley, 2000
; Storchova and Olson, 2004
), one might predict that joint leakage is more common than leakage of just one genome or the other. If so, this could also explain the similarity in mtDNA and cpDNA based estimates of Fst in S. vulgaris.
Paternal transmission of the chloroplast genome also has consequences for the application of cpDNA to phylogenetic questions because transmission through pollen could enhance the opportunity for chloroplast capture, a phenomenon that can obfuscate interpretation of cpDNA-based phylogenetic relationships. Further, because pollen and seeds often have different dispersal properties, the dynamics of chloroplast capture could be quite different when paternal transmission is allowed, especially in taxa with long-distance pollen dispersal.
Finally, recent evidence of mitochondrial heteroplasmy in S. vulgaris has been attributed to occasional paternal leakage of that genome (Welch et al., 2006
). The potential for chloroplast heteroplasmy has not been studied in S. vulgaris, though the results presented here suggest that heteroplasmy could sometimes occur. Studies seeking to quantify chloroplast heteroplasmy, such as that conducted by Frey et al. (2005)
in Senecio vulgaris, would seem warranted in bladder campion.
FOOTNOTES
1 The authors acknowledge financial support provided by U.S. Department of Agriculture Award 2002–02213 and National Science Foundation Award 0621867. 
2 Author for correspondence (david.e.mccauley{at}vanderbilt.edu
)
3 Current address: Department of Biology, Indiana University, Bloomington, IN 47405 USA
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420-bp PCR product amplified with e&f cpDNA primers and electrophoresed on a 4% Metaphor agarose gel. Profiles of 17 Silene vulgaris individuals are presented including the maternal (M) and paternal (P) parents and 15 of their offspring. Note that the maternal haplotype contains an extra MseI restriction site compared with the paternal haplotype. Offspring 9 indicates paternal inheritance, while the other 14 offspring carry the maternal phenotype. Paternal inheritance was also evident in this individual on the basis of MseI digestion of PCR products obtained from the H&PSBA primers