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One- and Two-Locus Population Models With Differential Viability Between Sexes: Parallels Between Haploid Parental Selection and Genomic Imprinting
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Alexey Yanchukov 《Genetics》2009,182(4):1117-1127
A model of genomic imprinting with complete inactivation of the imprinted allele is shown to be formally equivalent to the haploid model of parental selection. When single-locus dynamics are considered, an internal equilibrium is possible only if selection acts in the opposite directions in males and females. I study a two-locus version of the latter model, in which maternal and paternal effects are attributed to the single alleles at two different loci. A necessary condition for the allele frequency equilibria to remain on the linkage equilibrium surface is the multiplicative interaction between maternal and paternal fitness parameters. In this case the equilibrium dynamics are independent at both loci and results from the single-locus model apply. When fitness parameters are additive, analytic treatment was not possible but numerical simulations revealed that stable polymorphism characterized by association between loci is possible only in several special cases in which maternal and paternal fitness contributions are precisely balanced. As in the single-locus case, antagonistic selection in males and females is a necessary condition for the maintenance of polymorphism. I also show that the above two-locus results of the parental selection model are very sensitive to the inclusion of weak directional selection on the individual''s own genotypes.PARENTAL genetic effects refer to the influence of the mother''s and father''s genotypes on the phenotypes of their offspring, not attributable just to the transfer of genes. Examples have been documented across a wide range of areas of organism biology; see, for example, Wade (1998) and and22 in Rasanen and Kruuk (2007). Parental selection is a more formal concept used in theoretical modeling and concerns situations where the fitness of the offspring depends, besides other factors, on the genotypes of its parent(s) (generalizing from Kirkpatrick and Lande 1989).
Open in a separate windowParentheses in the first column indicate maternal genotype (parental selection model) or inactivation of the maternally derived allele (imprinting model). Whether selection occurs at the diploid (first column) or subsequent haploid (second column) stage does not change the resulting allele frequencies.
Open in a separate windowAnother well-known parent-of-origin phenomenon is genomic imprinting. Here, the level of expression of one of the alleles depends on which parent it is inherited from. Often it is difficult to tell apart the phenotypic patterns due to parental effects and genomic imprinting, and thus a problem arises in the process of identifying the candidate genes for such effects (Hager et al. 2008). Analytic methods (Weinberg et al. 1998; Santure and Spencer 2006; Hager et al. 2008) have been developed to quantify subtle differences between the two. In this article, I point out that a simple mathematical model, first suggested for genomic imprinting at a diploid locus, can be interpreted, without any formal changes, to describe parental selection on haploids.While there has been much progress in understanding the evolution of genomic imprinting (Hunter 2007), including advances in modeling (Spencer 2000, 2008), the population genetics theory of parental effects received less attention. Existing major-locus effect models of parental selection are single-locus, two-allele, and mostly concern uniparental (maternal) selection (Wright 1969; Spencer 2003; Gavrilets and Rice 2006; Santure and Spencer 2006), with only one specific case where the fitness effects of both parents interact studied by Gavrilets and Rice (2006). No attempt to extend this theory into multilocus systems has yet been made. Considering a two-locus model with both parents playing a role in selection on the offspring is called for by the observation that many maternal and paternal effects aim at the different traits or different life stages of their progeny. Among birds, for example, body condition soon after hatching is largely determined by the mother, while paternally transmitted sexual display traits develop much later in life (Price 1998). Such effects are therefore unlikely to be regulated within a single locus. Sometimes the effects are on the same trait, but still attributed to different loci: expression of gene Avy that causes the “agouti” phenotype (yellow fur coat and obesity) in mice is enhanced by maternal epigenetic modification (Rakyan et al. 2003), while paternal mutations at the other locus, MommeD4, contribute to a reverse phenotypic pattern in the offspring (Rakyan et al. 2003). The epigenetic state of the murine AxinFu allele is both maternally and paternally inherited (Rakyan et al. 2003).Focusing selection on haploids reduces the number of genotypes that need to be taken into account, while preserving the main properties of the multilocus system. Genes with haploid expression and a potential of parental effects can be found in two major taxonomic kingdoms. A notable candidate is Spam1 in mice, which is expressed during spermogenesis and encodes a factor that enables sperm to penetrate the egg cumulus (Zheng et al. 2001). This gene remains a target for effectively haploid selection, because its product is not shared via cytoplasm bridges between developing spermatides. Mutations at Spam1 alter performance of the male gametes that carry it and might indirectly, perhaps by altering the timing of fertilization, affect the fitness of the zygote. The highest estimated number of mouse genes expressed in the male gametes is currently 2375 (Joseph and Kirkpatrick 2004), and one might expect some of them to have similar paternal effects. Plants go through a profound haploid stage in their life cycles, and genes involved at this stage have an inevitable effect on the fitness of the future generations. In angiosperms, seed development is known to be controlled by both maternal (Chaudhury and Berger 2001; Yadegari and Drews 2004) and paternal (Nowack et al. 2006) effect genes, expressed, respectively, in female and male gametophytes.Under haploid selection, there can be no overdominance, and thus polymorphism is much more difficult to maintain than in diploid selection models (summarized in Feldman 1971). Nevertheless, differential or antagonistic selection between sexes can lead to a new class of stable internal equilibria in the diploid systems (Owen 1953; Bodmer 1965; Mandel 1971; Kidwell et al. 1977; Reed 2007), and I make use of this property in the haploid models developed below. In the experiment by Chippindale and colleagues (Chippindale et al. 2001), ∼75% of the total fitness variation in the adult stage of Drosophila melanogaster was negatively correlated between males and females, which suggests that a substantial portion of the fruit fly expressed genome is under sexually antagonistic selection. I assume that the effect of either parent on the fitness of the individual depends on the sex of the latter, which in respect to modeling is equivalent to the assumption of differential viability between the sexes in the progeny of the same parent(s). Biological systems that satisfy the latter assumptions can be found among colonial green algae: many members of the order Volvocales are haploid except for the short zygotic stage, and during sexual reproduction, they are also dioecious and anisogametic. I return to this example in the discussion. The possibility that genes expressed in animal gametes may be under antagonistic selection between sexes has been discussed (Bernasconi et al. 2004). For example, a (hypothetical) mutation increasing the ATP production in mitochondria would be beneficial in sperm, because of the increased mobility of the latter, but neutral or detrimental in the egg, due to a higher level of oxidative damage to DNA (Zeh and Zeh 2007).My main purpose was to derive conditions for existence and stability of the internal equilibria of the model(s). I begin with a simple one-locus case, which can be analyzed explicitly, and show how these one-locus results can be extended to the case of two recombining loci with multiplicative fitness. Then, I assume an additive relation between the maternal and paternal effect parameters and study the special cases where parental effects are symmetric. 相似文献
TABLE 1
Frequencies of genotypes and fitness parameterizations in model 1Gametes/haploids | Frequency before selection | Fitness
| ||
---|---|---|---|---|
Zygote | Male | Female | ||
(A)A | A | pfpm | 1 − α | 1 − δ |
(A)a | 1/2 A 1/2 a | pf(1 − pm) | 1 | 1 |
(a)A | 1/2 a 1/2 A | (1 − pf)pm | 1 − α | 1 − δ |
(a)a | A | (1 − pf)(1 − pm) | 1 | 1 |
TABLE 2
Offspring genotypic proportions from different mating types, sorted among four phenotypic groups/combinations of maternal and paternal effects: model 2Offspring genotypes/phenotypes
| |||||||||
---|---|---|---|---|---|---|---|---|---|
Parental genotypes
| Paternal (φ = 1)
| Joint (φ = 4)
| |||||||
Male | Female | AB | Ab | aB | Ab | AB | Ab | aB | ab |
AB | AB | 1 | |||||||
Ab | |||||||||
aB | |||||||||
ab | (1−r)/2 | r/2 | r/2 | (1−r)/2 | |||||
Ab | AB | ||||||||
Ab | 1 | ||||||||
aB | r/2 | (1−r)/2 | (1−r)/2 | r/2 | |||||
ab | |||||||||
Offspring genotypes/phenotypes
| |||||||||
Parental genotypes
| Maternal (φ = 2)
| None (φ = 3)
| |||||||
Male | Female | AB | Ab | aB | Ab | AB | Ab | aB | ab |
aB | AB | ||||||||
Ab | r/2 | (1 − r)/2 | (1 − r)/2 | r/2 | |||||
aB | 1 | ||||||||
ab | |||||||||
ab | AB | (1 − r)/2 | (1 − r)/2 | ||||||
Ab | |||||||||
aB | |||||||||
ab | 1 |
3.
Adaptive Divergence in Experimental Populations of Pseudomonas fluorescens. IV. Genetic Constraints Guide Evolutionary Trajectories in a Parallel Adaptive Radiation
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Michael J. McDonald Stefanie M. Gehrig Peter L. Meintjes Xue-Xian Zhang Paul B. Rainey 《Genetics》2009,183(3):1041-1053
The capacity for phenotypic evolution is dependent upon complex webs of functional interactions that connect genotype and phenotype. Wrinkly spreader (WS) genotypes arise repeatedly during the course of a model Pseudomonas adaptive radiation. Previous work showed that the evolution of WS variation was explained in part by spontaneous mutations in wspF, a component of the Wsp-signaling module, but also drew attention to the existence of unknown mutational causes. Here, we identify two new mutational pathways (Aws and Mws) that allow realization of the WS phenotype: in common with the Wsp module these pathways contain a di-guanylate cyclase-encoding gene subject to negative regulation. Together, mutations in the Wsp, Aws, and Mws regulatory modules account for the spectrum of WS phenotype-generating mutations found among a collection of 26 spontaneously arising WS genotypes obtained from independent adaptive radiations. Despite a large number of potential mutational pathways, the repeated discovery of mutations in a small number of loci (parallel evolution) prompted the construction of an ancestral genotype devoid of known (Wsp, Aws, and Mws) regulatory modules to see whether the types derived from this genotype could converge upon the WS phenotype via a novel route. Such types—with equivalent fitness effects—did emerge, although they took significantly longer to do so. Together our data provide an explanation for why WS evolution follows a limited number of mutational pathways and show how genetic architecture can bias the molecular variation presented to selection.UNDERSTANDING—and importantly, predicting—phenotypic evolution requires knowledge of the factors that affect the translation of mutation into phenotypic variation—the raw material of adaptive evolution. While much is known about mutation rate (e.g., Drake et al. 1998; Hudson et al. 2002), knowledge of the processes affecting the translation of DNA sequence variation into phenotypic variation is minimal.Advances in knowledge on at least two fronts suggest that progress in understanding the rules governing the generation of phenotypic variation is possible (Stern and Orgogozo 2009). The first stems from increased awareness of the genetic architecture underlying specific adaptive phenotypes and recognition of the fact that the capacity for evolutionary change is likely to be constrained by this architecture (Schlichting and Murren 2004; Hansen 2006). The second is the growing number of reports of parallel evolution (e.g., Pigeon et al. 1997; ffrench-Constant et al. 1998; Allender et al. 2003; Colosimo et al. 2004; Zhong et al. 2004; Boughman et al. 2005; Shindo et al. 2005; Kronforst et al. 2006; Woods et al. 2006; Zhang 2006; Bantinaki et al. 2007; McGregor et al. 2007; Ostrowski et al. 2008)—that is, the independent evolution of similar or identical features in two or more lineages—which suggests the possibility that evolution may follow a limited number of pathways (Schluter 1996). Indeed, giving substance to this idea are studies that show that mutations underlying parallel phenotypic evolution are nonrandomly distributed and typically clustered in homologous genes (Stern and Orgogozo 2008).While the nonrandom distribution of mutations during parallel genetic evolution may reflect constraints due to genetic architecture, some have argued that the primary cause is strong selection (e.g., Wichman et al. 1999; Woods et al. 2006). A means of disentangling the roles of population processes (selection) from genetic architecture is necessary for progress (Maynard Smith et al. 1985; Brakefield 2006); also necessary is insight into precisely how genetic architecture might bias the production of mutations presented to selection.Despite their relative simplicity, microbial populations offer opportunities to advance knowledge. The wrinkly spreader (WS) morphotype is one of many different niche specialist genotypes that emerge when experimental populations of Pseudomonas fluorescens are propagated in spatially structured microcosms (Rainey and Travisano 1998). Previous studies defined, via gene inactivation, the essential phenotypic and genetic traits that define a single WS genotype known as LSWS (Spiers et al. 2002, 2003) (Figure 1). LSWS differs from the ancestral SM genotype by a single nonsynonymous nucleotide change in wspF. Functionally (see Figure 2), WspF is a methyl esterase and negative regulator of the WspR di-guanylate cyclase (DGC) (Goymer et al. 2006) that is responsible for the biosynthesis of c-di-GMP (Malone et al. 2007), the allosteric activator of cellulose synthesis enzymes (Ross et al. 1987). The net effect of the wspF mutation is to promote physiological changes that lead to the formation of a microbial mat at the air–liquid interface of static broth microcosms (Rainey and Rainey 2003).Open in a separate windowFigure 1.—Outline of experimental strategy for elucidation of WS-generating mutations and their subsequent identity and distribution among a collection of independently evolved, spontaneously arising WS genotypes. The strategy involves, first, the genetic analysis of a specific WS genotype (e.g., LSWS) to identify the causal mutation, and second, a survey of DNA sequence variation at specific loci known to harbor causal mutations among a collection of spontaneously arising WS genotypes. For example, suppressor analysis of LSWS using a transposon to inactivate genes necessary for expression of the wrinkly morphology delivered a large number of candidate genes (top left) (Spiers et al. 2002). Genetic and functional analysis of these candidate genes (e.g., Goymer et al. 2006) led eventually to the identity of the spontaneous mutation (in wspF) responsible for the evolution of LSWS from the ancestral SM genotype (Bantinaki et al. 2007). Subsequent analysis of the wspF sequence among 26 independent WS genotypes (bottom) showed that 50% harbored spontaneous mutations (of different kinds; see Open in a separate windowFigure 2.—Network diagram of DGC-encoding pathways underpinning the evolution of the WS phenotype and their regulation. Overproduction of c-di-GMP results in overproduction of cellulose and other adhesive factors that determine the WS phenotype. The ancestral SBW25 genome contains 39 putative DGCs, each in principle capable of synthesizing the production of c-di-GMP, and yet WS genotypes arise most commonly as a consequence of mutations in just three DGC-containing pathways: Wsp, Aws, and Mws. In each instance, the causal mutations are most commonly in the negative regulatory component: wspF, awsX, and the phosphodiesterase domain of mwsR (see text).To determine whether spontaneous mutations in wspF are a common cause of the WS phenotype, the nucleotide sequence of this gene was obtained from a collection of 26 spontaneously arising WS genotypes (WSA-Z) taken from 26 independent adaptive radiations, each founded by the same ancestral SM genotype (Figure 1): 13 contained mutations in wspF (Bantinaki et al. 2007). The existence of additional mutational pathways to WS provided the initial motivation for this study.
Open in a separate windowaP206Δ(8) indicates a frameshift; the number of new residues before a stop codon is reached is in parentheses.bSuppressor analysis implicates the wsp locus (17 transposon insertions were found in this locus). However, repeated sequencing failed to identify a mutation.Here we define and characterize two new mutational routes (Aws and Mws) that together with the Wsp pathway account for the evolution of 26 spontaneously arising WS genotypes. Each pathway offers approximately equal opportunity for WS evolution; nonetheless, additional, less readily realized genetic routes producing WS genotypes with equivalent fitness effects exist. Together our data show that regulatory pathways with specific functionalities and interactions bias the molecular variation presented to selection. 相似文献
TABLE 1
Mutational causes of WSWS genotype | Gene | Nucleotide change | Amino acid change | Source/reference |
---|---|---|---|---|
LSWS | wspF | A901C | S301R | Bantinaki et al. (2007) |
AWS | awsX | Δ100-138 | ΔPDPADLADQRAQA | This study |
MWS | mwsR | G3247A | E1083K | This study |
WSA | wspF | T14G | I5S | Bantinaki et al. (2007) |
WSB | wspF | Δ620-674 | P206Δ (8)a | Bantinaki et al. (2007) |
WSC | wspF | G823T | G275C | Bantinaki et al. (2007) |
WSD | wspE | A1916G | D638G | This study |
WSE | wspF | G658T | V220L | Bantinaki et al. (2007) |
WSF | wspF | C821T | T274I | Bantinaki et al. (2007) |
WSG | wspF | C556T | H186Y | Bantinaki et al. (2007) |
WSH | wspE | A2202C | K734N | This study |
WSI | wspE | G1915T | D638Y | This study |
WSJ | wspF | Δ865-868 | R288Δ (3)a | Bantinaki et al. (2007) |
WSK | awsO | G125T | G41V | This study |
WSL | wspF | G482A | G161D | Bantinaki et al. (2007) |
WSM | awsR | C164T | S54F | This study |
WSN | wspF | A901C | S301R | Bantinaki et al. (2007) |
WSO | wspF | Δ235-249 | V79Δ (6)a | Bantinaki et al. (2007) |
WSP | awsR | 222insGCCACCGAA | 74insATE | This study |
WSQ | mwsR | 3270insGACGTG | 1089insDV | This study |
WSR | mwsR | T2183C | V272A | This study |
WSS | awsX | C472T | Q158STOP | This study |
WST | awsX | Δ229-261 | ΔYTDDLIKGTTQ | This study |
WSU | wspF | Δ823-824 | T274Δ (13)a | Bantinaki et al. (2007) |
WSV | awsX | T74G | L24R | This study |
WSW | wspF | Δ149 | L49Δ (1)a | Bantinaki et al. (2007) |
WSXb | ? | ? | ? | This study |
WSY | wspF | Δ166-180 | Δ(L51-I55) | Bantinaki et al. (2007) |
WSZ | mwsR | G3055A | A1018T | This study |
4.
Retrograde Intraflagellar Transport Mutants Identify Complex A Proteins With Multiple Genetic Interactions in Chlamydomonas reinhardtii
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The intraflagellar transport machinery is required for the assembly of cilia. It has been investigated by biochemical, genetic, and computational methods that have identified at least 21 proteins that assemble into two subcomplexes. It has been hypothesized that complex A is required for retrograde transport. Temperature-sensitive mutations in FLA15 and FLA17 show defects in retrograde intraflagellar transport (IFT) in Chlamydomonas. We show that IFT144 and IFT139, two complex A proteins, are encoded by FLA15 and FLA17, respectively. The fla15 allele is a missense mutation in a conserved cysteine and the fla17 allele is an in-frame deletion of three exons. The flagellar assembly defect of each mutant is rescued by the respective transgenes. In fla15 and fla17 mutants, bulges form in the distal one-third of the flagella at the permissive temperature and this phenotype is also rescued by the transgenes. These bulges contain the complex B component IFT74/72, but not α-tubulin or p28, a component of an inner dynein arm, which suggests specificity with respect to the proteins that accumulate in these bulges. IFT144 and IFT139 are likely to interact with each other and other proteins on the basis of three distinct genetic tests: (1) Double mutants display synthetic flagellar assembly defects at the permissive temperature, (2) heterozygous diploid strains exhibit second-site noncomplemention, and (3) transgenes confer two-copy suppression. Since these tests show different levels of phenotypic sensitivity, we propose they illustrate different gradations of gene interaction between complex A proteins themselves and with a complex B protein (IFT172).CILIA and flagella are microtubule-based organelles that are found on most mammalian cells. They provide motility to cells and participate in many sensory processes. Defects in or loss of cilia/flagella cause a variety of human diseases that include polycystic kidney disease, retinal degeneration, infertility, obesity, respiratory defects, left–right axis determination, and polydactyly (Fliegauf et al. 2007). Mouse mutants demonstrate that cilia are essential for viability, neural tube closure, and bone development (Eggenschwiler and Anderson 2007; Fliegauf et al. 2007). Cilia and flagella are also present in protists, algae, moss, and some fungi.The assembly and maintenance of cilia and flagella require intraflagellar transport (IFT) (Kozminski et al. 1995). IFT involves the movement of 100- to 200-nm-long protein particles from the basal body located in the cell body to the tip of the flagella using the heterotrimeric kinesin-2 (anterograde movement) (Kozminski et al. 1995) and movement back to the cell body (retrograde movement) using the cytoplasmic dynein complex (Pazour et al. 1999; Porter et al. 1999). IFT particles change their direction of movement as well as their size, speed, and frequency at the ends of the flagella as they switch from anterograde to retrograde movement (Iomini et al. 2001). Biochemical isolation of IFT particles reveals that they are composed of at least 16 proteins and that these particles can be dissociated into two complexes in vitro by changing the salt concentration (Cole et al. 1998; Piperno et al. 1998). Recent genetic and bioinformatics analysis adds at least 7 more proteins to the IFT particle (Follit et al. 2009) (Eggenschwiler and Anderson 2007).
Open in a separate window—, no mutant found to date in Chlamydomonas.A collection of temperature-sensitive mutant strains that fail to assemble flagella at the restrictive temperature of 32° was isolated in Chlamydomonas (Huang et al. 1977; Adams et al. 1982; Piperno et al. 1998; Iomini et al. 2001). Analysis of the flagella at 21° permits the measurement of the velocity and frequency of IFT particles in the mutant strains. This analysis suggested that assembly has four phases: recruitment to the basal body, anterograde movement (phases I and II), retrograde movement, and return to the cytoplasm (phases III and IV) (Iomini et al. 2001). Different mutants were classified as defective in these four phases. However, because different alleles of FLA8 were classified as defective in different phases (Iomini et al. 2001; Miller et al. 2005), we combined mutants with IFT defects into just two classes. The first group (phases I and II) includes mutant strains that show decreased anterograde velocities, a decreased ratio of anterograde to retrograde particles, and an accumulation of complex A proteins at the basal body. This group includes mutations in the FLA8 and FLA10 genes, which encode the two motor subunits of kinesin-2 (Walther et al. 1994; Miller et al. 2005), as well as mutations in three unknown genes (FLA18, FLA27, and FLA28). The second group includes mutant strains that show the reciprocal phenotype (phases III and IV); these phenotypes include decreased retrograde velocities, an increased ratio of anterograde to retrograde particles, and an accumulation of complex B proteins in the flagella. With the exception of the FLA11 gene, which encodes IFT172, a component of complex B (Pedersen et al. 2005), the gene products in this class are unknown (FLA2, FLA15, FLA16, FLA17, and FLA24). One might predict that mutations in this group would map to genes that encode complex A or retrograde motor subunits. Interestingly, IFT particles isolated from fla11, fla15, fla16, and fla17-1 flagella show depletion of complex A polypeptides (Piperno et al. 1998; Iomini et al. 2001). The inclusion of IFT172 in this class is explained by the observations that IFT172 plays a role in remodeling the IFT particles at the flagellar tip to transition from anterograde to retrograde movement (Pedersen et al. 2005). The remaining mutant strains do not show obvious defects in velocities, ratios, or accumulation at 21° and may reflect a less severe phenotype at the permissive temperature or a non-IFT role for these genes.Direct interactions occur between components of complex B. IFT81 and IFT74/72 interact to form a scaffold required for IFT complex B assembly (Lucker et al. 2005). IFT57 and IFT20 also interact with each other and kinesin-2 (Baker et al. 2003). While physical interactions are being used to define IFT particle architecture, genetic interactions among loci encoding IFT components should be instructive regarding their function as well. To probe retrograde movement and its function, we have identified the gene products encoded by two retrograde defective mutant strains. They are FLA15 and FLA17 and encode IFT144 and IFT139, respectively. The genetic interactions of these loci provide interesting clues about the assembly of the IFT particles and possible physical interactions in the IFT particles. 相似文献
TABLE 1
Proteins and gene names for the intraflagellar transport particles in Chlamydomonas, C. elegans, and mouseProtein | Motif | Chlamydomonas gene | C. elegans gene | Mouse gene | References to worm and mouse genes |
---|---|---|---|---|---|
Complex A | |||||
IFT144 | WD | FLA15 | |||
IFT140 | WD | — | che-11 | Qin et al. (2001) | |
IFT139 | TRP | FLA17 | dyf-2 | THM1 | Efimenko et al. (2006); Tran et al. (2008) |
IFT122 | WD | — | IFTA-1 | Blacque et al. (2006) | |
IFT121 | WD | — | daf-10 | Bell et al. (2006) | |
IFT43 | — | ||||
Complex B | |||||
IFT172 | WD | FLA11 | osm-1 | Wimple | Huangfu et al. (2003); Pedersen et al. (2005); Bell et al. (2006) |
IFT88 | TRP | IFT88 | osm-5 | Tg737/Polaris | Pazour et al. (2000); Qin et al. (2001) |
IFT81 | Coil | — | ift-81 | CDV1 | Kobayashi et al. (2007) |
IFT80 | WD | — | che-2 | Wdr56 | Fujiwara et al. (1999) |
IFT74/72 | Coil | — | ift-74 | Cmg1 | Kobayashi et al. (2007) |
IFT57/55 | Coil | — | che-13 | Hippi | Haycraft et al. (2003) |
IFT54 | Microtubule binding domain MIP-T3 | — | dyf-11 | Traf3IP1 | Kunitomo and Iino (2008); Li et al. (2008); Omori et al. (2008); Follit et al. (2009) |
IFT52 | ABC type | BLD1 | osm-6 | Ngd2 | Brazelton et al. (2001); Bell et al. (2006) |
IFT46 | IFT46 | dyf-6 | Bell et al. (2006); Hou et al. (2007) | ||
IFT27 | G protein | — | Not present | Rabl4 | |
IFT25 | Hsp20 | — | Not present | HSP16.1 | Follit et al. (2009) |
IFT22 | G protein | — | IFTA-2 | Rabl5 | Schafer et al. (2006) |
IFT20 | Coil | — | Follit et al. (2006) | ||
FAP22 | Cluamp related protein | — | dyf-3 | Cluamp1 | Murayama et al. (2005); Follit et al. (2009) |
DYF13 | — | dyf-13 | Ttc26 | Blacque et al. (2005) |
5.
Evolutionary Strata in a Small Mating-Type-Specific Region of the Smut Fungus Microbotryum violaceum
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DNA sequence analysis and genetic mapping of loci from mating-type-specific chromosomes of the smut fungus Microbotryum violaceum demonstrated that the nonrecombining mating-type-specific region in this species comprises ∼25% (∼1 Mb) of the chromosome length. Divergence between homologous mating-type-linked genes in this region varies between 0 and 8.6%, resembling the evolutionary strata of vertebrate and plant sex chromosomes.EVOLUTION of mating types or sex-determining systems often involves the suppression of recombination around the primary sex-determining or mating-type-determining locus. In animals and plants, it is often an entire or almost entire chromosome (Y or W in male or female heterogametic species, respectively) that ceases to recombine with its homologous (X or Z) chromosome (Charlesworth and Charlesworth 2000; Charlesworth 2008). Self-incompatibility loci in plants are also thought to be located in regions of suppressed recombination (Charlesworth et al. 2005; Kamau and Charlesworth 2005; Kamau et al. 2007; Li et al. 2007; Yang et al. 2007). Regardless of the phylogenetic position of a species, such nonrecombining regions are known to follow similar evolutionary trajectories. The nonrecombining region on the sex-specific chromosome expands in several steps, forming evolutionary strata—regions of different X/Y (or Z/W) divergence (Lahn and Page 1999; Handley et al. 2004; Sandstedt and Tucker 2004; Nicolas et al. 2005)—and genes in the nonrecombining regions gradually accumulate deleterious mutations that eventually render them dysfunctional (Charlesworth and Charlesworth 2005; Charlesworth 2008).Fungal mating-type systems are very diverse, with the number of mating types varying from two to several hundred (Casselton 2002). Like sex chromosomes in several animals and plants, suppressed recombination has evolved in regions near fungal mating-type loci, including in Ustilago hordei (Lee et al. 1999), Cryptococcus neoformans (Lengeler et al. 2002), and Neurospora tetrasperma (Menkis et al. 2008). These species have two mating types, but no morphologically distinct sexes. The mating-type locus (the region of suppressed recombination) of C. neoformans is small (∼100 kb) compared with known sex chromosomes and contains only ∼20 genes that, unlike many sex chromosomes (Y or W chromosomes), show no obvious signs of genetic degeneration (Lengeler et al. 2002; Fraser et al. 2004). Judging from the divergence between the homologous genes on the two mating-type-specific chromosomes, C. neoformans started to evolve sex chromosomes a long time ago because silent divergence between the two mating types in the most ancient region exceeds 100% (Fraser et al. 2004). Genes in the younger mating-type-specific region are much less diverged between the two sex chromosomes, suggesting that the evolution of the sex locus in C. neoformans might have proceeded through several steps. The nonrecombining region around the mating-type locus of N. tetrasperma is much larger than in C. neoformans (at least 6.6 Mb), and silent divergence between homologous genes on the mating-type-specific chromosomes ranges from zero to 9%, demonstrating that these mating-type-specific chromosomes evolved recently (Menkis et al. 2008).M. violaceum, which causes anther smut disease in Silene latifolia and other species in the family Caryophyllaceae, has two mating types, A1 and A2 (reviewed by Giraud et al. 2008), which are determined by the presence of mating-type-specific chromosomes (hereafter A1 and A2 chromosomes, or sex chromosomes) in the haploid stage of the life cycle (Hood 2002; Hood et al. 2004). The A1 and A2 chromosomes are distinguishable by size in pulsed-field electrophoresis, and it is possible to isolate individual chromosomes electrophoretically (Hood et al. 2004). Random fragments of A1 and A2 chromosomes have previously been isolated from mating-type-specific bands of pulsed-field separated chromosomes of M. violaceum (Hood et al. 2004). These fragments were assumed to be linked to mating type. The same method was used to isolate fragments of non-mating-type-specific chromosomes. On the basis of the analysis of their sequences, (Hood et al. 2004) proposed that mating-type-specific chromosomes in M. violaceum might be degenerate because they contained a lower proportion of protein-coding genes than other chromosomes. However, it was not determined whether the sequences isolated from the mating-type chromosomes originated from the mating-type-specific or from the recombining regions (Hood et al. 2004), and the relative sizes of these regions are not known for these M. violaceum chromosomes. We tested the mating-type specificity of 86 of these fragments and demonstrate that fewer than a quarter of these loci are located in the mating-type-specific region, suggesting that the nonrecombining region on the A1 and A2 chromosomes is quite small, while the rest of the chromosome probably recombines (like pseudoautosomal regions of sex chromosomes) and is therefore not expected to undergo genetic degeneration. Genetic mapping confirms the presence of two pseudoautosomal regions in the M. violaceum mating-type-specific chromosomes.As these chromosomes are mating type specific in the haploid stage of M. violaceum, mating-type-specific loci (or DNA fragments) can be identified by testing whether they are present exclusively in A1 or A2 haploid strains. We therefore prepared haploid A1 and A2 M. violaceum cultures from S. latifolia plants from two geographically remote locations (accessions Sl405 from Sweden and Sl127 from the French Pyrenees). Haploid sporidial cultures were isolated by a standard dilution method (Kaltz and Shykoff 1997; Oudemans and Alexander 1998). Mating types were determined by PCR amplification of each culture with primers designed for A1 and A2 pheromone receptor genes linked to A1 and A2 mating types (Yockteng et al. 2007). The primers were as follows: 5′-TGGCATCCCTCAATGTTTCC-3′ and 5′-CACCTTTTGATGAGAGGCCG-3′ for the A1 pheromone receptor (GenBank accession no. ) and 5′-TGACGAGAGCATTCCTACCG-3′ and 5′-GAAGCGGAACTTGCCTTTCT-3′ for the A2 pheromone receptor (GenBank accession no. EF584742). Cultures with PCR product amplified only from an A1 or A2 pheromone receptor gene were selected for further use. The mating types of the cultures were verified by conjugating them in all combinations.The GenBank nucleotide database was searched using BLAST for sequences similar to those isolated by EF584741Hood et al. (2004). Sequences with similarity to transposable elements (TE) and other repeats were excluded. The resulting set of nonredundant sequences was used to design PCR primers for 98 fragments. Half of these were originally isolated from the A1 and half from the A2 chromosomes and are hereafter called A1-NNN or A2-NNN (where NNN is the locus number; supporting information, Table S1), which does not imply that these loci are A1 or A2 specific, but merely indicates that they were originally isolated from the A1 or A2 chromosomes. Amplification of these regions from new A1 and A2 M. violaceum cultures, independently isolated by ourselves, revealed that only 5 of the 49 loci isolated from the A1 chromosome are indeed A1 specific and only 6 of 49 isolated from the A2 chromosome are A2 specific. All other loci amplified from both A1 and A2 cultures. Figure 1 illustrates some of these results from the Swedish sample (Sl405).Open in a separate windowFigure 1.—Testing of mating-type specificity for loci isolated from A1 and A2 chromosomes. (a) PCR amplifications from haploid cultures from Sl405 using primers designed from six A1-originated loci. Loci in which a PCR product could be amplified only from A1 cultures (boxed) were classified as specific to mating type A1. (b) PCR tests of six A2-originated loci on the same set of haploids as in a. Loci in which a PCR product amplified only from A2 cultures (boxed) were classified as specific to mating type A2. Loci amplified from both A1 and A2 cultures are not mating type specific.The fragments that amplified from both A1 and A2 mating types may be in recombining regions, or they could be present in mating-type-specific regions on both A1 and A2 chromosomes. If they are in recombining regions, the A1- and A2-linked homologs should not be diverged from each other, but if they are in nonrecombining, mating-type-specific regions, the divergence of the A1- and A2-linked homologs should be roughly proportional to the time since recombination stopped in the region. We therefore sequenced and compared PCR fragments amplified from the two mating types of Sl405 or Sl127 cultures (GenBank accession nos. – FI855822). Sequencing of PCR products showed that 12 (4 A1 and 8 A2) loci have more than one copy, and they were excluded from further analysis. Sequences of 61 loci were identical between the A1 and A2 strains, and four loci demonstrated low total divergence (0.24–0.61%) between the two mating types ( FI856001otintseva and D. Filatov, unpublished results). Thus, these loci might be located in the recombining part of the mating-type-specific chromosomes. Ten of 75 loci that amplified in both mating types demonstrated multiple polymorphisms fixed between the mating types rather than between the locations. Given that the strains that we used in the analysis originated from two geographically distant locations, it is highly unlikely that multiple polymorphisms distinguishing the A1 and A2 sequences arose purely by chance; thus, these loci are probably located in the nonrecombining mating-type-specific region of the M. violaceum A1 and A2 chromosomes.
Open in a separate windowaA1, loci originated from the A1 sex chromosome; A2, loci originated from the A2 sex chromosome.bThe number of loci used for genetic map construction is in parentheses.To confirm the mating-type-specific or pseudoautosomal locations of the loci with and without A1/A2 divergence, we conducted genetic mapping in a family of 99 individuals, 50 of which were of mating type A1 and 49 of mating type A2. The family was generated by a cross between A1 and A2 M. violaceum strains from S. latifolia accessions Sl405 (Sweden) and Sl127 (France), respectively. The choice of strains from geographically distant locations was motivated by the hope of maximizing the number of DNA sequence differences between them that can be used as molecular genetic markers in segregation analysis. We inoculated S. latifolia seedlings with sporidial cultures of both mating types. For inoculation, petri dishes with 12-day-old seedlings of S. latifolia were flooded with 2.5 ml of inoculum suspension. Inoculum suspension consisted of equal volumes of the A1 and A2 sporidial cultures that were mixed and conjugated overnight at 14° under rotation (Biere and Honders 1996; Van Putten et al. 2003). Seedlings were potted 3 days after inoculation. Two months later, teliospores were collected from the flowers of the infected plant and grown in petri dishes on 3.6% potato dextrose agar medium. Haploid sporidia formed after meiosis were isolated and grown as separate cultures for DNA extraction. The mating types of single sporidia cultures were identified as described above. The loci analyzed in the segregation analysis were sequenced in the two parental haploid strains and in 99 (50 A1 and 49 A2) haploid strains that were generated in the cross. Single nucleotide differences between the parental strains were used as molecular genetic markers for segregation analysis in the progeny. The genetic map was constructed using MAPMAKER/EXP v3.0 (Lincoln et al. 1992) and MapDisto v1.7 (http://mapdisto.free.fr/).The resulting genetic map is shown in Figure 2. As expected, no recombination was observed between the 10 loci with diverged A1- and A2-linked copies. In addition, one marker with no A1/A2 divergence, A2-397, was also completely linked to the loci with significant A1/A2 divergence. This locus either may be very tightly linked to the nonrecombining mating-type-specific region or may have been added to that region more recently than the loci that had already accumulated some divergence between the alleles in the two mating types. The mating-type-specific pheromone receptor locus (Devier et al. 2009) and 11 mating-type-specific loci are also located in this nonrecombining region (Figure 2). Interestingly, the cluster of nonrecombining markers is flanked on both sides with markers that recombine in meiosis, demonstrating that there are pseudoautosomal regions on both ends of the mating-type-specific chromosomes.Open in a separate windowFigure 2.—Genetic map of the mating-type-determining chromosome in M. violaceum. Genetic distance (in centimorgans) and the relative positions of the markers are shown to the left and the right of the chromosome, respectively. The position of the nonrecombining region corresponds to the cluster of linked markers shown on the right of the figure. Total A1/A2 divergence is shown in parentheses. Eleven mating-type-specific markers (for which sequences are available from only one mating type), located in the nonrecombining mating-type-specific region, are not shown.Our results demonstrate that although the loci reported by Hood et al. (2004) were isolated from the A1 and A2 chromosomes, most of these loci are not located in the nonrecombining mating-type-specific regions. In fact, the nonrecombining region might be relatively small: of 86 tested fragments, only 21 appeared to be either mating type specific or linked to the mating-type locus. Assuming that these loci represent a random set of DNA fragments isolated from the A1 and A2 chromosomes, it is possible to estimate the size of the nonrecombining region using the binomial distribution: the nonrecombining region is expected to be 24.4% (95% CI: 16.7–33.6%) of the chromosome length. As the sizes of the A1 and A2 chromosomes are ∼3.4 and 4.2 Mb long (Hood 2002; Hood et al. 2004), the nonrecombining region might be ∼1 Mb long.Interestingly, total A1/A2 divergence for the 11 loci with A1- and A2-linked copies mapped to the nonrecombining region varied from 0% to 8.6% (Figure 2). In addition, 11 loci amplified from only one mating type. These genes could represent degenerated genes, some of which degenerated in A1 strains, and some in A2 strains. Alternatively, they might be highly diverged genes, such that the PCR primers amplify only one allele, and not the other. Variation in divergence may be the result of the stepwise cessation of recombination between the A1 and A2 chromosomes in M. violaceum, resembling the evolutionary strata reported for human, chicken, and white campion sex chromosomes (Lahn and Page 1999; Handley et al. 2004; Bergero et al. 2007). However, only the differences between the most and the least diverged loci are statistically significant (Devier et al. 2009), the M. violaceum mating-type region has at least three strata: one oldest stratum, including the pheromone receptor locus; a younger stratum with ∼5–9% A1/A2 divergence; and the youngest stratum with 1–4% divergence between the two mating types. There may also be an additional very recently evolved stratum containing the locus named A2-397, which is also present in all A1 strains tested, with no fixed differences between the A1 and A2 strains (No. of sites analyzed Within A1
Within A2
Fixed differences between A1 and A2 A1/A2 divergence (%) Locia Sb total S π (%)c S π (%)c A1/A2 divergence <1% A1-236 456 3 0 0 2 0.44 1 0.44 A1-045 654 4 0 0 0 0 4 0.61 A2-568 413 2 2 0.48 2 0.48 0 0.24 A2-411 480 2 1 0.21 0 0 1 0.31 A1/A2 divergence >1% A1-217 667 9 0 0 0 0 9 1.35 A1-128 569 9 0 0 1 0.18 8 1.49 A1-199 618 13 0 0 1 0.16 12 2.02 A2-422 344 9 0 0 0 0 9 2.62 A2-516 470 14 0 0 0 0 14 2.98 A2-404 508 20 0 0 3 0.59 17 3.64 A2-435 506 22 2 0.39 2 0.39 18 3.95 A2-473 457 23 1 0.22 1 0.22 21 4.81 A2-457 303 17 1 0.33 0 0 16 5.54 A2-575 503 47 5 0.99 3 0.59 39 8.55
TABLE 1
Loci from mating-type-specific chromosomes of M. violaceum used for PCR analysis and genetic map constructionWith nonzero A1/A2 divergenceb
| |||||
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Loci | Mating type specific | <1% | >1% | With zero A1/A2 divergenceb | Total |
A1a | 5 | 2 (1) | 3 (3) | 35 (3) | 45 (7) |
A2a | 6 | 2 (0) | 7 (7) | 26 (3) | 41 (10) |
Subtotal | 4 (1) | 10 (10) | |||
Total | 11 | 14 (11) | 61 (6) | 86 (17) |