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Widespread horizontal transfer of mitochondrial genes in flowering plants
Author: Ulfar Bergthorsson
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"19. Kihm, A. J. et al. An abundant erythroid protein that stabilizes free a-haemoglobin. Nature 417, 758?763 (2002). 20. Hughes, T. R. et al. Functional discovery via a compendium of expression profiles. Cell 102, 109?126 (2000). 21. Carroll, S. B., Grenier, J. K. & Weatherbee, S. D. From DNA to Diversity (Blackwell Science, Malden, Massachusetts, 2001). 22. Hodgkin, J. Fluxes, doses and poisons?molecular perspectives on dominance. Trends Genet. 9, 1?2 (1993). 23. Kratz, E., Dugas, J. C. & Ngai, J. Odorant receptor gene regulation: Implications from genomic organization. Trends Genet. 18, 29?34 (2002). 24. Johnston, M. Feasting, fasting and fermenting. Glucose sensing in yeast and other cells. Trends Genet. 15, 29?33 (1999). 25. Hodges, P. E., McKee, A. H., Davis, B. P., Payne, W. E. & Garrels, J. I. The Yeast Proteome Database (YPD): A model for the organization and presentation of genome-wide functional data. Nucleic Acids Res. 27, 69?73 (1999). 26. Gavin, A. C. et al. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415, 141?147 (2002). 27. von Mering, C. et al. Comparative assessment of large-scale data sets of protein?protein interactions. Nature 417, 399?403 (2002). 28. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389?3402 (1997). 29. Eisen, M. B., Spellman, P. T., Brown, P. O. & Botstein, D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl Acad. Sci. USA 95, 14863?14868 (1998). 30. Sokal, R. & Rohlf, M. Biometry (Freeman, New York, 1995). Supplementary Information accompanies the paper on www.nature.com/nature. Acknowledgements We thank C. Scharfe, L. Steinmetz, D. Bray and B. Charlesworth for comments on the manuscript. B.P. is supported by an EU Marie Curie Fellowship, C.P. by a Royal Society/Nato Fellowship and L.D.H. by the BBSRC. Competing interests statement The authors declare that they have no competing financial interests. Correspondence and requests for materials should be addressed to L.D.H. (bssldh@bath.ac.uk). .............................................................. Widespread horizontal transfer of mitochondrial genes in flowering plants Ulfar Bergthorsson*, Keith L. Adams*?, Brendan Thomason*? & Jeffrey D. Palmer* * Department of Biology, Indiana University, Bloomington, Indiana 47405, USA ? Department of Botany, Iowa State University, Ames, Iowa 50011, USA ? Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan 48109, USA ............................................................................................................................................................................. Horizontal gene transfer?the exchange of genes across mating barriers?is recognized as a major force in bacterial evolution 1,2 . However, in eukaryotes it is prevalent only in certain phago- trophic protists and limited largely to the ancient acquisition of bacterial genes 3?5 . Although the human genome was initially reported 6 to contain over 100 genes acquired during vertebrate evolution from bacteria, this claim was immediately and repeat- edly rebutted 7,8 . Moreover, horizontal transfer is unknown within the evolution of animals, plants and fungi except in the special context of mobile genetic elements 9?12 . Here we show, however, that standard mitochondrial genes, encoding ribosomal and respiratory proteins, are subject to evolutionarily frequent horizontal transfer between distantly related flowering plants. These transfers have created a variety of genomic outcomes, including gene duplication, recapture of genes lost through transfer to the nucleus, and chimaeric, half-monocot, half-dicot genes. These results imply the existence of mechanisms for the delivery of DNA between unrelated plants, indicate that hori- zontal transfer is also a force in plant nuclear genomes, and are discussed in the contexts of plant molecular phylogeny and genetically modified plants. We first suspected that there is horizontal transfer of mitochon- drial genes by finding three striking distributional anomalies in a survey of mitochondrial gene content in angiosperms 13 . Two ribo- somal protein genes, rps2 and rps11, were inferred 13 from blot hybridization data to be absent from mitochondrial DNA of all members of a vast eudicot clade comprising, respectively, 180 and 182 of the 280 angiosperms examined, with the exception of one or two highly derived members of this clade (Fig. 1). Three biological models could account for these anomalies. Two models involve the loss of each gene from mitochondrial DNA early in eudicot evolution and their subsequent re-acquisition by mitochondrial DNA much later (Fig. 1), either, by horizontal gene transfer (HGT) from some unrelated plant or, by vertical transmission, by means of intracellular gene transfer (IGT) from the nucleus of the same plant lineage. A third alternative, that these genes could have been transmitted strictly vertically and exclusively through mitochon- drial DNA, would mean extraordinarily frequent and pervasive mitochondrial loss throughout all other eudicot clades in which the three ?special retention? cases shown in Fig. 1 are phylogenetically embedded. To distinguish between these three possibilities, we analysed levels of sequence divergence and the phylogenetic position of 31 rps2 and 44 rps11 genes from a broad array of angiosperms, including the three anomalous plants and their close relatives. All three sets of anomalous genes should, if they are the product of vertical trans- mission (by the second or third models), group in phylogenetic trees with basal eudicots that never lost these genes from their mitochondrial genomes. Instead, however, rps2 from Actinidia (kiwifruit) groups with monocot rps2 sequences with high support (Fig. 2a). This placement strongly indicates an HGT event from monocots to eudicots. The rps11 genes of Lonicera (honeysuckle; Fig. 1a) and other Caprifoliaceae (order Dipsacales) also fail to group in the position expected for vertical transmission, nesting instead within the unrelated order (Ranunculales) with strong support from bayesian analysis and alternative topology tests (see Fig. 2b, Methods and Supplementary Information). Important additional evidence for rps11 HGT from Ranunculales to Caprifoliaceae comes from a non- coding sequence immediately upstream of rps11. The two Caprifo- liaceae upstream sequences cluster strongly with the Berberis (Ranunculales) sequence in phylogenetic trees to the exclusion of Trochodendraceae (Fig. 2c), the position expected if vertically transmitted. The phylogenetic position of rps11 sequences from the third anomalous group, Betula (birch; Fig. 1b) and other Betulaceae, is unresolved and is indeed consistent with vertical transmission (Fig. 2b). The phylogenetic evidence for recapture of rps11 in Betulaceae therefore rests on the phylogenetically anomalous pres- ence of rps11 in mitochondrial DNA in this family, together with the evidence that both other such anomalies are very likely to reflect gene recapture. Analysis of sequence divergence levels provides important evidence that the putatively recaptured rps11 gene of Betulaceae is the result of HGT rather than IGT from nucleus to mitochondrion (and further supports a horizontal origin of the Actinidia rps2 and Capriofoliaceae rps11 genes). Nuclear substi- tution rates are far higher than mitochondrial rates in angio- sperms 14,15 , such that nuclear genes of mitochondrial origin quickly become long branches in mitochondrial gene trees (refs 15 and 16, and Supplementary Fig. 1). Reverse IGT (the second model) therefore predicts a highly divergent mitochondrial rps11 or rps2 gene in each plant group. This is clearly not so (Fig. 2a, b, and Supplementary Fig. 1), and thus mitochondrial HGT is the best explanation. The rps11 phylogeny serendipitously revealed a fourth, quite remarkable and well-supported case of HGT. Phylogenetic analysis letters to nature NATURE | VOL 424 | 10 JULY 2003 | www.nature.com/nature 197� 2003 Nature Publishing Group of full-length rps11 placed Sanguinaria canadensis (bloodroot; Papaveraceae), a basal eudicot, in a basal position of the monocot rps11 clade with high support (data not shown). On closer exami- nation, Sanguinaria rps11 turns out to be chimaeric: its 5 0 half is of expected eudicot, vertical origin (Fig. 2d), but its 3 0 half is indis- putably of monocot, horizontal origin (Fig. 2e). A test of recombi- nation 17 , using Bocconia and Disporum to represent Papaveraceae and monocots, respectively, was highly significant (x 2 27.5, P , 0.0001) and placed the point of recombination midway in the gene (Fig. 3). Other genera in the Papaveraceae contain only a non-chimaeric, vertically transmitted rps11 gene (Fig. 2d, e), making this transfer evolutionarily recent. Finding four cases of HGT for just two mitochondrial genes, each only modestly sampled taxonomically, implies that HGT occurs at an appreciable frequency for plant mitochondrial genes in general. Indeed, perusal of the limited literature on plant mitochondrial phylogenies identified a fifth, strongly supported but previously misinterpreted, case of HGT. Amborella trichopoda, the sole extant member of the earliest branch of angiosperm evolution (see, for example, refs 18, 19), was reported by two different groups to contain a mitochondrial atp1 gene of anomalous phylogenetic placement within eudicots. One study 18 attributed this placement to the Amborella gene?s ?divergent sequence?, implying that it was misplaced as an artefact of long-branch attraction. The other study 19 found an additional mitochondrial atp1 gene in Amborella,of expected basal position; the authors invoked gene duplication, calling the eudicot-like atp1 gene a ?paralogue? of this basal gene. We independently isolated the same two atp1 genes from Ambor- ella as those reported in ref. 19, and our phylogenetic analyses strongly support a eudicot placement for one of these genes (Fig. 2f). We are convinced that neither published explanation is correct and that instead the ?misplaced? atp1 duplicate in Amborella is the result of HGT from eudicots. If long-branch attraction were the expla- nation, then this gene should itself represent a long branch and should group with other long-branched atp1 genes. This does not happen (Fig. 2f). Moreover, that this gene is more similar to atp1 genes of eudicots than to atp1 genes of basal angiosperms also negates long-branch attraction. Paralogy as an explanation fails because, given the basal position of Amborella among angiosperms, this implies gene duplication in a common ancestor of angiosperms. If so, the two Amborella genes should each branch at the base of two separate clades of angiosperm atp1 genes, each containing various diverse angiosperms (even allowing differential gene loss), in a pattern recapitulating the generally understood branching pattern of angiosperm phylogeny. This is clearly not so (Fig. 2f), leaving HGT as the only viable explanation. We examined the expression status of two of the five cases of HGT. Fifteen rps11 complementary DNAs were sequenced from Sanguinaria and each was found to be identical to its chimaeric rps11 gene except for five sites of partial C ! U RNA editing (Table 1). This result establishes that the chimaeric Sanguinaria gene is both transcribed and RNA edited, and indicates, in concert with its being an intact open reading frame, that it is probably functional. The horizontally acquired atp1 gene of Amborella is also transcribed and RNA edited (U.B., C. Mathews, and J.D.P., unpublished observations). Roughly half of the genes characterized in the three other HGT cases are intact and therefore merit studies on their expression, whereas half show signs of being pseudogenes. The intact open reading frames include four of five Caprifoliaceae rps11 genes and one of four Betulaceae rps11 genes (the non-intact genes each contain a single frameshift mutation of four or five nucleo- tides). The phylogenetic mixture of both intact and probably Figure 1 Anomalous presence of ribosomal protein genes in three angiosperm mitochondrial DNAs. A consensus phylogeny of 280 angiosperms is marked according to the presence (red branches) or absence (blue branches) of rps2 (a) and rps11 (b)in mitochondrial DNA (tree topology and gene presence/absence data are from ref. 13). Blue and red bullets mark inferred losses and regains, respectively, of these genes. Names of taxa with gene regain are shown in red lettering, selected taxa with gene loss are in blue, and names of major groups of angiosperms are in black. Trochodendrac., Trochodendraceae. letters to nature NATURE | VOL 424 | 10 JULY 2003 | www.nature.com/nature198 � 2003 Nature Publishing Group disabled genes in these two families might mean that these are all non-functional genes, with only some having already been hit by disabling mutations. Alternatively, it might reflect differential usage and fixation of a duplicated gene (relative to a transferred nuclear homologue; see Supplementary Fig. 1), perhaps analogous to the situation reported for the transcompartmental cox2 gene family created by gene transfer from mitochondrion to nucleus in legumes 20 . Finally, all Actinidia rps2 genes contain a single NT substitution early in the gene that creates a stop codon, unless remedied by rare U ! C RNA editing. Artefacts of DNA contamination or mislabelled samples, always a concern when invoking HGT, can be ruled out in all five transfer cases because multiple sampling (see Fig. 2b, for example) showed Table 1 RNA editing of Sanguinaria rps11 Site (nucleotide) Codon change Efficiency* ............................................................................................................................................................................. 78? TTC (Phe) ! TTT (Phe) 3/15 92? TCG (Ser) ! TTG (Leu) 8/15 143 CCA (Phe) ! CTA (Leu) 9/15 146 CCG (Pro) ! CTG (Leu) 8/15 351? TTC (Phe) ! TTT (Phe) 7/15 ............................................................................................................................................................................. *Efficiency is shown as the fraction of the 15 cDNA clones that have been edited at a particular site; although editing efficiency at any one site did not exceed 60%, 7 of 15 cDNAs were edited at all three sites of non-synonymous editing. ?Sites that are also edited in rice rps11 (ref. 30); the other two editing changes conserve the amino acids coded at these positions in monocots. Figure 2 Phylogenetic evidence for HGT in angiosperm mitochondrial DNA. Maximum likelihood trees of rps2 (474-nucleotide alignment) (a), rps11 (456 nucleotides) (b), sequences immediately upstream of rps11 (457 nucleotides) (c), 5 0 half of rps11 (219 nucleotides) (d), 3 0 half of rps11 (237 nucleotides) (e) and atp1 (1,254 nucleotides) (f). Dendroc., Dendrocalamus. Bootstrap support values more than 60% from parsimony analyses are given above nodes, and bayesian posterior probability values more than 90% are given below. All scale bars correspond to 0.01 nucleotide substitutions per site. Asterisks in a?c indicate the positions of Actinidia rps2 and Caprifoliaceae and Betulaceae rps11 expected according to models of vertical transmission. letters to nature NATURE | VOL 424 | 10 JULY 2003 | www.nature.com/nature 199� 2003 Nature Publishing Group the results to be entirely reproducible (see Supplementary Infor- mation for details). Evidence that all five transferred genes are located in the mitochondrial genome and were horizontally acquired from mitochondrial rather than nuclear genomes relates to three factors: their lack of divergence (Fig. 2 and Supplementary Fig. 1), their hybridization intensity 13 and their RNA editing (for at least Sanguinaria rps11 and Amborella atp1), all of which are mitochondrion-like (see Supplementary Information for details). Here we have identified strong evidence for four cases of plant-to- plant horizontal transfer of mitochondrial genes, and weaker evidence for a fifth. Three transfers involve the recapture of a gene lost early during eudicot evolution owing to functional transfer to the nucleus (?recapture HGT?), whereas Amborella contains intact genes of vertical and horizontal transmission (?duplicative HGT?) and two such genes have recombined in Sanguinaria to create a strikingly chimaeric and expressed gene (?chimaeric HGT?). All five cases involve wide HGTwithin the context of angiosperm evolution (Fig. 4), including two transfers from monocots to eudicots. On the basis of current sampling and molecular-clock-based divergence times 21 , we can very roughly estimate the age(s) of each transfer ?event? (Fig. 4). Further sampling promises to improve the precision of these estimates, to improve the identification of donor and recipient groups and to identify cases of long-term residency of a transferred gene in an intermediate genome, either of a vectoring agent or another plant group (if donors are found to be convinc- ingly older than recipients for any well-dated cases; see Fig. 4 for two potential cases). These results establish for the first time that conventional genes are subject to evolutionarily frequent HGT during plant evolution and provide the first unambiguous evidence that plants can donate DNA horizontally to other plants (compare refs 12 and 22 on both issues). This is also the best evidence (see also ref. 23) that eukaryotic genomes regularly acquire genes by means of horizontal events that are relatively recent, datable, and definable as to donor and recipient. For several reasons (see Supplementary Information) we believe the five cases reported here are merely the tip of a large iceberg of mitochondrial HGT in plants. Given this and the evolutionarily frequent occurrence of IGT to plant nuclear gen- omes 13,16,24,25 , it seems likely that plant nuclear genomes are also significantly affected by HGT. Indeed, a few cases of horizontal acquisition of bacterial genes by plant nuclear genomes have been reported 23,26 . Despite extensive phylogenetic analysis of chloroplast genes, there is no published evidence for the acquisition of foreign DNA by chloroplasts in any land plant. We therefore predict a much lower incidence of chloroplast HGT than for mitochondrial or nuclear genomes. It is fortunate that the two major sets of genes used to reconstruct plant phylogeny?chloroplast genes and nuclear rRNA genes?seem relatively immune to HGT. Our findings raise many other questions. Are these results relevant to concerns over the potential escape of transgenes from genetically modified plants by means of HGT? We think not, because although reasonably frequent on an evolutionary time scale of millions of years, HGT is highly unlikely to be a factor on a human time scale. Are certain plants especially susceptible to HGT, as is clearly true for IGT 13 ? Does HGT ever occur on a grand scale, leading to the horizontal acquisition of much or all of a mitochondrial genome, and/or of many nuclear genes, as has been seen for IGT 25 ? How do genes move from one plant to another, sexually unrelated, plant? Is HGT driven predominantly by poten- tial vectoring agents such as viruses, bacteria, fungi, insects, pollen or even meteorites; or by the transformational uptake of plant DNA released into the soil; or by unrelated plants occasionally grafting together? A Methods Gene isolation and characterization Mitochondrial rps2, rps11 and atp1 genes were amplified by standard, direct polymerase chain reaction (PCR) in an Idaho Technologies Air Thermocycler. In general, each reaction consisted of 36 cycles of 10 s at 94 8C, 15 s at 50 8C and 45 s at 72 8C. The extension time was 90 s and the annealing temperature was 55 8Cforatp1 amplification and for inverse PCR. A list of PCR primers can be found in Supplementary Information. Sequences flanking rps2 from Actinidia arguta were obtained by inverse PCR: A. arguta DNA (2 mg) was digested with either ApoIorBamHI plus BglI (New England Biolabs) and then ligated overnight at 12 8C with T4 ligase (New England Biolabs) in 400 ml. After extraction with chloroform and precipitation with ethanol, the ligated DNA was used for inverse PCR. Primers to conserved sequences immediately upstream of rps11 in Lonicera and Sanguinaria (initially amplified by Vectorette PCR; Sigma-Genosys) were used to amplify this region in other species. To verify the authenticity of the Sanguinaria rps11 sequence, PCR was performed on DNA isolated from three independent sources, and one set of Sanguinaria DNA extractions and PCR reactions were done in a different laboratory. Sanguinaria RNA was isolated from roots and flower buds using RNeasy Plant Mini Kit (Qiagen) and treated twice with DNAse I (TaKaRa). Reverse transcription was done on 2 mg RNA with random hexamer primers (Invitrogen) and Moloney-murine-leukaemia virus reverse transcriptase (New England Biolabs). Gel-purified RT?PCR products (Qiaquick; Qiagen) of Sanguinaria rps11 were cloned with TOPO TA Cloning (Invitrogen) in accordance with the manufacturer?s directions. Uncloned PCR products and cloned RT?PCR products were sequenced on both strands at the DNA sequencing facility of the Indiana Molecular Biology Institute. Figure 3 Chimaeric structure of the Sanguinaria rps11 gene. Shown are all rps11 variations in two Papaveraceae (Bocconia frutescens (Bf) and Sanguinaria canadensis (Sc)) and the monocot Disporum hookeri (Dh). Shading marks taxa that have the same nucleotide at a given position, numbered according to its location in Sanguinaria. Triangles mark deletions. The six variations (sites 192, 270, and so on) that do not follow the general shaded patterns are uniquely derived among either all 44 rps11 genes sequenced (positions 192, 344 and 395, see Supplementary Fig. 3), or within the relevant group (Ranunculales for position 270, and monocots for positions 341 and 347; see Supplementary Fig. 3). Figure 4 Approximate timing and donor?recipient relationships of five HGT ?events? in angiosperm mitochondrial DNA. Divergence times are from ref. 21. Shadowed ovals indicate rough identity of donor groups (Fig. 2). The exact placement of arrowheads on recipient lineages is arbitrary. If correct, the older ages of donors relative to recipients for the rps2 and 3 0 rps11 transfers imply the existence of the transferred gene in an intermediate, unidentified vectoring agent or host plant for millions of years, but these discrepancies could easily be due to imprecision in the gene trees (Fig. 2) and/or in molecular-clock-based estimates 21 of divergence times. letters to nature NATURE | VOL 424 | 10 JULY 2003 | www.nature.com/nature200 � 2003 Nature Publishing Group Phylogenetic analyses Phylogenetic analyses were performed with PAUP v. 4.0b10 (ref. 27) and MrBayes v. 2.01 (ref. 28). Sites of known RNA editing were excluded from the analyses. Maximum- likelihood trees were constructed with a HKY85 substitution model; trees in Fig. 2 used a transition-to-transversion ratio of 2.0. For alternative topology tests (see below for Shimodaira?Hasegawa tests, and Supplementary Information for parametric bootstrap analyses), transition-to-transversion ratios and gamma distribution parameters were first estimated from the data. Bootstrap support values are from maximum-parsimony analyses of 1,000 bootstrap replicates and 100 random addition replicates. Posterior probability for clade support was estimated with Markov chain Monte Carlo as implemented in MrBayes. Four Markov chains were run for 10 5 to 10 6 generations after burn-in, using random initial trees and a general time-reversible (GTR) codon-site- specific substitution model for coding sequences and GTR with gamma distribution for non-coding sequences. The Shimodaira?Hasegawa 29 test favoured the horizontal placements shown in the unconstrained trees of Fig. 2 over alternative topologies based on vertical transmission: first, the unconstrained rps2 tree (Fig. 2a) was favoured over the constrained tree grouping Actinidia with Grevillea/Platanus as a monophyletic group (P 0.012); second, the unconstrained rps11 tree (Fig. 2b) was favoured over the tree grouping Caprifoliaceae plus Betulaceae plus Trochodendraceae and/or Proteales (P 0.036); third, the unconstrained 3 0 rps11 tree (Fig. 2e) was favoured over the tree grouping Sanguinaria with other Papaveraceae (P , 0.001); and last, the unconstrained atp1 tree (Fig. 2f) was favoured over the tree grouping the two Amborella sequences (P , 0.001). A test of recombination was performed with Maximum Chi-squared for Macintosh, version 1.0, by N. Ross, which implements the original method by J. Maynard Smith 17 . Received 27 February; accepted 13 May 2003; doi:10.1038/nature01743. 1. 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Biol. Evol. 16, 1114?1116 (1999). 30. Kadowaki, K., Kubo, N., Ozawa, K. & Hirai, A. Targeting presequence acquisition after mitochondrial gene transfer to the nucleus occurs by duplication of existing targeting signals. EMBO J. 15, 6652?6666 (1996). Supplementary Information accompanies the paper on www.nature.com/nature. Acknowledgements We thank C. Mathews for technical assistance; E. Knox for creating Fig. 4, for drafting Fig. 1 and for discussion; L. Goertzen, E. Knox, R. Olmstead, D. Rice and S. Stefanovic for critical reading of the manuscript; R. Gardner for providing several Actinidia DNAs; M. Stoutemyer and J. Gastony for help in obtaining plant material; and B. Hall and the University of California Santa Cruz arboretum for supplying leaf material for Amborella. Financial support was provided by the US NIH. Competing interests statement The authors declare that they have no competing financial interests. Correspondence and requests for materials should be addressed to J.D.P. (jpalmer@bio.indiana.edu). The sequences reported in this study have been deposited in GenBank under the accession numbers AY293002?AY293057. .............................................................. Topography and synaptic shaping of direction selectivity in primary auditory cortex Li I. Zhang*?, Andrew Y. Y. Tan*?, Christoph E. Schreiner* & Michael M. Merzenich* * Coleman Memorial Laboratory and W.M. Keck Foundation Center for Integrative Neuroscience, University of California, San Francisco, California 94143, USA ? These authors contributed equally to this work ............................................................................................................................................................................. The direction of frequency-modulated (FM) sweeps is an import- ant temporal cue in animal and human communication. FM direction-selective neurons are found in the primary auditory cortex (A1) 1,2 , but their topography and the mechanisms under- lying their selectivity remain largely unknown. Here we report that in the rat A1, direction selectivity is topographically ordered in parallel with characteristic frequency (CF): low CF neurons preferred upward sweeps, whereas high CF neurons preferred downward sweeps. The asymmetry of ?inhibitory sidebands?, suppressive regions flanking the tonal receptive field (TRF) of the spike response, also co-varied with CF. In vivo whole-cell recordings showed that the direction selectivity already present in the synaptic inputs was enhanced by cortical synaptic inhi- bition, which suppressed the synaptic excitation of the non- preferred direction more than that of the preferred. The excit- atory and inhibitory synaptic TRFs had identical spectral tuning, but with inhibition delayed relative to excitation. The spectral asymmetry of the synaptic TRFs co-varied with CF, as had direction selectivity and sideband asymmetry, and thus suggested a synaptic mechanism for the shaping of FM direction selectivity and its topographic ordering. Extracellular multiunit spike responses to sweeps of various speeds and intensities were recorded in the mid-layers of the adult rat A1. Responses from a representative low CF site are shown in Fig. 1. Sweeps of different speeds evoked distinct responses (Fig. 1a). The onset and duration of each response mostly reflected the timing of the sweep?s intersection with the TRF of the spike response (Fig. 1b). A direction selectivity index (DSI) was calculated for letters to nature NATURE | VOL 424 | 10 JULY 2003 | www.nature.com/nature 201� 2003 Nature Publishing Group "
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