The Regulatory Functions of the rolB and rolC Genes of Agrobacterium rhizogenes are Conserved in the Homologous Genes (Ngrol) of Nicotiana glauca in Tobacco Genetic Tumors

To compare patterns of expression between the Ngrol genes ofN. glauca and the Rirol genes of Agrobacterium rhizogenes, weperformed fluorometric and histochemical analysis of transgenicgenetic tumors on the hybrid of Nicotiana glauca x N. langsdorffü(Fl) that harbored a rß- glucuronidase (GUS) reportergene fused to the promoter of NgrolB, NgrolC, RirolB or RirolC The promoters of NgrolB and NgrolCNgrolC had 2- to 3-fold loweractivity than those of RirolB and RirolC However, the changesin patterns of GUS activity caused by deletion of NgrolB andNgrolCpromoters were similar to those of RirolB and RirolC promoters.This result suggests that the cis-acting sequences that regulatethe level of expression of RirolB and RirolC are conserved inthe NgrolB and NgrolC promoters. Furthermore, an auxin dependent(NAA-dependent) increase in GUS activity was observed in thecase of NgrolB-GUS and RirolB-GUS. Histochemical analysis showedGUS activity encoded by both NgrolB-GUS and RirolB-GUS in normal-typeFl transgenic plants was located in meristematic zones, whilethat encoded by NgrolC-GUS and RirolC-GUS was detected mainlyin vascular systems of various organs. Thus, the patterns ofexpression of the Ngrol genes were the same as those of theRirol genes in terms of promotion by auxin and tissue-specificity,indicating that regulatory mechanisms for both sets of geneshave been conserved during the evolution of the genus Nicotianaafter transfer from a progenitor of Agrobacterium to that ofNicotiana. (Received May 2, 1995; Accepted June 13, 1995)     

Synergistic Function of rolB, rolC, ORF13 and ORF14 of TL-DNA of Agrobacterium rhizogenes in Hairy Root Induction in Nicotiana tabacum

Comparison of the frequency of rooting in the tobacco leaf segmentsinoculated with Agrobacterium tumefaciens harboring variouscombinations of rolB, rolC, ORF13 and ORF14 of TL-DNA of Riplasmid (pRiHRI) revealed that the genes differ in their functionto stimulate adventitious root induction. A single gene rolBinduced roots, while rolC, ORF13 and ORF14 independently promotedthe root induction by the rolB gene. The effects of these geneson the rolB-mediated rooting were in the order of ORF13>rolCORF14. Present address: Laboratory of Phylogenetic Botany, Departmentof Biology, Chiba University, 1-33 Yayoi-cho, Inage-ku, Chiba,263-8522 Japan. ² Present address: Department of Chemical and Biological Sciences,Faculty of Science, Japan Women's University, 2-8-1 Mejirodai,Bunkyo-ku, Tokyo, 112-8681 Japan.     

Comparison of cleft palate induction by Nicotiana glauca in goats and sheep

The induction of cleft palate by Nicotiana glauca (wild tree tobacco) during the first trimester of pregnancy was compared between Spanish-type goats and crossbred western-type sheep. Cleft palate was induced in 100% of the embryonic/fetal goats when their pregnant mothers were gavaged with N. glauca plant material or with anabasine-rich extracts from the latter, during gestation days 32-41. Seventy-five percent of newborn goats had cleft palate after maternal dosing with N. glauca during gestation days 35-41, while no cleft palates were induced when dosing periods included days 36-40, 37-39, or day 38 only. The induced cleft palates were bilateral, involving the entire secondary palates with complete detachment of the vomer. Eleven percent of the newborn goats from does gavaged during gestation days 32-41 had extracranial abnormalities, most often contractures of the metacarpal joints. Most of these contractures resolved spontaneously by 4-6 weeks postpartum. One newborn kid also had an asymmetric skull due to apparent fetal positioning. No cleft palates were induced in lambs whose mothers were gavaged with N. glauca plant or anabasine-rich extracts during gestation days 34-41, 35-40, 35-41, 36-41, 35-51, or 37-50. Only one of five lambs born to three ewes gavaged with N. glauca plant material during gestation days 34-55 had a cleft palate, but all five of these lambs had moderate to severe contractures in the metacarpal joints. The slight to moderate contracture defects resolved spontaneously by 4-6 weeks postpartum, but the severe contractures resolved only partially. Embryonic/fetal death and resorption (determined by ultrasound) occurred in 25% of pregnant goats fed N. glauca compared to only 4% of pregnant sheep. Nicotiana glauca plant material contained the teratogenic alkaloid anabasine at 0.175% to 0.23%, dry weight, demonstrating that Spanish-type goats are susceptible to cleft palate induction by the natural toxin anabasine, while crossbred western-type sheep are resistant. However, clinical signs of toxicity were equally severe in goats and sheep, even though maternal alkaloid tolerance was generally lower in sheep. We postulate that an alkaloid-induced reduction in fetal movement during the period of normal palate closure is the cause of the cleft palate and multiple flexion contractures. Teratology 61:203-210, 2000. Published 2000 Wiley-Liss, Inc.     

Sequence of the cellular T-DNA in the untransformed genome of Nicotiana glauca that is homologous to ORFs 13 and 14 of the Ri plasmid and analysis of its expression in genetic tumors of N. glauca x N. langsdorffii

A region homologous to the TL-DNA of Agrobacterium rhizogenes was previously detected in the genome of untransformed Nicotiana glauca and designated cellular T-DNA (cT-DNA). Subsequently, part of this region was sequenced and two genes, which corresponded to rolB and rolC and were named NgrolB and NgrolC, were found. We have now sequenced a region of the cT-DNA other than the region that includes NgrolB and C and we have found two other open reading frames (ORFs), NgORF13 and NgORF14. These ORFs correspond to ORFs 13 and 14 of the TL-DNA of A. rhizogenes and exhibit a high degree of homology to these ORFs, without having a nonsense codon. We have not found any sequence homologous to rolD (ORF15). The two genes, NgORF13 and 14, as well as the NgrolB and C genes, are expressed in genetic tumors of hybrids between N. glauca and N. langsdorffii but not in leaf tissues of the hybrid.     

Initiation of auxin autonomy in Nicotiana glutinosa cells by the cytokinin-biosynthesis gene from Agrobacterium tumefaciens

Agrobacteria carrying mutations at the auxin-biosynthesizing loci (iaaH and iaaM of the Ti plasmid) induce shoot-forming tumors on many plant species. In some cases, e.g. Nicotiana glutinosa L., tumors induced by such mutant strains exhibit an unorganized and fully autonomous phenotype. These characteristics are stable in culture at both the tissue and cellular level. We demonstrate that the cytokinin-biosynthesis gene (ipt) of the Ti plasmid is responsble for the induction of both auxin and cytokinin autonomy in N. glutinosa. Cloned cell lines carrying an ipt gene but lacking iaaH and iaaM are capable of accumulating indole-3-acetic acid. Interestingly, non-transformed N. glutinosa tissues exhibit an auxin-requiring phenotype when they are grown on medium supplemented with an exogenous supply of cytokinin. These results strongly indicate that exogenously supplied cytokinin does not mimic all the effects of the expression of the ipt gene in causing the auxin-autonomous growth of N. glutinosa cells.Abbreviations FW fresh weight - IAA indole-3-acetic acid - I⁶ Ado isopentenyladenosine - kb kilobase - MS Murashige and Skoog (medium) - NAA -naphthaleneacetic acid - NAM -naphthaleneacetamide - T-DNA transferred DNA     

Single rol Genes from the Agrobacterium rhizogenes T(L)-DNA Alter Some of the Cellular Responses to Auxin in Nicotiana tabacum

Two kinds of cellular responses to auxin, the hyperpolarization of protoplasts and the division of protoplast-derived cells, were compared in Nicotiana tabacum plants transformed by different T-DNA fragments of Agrobacterium rhizogenes strain A4. Using transmembrane potential difference measurements to characterize hormonal sensitivity of mesophyll protoplasts, we found a 30-fold increase in sensitivity to auxin in protoplasts transformed by the whole Ri A4 T-DNA. Furthermore, the rol genes of the Ri A4 T_L-DNA, together or as single genes, were able to increase the sensitivity to auxin by factors up to 10⁴. The different effects of the single rol genes on the sensitivity of mesophyll protoplasts to auxin, rolB being the most powerful, were consistent with their respective rhizogenic effects on leaf fragments (A Spena, T Schmülling, C Koncz, J Schell [1987] EMBO J 6: 3891-3899). No difference was seen concerning the effects of auxin on division of cells derived from normal or transformed protoplasts. These results suggest that only some cellular responses to auxin could be selectively altered by rol genes. They also show that rol-transformed tobaccos can be a model system to study auxin action in plants.     

PRD-Class Homeobox Genes in Bovine Early Embryos: Function,Evolution, and Overlapping Roles

Eutherian Totipotent Cell Homeobox (ETCHbox) genes are mammalian-specific PRD-class homeobox genes with conserved expression in the preimplantation embryo but fast-evolving and highly divergent sequences. Here, we exploit an ectopic expression approach to examine the role of bovine ETCHbox genes and show that ARGFX and LEUTX homeodomain proteins upregulate genes normally expressed in the blastocyst; the identities of the regulated genes suggest that, in vivo, the ETCHbox genes play a role in coordinating the physical formation of the blastocyst structure. Both genes also downregulate genes expressed earlier during development and genes associated with an undifferentiated cell state, possibly via the JAK/STAT pathway. We find evidence that bovine ARGFX and LEUTX have overlapping functions, in contrast to their antagonistic roles in humans. Finally, we characterize a mutant bovine ARGFX allele which eliminates the homeodomain and show that homozygous mutants are viable. These data support the hypothesis of functional overlap between ETCHbox genes within a species, roles for ETCHbox genes in blastocyst formation and the change of their functions over evolutionary time.     

植物抗病基因结构、功能及其进化机制研究进展

植物与病原菌在长期的共进化和相互选择的过程中,逐渐形成了组织障碍、非寄主抗性和小种专化抗性等有效的防御机制。小种专化抗性(基因对基因抗性)主要是由植物抗病基因识别相应的病原菌无毒基因并激活植物体内抗病信号进而抵御病原菌的侵染。从目前已克隆的 70 多个抗病基因来看,它们在结构上具有高度保守性,主要包括核苷酸结合位点(NBS),亮氨酸重复结构(LRR), 蛋白激酶结构域(PK), 果蝇蛋白 Toll 和哺乳动物蛋白质白细胞介素 1 受体[interleukin(IL)-1 receptor]类似结构域(TIR), 双螺旋结构(CC)或亮氨酸拉链(LZ)和跨膜结构域(TM)等,其在抗病基因与病原菌无毒(效应)蛋白互作以及植物内部免疫信号传导中起着重要的作用。同时,抗病基因又通过基因复制、遗传重组等进化机制形成多基因家族,为植物抗病的专化性和多样性提供了重要的遗传基础。本文主要讨论了近来已克隆抗病基因的结构特征、功能以及抗病基因进化机制研究的进展。     

Missing Pieces of an Ancient Puzzle: Evolution of the Eukaryotic Membrane-Trafficking System

The membrane-trafficking system underpins cellular trafficking of material in eukaryotes and its evolution would have been a watershed in eukaryogenesis. Evolutionary cell biological studies have been unraveling the history of proteins responsible for vesicle transport and organelle identity revealing both highly conserved components and lineage-specific innovations. Recently, endomembrane components with a broad, but patchy, distribution have been observed as well, pieces that are missing from our cell biological and evolutionary models of membrane trafficking. These data together allow for new insights into the history and forces that shape the evolution of this critical cell biological system.A major feature of eukaryotic cells is subcompartmentalization. Specific components are concentrated within restricted regions of the cell, necessitating the presence of one or more targeting mechanisms. The eukaryotic membrane-trafficking system facilitates intracellular transport of proteins and lipids between organelles and further acts to build the interface between the cell and external environment. This system touches, at some level, virtually every cellular compartment and component; its proper function is crucial for modern eukaryotes.The establishment of the membrane-trafficking system represented a tremendous milestone in the restructuring that took place during the transition from the prokaryotic to eukaryotic cellular configuration. As it does today, a membrane-trafficking system would have enhanced the ability of even the earliest eukaryotes to remodel their cell surface, export proteins to modify their external environment by exocytosis, as well as acquire nutrients by endocytosis. Subcompartmentalization of the cell and the ability to direct material to specific compartments would have allowed for intracellular specializations, for example, the sequestration of metabolic processes. Membrane trafficking also likely served to integrate fledgling endosymbiotic interactions (Flinner et al. 2013; Wideman et al. 2013), regardless of the precise timing of the mitochondrial endosymbiotic event with respect to the evolution of endogenously derived organelles (Martin and Muller 1998; Cavalier-Smith 2002; Martin and Koonin 2006; Forterre 2011). Finally, trafficking could have also facilitated a size increase for the proto-eukaryotic organisms and enabled their colonization of novel ecological niches; for example, phagocytosis is a critical function that would have been made possible by this change in morphology.In the textbook definition (e.g., Alberts 2002), the membrane-trafficking system consists of the endoplasmic reticulum, the Golgi body, trans-Golgi network (TGN), various types of endolysosomal organelles (early, recycling, and late endosomes and lysosomes/vacuoles), as well as the plasma membrane (Fig. 1A). However, recent work has uncovered greater integration between these classical membrane-trafficking compartments and other organelles including the nucleus (Dokudovskaya et al. 2009), peroxisomes (Agrawal and Subramani 2013), and even the endosymbiotic organelles, particularly the mitochondria (Braschi et al. 2010; Michel and Kornmann 2012; Sandoval and Simmen 2012). Although the molecular details of the latter are still being unearthed, much insight has been gained into the processes of transport between membrane-trafficking organelles by vesicle formation and the subsequent delivery and fusion of the transport vesicle with a target organelle.Open in a separate windowFigure 1.Eukaryotic endomembrane organelles and evolution. (A) A eukaryotic cell depicting the major endomembrane organelles and trafficking pathways (denoted by arrows). Figure created from data in Wideman et al. (2013). (B) Depiction of specificity machinery encoded by multiple components of the vesicle formation and fusion machinery. For diagrammatic simplicity only the Coats, Rabs, and SNAREs are shown. (C) The organelle paralogy hypothesis for the evolution of novel endomembrane organelles by duplication and coevolution of identity-encoding genes.The core molecular machinery for transport between endomembrane organelles consists of proteins and lipids that must, in a combinatorial manner, encode the information required for transport specificity (Cai et al. 2007). The generally accepted model for packaging of material into vesicles at a given organelle involves GTPases of the Arf/Sar family, along with a number of activating and effector proteins (Bonifacino and Glick 2004). Further to this is a requirement for cargo selection, membrane deformation, and scission involving one or more coat protein complexes (COPI, COPII, clathrin/adaptins, ESCRTs, retromer) to generate the transport carriers. Delivery of the carrier initially involves a tethering step involving Rab GTPases, and their modulating GTPase-activating proteins (GAPs) and guanine nucleotide exchange factors, as well as multisubunit tethering complexes (MTCs). The final fusion between the transport carrier and target organelle involves additional protein families such as SNAREs and SM proteins (Bonifacino and Glick 2004). Increasingly, the lines between these various sets of machineries have been blurring, with complexes being identified composed of a mixture of proteins initially identified as involved in either vesicle formation or fusion (e.g., Miller et al. 2007; Pryor et al. 2008). To add a level of complexity, many of the aforementioned proteins are, in fact, protein families in which each paralog performs the same mechanistic role, but at defined organelles or transport pathways within the cell (Bonifacino and Glick 2004). With the number of individual components involved in the membrane-trafficking process, the interconnectivity between the machineries and organelles, and with the diversity of eukaryotic organisms possessing membrane-trafficking machinery, understanding the processes of transport specificity and organelle identity benefits from a more holistic view.Evolutionary cell biology, one aspect of which is the application of comparative molecular evolutionary analysis to cell biology (Brodsky et al. 2012), is particularly valuable in addressing such sweeping questions. Using a toolkit comprising comparative genomics, molecular phylogenetics, and, more recently, mathematical modeling, it has been possible to reconstruct the characteristics and complements of the membrane-trafficking machinery in early eukaryotic ancestors. Importantly, it has been possible to validate some of these in silico predictions of function and behavior of protein components through molecular cell biological characterization in model eukaryotes beyond mammals and yeast. This provides increased confidence in predictions of ancient membrane-trafficking systems, rather than being solely reliant on deduced histories of protein families. Furthermore, by considering the evolutionary histories of trafficking components as an integrated set or cohort, it has been possible to begin deriving mechanistic models of how nonendosymbiotic organelles may evolve. Interestingly, as surveys have advanced in scope, some unexpected patterns of conservation have begun to emerge in the machinery of membrane trafficking that have shed light on the evolution of the system, but also raised questions as to the processes that have shaped it.     

Elicitation of systemic resistance and growth promotion of Arabidopsis thaliana by PGPRs from Nicotiana glauca: a study of the putative induction pathway

The ability of six putative plant growth promoting rhizobacteria, isolated from the rhizosphere of Nicotiana glauca L., to stimulate growth and induce systemic resistance against Xanthomonas campestris CECT 95 in Arabidopsis thaliana L. Col-0 was evaluated. The six bacterial strains significantly reduced the disease symptoms caused by the pathogen compared to the controls, with the best results obtained with the Bacillus strain N11.37 and the Stenotrophomonas strain N6.8. These two strains were tested on A. thaliana NahG plants and jar1-1 and etr1-1 mutants, to elucidate whether the salicylic acid (SA)-dependent or SA-independent pathway was involved in the induction of systemic resistance. The results indicate that N6.8 induces the SA-dependent pathway. For N11.37 it is as yet not clear as in the etr1-1 mutants and NahG plants ISR is not expressed, while in jar1-1 it is. In addition, levels of SA were measured in Col-0 plants treated with N6.8 and N11.37 to confirm whether or not the two strains produced an increased level of SA. N6.8- and N11.37-induced plants showed higher levels of SA than the controls. It is concluded that N6.8 induces a SA-dependent pathway while N11.37 induces a pathway that is both ethylene (ET)- and SA-dependent.     

Self-pollination in island and mainland populations of the introduced hummingbird-pollinated plant, Nicotiana glauca (Solanaceae)

Traits associated with self-pollination are common in island plants. This pattern could simply reflect the vestige of selection during colonization. Alternatively (or in addition), the ability to self-pollinate may provide a reproductive assurance benefit in established island plant populations due to inferior island pollinator service. To test these alternatives I studied an introduced plant (Nicotiana glauca; Solanaceae) on the California mainland and on two Channel Islands colonized at different times (approximately 30 and 100 yr ago). I compared these populations in terms of (1) capacity for self-pollination (self-compatibility, autogamy, stigma-anther distance, and incidence of a crumpled floral morph) and (2) current selection for the ability to self-pollinate (pollinator service by hummingbirds and the effect of emasculation on reproductive success). In general, island plants exhibited a higher capacity for self-pollination than mainland plants, especially on the most recently colonized island. However, island plants were not visited less frequently or more variably, nor did I detect current selection for selfing on islands. This supports the hypothesis that selfing traits in island plants are the product of a filter to successful establishment during colonization and not of selection for selfing in established island populations.     

Global Analysis of Differentially Expressed Genes and Proteins in the Wheat Callus Infected by Agrobacterium tumefaciens

Agrobacterium-mediated plant transformation is an extremely complex and evolved process involving genetic determinants of both the bacteria and the host plant cells. However, the mechanism of the determinants remains obscure, especially in some cereal crops such as wheat, which is recalcitrant for Agrobacterium-mediated transformation. In this study, differentially expressed genes (DEGs) and differentially expressed proteins (DEPs) were analyzed in wheat callus cells co-cultured with Agrobacterium by using RNA sequencing (RNA-seq) and two-dimensional electrophoresis (2-DE) in conjunction with mass spectrometry (MS). A set of 4,889 DEGs and 90 DEPs were identified, respectively. Most of them are related to metabolism, chromatin assembly or disassembly and immune defense. After comparative analysis, 24 of the 90 DEPs were detected in RNA-seq and proteomics datasets simultaneously. In addition, real-time RT-PCR experiments were performed to check the differential expression of the 24 genes, and the results were consistent with the RNA-seq data. According to gene ontology (GO) analysis, we found that a big part of these differentially expressed genes were related to the process of stress or immunity response. Several putative determinants and candidate effectors responsive to Agrobacterium mediated transformation of wheat cells were discussed. We speculate that some of these genes are possibly related to Agrobacterium infection. Our results will help to understand the interaction between Agrobacterium and host cells, and may facilitate developing efficient transformation strategies in cereal crops.     

Floral colour variation of Nicotiana glauca in native and non-native ranges: Testing the role of pollinators' perception and abiotic factors

• Invasive plants displaying disparate pollination environments and abiotic conditions in native and non-native ranges provide ideal systems to test the role of different ecological factors driving flower colour variation.
• We quantified corolla reflectance of the ornithophilous South American Nicotiana glauca in native populations, where plants are pollinated by hummingbirds, and in populations from two invaded regions: South Africa, where plants are pollinated by sunbirds, and the Balearic island of Mallorca, where plants reproduce by selfing. Using visual modelling we examined how corolla reflectance could be perceived by floral visitors present in each region. Through Mantel tests we assessed a possible association between flower colour and different abiotic factors.
• Corolla reflectance variation (mainly along medium to long wavelengths, i.e. human green-yellow to red colours) was greater among studied regions than within them. Flower colour was more similar between South America and South Africa, which share birds as pollinators. Within invaded regions, corolla reflectance variation was lower in South Africa, where populations could not be distinguished from each other by sunbirds, than in Spain, where populations could be distinguished from each other by their occasional visitors. Differences in corolla colour among populations were partially associated with differences in temperature.
• Our findings suggest that shifts in flower colour of N. glauca across native and invaded ranges could be shaped by changes in both pollination environment and climatic factors. This is the first study on plant invasions considering visual perception of different pollinators and abiotic drivers of flower colour variation.

     

Nocturnal to Diurnal Transition in the Common Ancestor of Haplorrhines: Evidence from Genomic-Scan for Positively Selected Genes

<正>Transition from a nocturnal to a diurnal lifestyle represents a major shift in primate evolution,plays a central role in the adaptation of these species to new habitats,and is involved in modifications to their physiological and social behaviors(Heesy and Ross,2001;Shultz et al.,2011).However,two core problems concerning the circadian rhythm transition r     

Restoration of shooty morphology of a nontumorous mutant of Nicotiana glauca x N. langsdorffii by cytokinin and the isopentenyltransferase gene

The shooty morphology of a nontumorous amphidiploid mutant of Nicotiana glauca Grah. x N. langsdorffii Weinm. was restored by cytokinins, whether exogenously applied or endogenously produced by transformation of the mutant with a transfer DNA (T-DNA) cytokinin-biosynthesis gene (isopentenyltransferase; ipt). Auxins alone did not confer this effect. Similar transformation was not achieved for the parental species. In the case of transformation with the ipt gene, selection of the transformed tissues was based on its hormone-independent growth in the presence of the antibiotic kanamycin. Transformed tissues exhibited a shooty morphology, indistinguishable from that of wildtype genetic tumors N. glauca x N. langsdorffii. This altered phenotype was caused by the presence and constitutive expression of the ipt gene. The insertion and expression of this gene in transformed tissues was confirmed by using the polymerase chain reaction (PCR) technique as well as conventional molecular hybridization analysis. Expression of the ipt gene led to an elevated level of cytokinin in the transformed mutant tissues. This evidence supports the notion that genetic tumors are caused, at least in part, by elevated levels of cytokinin in interspecific hybrids.     

Evolution of X-Degenerate Y Chromosome Genes in Greater Apes: Conservation of Gene Content in Human and Gorilla,But Not Chimpanzee

Compared with the X chromosome, the mammalian Y chromosome is considerably diminished in size and has lost most of its ancestral genes during evolution. Interestingly, for the X-degenerate region on the Y chromosome, human has retained all 16 genes, while chimpanzee has lost 4 of the 16 genes since the divergence of the two species. To uncover the evolutionary forces governing ape Y chromosome degeneration, we determined the complete sequences of the coding exons and splice sites for 16 gorilla Y chromosome genes of the X-degenerate region. We discovered that all studied reading frames and splice sites were intact, and thus, this genomic region experienced no gene loss in the gorilla lineage. Higher nucleotide divergence was observed in the chimpanzee than the human lineage, particularly for genes with disruptive mutations, suggesting a lack of functional constraints for these genes in chimpanzee. Surprisingly, our results indicate that the human and gorilla orthologues of the genes disrupted in chimpanzee evolve under relaxed functional constraints and might not be essential. Taking mating patterns and effective population sizes of ape species into account, we conclude that genetic hitchhiking associated with positive selection due to sperm competition might explain the rapid decline in the Y chromosome gene number in chimpanzee. As we found no evidence of positive selection acting on the X-degenerate genes, such selection likely targets other genes on the chimpanzee Y chromosome. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.