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Genetics, Vol. 174, 753-762, October 2006, Copyright © 2006
doi:10.1534/genetics.105.053942
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Department of Genetics, Development and Cell Biology and Department of Agronomy, Iowa State University, Ames, Iowa 50011
2 Corresponding author: 2208 Molecular Biology Bldg., Iowa State University, Ames, IA 50011.
E-mail: thomasp{at}iastate.edu
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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6 kb in length). Given that tandem and segmental duplications are common in both animal and plant genomes, our studies suggest that recombination between noncoding duplicated sequences could play an important role in creating genetic and phenotypic variations.
Recent analyses of the maize p1 gene provide further evidence that variations in cis-regulatory regions are involved in phenotypic diversification. The p1 gene encodes an R2R3 Myb-like transcription factor (JIANG et al. 2004). Expression of the p1 gene is observed predominantly in the floral organs, most notably the kernel pericarp and cob glumes. According to the pigmentation patterns in these two organs, p1 alleles are commonly classified into four major types: P1-rr (red pericarp/red cob), P1-wr (white pericarp/red cob), P1-rw (red pericarp/white cob) and p1-ww (white pericarp/white cob). Three distinct p1 alleles, P1-rr4B2, P1-rw1077, and P1-wr[w22], have been characterized and compared at the molecular level. All of these p1 alleles share highly similar coding regions, but differ in the flanking regulatory sequences (CHOPRA et al. 1998; SIDORENKO et al. 2000). Our recent data have demonstrated that changes in the enhancer region, located 5 kb 5' of the transcription start site, result in phenotypic variations between P1-rr4B2 and P1-rw1077 (ZHANG and PETERSON 2005).
More than 100 natural variants of p1 have been reported, each exhibiting distinctive patterns and intensity of pigmentation in kernel pericarp and cob glumes (BRINK and STYLES 1966). This rich collection of naturally occurring alleles provides an excellent system to study the evolution of cis-regulatory regions at the p1 locus. In this study, 6 distinct single-copy p1 alleles were characterized and compared. The goals of the study were: (i) to investigate DNA variations in noncoding regions of the p1 locus, particularly the distal enhancer regions; (ii) to examine correlation between variations in cis-regulatory regions and phenotypic changes; and (iii) to identify the forces affecting evolution of the regulatory regions and the generation of genetic and phenotypic diversity at the p1 locus.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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6 kb from the 5' noncoding regions. The primer pair, P1rr-18 and PA-B4, was used in the first-round reaction. A 1-µl aliquot of the first-round PCR product was subjected to a second-round PCR with the primer pair, P1rr-14 and PA-B6. For the p1 allele, P1-rrCFS36, two additional primers, P1rr-32 and P1rr-25, were used due to the presence of a 1.6-kb transposon-like sequence inserted in the 5' copy of fragment 15 (Figure 2). The 3' noncoding regions were amplified in two overlapping pieces separately by using the primers EP5-16 and P1rr-16, as well as nested primers, P1rr-13r and P1rr-30 and P1rr-16r and P1rr-29. The 723-bp sequences in the second intron were amplified with primers 723-5 and 723-3. Locations and sequences of all primers are shown in Figures 2 and 4 and Table 2. The PCR reactions were performed using enhanced DNA polymerase, Elongase (Invitrogen, Carlsbad, CA) with 1 min of extension time for every 1-kb fragment size. Optimal PCR parameters were followed as suggested by the manufacturer. To minimize the problems caused by PCR artifacts due to annealing of partial extension products to homologous regions in the template DNA pool, the PCR products from three independent reactions were mixed, purified using a gel extraction kit (QIAGEN, Valencia, CA), and sequenced directly from both directions. Sequencing reactions were provided by the Iowa State University DNA Sequencing Facility. The final sequences were inspected and assembled using the software package, Vector NTI Advance 9.0 (InforMax, Frederick, MD). 5' and 3' noncoding repeats of the newly sequenced p1 alleles, P1-rr1088, P1-rrCFS36, P1-rwCFS302, and P1-rwCFS342, have GenBank accession nos. DQ160218–DQ160223.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Structural comparisons of p1 alleles:
Previous studies have shown that the coding regions of different p1 alleles share high sequence similarity; and DNA polymorphisms in noncoding regulatory regions other than in coding regions could be responsible for phenotypic variations of the p1 alleles (LECHELT et al. 1989; SIDORENKO et al. 2000; ZHANG and PETERSON 2005). To examine sequence polymorphisms in noncoding regions of the single-copy p1 alleles studied here, we used genomic PCR with p1-specific primers to amplify both 5' and 3' noncoding regions of the P1-rr and P1-rw alleles. In each allele, 6 kb PCR products from both 5' and 3' regions were sequenced and assembled, and the sequence assemblies match DNA gel blot patterns (see MATERIALS AND METHODS). The structures of the noncoding regions of all six single-copy p1 alleles were compared as shown in Figure 2. Like those in P1-rr4B2 and P1-rw1077, the 5' and 3' noncoding regions in the four newly sequenced p1 alleles are also present as long direct repeats flanking the p1 coding sequences. The repeat unit could extend as long as 6.3 kb (as in P1-rw1077) from a 1.1-kb region, termed fragment C, to a 15-bp small repeat near the transcription start site (5'-GCGGGAGTGCGGCCT-3')2.
Structural and sequence comparisons between the simplex p1 alleles revealed a number of DNA polymorphisms in both 5' and 3' noncoding direct repeats. In the 5' repeats, the most notable polymorphic regions overlap with the previously identified enhancer regions (Figure 2). The distal enhancer region is located 5 kb upstream of the p1 transcription start site and includes the 405-bp fragment 15 and a 666-bp sequence termed fragment 14 (SIDORENKO et al. 2000; ZHANG and PETERSON 2005; Figure 2). Based on the copy number of fragment 15 and fragment 14 sequences in the enhancer-containing regions, three distinct structural types can be defined in six simplex p1 alleles: (i) 1 copy of fragment 15 and 0 copy of fragment 14, i.e., the enhancer-containing region contains only fragment 15, as shown in P1-rwCFS302 and P1-rwCFS342; (ii) 1.5 copies of fragment 15 and 1 copy of fragment 14, i.e., the enhancer-contaning region contains a partial copy of fragment 15 followed by fragment 14 and a full copy of fragment 15, as seen in P1-rw1077; (iii) 2 copies of fragment 15 and 1 copy of fragment 14, i.e., the enhancer-containing region contains a full copy of fragment 15 followed by fragment 14 and an additional full copy of fragment 15, as shown in P1-rr1088, P1-rrCFS36, and P1-rr4B2. The type iii sequences can be further classified as two subtypes: (a) P1-rrCFS36 and P1-rr4B2, in which a 1.6-kb transposon-like sequence (SIDORENKO et al. 2000) is present in the midpoint of the upstream fragment 15; (b) P1-rr1088, in which the 1.6-kb sequence is absent (Figure 2). The 1.6-kb transposon is flanked by an 8-bp direct repeat (CCAGTGAG), which may represent a target site duplication (TSD) generated upon insertion of the 1.6-kb transposon-like sequence. The P1-rr1088 allele contains only a single copy of the 8-bp sequence and no evidence of a sequence alteration (footprint), which commonly accompanies transposon excision. We conclude that the polymorphism between the two subtypes reflects a sequence insertion, rather than a deletion.
In the 3' noncoding regions, the sequences composing fragment 15 and fragment 14 are also highly variable. Similar to the 5' noncoding sequences, the 3' regions of the simplex p1 alleles can also be classified as three distinct types: (i) 1 copy of fragment 14 and 1 copy of fragment 15 as shown in P1-rrCFS36, P1-rr1088, and P1-rwCFS342; (ii) 1.5 copies of fragment 15 and 1 copy of fragment 14 as seen in P1-rw1077; and (iii) 2 copies of fragment 14 and 2 copies of fragment 15 as shown in P1-rr4B2 (equivalent to two copies of type i sequences arranged in direct orientation).
Sequence alignment also revealed two large deletions in the 5' and 3' noncoding regions of the P1-rwCFS342 alleles: a 549-bp sequence (738 bp downstream of fragment 15) that is absent from both 5' and 3' noncoding direct repeats of P1-rwCFS342 (Figure 2) and a 148-bp sequence (3500 bp downstream of fragment 15 in the 3' repeat, Figure 2) that is absent from the 3' noncoding regions of P1-rwCFS342. Sequence analysis of a p1 homologous gene from teosinte (Zea mays subsp. parviglumis) (ZHANG et al. 2000), the immediate progenitor of modern maize, indicated that both 549- and 148-bp sequences are present in teosinte (data not shown). Possibly, these two polymorphic regions resulted from deletions in P1-rwCFS342 rather than insertions in other p1 alleles.
Variations in the distal enhancers correlate with changes of pigmentation patterns in cob glumes:
Comparisons of the simplex p1 alleles reveal three distinct structural types in the 5' enhancer-containing region. In all the simplex P1-rr alleles, this region carries duplicated fragment 15 sequences as well as a fragment 14 sequence between them. A 386-bp cob glume-specific regulatory region has been identified from the P1-rr4B2 allele, which overlaps with the upstream copy of fragment 15 plus the downstream 197-bp sequence (Figure 2). Although this particular sequence is present in both 5' and 3' direct noncoding repeats, the observation that the P1-rw1077 allele lacks this region in that specific location at the enhancer-containing region suggests that this cob glume enhancer region functions in a position-specific manner (ZHANG and PETERSON 2005). Absence of the cob glume-specific enhancer in that specific location is also observed in the newly sequenced P1-rw alleles, P1-rwCFS302 and P1-rwCFS342, which carry only one copy of fragment 15 (without duplication and fragment 14 sequence) in the enhancer-containing region (Figure 2). Therefore, in the single-copy p1 alleles examined in this study, the presence/absence of the cob glume-specific regulatory region in a particular position is correlated with gain/loss of pigmentation in cob glumes. Moreover, structural comparisons between the P1-rr and P1-rw alleles indicated that the cob glume-specific region is formed by complete duplication of fragment 15 and insertion of fragment 14 sequences. Our further analysis suggested that gene conversion between 5' and 3' noncoding repeats could account for the duplication and insertion events observed in the enhancer-containing regions of the simplex p1 alleles, which brought the cob glume-specific regulatory elements into the right position (see below).
Evidence for gene conversion between noncoding regions in the p1 alleles:
The 5' and 3' noncoding regions of the p1 locus are arranged as direct repeats, separated by the 6-kb transcribed region. The observation that a 549-bp deletion is located at identical positions in both 5' and 3' noncoding regions (P1-rwCFS342; Figure 2) suggests that gene conversion events occurred between the noncoding direct repeats in the p1 locus. Gene conversion has been indicated as a candidate mechanism for both homogenizing and diversifying tandem repeats (TESHIMA and INNAN 2004). As mentioned above, the enhancer-containing regions in the 5' noncoding repeats have diverse structures in the distinct p1 simplex alleles. The primary aim of this study is to understand how the 5' enhancer-containing region was diversified and how the cob glume-specific sequence came to occupy its specific position in the P1-rr alleles. To assess the potential role of gene conversion in the creation of diversity in that region, phylogenetic analysis was performed on a 602-bp sequence, which includes fragment 15 and a 3' adjacent 197-bp sequence. This 602-bp sequence is present in both 5' and 3' noncoding regions of all single-copy p1 alleles and can be viewed as a small repeat unit. Thus, it will be more informative to use the entire 602-bp region in the phylogenetic analysis than to use only the 386-bp cob glume enhancer-containing region. In the P1-rw alleles, only one copy of the 602-bp sequence is present in the 5' noncoding regions, while two P1-rr alleles (P1-rr1088 and P1-rrCSF36) have duplicated 602-bp sequences in their 5' repeats; and P1-rr4B2 has the 602-bp sequence duplicated in both 5' and 3' repeats (Figure 2). A total of 17 sequences were used to generate a maximum-likelihood consensus tree (Figure 3): 16 sequences from 5' and 3' repeats of the simplex p1 alleles and one sequence from the 3' noncoding region of the teosinte p gene (p2t) used as the outgroup (ZHANG et al. 2000). The 1.6-kb transposon-like sequence and a flanking 8-bp TSD were removed from the 5' 602-bp sequence of P1-rr4B2 and P1-rr1088 for this analysis. If the 5' repeats evolved independently from the 3' repeats, then the 5' sequences and the 3' sequences should form distinct groups in the phylogenetic tree. Gene conversion events between the 5' and 3' repeats, however, could change the phylogenetic patterns by clustering the 5' sequence with the 3' sequence from the same p1 allele. On the basis of this logic, from the resulting phylogenetic tree, potential gene conversion events were detected between the 5' and 3' 602-bp sequences from four p1 alleles, i.e., P1-rw1077, P1-rr4B2, P1-rrCFS36, and P1-rr1088. Interestingly, the second copies (3' copies) of the duplicated 602-bp sequences in the 5' repeats of all P1-rr alleles are more closely related to the 602-bp sequences in the 3' repeats than to their adjacent 5' copies. This observation suggests that gene conversion events are involved in generating P1-rr-specific enhancer structures (see DISCUSSION). In contrast to the sequences from the P1-rr alleles, which form a monophyletic group with a high bootstrapping value (99%), those sequences from the P1-rw alleles are closely related to that from the p homologous gene in teosintes. This could suggest early divergence of the P1-rw alleles from the p1 ancestral gene during evolution (see DISCUSSION).
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) for DNA diversity also indicated that the 3' regions are more diverse than the 5' regions (e.g., -value 0.02929 vs. 0.00906; Table 3). This suggests that the 5' noncoding repeats, but not the 3' repeats, contain the critical regulatory regions for p1 expression and are therefore under functional constraints (SIDORENKO et al. 2000).
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Phylogenetic analysis has suggested that DNA diversity of 5' and 3' repeats at the simplex p1 alleles could have been affected by gene conversion. To further test this idea, we compared nucleotide diversity between duplicated and nonduplicated p1 sequences. An ideal single-copy p1 sequence for this analysis is the 723-bp sequence located in the second intron of p1 (Figure 4), because (i) this sequence is present only in the p1 locus but not in the p2 gene, the tightly linked paralogous gene of p1, which has potential to undergo gene conversion with p1 (ZHANG et al. 2000; ZHANG and PETERSON 2005), and (ii) this sequence seems to be subject to no functional constraints as it is dispensable for expression of P1-rw1077 (ZHANG and PETERSON 2005). Interestingly, the values for DNA diversity of the 723-bp sequence (-value is 0.00133 and -value is 0.00111) are 8–26 times lower than those of the 5' and 3' noncoding regions (Table 3). This result is consistent with the idea that homologous recombination, e.g., gene conversion, between duplicated sequences increased the diversity in the p1 noncoding repeats.
Estimated divergence time of the p1 alleles:
As stated above, the 723-bp sequence in the p1 second intron likely evolved neutrally; and nucleotide diversity of this region could not have been affected by local gene conversion events. Thus, this sequence can be used to estimate the divergence time of the p1 alleles. The pairwise nucleotide substitution rates were estimated between the simplex p1 alleles (Table 4). Because P1-rw1077 lacks the 723-bp sequence, the substitution rates between P1-rw1077 and other p1 alleles cannot be determined. On the basis of the published estimates of substitution rates in plant nuclear genes (ranging from 2.6 x 10–9 to 1.5 x 10–8 substitutions per synonymous site per year; GAUT 1998; SENCHINA et al. 2003), the divergence time of two P1-rw alleles, P1-rwCFS342 and P1-rwCFS302, is estimated as 93,000–540,000 years ago, while the time between P1-rw (either P1-rwCFS342 or P1-rwCFS302) and P1-rr is 47,000–270,000 years ago (Figure 5). The time of divergence between the P1-rr alleles cannot be estimated, because no substitutions were detected between these alleles (using the formula T = K/2r, where K represents divergence amount and r equals the rate of mutation).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Sequence comparisons of six distinct single-copy p1 alleles have revealed that they all contain the long direct noncoding repeats that flank the p1 coding sequence. The gene structure of the common ancestor of all p1 alleles has been deduced on the basis of analysis of a p-homologous gene in teosinte (ZHANG et al. 2000). As indicated in Figure 5, in the p1 progenitor gene, the long direct repeat is 6 kb and extends from a 5' sequence termed fragment C to a small 15-bp repeat. Subsequent sequence rearrangements in both 5' and 3' repeats diversified the p1 alleles (Table 3).
Structural comparisons of the distinct p1 alleles as well as evidence from phylogenetic analysis and nucleotide diversity analysis allowed us to propose a stepwise evolutionary model to most parsimoniously account for generation of the distinct single-copy p1 alleles. In this model, as indicated in Figure 5, the DNA rearrangements started at the 3' noncoding repeats with insertion of fragment 14 and partial duplication of fragment 15, i.e., the structure shown in P1-rwCFS302. Such rearrangements could be transferred to the 5' noncoding region by gene conversion as shown in P1-rw1077; or they can be further modified by deletion, giving rise to the structures of the 3' noncoding regions observed in the P1-rwCFS342 and P1-rr alleles (Figures 2 and 5).
Because of low nucleotide polymorphisms in the enhancer-containing region, the relationship between the simplex p1 alleles is not well resolved in the maximum-likelihood tree. Although our proposed evolution model is not in agreement with the phylogenetic tree in every detail, both scenarios state that the P1-rw alleles were present early in the evolutionary pathway, while the P1-rr alleles likely originated more recently. The divergence time of the p1 alleles, estimated on the basis of the 723-bp sequence from the p1 second intron (Figure 4), seems to postdate the estimated birth date of the p1 progenitor gene (2.75 MYA; ZHANG et al. 2000). This is consistent with the hypothesis that all p1 alleles studied to date are derived from tandem duplication of a single p1 ancestral gene (ZHANG et al. 2000). On the other hand, the diversification of the p1 gene appears to predate domestication of maize from teosinte 7500 years ago (ILTIS 1983). Most likely, introgression of various p1 alleles from teosinte into the domesticated maize gene pool was facilitated by positive human selection for the obvious pigmentation phenotypes. However, our estimation does not preclude the possibility that divergence of the p1 alleles occurred during or after maize domestication, as the DNA diversity of the p1 alleles is very low. Further investigation of p1-homologous genes in representative teosinte stocks is needed to more precisely estimate the divergence time.
Gene conversion could promote diversification of the p1 noncoding repeats:
In our model, the most interesting step in the evolution of the simplex p1 locus is the change from the P1-rwCFS342-like structure, which contains only one copy of fragment 15 in the enhancer-containing region, to a P1-rr-like structure that has two copies of fragment 15 and one copy of fragment 14 in that region (Figures 2 and 5). The phylogenetic analysis based on the sequences containing the distal enhancer indicated that the second copy of the duplicated fragment 15 sequences at the 5' noncoding region is more closely related to fragment 15 in the 3' noncoding region rather than to the 5' duplicated copy. These results suggest that the 5' P1-rr-type structure in the enhancer-containing region could be generated by gene conversion between the 5' and 3' repeats. More specifically, we propose that, in an allele with a structure similar to that of P1-rwCFS342, fragment 14 and 15 sequences were converted from the 3' repeat into the 5' repeat, with the original fragment 15 sequence adjoined to the newly transferred sequence. After gene conversion, the enhancer-containing region of the resultant p1 allele acquired an extra fragment 15 sequence as well as a fragment 14 sequence downstream of the original fragment 15. It has been suggested that gene conversion can create a new mosaic sequence by transferring a segment of differential sequence from a homologous donor region (MARTINSOHN et al. 1999). In this study, the conversion-generated mosaic sequences in the P1-rr alleles contain duplicated fragment 15 sequences with insertion of a fragment 14 sequence. As the result, a novel cob glume-specific regulatory region was created in the distal enhancer of P1-rr.
Diversifying gene conversion events between duplicated sequences could also explain the increased DNA diversity in the p1 noncoding repeats compared to the single-copy sequence within the second intron. Recent studies have identified gene conversion as a major force to generate nucleotide diversity between homologous sequences (OHTA 1995; ANGERS et al. 2002; NIELSEN et al. 2003; TESHIMA and INNAN 2004; BACKSTROM et al. 2005). It has been suggested that gene conversion could be an error-prone process due to biased tendency toward GC in repair systems as well as a higher rate of misincorporation relative to replicative DNA synthesis (MARTINSOHN et al. 1999; MARAIS 2003). In addition, polarity gradients of gene conversion rates have been reported for conversion tracts in yeast (MARTINSOHN et al. 1999). Unequal gene conversion rates may explain the uneven distribution of polymorphisms in the 5' p1 noncoding repeats. For example, gene conversion rates may be higher in the first 2-kbp region than in the further downstream regions. As a result, DNA diversity in the first 2-kbp region in the 5' noncoding region could have increased by converting nucleotide variations present in the 3' noncoding regions, which probably accumulated more freely there due to fewer functional constraints. Uneven distribution of recombination events has also been reported in a1, b1, and r1 loci in maize (EGGLESTON et al. 1995; PATTERSON et al. 1995; YAO et al. 2002). Because of the small sample size (six p1 alleles) used in this study, however, investigation of additional p1 variations is necessary to test these hypotheses.
Evolution of the distal enhancer and phenotypic variations at the p1 locus:
The stepwise evolution model proposed that the p1 distal enhancer evolved from a simple to complex structures, i.e., from a single copy of fragment 15 to duplicated fragment 15 sequences with insertion of fragment 14. In a recent study (ZHANG and PETERSON 2005), a cob glume-specific regulatory region was identified within the complex enhancer types (Figure 2). This particular structure is associated with all P1-rr alleles, but is absent from the P1-rw alleles. Thus, the evolution of the distal enhancer region appears to accompany the evolution of phenotypic variations observed at the p1 gene. We propose that the early p1 alleles conferred the red kernel pericarp and white cob glumes (RW) phenotype and that a later event may have converted the distal enhancer into a type that contains the cob glume-specific regulatory region. Such change resulted in acquisition of p1 expression in cob glumes and thereby gave rise to the red kernel pericarp and red cob glumes (RR) phenotype.
Taken together, these results suggest that gene conversion between noncoding repeat sequences could be a major driving force for generation of genetic and phenotypic diversity at the p1 locus. Given that tandem and segmental duplications are common in both animal and plant genomes (BLANC et al. 2000; MCLYSAGHT et al. 2002; YU et al. 2005), recombination between noncoding duplicated sequences could have a major impact on molecular evolution and diversity in gene expression.
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ACKNOWLEDGEMENTS |
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FOOTNOTES |
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Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. DQ160218–DQ160223.
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LITERATURE CITED |
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