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Ratcliffe, O. However, occasional reports suggest that rare, white-flowered variants exist within natural populations. Here, we characterize the genetic basis of one of these white-flowered alleles that segregates at low frequency in a population in Oregon. We take advantage of the wealth of information available for the anthocyanin pathway and use classic genetic techniques, along with gene expression and population genetic approaches to identify the putative, loss-of-function mutation that generates white flowers.
We then combine this information with data on the genetic basis of flower color shifts that segregate within populations in other species to examine whether the spectrum of mutations segregating in populations differs from the spectrum of mutations that fixes between populations. Mimulus lewisii Pursh Phrymaceae is a widely-distributed, self-compatible, perennial herb that grows along stream banks in western North America [22] , [23]. Primarily bee-pollinated, M.
The species is comprised of two well-supported sister clades, a southern race with populations in the Sierra Nevada Mountains of California, and a northern race distributed from southern coastal Alaska through the Cascade Mountains of southern Oregon [25].
Rarely, populations of M. We located a population of M. Rhizomes were transported back to the Duke University greenhouses, where they were planted in moist Fafard 4P potting mix and maintained in 16 h days.
Upon flowering, individuals were self-fertilized and seeds collected. Bradshaw, Jr. This allopatric MPL population was chosen as the source of wild-type pink-flowered M. Although we cannot know for sure whether any white alleles are segregating at extremely low frequency in this MPL population, extensive sampling notes P.
Beardsley, personal communication , herbarium records, field guides, and other sources have failed to report white-flowered individuals in MPL or nearby populations. Top row: Leaf and flower from a typical wild-type individual left show dark pink coloration, while the rare, white-flowered morph does not show evidence for anthocyanin production in either flower or leaf tissue.
Previous work in M. To determine whether the level of cyanidin production was reduced in the leaf and floral tissue of white-flowered individuals, we extracted anthocyanidins from mg of bud and mg of leaf tissue from each of three plants per color morph following previously described methods [27]. Floral anthocyanin extractions were also performed on buds from F 1 hybrids between the color morphs see below. To determine whether flower color was a quantitative character, we conducted classic segregation analysis.
Plants grown from field-collected rhizomes at Duke University were self-fertilized to generate the parental individuals. Reciprocal F 1 seeds were generated by crossing a white-flowered individual from CRA with a pink-flowered individual from MPL in the Duke University greenhouses, and were transported to the University of Richmond for planting under similar conditions in a Percival VLT chamber. Upon maturation, F 1 individuals were self-fertilized to produce F 2 seeds.
From one such cross, 96 F 2 offspring were grown in standard potting mix under 16 h days until flowering and scored for flower color as pink or white. We tested whether segregation patterns deviated from Mendelian ratios using a goodness-of-fit test. From five white-flowered CRA and pink-flowered MPL individuals, partial coding sequences from four of the six core structural anthocyanin genes chalcone synthase [Chs], flavanone 3-hydroxylase [F3h], dihydroflavonol 4-reductase [Dfr] , and anthocyanidin synthase [Ans] were cloned using degenerate primers, and reverse-transcribed polymerase chain reaction RT-PCR.
Degenerate primers were designed based on conserved regions in alignments from two closely-related Mimulus species M. Primer sequences are presented in Table S1. PCR products were cloned into the pCR 2. While the anthocyanin pathway genes may be found in multiple copies, only single copies were identified from M. As an initial screen to test if variation between the color morphs co-segregated with sequence variation at any of the structural genes, we sequenced partial coding regions for the four loci from 5 white-flowered and 5 pink-flowered F 2 s from the cross described above.
Based on these results, MlDfr emerged as a potential candidate to explain the flower color change in M. To confirm this, we used a new set of controlled crosses between a white-flowered and pink-flowered individual to score a total of 96 F 2 progeny for flower color pink or white and genotype at MlDfr.
Primers were designed to amplify a bp fragment of MlDfr. Within this fragment, the MlDfr allele from the white-flowered parent contains a SNP relative to the allele from the pink-flowered parent used in this cross that introduces a recognition site for the restriction enzyme SspI. Digested products were separated in 1. In addition to coding sequence mutations in pathway enzymes, mutations that affect gene expression can also account for the differences in flower color between the morphs of M.
Expression differences can occur either via cis -regulatory changes to pathway enzymes or via coding or cis -regulatory mutations in transcription factors that regulate the pathway enzymes. In all other species that have been examined, multiple anthocyanin genes have been shown to be co-regulated by a common set of transcription factors [20] , [21] , [28]. Moreover, cases where anthocyanin pigmentation differences are caused by altered expression levels typically involve considerable changes in transcript abundance [29] — [32].
Therefore, to examine whether prominent differences in gene expression could explain the lack of pigment production in white-flowered plants, we conducted qualitative gene expression assays. From the cloned sequences described above, M. Specificity of the primers was confirmed by sequencing the PCR products.
We used two approaches to obtain full-length coding sequences of the pink and white alleles of MlDfr. These samples were chosen to balance sampling depth within a population, and breadth across representative pink-flowered populations, to identify mutations that were unique to sequences from white-flowered plants.
The full-length coding regions were directly sequenced from each individual. From the above sequences, a 2-bp indel in the coding region of MlDfr emerged as the most likely candidate to explain the presence of white flowers in the CRA population see Results. To provide an unbiased estimate of the frequency of this allele in CRA, we determined the genotype at this 2-bp indel from 19 individuals collected from this natural field population.
Because M. In addition, to minimize sampling biases during collection, we sampled plants after they were finished flowering, at which point flower color could not be determined by visual inspection. Leaves were dried in silica and genomic DNA was isolated as above. This forward primer contains a mismatch with the template DNA, such that the indel plus this mismatch differentially introduces a MslI restriction site. PCR products were direct sequenced from a subset of individuals to validate genotype calls.
No errors were detected. To determine the extent that anthocyanin production was reduced in white flowers relative to pink flowers, we extracted anthocyanin pigments from floral tissue of each morph. Moreover, to determine whether differences in anthocyanins between the morphs were restricted to floral tissue, we also extracted anthocyanins from leaves. Pink-flowered M. Genotypic classes with significant differences in mean flower color are indicated with different letters.
Note the different scales for the two tissue types. To explore the genetic architecture of this difference in flower color, we conducted classic genetic crosses between white-flowered and pink-flowered plants. The anthocyanin content from F 1 hybrid flowers was indistinguishable from wild-type plants Fig. In addition, only two discrete flower color classes segregated in the F 2 that were similar in appearance to the pink and white parental forms Figs.
The absence of cyanidin from both the floral and vegetative tissue of the white-flowered plants suggests that the anthocyanin pathway is blocked in both tissues.
As an initial screen to test if variation in flower color co-segregated with sequence variation in enzyme-coding anthocyanin genes, we sequenced partial coding regions at four of these loci Chs, F3h, Dfr , and Ans from 5 white-flowered and 5 pink-flowered F 2 s. Because of the Mendelian nature of this flower color transition, we focused our efforts further on the genomic region containing MlDfr. We subsequently genotyped 96 F 2 hybrids at a synonymous single-nucleotide difference in the coding sequence of MlDfr.
Assuming a recessive loss-of-function mutation responsible for white flowers, allelic variation in MlDfr co-segregated perfectly with flower color. All F 1 plants were pink-flowered and heterozygous. In the F 2 , all white-flowered individuals were homozygous for the white allele i.
Similar to patterns observed in the parental plants, white-flowered F 2 plants did not produce any detectable cyanidin. While this pattern of co-segregation in an anthocyanin gene essential for pigment production is consistent with the hypothesis that a loss-of-function mutation in MlDfr is responsible for white flowers in the CRA population, additional hypotheses also must be considered.
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Such shifts could produce homeotic changes in morphology Bowman , Albert et al. Floral diagrams for Arabidopsis left and Antirrhinum right. In each flower there are four concentric whorls of different floral organs, starting with the outermost: sepals, petals, stamens, and carpels.
The flower of Arabidopsis has two planes of symmetry disymmetric , while that of Antirrhinum has only one zygomorphic. There are three distinct types of petals in Antirrhinum , dorsal D , lateral L , and ventral V. In the stamen whorl of Antirrhinum , the dorsal stamen is aborted. Photographs: Elena M. Simplified phylogeny of the angiosperms based on recent molecular analyses Soltis and Soltis Oxford University Press is a department of the University of Oxford.
It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign In. Advanced Search. Search Menu. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents Abstract. Evo-devo: Approaches and interpretation.
The basics of floral development. Evolutionary change in floral organ identity: The roles of homeosis and gene duplication. Floral symmetry as a model for independent co-option events. Moving beyond the candidate gene approach. References cited. Understanding the Genetic Basis of Floral Diversity.
Kramer Elena M. Oxford Academic. Cite Cite Elena M. Select Format Select format. Permissions Icon Permissions. Abstract The major radiations that punctuate angiosperm evolution are often associated with innovations in floral architecture. Google Scholar Crossref. Search ADS. Google Scholar PubMed.
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