Here we report that the change from the red seeds of wild rice to the white seeds of cultivated rice (Oryza sativa) resulted from the strong selective sweep of a single mutation, a frame-shift deletion within the Rc gene that is found in 97.9% of white rice varieties today. A second mutation, also within Rc, is present in less than 3% of white accessions surveyed. Haplotype analysis revealed that the predominant mutation originated in the japonica subspecies and crossed both geographic and sterility barriers to move into the indica subspecies. A little less than one Mb of japonica DNA hitchhiked with the rc allele into most indica varieties, suggesting that other linked domestication alleles may have been transferred from japonica to indica along with white pericarp color. Our finding provides evidence of active cultural exchange among ancient farmers over the course of rice domestication coupled with very strong, positive selection for a single white allele in both subspecies of O. sativa.
Understanding the history and origin of genetic mutations that have changed wild plants into crops can help us understand the history of the people who cultivated these plants. Rice is one of the oldest crops grown in Asia and it contains two different subspecies that are believed to have been domesticated in different locations by different people. Surprisingly, some of the genetic mutations responsible for domestication are common in all rice. We here show that a mutation in the Rc gene that changed the red seed of wild rice into the white seeds of modern rice is shared by a large majority of all rice varieties, regardless of subspecies. This transfer of genes requires contact among rice types and implies contact among the people who cultivated the different subspecies. We have traced the origin of the mutation in Rc to the japonica subspecies. As additional domestication genes are cloned and their evolutionary history described, we will see how many times and in how many directions such gene transfers have occurred.
Citation: Sweeney MT, Thomson MJ, Cho YG, Park YJ, Williamson SH, Bustamante CD, et al. (2007) Global Dissemination of a Single Mutation Conferring White Pericarp in Rice. PLoS Genet 3(8): e133. https://doi.org/10.1371/journal.pgen.0030133
Editor: Jonathan Pritchard, University of Chicago, United States of America
Received: May 4, 2007; Accepted: June 25, 2007; Published: August 10, 2007
Copyright: © 2007 Sweeney et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: We gratefully acknowledge financial support from the Plant Genome Program of the National Science Foundation (Award Number 0606461 to SRM and CDB, 0110004 to SRM, 0319553 to SMc and CDB, and 0301919 to MJT), the Generation Challenge Program (GCP 4748/A001 to SRM), and Chungbuk National University/National Institute of Agricultural Biotechnology (NIAB-05-6-11-30-2).
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: RID, rice insertion/deletion polymorphism; RM, rice microsatellite
Human efforts to domesticate plant and animal species began thousands of years before recorded history, leaving us to guess at the methods that transformed wild species into agriculturally important crops and livestock. Rice, Oryza sativa, was domesticated in Asia and is now grown on every continent throughout the world, with the exception of Antarctica. The species consists of two major subspecies, indica and japonica, whose separate genetic identities were recognized in ancient times and are maintained by sterility barriers coupled with the inbreeding habit of O. sativa [1–3]. The indica and japonica subspecies can be further subdivided into five genetically distinct subpopulations. Several estimates have been made for the time of divergence between indica and japonica based on intron sequence and retrotransposon insertions, and all of these calculations place the time to the recent common ancestor at more than 100,000 years ago [4–6]. This divergence time is an order of magnitude larger than the oldest estimates for rice domestication. The data strongly support at least two independent domestications of O. sativa from predifferentiated pools of the O. rufipogon wild ancestor [3,4,7,8].
With such evidence for independent domestications, we would expect to see different mutations conditioning domestication traits fixed within the different subspecies. We recently cloned the Rc gene, a bHLH protein, which is the only reported locus in rice that effects a change from red grain to white grain . The change in pericarp color from red to white is an important hallmark of rice domestication. Most rice cultivars grown and consumed throughout the world today have a white or beige pericarp, the color of unpolished “brown rice” while all known accessions of the wild ancestor, O. rufipogon, invariably have grains with a red pericarp. Here, we investigate the number and origin of mutations that give rise to diverse white-grained rice cultivars from around the world, and the extent to which they were disseminated throughout the genetically and geographically diverse range of O. sativa. The evolutionary history of the Rc locus provides clear documentation that a single mutation moved rapidly from the japonica into the indica subspecies, while an independent mutation in the aus subpopulation was not widely disseminated during rice domestication.
How Many Independent Mutations Are Responsible for White Pericarp in O. sativa?
To determine the frequency and distribution of the 14-bp deletion in the Rc gene that has been shown to cause white pericarp in rice [9,10], a set of 440 geographically and genetically diverse rice cultivars were genotyped using the rice indel RID 12 primers reported in Sweeney et al. (2006). Our panel of varieties was selected to represent the range of diversity within Asian cultivated rice. It included both landrace and modern varieties from the five well-defined subpopulations of O. sativa  (Figure 1) (204 indica, 33 aus, 87 temperate japonica, 99 tropical japonica, and 17 aromatic rices) collected in 24 different countries on three different continents (Table S1). Molecular polymorphism data groups the indica and aus subpopulations within the indica subspecies and the tropical japonica, temperate japonica, and aromatic subpopulations within the japonica subspecies [2,3].
For details about the geographical distribution of accessions used in this study, see Table S1.
One hundred percent of the varieties from the indica, tropical japonica, and temperate japonica populations (n = 311) with white pericarp contained an identical 14-bp deletion in the bHLH gene; this deletion was found in none of those with red pericarp (n = 103) (Figure 2). This mutation was also found in 15 of the 17 white aromatic and four of the nine white aus varieties. Thus, a single 14-bp deletion in the Rc gene is present in both subspecies and in all five subpopulations and is responsible for white pericarp in 97.9% (330/337) of rice varieties surveyed.
The gene model for Rc, containing seven exons and comprising a region of approximately 8 kb, is shown horizontally along the top; arrows on the gene model and promoter region of Rc indicate positions of markers: RID-number markers amplify rice insertion/deletion polymorhisms, RM-number markers amplify rice microsatellite polymorphisms, and the RS-number marker detects a rice SNP. Physical positions along the rice Chromosome 7 pseudomolecule are indicated by the ruler below the gene model. In the tables below, allele sizes for RID marker loci are given in bp and allele sizes for RM markers show the number of repeats at each microsatellite locus. The number of varieties in each subpopulation that carry each haplotype is provided in boxed squares in the table to the right. Haplotypes found in varieties with red pericarp are shaded red.
To identify mutations that could explain the lack of pigment in the seven white rice varieties that did not contain the 14-bp deletion, we sequenced the entire coding region of Rc in two of the white aus varieties and one white aromatic variety that lacked the 14-bp deletion. As a control, nine red pericarp varieties from different subpopulations were also sequenced. A SNP (C→A) in exon 6 of the Rc gene distinguished these white- and red-grained rices. This SNP introduces a premature stop codon that truncates the protein before the bHLH domain. Further sequencing confirmed that this SNP was predictive of white pericarp in all seven white rices that did not contain the 14-bp deletion in Rc (DQ902346-DQ902352). Thus, the C→A SNP in exon 6 represents an independent mutation in the Rc gene that was not found in any of the indica, tropical, or temperate japonica varieties but exists at moderate frequency in white aus varieties (five of nine, 55.5%) and in two accessions out of 17 aromatic cultivars (Figure 2).
Ancestral Haplotypes and the Origin of Rc Mutations
To determine the subpopulation origin of the Rc mutations, we examined ancestral haplotypes across the Rc coding sequence and promoter region in 103 genetically diverse, red-grained rices. Four rice insertion/deletion polymorphism (RID) and two rice microsatellite (RM) polymorphisms were used to construct haplotypes across the 6.5-kb region containing the Rc gene (Figure 2). A single haplotype, H1, was detected among the 44 red-grained tropical and temperate japonica plants; we will refer to this as the ancestral japonica haplotype. No red rices belonging to the aromatic subpopulation were available for in this study. Five closely related haplotypes were identified among the 24 red aus and 35 red indica landraces, and all are clearly differentiated from the japonica haplotype. Haplotypes 6–7 and 9–11 (Figure 2) are derivatives of each other and the similarity among them reflects the close evolutionary relationship between the indica and aus subpopulations . When all red-grained indica, aus, and japonica accessions (n = 103) are compared, it can be seen that they share the wild-type alleles at both functional markers (the non-deletion allele at RID12 and the C allele at SNP marker RS40, Figure 2). All flanking marker alleles were unique to one of the subspecies or subpopulation groups. Additionally, we collected ∼6,350 bp of sequence data for the Rc gene and ∼650 bp of downstream DNA from four red indicas and four red japonica varieties. Within this 7-kb region there are 21 SNPs whose alleles are subspecies specific. Thus, there are clearly differentiated haplotypes that distinguish the ancestral japonica gene pool (Haplotype Group A) from the ancestral indica and aus gene pools (Haplotype Group B) across this genic region. Based on these ancestral haplotypes, we were able to trace the origin of both functional mutations leading to white pericarp.
The most common haplotype of white pericarp rices, H2, contained the 14-bp deletion at RID12, and differed from the ancestral japonica haplotype, H1, only at this functional mutation. In contrast, the white H2 haplotype differed from the aus and indica red haplotypes (Haplotype Group B) at every marker tested (Figure 2). This provides strong support for the conclusion that the H2 haplotype originated in a japonica ancestor. White haplotypes H3 and H4 are derived from H1, differing at a single marker locus in each case. Haplotype 5 provides evidence of a putative recombination event. It is found only in indica accessions and cultivars carrying this haplotype have ancestral indica alleles across the promoter and first intron of Rc and ancestral japonica alleles across the remaining sequence of the gene, including the 14-bp deletion. These data strongly support a single origin of the 14-bp deletion from a japonica background that then was introgressed into indica and aus.
Sequence data (7 kb across Rc, Table S2) from white accessions with the deletion (eight indica, two aus, eight tropical japonica, two temperate japonica, and one aromatic) and eight red accessions from both the indica and japonica subspecies were used to create a gene tree (Figure 3). If the Rc gene tree and the tree created using genome-wide SSR data  had similar typologies, it would suggest an independent origin of white pericarp in indica and japonica. However, these trees are not consistent, suggesting introgression from one subspecies into the other. Accessions with red pericarp share a similar distribution pattern in both tress, but all whites with the deletion have japonica alleles at the 21 subspecies specific SNPs within the Rc gene and form a cluster with the red japonicas regardless of their subpopulation identity (Figure 3). Thus, phylogenetic analysis confirms the japonica origin of the 14-bp deletion. Together, the lack of concordance between the Rc gene and rice genomic trees and the marker analysis provides strong support for the conclusion that the 14-bp deletion conferring white pericarp in rice arose once in the japonica gene pool and was widely introgressed into indica and aus landraces. The presence of this deletion within 97.9% of white-grained rice varieties found throughout the world today suggests either that the gene was dispersed during the early phases of domestication and is common by descent in modern varieties or a that very strong, positive selection for the allele lead to its introgression and maintenance in already established gene pools.
Sequence alignment adjusted manually in MacClade 4.05. A heuristic parsimony search was conducted on the data matrix, excluding gapped characters, with TBR branch swapping. This identified a single tree at 53 steps, with a consistency index of 0.98 (0.97 without autapomorphies) and a retention index of 0.99. Bootstrap support was estimated using 100 replications of the same search strategy. Pericarp color and subpopulation of each variety sequenced is labeled.
The second mutation Rc-s is only found in haplotype 8 and is restricted to six aus and two aromatic accessions. These white-grained varieties share no marker alleles with any of the tropical or temperate japonica accessions, suggesting that the origin of this allele is different from that of the 14-bp deletion. H8 differs from H7, a red aus haplotype, by only the functional C→A SNP. Since H7 is restricted to the aus subpopulation, we conclude that the C→A functional polymorphism originated in the aus subpopulation and that this allele was not widely disseminated during the domestication of O. sativa.
How Extensive Was Genetic Hitchhiking around the rc Allele?
How much DNA of japonica ancestry was introgressed into indica cultivars along with the 14-bp deletion conferring white pericarp is of particular interest because the Rc locus falls within the map positions of several quantitative trait loci associated with other domestication-related traits (dormancy, shattering, tillering, and panicle architecture) on Chromosome 7 [11–17]. It is possible that an array of domestication alleles arose in the japonica background and were transferred as a block into indica cultivars. In order to define the extent of the introgression, we designed a series of indel and SNP markers that clearly distinguished the ancestral indica and japonica gene pools across Chromosome 7. To identify these markers, we evaluated polymorphism on a panel of 30 japonicas and 15 red-seeded indicas. Red indicas contain ancestral indica sequence in this region while both red and white japonicas (as well as white indicas) are expected to contain ancestral japonica sequence. FST values provide a quantitative estimate of the degree of allelic differentiation between subpopulations. The indel and SNP markers used to distinguish the ancestral gene pools all had FST values above 0.8 (see upper portion of Figure 4).
Arrows indicate the location of markers on the physical map of Chromosome 7, numbers are in Mb. FST values for red indica versus japonica are plotted across the chromosome using diamonds, white indica versus japonica are plotted using squares. The expanded region shows a detailed view of the 1-Mb window around the Rc gene. All varieties genotyped are white indicas containing the 14-bp deletion. DNA segments containing alleles of japonica ancestry (in the indica background) are shown in white, segments containing alleles of indica ancestry are shown in black, and segments containing a breakpoint between alleles of japonica and indica ancestry are shown in grey. Locations of the Rc and Hsh genes indicated by brackets.
These markers were used to genotype 88 diverse white indica varieties to explore the extent of japonica DNA in the Rc region (Table S3). In this study, nine extended haplotype patterns were identified and they showed varying sizes of japonica introgressions (Figure 4, upper portion). Ninety-one percent of the indica varieties contained less than 1 Mb of japonica derived DNA in the region, with asymmetric distribution around rc. This is similar to haplotype patterns described for the Arabidopsis FRI gene  The haplotype with the smallest introgression, H2, which was observed in two varieties, was only 247–371 kb in size (Figure 4, lower portion) and contained approximately 100 genes. Ten white indica varieties, H8 and H9, contained an introgression that included the recently mapped shattering locus, Hsh , although in most white indicas the japonica introgression does not extend that far. In an extreme case, H9, eight indica landraces collected from an isolated population in Kalimantan, Indonesia (on the island of Borneo) had japonica-derived alleles across the entire length of Chromosome 7 (29.7 Mb) (Figure 4).
When FST values were calculated using data from 88 white indicas and 30 japonicas, we observed a dramatic drop around Rc, from values of over 0.75, down to 0 and back above 0.75 within a 1-Mb region (Figure 4, upper portion). FST values around 0 indicate no differentiation between subpopulations and the drop around Rc illustrates the location and size of the japonica introgression (Figure 4). The difference in FST values outside the Rc region between the red or white indicas compared to japonica is due to the inclusion of the eight white indicas from Kalimantan that carry japonica alleles across the entire length of Chromosome 7. As more domestication genes are cloned from this region, the pattern and extent of introgression reported here can be used to determine if japonica alleles for other domestication traits hitchhiked along with the rc mutation when it was introduced into indica landrace varieties.
Genetic Diversity in Rc
To investigate the reduction in diversity around the 14-bp deletion in Rc, we used sequences from a portion of the Rc gene in 21 diverse varieties of white rice carrying the 14-bp deletion and eight red varieties representing indica, aus, tropical, and temperate japonica subpopulations (Table S2). A summary of DNA polymorphism in the Rc gene is given in Table 1. Levels of polymorphism are reduced by 98% in the white pericarp rices, compared to the red landraces. Notably, the levels of DNA polymorphism in red landraces is comparable to randomly chosen loci in an unbiased sample of O. sativa landraces. For red landraces in the Rc region π (the level of nucleotide diversity) = 0.0025 per base pair, whereas in a survey of randomly chosen loci in O. sativa, π = 0.0032 (Ana Caicedo and Scott Williamson, personal communication, University of Massachusetts, Amherst, Massachussetts and Cornell University, respectively). Thus, other than the extreme reduction in diversity in white pericarp rices, the Rc region is not atypical of the rice genome. Furthermore, the site-frequency spectrum of the white rice sample is completely skewed towards polymorphisms with rare derived alleles. All of these observations are consistent with very strong, recent selection in favor of the 14-bp deletion in the Rc gene.
Here, we show that the previously described 14-bp deletion in Rc leading to white pericarp in rice is found in over 97% of white pericarp rice varieties surveyed, including landrace representatives from all of the major rice subpopulations. This allele arose in a japonica background and was introgressed into the other subpopulations. We determined that the size of the japonica introgression surrounding rc in many indica varieties is less than 1 Mb.
A second mutation leading to white pericarp in 3% of rice varieties surveyed was identified and shown to have arisen in an aus background. This mutation is identical to the one described by  for the Rc-s allele conditioning light red or amber pericarp in the aus variety Surjamkuhi. As previously reported, the C→A transversion in exon 6 of the Rc gene results in a premature stop codon that truncates the protein before the bHLH domain. While it is not surprising that a truncated version of the bHLH protein would result in white pericarp, it is curious that the same truncated protein leads to light red pericarp in some genetic backgrounds. The explanation is expected to lie in the fact that bHLH proteins are found in complexes in maize, Arabidopsis, and petunia [19–21], and different alleles of the interacting proteins are likely to determine the phenotype when Rc is truncated by the C→A substitution. A segregating population derived from a cross between white and light red varieties, both carrying the Rc-s allele, could pinpoint the genetic cause(s) of the difference in phenotype.
The lack of global dissemination of the Rc-s allele leading to either white or light-red pericarp may be partly a question of timing. If the Rc-s allele occurred after the rc allele (14-bp deletion) had become prevalent, there would have been no strong selective pressure driving its spread. The fact that in some genetic backgrounds the Rc-s allele produces a light red grain may be another reason why this allele was considered less desirable for early farmers, reducing the selective advantages and limiting its distribution.
How Was the rc Allele Disseminated across Asia?
In an outcrossing species, it is not surprising to see the rapid spread of a favorable mutation. However, O. sativa is 97%–98% inbreeding [1,22], has a closed-flower morphology, and short-lived pollen grains. Gene flow is further constrained by the presence of a complex network of sterility barriers between the two independently domesticated indica and japonica subspecies of rice [1,23]. Even among largely out-crossing wild Oryza relatives, viable pollen rarely travels more than 10 m , making it difficult for a favorable allele to be widely disseminated through natural pollen flow. Thus, it is unlikely that the rc mutation would have traveled far beyond its point of origin if not for the activities of humans who valued the white grains as a source of food and presumably as a commodity for trade. The importance of the rc mutation to early agriculturalists is evidenced by the fact that it moved around the Himalayan mountain range that is found between the proposed centers of indica and japonica domestication [4,8], and, having traversed this substantial geographic barrier, was rapidly introgressed into all major subpopulations of rice despite an emerging fertility barrier.
Three key genetic features of white pericarp contributed to the rapid spread of this trait. First, rc is a single gene mutation that causes a qualitative change in phenotype so it is straightforward to visually distinguish red from white grains. However, the color of the seed coat is not visible on plants in the field because each grain of rice is completely covered by a hull, or glume. As dehulling reduces the germination rate, seeds that were to be planted the following season would be maintained with the hulls on. The pericarp color would only have been obvious to those who dehulled the grains, something that is normally done just prior to cooking. The pericarp is a maternally derived cell layer and its color is determined by the maternal genotype rather than the genotype of the fertilized embryo. Therefore, all seeds on any one plant are the same color. By dehulling only a few grains on any plant, it would be apparent which plants carried red or white seeds, allowing for selection. Third, the rc mutation is recessive, and in a highly self-pollinated species such as O. sativa, this means that the trait breeds true; seeds with white pericarp will produce offspring having grains with white pericarp for generations to come.
Why Did Farmers Prefer White Rice?
Almost all wild plants have pigmented seed coats, skin, and flesh, yet humans seem to prefer white starchy staples, and selection against pigmentation is a common theme in the evolutionary history of crop plants. The reasons our ancestors selected against pigmentation in these staple foods are not entirely clear, although it is tempting to speculate.
The novelty of a different color rice may have contributed to its popularity. White rice has the very practical advantage that it is far easier to detect and eliminate insects and pathogens against a light background than a darker red background. Alternatively, differences in cooking properties between red and white rice may have resulted in the preference for white. Colored rice has a harder seed coat than white rice. This means longer cooking times as well as more time spent finding fuel with which to cook. In many cultures, the rice hull and bran layers were removed by pounding. As red rice has a harder seed coat than white, it requires more work to remove the bran layer from reds. No matter what the reason for selecting against red pericarp in rice, selection was strong enough to catalyze a major change from red to white grains across a vast geographic area in a surprisingly short period of time.
Despite the lack of human records, the history of domestication is written in the genomes of the plants and animals that have been changed by our choices. As we begin to decipher these stories, we gain new insight into our own history as part of the domestication process. In rice, at least two important and unlinked domestication alleles, rc (discussed in this paper) and the shattering allele, sh4 (located on Chromosome 4) , are now known to have arisen only once in evolution and to have been introgressed across the indica–japonica divide, with almost complete prevalence in modern forms of cultivated rice. Other loci affecting domestication traits, such as the Rc-s allele for white pericarp (this paper) or the sh1 allele for non-shattering , confer alternative or complementary alleles for the same domestication phenotypes, but their distribution is restricted to a specific subpopulation. The fact that cultivars belonging to the deeply divergent indica and japonica subspecies have both common and distinct domestication genes suggests that the process of domestication in O. sativa involves complex patterns of subpopulation isolation and convergence, underwritten by a rich tapestry of cross-talk among ancient farmers. Whether a majority of key domestication alleles are subpopulation-specific or are shared among all Asian rice varieties, and whether the shared alleles arose predominantly within a single subspecies or subpopulation, is not yet known. The answer to this question will illuminate the paths traveled by ancient peoples and their innovations in the rice-growing world.
Materials and Methods
PCR and primer development.
List of primers in Table S4 All primers have an annealing temperature of 55 °C. For the introgression study, primers were designed to amplify small (4–30 bp) insertion/deletion events that were originally detected computationally by aligning the sequences from cv Nipponbare (japonica) and cv 9311 (indica) [27,28]. As 9311 is a white indica, it carries a japonica introgression around rc. In order to identify indels between ancestral indica and japonicas in this region, short stretches of sequence from the red indica cv Mudgo were aligned with Nipponbare. To determine the pericarp color, ten seeds per plant were dehulled and then visually inspected.
Phylogenetic tree construction.
Rc DNA sequenced using overlapping primers. SNPs were confirmed with multiple reads through independent amplicons. Amplified products were sequenced at the Cornell Biotechnology Resource Center. Alignment adjusted manually in MacClade 4.05 (http://macclade.org/macclade.html). A heuristic parsimony search was conducted on the data matrix, excluding gapped characters, with TBR branch swapping. This identified a single tree at 53 steps, with a consistency index of 0.98 (0.97 without autapomorphies) and a retention index of 0.99. Bootstrap support was estimated using 100 replications of the same search strategy.
Table S1. List of Rice Varieties and Corresponding Genotypes for the Association Study
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Table S2. Sequence Polymorphisms across the Rc Gene for 29 Rice Varieties
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Table S3. List of Rice Varieties and Corresponding Genotypes Used for the Introgression Study
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Table S4. Primers Used in This Study
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The sequences discussed in this paper were assigned National Center for Biotechnology Information (NCBI) GenBank (http://www.ncbi.nlm.nih.gov/gquery/gquery.fcgi) accession numbers DQ885795–DQ885823 and DQ902346–DQ902352.
We are grateful to Gurdev Khush, Martha Hamblin, and Gael Pressoir for critical reading of the manuscript; Jeff Doyle for help constructing the phylogenetic trees in Figure 3; Gael Pressoir for suggesting the plotting of FST values in Figure 4; Dr. Sutrisno and Fatimah Suwardjo of the Indonesian Center for Agricultural Biotechnology and Genetic Resources Research and Development in Bogor, Indonesia for providing DNA samples of the Indonesian rice varieties; the International Rice Germplasm Collection (IRGC) in the Philippines for access to diverse rice germplasm; Melissa Fitzgerald for helpful discussions concerning reason for rice preferences; and Lois Swales for help with formatting.
MTS and SRM wrote the paper. SHW and MTS analyzed data. MTS, MJT, YGC, and YJP performed research. MTS, SRM, and CDB designed research.
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