- Email: [email protected]
C4 Photosynthesis: Need a Gene? Borrow One!
Dispatch R161
model of speech acquisition developed further and tested with caregiver reformulations as input to an infant computer model that learns the pronunciation of words [11,12]. Independently, the Asada group in Osaka [13,14] have also used reformulation/mirroring by a caregiver to train vowel qualities in a physical vocal tract model. Returning to the first question identified by MacDonald et al. [4], of why self-monitoring is delayed, it is not surprising within this new paradigm that reliance on auditory information for self-monitoring comes late in a child’s speech development. The starting point for speech production is motor exploration and the proposal is that an infant has no early need to reconceive his speech sounds in auditory terms in order to compare and evaluate his production with that of others. As auditory feedback is then only a secondary sensory information source for speech sounds, its use will develop accordingly. For haptic and spatial information, Gori et al. [15] recently found that one sense dominates totally in tests of multisensory integration in children up to 8 years of age. Reviewing this and recent papers reporting similar results, Ernst [16] said that it is unclear why integration emerges so late, but argued that it is unlikely to only be the result of the challenges caused by growth and sensory reorganisation. Whatever the reasons, young children do ignore sensory data that they do not consider to be primary. Children who are usually a little older than the toddlers tested by MacDonald
et al. [4] have often been reported to persist with the pronunciation of an incorrect word form, even when they deploy the speech sound they need elsewhere. The phenomena are discussed under various labels: ‘‘fis/fish’’, ‘‘puzzle/puddle/puggle’’, ‘‘guck’’ for ‘‘duck’’ (persistently), and so on. The puzzle is that the child hears adult speech correctly, but not, it seems, his own. Out of a range of hypotheses addressing this (summarised in [17,18]), none conclusively explains the whole range of situations where children are apparently oblivious to the reality of what they are saying. MacDonald et al.’s [4] results suggest that these behaviours may not be the manifestation of a novel absence of attention by a child to his own output, but a continuation of what is systematic in the behaviour of toddlers.
9.
10.
11.
12.
13.
14.
References 1. Houde, J.F., and Jordan, M.I. (1998). Sensorimotor adaptation in speech production. Science 279, 1213–1216. 2. Fry, D.B. (1968). The phonemic system in children’s speech. Br J. Disord. Commun. 3, 13–19. 3. Kuhl, P.K. (2000). A new view of language acquisition. Proc. Natl. Acad. Sci. USA 97, 11850–11857. 4. MacDonald, E.N., Johnson, E.K., Forsythe, J., Plante, P., and Munhall, K.G. (2012). Children’s development of self-regulation in speech production. Curr. Biol. 22, 113–117. 5. Gros-Louis, J., West, M.J., and King, A.P. (2010). Comparative perspectives on the missing link: communicative pragmatics. In The Oxford Handbook of Developmental and Comparative Neuroscience, M.S. Blumberg, J.H. Freeman, and S.R. Robinson, eds. (OUP), pp. 684–707. 6. Goldstein, M.H., and Schwade, J.A. (2010). From birds to words: perception of structure in social interactions guides vocal development and language learning. In The Oxford Handbook of Developmental and Comparative Neuroscience, M.S. Blumberg,
Horizontal gene transfer has been increasingly documented between eukaryotes, but a new study suggests a much larger role for horizontal gene transfer in physiological adaption through the transfer of photosynthetic pathway genes.
Christin et al. [1] report in this issue of Current Biology that horizontal gene transfer (HGT) is the most likely origin of C4 photosynthetic pathway genes in
8.
15.
C4 Photosynthesis: Need a Gene? Borrow One!
Eric H. Roalson
7.
the grass genus Alloteropsis [1]. This is novel, not only because the transfer conveys a change in the functional traits of these grasses (from C3 to C4), but also because there have been an inferred four transfers of two genes
16. 17.
18.
J.H. Freeman, and S.R. Robinson, eds. (Oxford: Oxford University Press), pp. 708–729. Pawlby, S.J. (1977). Imitative interaction. In Studies in Mother-Infant Interaction, H.R. Schaffer, ed. (London: Academic Press), pp. 203–223. Heyes, C. (2010). Where do mirror neurons come from? Neurosci. Biobehav. Rev. 34, 575–583. Gattegno, C. (1962). Teaching Foreign Languages in Schools: the Silent Way, 1st edn. (Reading: Educational Explorers). Messum, P.R. (2007). The Role of Imitation in Learning to Pronounce. (London University: PhD thesis). Howard, I.S., and Messum, P.R. (2007). A computational model of infant speech development. In Speech and Computer (SpeCom XII) (Moscow: Moscow State Linguistics University), pp. 756–765. Howard, I.S., and Messum, P.R. (2011). Modeling the development of pronunciation in infant speech acquisition. Motor Control 15, 85–117. Yoshikawa, Y., Asada, M., Hosoda, K., and Koga, J. (2003). A constructivist approach to infants’ vowel acquisition through mother-infant interaction. Connection Sci. 14, 245–258. Miura, K., Yoshikawa, Y., and Asada, M. (2007). Unconscious anchoring in maternal imitation that helps finding the correspondence of caregiver’s vowel categories. Adv. Robotics 21, 1583–1600. Gori, M., Del Viva, M., Sandini, G., and Burr, D.C. (2008). Young children do not integrate visual and haptic form information. Curr. Biol. 18, 694–698. Ernst, M.O. (2008). Multisensory integration: a late bloomer. Curr. Biol. 18, R519–R521. Locke, J.L. (1979). The child’s processing of phonology. In Child Language and Communication: Minnesota Symposium on Child Psychology Volume 12, W.A. Collins, ed. (Hillsdale, NJ: LEA), pp. 83–119. Alvater-Mackensen, N., and Fikkert, P. (2010). The acquisition of the stop-fricative contrast in perception and production. Lingua 120, 1898–1909.
1112
Warner Road, London SE5 9HQ, UK. & Biological Learning Laboratory, Department of Engineering, University of Cambridge, Trumpington Street, Cambridge CB2 1PZ, UK. E-mail: [email protected], [email protected] 2Computational
DOI: 10.1016/j.cub.2012.01.032
from three different grass lineages into Alloteropsis! HGT has been demonstrated most frequently among prokaryotes [2], or from prokaryotes to eukaryotes [3], but transfers from one eukaryote to another are increasingly documented [4–7]. Plant–plant HGT has been primarily found in the transfer between a host and parasite [8–10] or through grafted stock [11], but the evidence for other types of HGT is increasing [12–15]. Most of this HGT has been found in the transfer of mitochondrial gene regions among a wide range of land plants, including mosses,
Current Biology Vol 22 No 5 R162
ferns, gymnosperms, and angiosperms [9,12,13]. Transfer of nuclear DNA among land plants has rarely been documented [14,15], and to date only found in grasses. The first documented plant–plant HGT of nuclear content was the transfer of a Mu-like transposable element (MULE) from rice to Setaria [14]. This was not entirely unexpected, as there are many well-documented cases of transposable element movement among animal species [16]. More surprising is the recently documented transfer of a functional nuclear gene between plant species [15]. There is substantial evidence for the transfer of a Poa cytosolic phosphoglucose isomerase (PgiC) gene to Festuca ovina, and there is evidence that the acquired copy has all of the necessary sequence to be expressed [15]. In fact, this transfer event was found because of an extra band in an isozyme study of these plants. As interesting as both of these cases are, it is not clear what if any functional or adaptive advantage either of these transfers convey — there is unlikely any with the MULE transfer, and there has been no indication that the PgiC transfer is in any way adaptive. The origins of C4 photosynthesis have been well documented to be complex, with at least 45 independent gains of the C4 pathway in flowering plants [17], and the strong molecular convergence in amino acid structure across numerous sites in the phosphoenolpyruvate carboxylase (ppc) gene [18]. While many photosynthesis genes have not been as rigorously tested for selection on C4 function as ppc, similar patterns have been found in some cases [19]. Selection-driven convergence in amino acid structure of critical genes in the C4 pathway complements a recently discovered set of conserved regulatory elements that appear to facilitate the repeated evolution of C4 photosynthesis [17]. All-in-all, these results suggest a rather complex pattern of convergence in an adaptive trait. Adding to this story of complex patterns of convergent evolution in C4 is the HGT of C4 pathway genes in the grass genus Alloteropsis [1]. This is of interest for several reasons. First, this is the first well-documented case of plant–plant HGT of functional genes in which there has been a presumed
adaptive advantage conveyed. Further, the Alloteropsis lineage has been the recipient of both C4-type ppc and C4-type phosphoenolpyruvate carboxykinase (pck), with three apparent transfers of ppc and one transfer of pck. These gene copies have been transferred from three different grass lineages, Andropogoneae, Cenchrinae, and Melinidinae, that diverged from Alloteropsis around 20–25 million years ago [1]. This has broad-ranging implications for adaptive diversification as it suggests that plants might be able to adapt to novel environments very quickly if HGT occurs in the right circumstances. Despite this, HGT-driven adaptive diversification does not appear to be occurring in Alloteropsis (at least not yet), as there are only five known species in the genus. While the first expectation when genes from one species are found in another is that this has happened through hybridization, there is strong evidence in this case that that is not how the ppc and pck genes were transferred. When hybridization occurs, there is a co-mingling of the genomes of the two species, and even if backcrossing to one parent leads to the genome being predominantly of one parent, we would expect there to continue to be numerous genes of the second parent present. However, in the case of Alloteropsis, Christin et al. [1] compared 454-sequenced cDNA libraries of both C4 and C3 Alloteropsis semialata to whole genome sequences of rice, Brachypodium, Sorghum, and Setaria, and found no conclusive evidence of the transfer of any of the more than 11,000 genes tested other than ppc and pck. If hybridization is not the mechanism of gene transfer, then how does HGT occur? There are several mechanisms that are most frequently postulated: vector-mediated transfer, plant–plant contact, transformation, and illegitimate pollination [1]. In the cases of HGT between a host and parasite or grafted plants, plant–plant contact is the presumed mechanism [8–11]; however, Alloteropsis and these other grass species are not known to be parasitic. These plants have not been transformed, and it is unlikely that they have come into contact with other transformed plants. While vector-mediated transfer cannot be ruled out, it seems somewhat unlikely given the complex series of events that
must happen — a vector must capture the ppc or pck gene, move to Alloteropsis from the donor plant, and then successfully insert the gene into the germ line. This leaves us with illegitimate pollination. What is the likelihood of that? Since these grasses are all wind pollinated, and therefore make prodigious amounts of pollen, the deposition of pollen from a nearby C4 grass on the stigma of Alloteropsis seems plausible. It is known that foreign grass pollen can germinate on a stigma, and in the laboratory, chromosomes have been transferred from maize to oats (more than 45 Ma divergence) through forced crossing and embryo rescue with resulting fertile plants [20]. This results in an embyo with unequal DNA contributions from the two parents — in some cases only a single chromosome from the pollen donor. Despite the plausibility of illegitimate pollination-mediated HGT in these grasses, there is yet to be evidence supporting this mechanism over others. It will be important to determine which of these mechanisms allow for HGT in plants, how to discriminate which mechanism is at work, and clarify the role of HGT in adaptation and lineage diversification. Is what we see in Alloteropsis the rare special case, or the tip of the iceberg? References 1. Christin, P.-A., Edwards, E.J., Besnard, G., Boxall, S.F., Gregory, R., Kellogg, E.A., Hartwell, J., and Osborne, C.P. (2012). Adaptive evolution of C4 photosynthesis through recurrent lateral gene transfer. Curr. Biol. 22, 445–449. 2. Koonin, E.V., Makarova, K.S., and Aravind, L. (2001). Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 55, 709–742. 3. Keeling, P.J., and Palmer, J.D. (2008). Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9, 605–618. 4. Andersson, J.O., Sjo¨gren, A˚.M., Horner, D.S., Murphy, C.A., Dyal, P.L., Sva¨rd, S.G., Logsdon, J.M., Ragan, M.A., Hirt, R.P., and Roger, A.J. (2007). A genomic survey of the fish parasite Spironucleus salmonicida indicates genomic plasticity among diplomonads and significant lateral gene transfer in eukaryote genome evolution. BMC Genomics 8, 51. 5. Rogers, M.B., and Keeling, P.J. (2003). Lateral gene transfer and re-compartmentalisation of Calvin cycle enzymes in plants and algae. J. Mol. Evol. 58, 367–375. 6. Richards, T.A., Dacks, J.B., Jenkinson, J.M., Thornton, C.R., and Talbot, N.J. (2006). Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr. Biol. 16, 1857–1864. 7. Friesen, T.L., Stukenbrock, E.H., Liu, Z., Meinhardt, S., Ling, H., Faris, J.D., Rasmussen, J.B., Solomon, P.S., McDonald, B.A., and Oliver, R.P. (2006). Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genet. 38, 953–956.
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8. Mower, J.P., Stefanovic, S., Young, G.J., and Palmer, J.D. (2004). Plant genetics: gene transfer from parasitic to host plants. Nature 432, 165–166. 9. Davis, C.C., and Wurdack, K.J. (2004). Host-toparasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305, 676–678. 10. Davis, C.C., Anderson, W.R., and Wurdack, K.J. (2005). Gene transfer from a parasitic flowering plant to a fern. Proc. Biol. Sci. 272, 2237–2242. 11. Stegemann, S., and Bock, R. (2009). Exchange of genetic material between cells in plant tissue grafts. Science 324, 649–651. 12. Won, H., and Renner, S.S. (2003). Horizontal gene transfer from flowering plants to Gnetum. Proc. Natl. Acad. Sci. USA 100, 10824–10829. 13. Bergthorsson, U., Richardson, A.O., Young, G.J., Goertzen, L.R., and Palmer, J.D. (2004). Massive horizontal transfer of mitochondrial genes from diverse land plant
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15.
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17.
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donors to the basal angiosperm Amborella. Proc. Natl. Acad. Sci. USA 101, 17747–17752. Diao, X., Freeling, M., and Lisch, D. (2006). Horizontal transfer of a plant transposon. PLoS Biol. 4, e5. Vallenback, P., Jaarola, M., Ghatnekar, L., and Bengtsson, B.O. (2008). Origin and timing of the horizontal transfer of a PgiC gene from Poa to Festuca ovina. Mol. Phylogenet. Evol. 46, 890–896. Silva, J.C., and Kidwell, M.G. (2000). Horizontal transfer and selection in the evolution of P elements. Mol. Biol. Evol. 17, 1542–1557. Brown, N.J., Newell, C.A., Stanley, S., Chen, J.E., Perrin, A.J., Kajala, K., and Hibberd, J.M. (2011). Independent and parallel recruitment of preexisting mechanisms underlying C4 photosynthesis. Science 331, 1436–1439. Christin, P.-A., Salamin, N., Savolainen, V., Duvall, M.R., and Besnard, G. (2007). C4 photosynthesis evolved in grasses via parallel
Visual Perception: Understanding Visual Cues to Depth A new study shows that, in vision, object blur can be a more accurate depth cue than stereo disparity. Jenny C.A. Read Most amateur photographers will have produced snapshots in which the faces of their loved ones are hazy blurs, while the tree behind is in sharp focus. Blur carries information about the object distance, but this information is usually considered to be weak and qualitative, compared to the sharp, quantitative depth provided by stereo disparity [1]. Indeed, stereo vision is often referred to simply as ‘3D’, and forms the basis of the vivid depth in modern 3D TV and cinema. A study reported in this issue of Current Biology by Held, Cooper and Banks [2] provides evidence that these two cues complement each other — and that blur can sometimes be the more accurate guide to depth. The simplest possible imaging system, a pinhole camera, samples light rays passing through a single point. In such a system, position in the image indicates the direction from which each light ray came, but there is no unambiguous information about the distance of the object which emitted that light. Nevertheless, even in such a simple system, depth can be deduced from cues such as shading, texture gradients, and perspective. Over the centuries, artists have learnt how to mimic these so as to produce the illusion of depth on the flat surface of a painting. However, these cues
require assumptions about the world, and when these are violated, the results can be misleading (Figure 1). Distance can, however, be solved for directly if one is able to compare two different light-rays emanating from the same point. This requires sampling the
adaptive genetic changes. Curr. Biol. 17, 1241–1247. 19. Christin, P.-A., Salamin, N., Muasya, M., Roalson, E.H., Russier, F., and Besnard, G. (2008). Evolutionary switch and genetic convergence on rbcL following the evolution of C4 photosynthesis. Mol. Biol. Evol. 25, 2361–2368. 20. Riera-Lizarazu, O., Rines, H.W., and Phillips, R.L. (1996). Cytological and molecular characterization of oat x maize partial hybrids. Theor. Appl. Genet. 93, 123–135.
School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA. E-mail: [email protected] DOI: 10.1016/j.cub.2012.01.043
optic array at multiple locations: not one pinhole camera, but several (Figure 2). Our visual systems do this in several ways. For example, we may move our heads so as to sample the optic array at different locations over time. This motion parallax is exploited by birds when they bob their heads back and forth. Second, our two eyes sample the optic array simultaneously at two different locations about 6 cm apart, enabling us to extract the disparity between an object’s image-position in the two eyes. Third, our pupils are not pinholes but have
Figure 1. Giant Boy: Ames Room at the Edinburgh World of Illusions. The room is trapezoidal; the woman is much further from the viewer than the child, and so subtends a similar angle on the retina even though she is much taller. Our brains interpret the perspective information on the false assumption that the room is rectangular. The child therefore appears enormous. Photo by Erika Fanselow.
model of speech acquisition developed further and tested with caregiver reformulations as input to an infant computer model that learns the pronunciation of words [11,12]. Independently, the Asada group in Osaka [13,14] have also used reformulation/mirroring by a caregiver to train vowel qualities in a physical vocal tract model. Returning to the first question identified by MacDonald et al. [4], of why self-monitoring is delayed, it is not surprising within this new paradigm that reliance on auditory information for self-monitoring comes late in a child’s speech development. The starting point for speech production is motor exploration and the proposal is that an infant has no early need to reconceive his speech sounds in auditory terms in order to compare and evaluate his production with that of others. As auditory feedback is then only a secondary sensory information source for speech sounds, its use will develop accordingly. For haptic and spatial information, Gori et al. [15] recently found that one sense dominates totally in tests of multisensory integration in children up to 8 years of age. Reviewing this and recent papers reporting similar results, Ernst [16] said that it is unclear why integration emerges so late, but argued that it is unlikely to only be the result of the challenges caused by growth and sensory reorganisation. Whatever the reasons, young children do ignore sensory data that they do not consider to be primary. Children who are usually a little older than the toddlers tested by MacDonald
et al. [4] have often been reported to persist with the pronunciation of an incorrect word form, even when they deploy the speech sound they need elsewhere. The phenomena are discussed under various labels: ‘‘fis/fish’’, ‘‘puzzle/puddle/puggle’’, ‘‘guck’’ for ‘‘duck’’ (persistently), and so on. The puzzle is that the child hears adult speech correctly, but not, it seems, his own. Out of a range of hypotheses addressing this (summarised in [17,18]), none conclusively explains the whole range of situations where children are apparently oblivious to the reality of what they are saying. MacDonald et al.’s [4] results suggest that these behaviours may not be the manifestation of a novel absence of attention by a child to his own output, but a continuation of what is systematic in the behaviour of toddlers.
9.
10.
11.
12.
13.
14.
References 1. Houde, J.F., and Jordan, M.I. (1998). Sensorimotor adaptation in speech production. Science 279, 1213–1216. 2. Fry, D.B. (1968). The phonemic system in children’s speech. Br J. Disord. Commun. 3, 13–19. 3. Kuhl, P.K. (2000). A new view of language acquisition. Proc. Natl. Acad. Sci. USA 97, 11850–11857. 4. MacDonald, E.N., Johnson, E.K., Forsythe, J., Plante, P., and Munhall, K.G. (2012). Children’s development of self-regulation in speech production. Curr. Biol. 22, 113–117. 5. Gros-Louis, J., West, M.J., and King, A.P. (2010). Comparative perspectives on the missing link: communicative pragmatics. In The Oxford Handbook of Developmental and Comparative Neuroscience, M.S. Blumberg, J.H. Freeman, and S.R. Robinson, eds. (OUP), pp. 684–707. 6. Goldstein, M.H., and Schwade, J.A. (2010). From birds to words: perception of structure in social interactions guides vocal development and language learning. In The Oxford Handbook of Developmental and Comparative Neuroscience, M.S. Blumberg,
Horizontal gene transfer has been increasingly documented between eukaryotes, but a new study suggests a much larger role for horizontal gene transfer in physiological adaption through the transfer of photosynthetic pathway genes.
Christin et al. [1] report in this issue of Current Biology that horizontal gene transfer (HGT) is the most likely origin of C4 photosynthetic pathway genes in
8.
15.
C4 Photosynthesis: Need a Gene? Borrow One!
Eric H. Roalson
7.
the grass genus Alloteropsis [1]. This is novel, not only because the transfer conveys a change in the functional traits of these grasses (from C3 to C4), but also because there have been an inferred four transfers of two genes
16. 17.
18.
J.H. Freeman, and S.R. Robinson, eds. (Oxford: Oxford University Press), pp. 708–729. Pawlby, S.J. (1977). Imitative interaction. In Studies in Mother-Infant Interaction, H.R. Schaffer, ed. (London: Academic Press), pp. 203–223. Heyes, C. (2010). Where do mirror neurons come from? Neurosci. Biobehav. Rev. 34, 575–583. Gattegno, C. (1962). Teaching Foreign Languages in Schools: the Silent Way, 1st edn. (Reading: Educational Explorers). Messum, P.R. (2007). The Role of Imitation in Learning to Pronounce. (London University: PhD thesis). Howard, I.S., and Messum, P.R. (2007). A computational model of infant speech development. In Speech and Computer (SpeCom XII) (Moscow: Moscow State Linguistics University), pp. 756–765. Howard, I.S., and Messum, P.R. (2011). Modeling the development of pronunciation in infant speech acquisition. Motor Control 15, 85–117. Yoshikawa, Y., Asada, M., Hosoda, K., and Koga, J. (2003). A constructivist approach to infants’ vowel acquisition through mother-infant interaction. Connection Sci. 14, 245–258. Miura, K., Yoshikawa, Y., and Asada, M. (2007). Unconscious anchoring in maternal imitation that helps finding the correspondence of caregiver’s vowel categories. Adv. Robotics 21, 1583–1600. Gori, M., Del Viva, M., Sandini, G., and Burr, D.C. (2008). Young children do not integrate visual and haptic form information. Curr. Biol. 18, 694–698. Ernst, M.O. (2008). Multisensory integration: a late bloomer. Curr. Biol. 18, R519–R521. Locke, J.L. (1979). The child’s processing of phonology. In Child Language and Communication: Minnesota Symposium on Child Psychology Volume 12, W.A. Collins, ed. (Hillsdale, NJ: LEA), pp. 83–119. Alvater-Mackensen, N., and Fikkert, P. (2010). The acquisition of the stop-fricative contrast in perception and production. Lingua 120, 1898–1909.
1112
Warner Road, London SE5 9HQ, UK. & Biological Learning Laboratory, Department of Engineering, University of Cambridge, Trumpington Street, Cambridge CB2 1PZ, UK. E-mail: [email protected], [email protected] 2Computational
DOI: 10.1016/j.cub.2012.01.032
from three different grass lineages into Alloteropsis! HGT has been demonstrated most frequently among prokaryotes [2], or from prokaryotes to eukaryotes [3], but transfers from one eukaryote to another are increasingly documented [4–7]. Plant–plant HGT has been primarily found in the transfer between a host and parasite [8–10] or through grafted stock [11], but the evidence for other types of HGT is increasing [12–15]. Most of this HGT has been found in the transfer of mitochondrial gene regions among a wide range of land plants, including mosses,
Current Biology Vol 22 No 5 R162
ferns, gymnosperms, and angiosperms [9,12,13]. Transfer of nuclear DNA among land plants has rarely been documented [14,15], and to date only found in grasses. The first documented plant–plant HGT of nuclear content was the transfer of a Mu-like transposable element (MULE) from rice to Setaria [14]. This was not entirely unexpected, as there are many well-documented cases of transposable element movement among animal species [16]. More surprising is the recently documented transfer of a functional nuclear gene between plant species [15]. There is substantial evidence for the transfer of a Poa cytosolic phosphoglucose isomerase (PgiC) gene to Festuca ovina, and there is evidence that the acquired copy has all of the necessary sequence to be expressed [15]. In fact, this transfer event was found because of an extra band in an isozyme study of these plants. As interesting as both of these cases are, it is not clear what if any functional or adaptive advantage either of these transfers convey — there is unlikely any with the MULE transfer, and there has been no indication that the PgiC transfer is in any way adaptive. The origins of C4 photosynthesis have been well documented to be complex, with at least 45 independent gains of the C4 pathway in flowering plants [17], and the strong molecular convergence in amino acid structure across numerous sites in the phosphoenolpyruvate carboxylase (ppc) gene [18]. While many photosynthesis genes have not been as rigorously tested for selection on C4 function as ppc, similar patterns have been found in some cases [19]. Selection-driven convergence in amino acid structure of critical genes in the C4 pathway complements a recently discovered set of conserved regulatory elements that appear to facilitate the repeated evolution of C4 photosynthesis [17]. All-in-all, these results suggest a rather complex pattern of convergence in an adaptive trait. Adding to this story of complex patterns of convergent evolution in C4 is the HGT of C4 pathway genes in the grass genus Alloteropsis [1]. This is of interest for several reasons. First, this is the first well-documented case of plant–plant HGT of functional genes in which there has been a presumed
adaptive advantage conveyed. Further, the Alloteropsis lineage has been the recipient of both C4-type ppc and C4-type phosphoenolpyruvate carboxykinase (pck), with three apparent transfers of ppc and one transfer of pck. These gene copies have been transferred from three different grass lineages, Andropogoneae, Cenchrinae, and Melinidinae, that diverged from Alloteropsis around 20–25 million years ago [1]. This has broad-ranging implications for adaptive diversification as it suggests that plants might be able to adapt to novel environments very quickly if HGT occurs in the right circumstances. Despite this, HGT-driven adaptive diversification does not appear to be occurring in Alloteropsis (at least not yet), as there are only five known species in the genus. While the first expectation when genes from one species are found in another is that this has happened through hybridization, there is strong evidence in this case that that is not how the ppc and pck genes were transferred. When hybridization occurs, there is a co-mingling of the genomes of the two species, and even if backcrossing to one parent leads to the genome being predominantly of one parent, we would expect there to continue to be numerous genes of the second parent present. However, in the case of Alloteropsis, Christin et al. [1] compared 454-sequenced cDNA libraries of both C4 and C3 Alloteropsis semialata to whole genome sequences of rice, Brachypodium, Sorghum, and Setaria, and found no conclusive evidence of the transfer of any of the more than 11,000 genes tested other than ppc and pck. If hybridization is not the mechanism of gene transfer, then how does HGT occur? There are several mechanisms that are most frequently postulated: vector-mediated transfer, plant–plant contact, transformation, and illegitimate pollination [1]. In the cases of HGT between a host and parasite or grafted plants, plant–plant contact is the presumed mechanism [8–11]; however, Alloteropsis and these other grass species are not known to be parasitic. These plants have not been transformed, and it is unlikely that they have come into contact with other transformed plants. While vector-mediated transfer cannot be ruled out, it seems somewhat unlikely given the complex series of events that
must happen — a vector must capture the ppc or pck gene, move to Alloteropsis from the donor plant, and then successfully insert the gene into the germ line. This leaves us with illegitimate pollination. What is the likelihood of that? Since these grasses are all wind pollinated, and therefore make prodigious amounts of pollen, the deposition of pollen from a nearby C4 grass on the stigma of Alloteropsis seems plausible. It is known that foreign grass pollen can germinate on a stigma, and in the laboratory, chromosomes have been transferred from maize to oats (more than 45 Ma divergence) through forced crossing and embryo rescue with resulting fertile plants [20]. This results in an embyo with unequal DNA contributions from the two parents — in some cases only a single chromosome from the pollen donor. Despite the plausibility of illegitimate pollination-mediated HGT in these grasses, there is yet to be evidence supporting this mechanism over others. It will be important to determine which of these mechanisms allow for HGT in plants, how to discriminate which mechanism is at work, and clarify the role of HGT in adaptation and lineage diversification. Is what we see in Alloteropsis the rare special case, or the tip of the iceberg? References 1. Christin, P.-A., Edwards, E.J., Besnard, G., Boxall, S.F., Gregory, R., Kellogg, E.A., Hartwell, J., and Osborne, C.P. (2012). Adaptive evolution of C4 photosynthesis through recurrent lateral gene transfer. Curr. Biol. 22, 445–449. 2. Koonin, E.V., Makarova, K.S., and Aravind, L. (2001). Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 55, 709–742. 3. Keeling, P.J., and Palmer, J.D. (2008). Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9, 605–618. 4. Andersson, J.O., Sjo¨gren, A˚.M., Horner, D.S., Murphy, C.A., Dyal, P.L., Sva¨rd, S.G., Logsdon, J.M., Ragan, M.A., Hirt, R.P., and Roger, A.J. (2007). A genomic survey of the fish parasite Spironucleus salmonicida indicates genomic plasticity among diplomonads and significant lateral gene transfer in eukaryote genome evolution. BMC Genomics 8, 51. 5. Rogers, M.B., and Keeling, P.J. (2003). Lateral gene transfer and re-compartmentalisation of Calvin cycle enzymes in plants and algae. J. Mol. Evol. 58, 367–375. 6. Richards, T.A., Dacks, J.B., Jenkinson, J.M., Thornton, C.R., and Talbot, N.J. (2006). Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr. Biol. 16, 1857–1864. 7. Friesen, T.L., Stukenbrock, E.H., Liu, Z., Meinhardt, S., Ling, H., Faris, J.D., Rasmussen, J.B., Solomon, P.S., McDonald, B.A., and Oliver, R.P. (2006). Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genet. 38, 953–956.
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8. Mower, J.P., Stefanovic, S., Young, G.J., and Palmer, J.D. (2004). Plant genetics: gene transfer from parasitic to host plants. Nature 432, 165–166. 9. Davis, C.C., and Wurdack, K.J. (2004). Host-toparasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305, 676–678. 10. Davis, C.C., Anderson, W.R., and Wurdack, K.J. (2005). Gene transfer from a parasitic flowering plant to a fern. Proc. Biol. Sci. 272, 2237–2242. 11. Stegemann, S., and Bock, R. (2009). Exchange of genetic material between cells in plant tissue grafts. Science 324, 649–651. 12. Won, H., and Renner, S.S. (2003). Horizontal gene transfer from flowering plants to Gnetum. Proc. Natl. Acad. Sci. USA 100, 10824–10829. 13. Bergthorsson, U., Richardson, A.O., Young, G.J., Goertzen, L.R., and Palmer, J.D. (2004). Massive horizontal transfer of mitochondrial genes from diverse land plant
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donors to the basal angiosperm Amborella. Proc. Natl. Acad. Sci. USA 101, 17747–17752. Diao, X., Freeling, M., and Lisch, D. (2006). Horizontal transfer of a plant transposon. PLoS Biol. 4, e5. Vallenback, P., Jaarola, M., Ghatnekar, L., and Bengtsson, B.O. (2008). Origin and timing of the horizontal transfer of a PgiC gene from Poa to Festuca ovina. Mol. Phylogenet. Evol. 46, 890–896. Silva, J.C., and Kidwell, M.G. (2000). Horizontal transfer and selection in the evolution of P elements. Mol. Biol. Evol. 17, 1542–1557. Brown, N.J., Newell, C.A., Stanley, S., Chen, J.E., Perrin, A.J., Kajala, K., and Hibberd, J.M. (2011). Independent and parallel recruitment of preexisting mechanisms underlying C4 photosynthesis. Science 331, 1436–1439. Christin, P.-A., Salamin, N., Savolainen, V., Duvall, M.R., and Besnard, G. (2007). C4 photosynthesis evolved in grasses via parallel
Visual Perception: Understanding Visual Cues to Depth A new study shows that, in vision, object blur can be a more accurate depth cue than stereo disparity. Jenny C.A. Read Most amateur photographers will have produced snapshots in which the faces of their loved ones are hazy blurs, while the tree behind is in sharp focus. Blur carries information about the object distance, but this information is usually considered to be weak and qualitative, compared to the sharp, quantitative depth provided by stereo disparity [1]. Indeed, stereo vision is often referred to simply as ‘3D’, and forms the basis of the vivid depth in modern 3D TV and cinema. A study reported in this issue of Current Biology by Held, Cooper and Banks [2] provides evidence that these two cues complement each other — and that blur can sometimes be the more accurate guide to depth. The simplest possible imaging system, a pinhole camera, samples light rays passing through a single point. In such a system, position in the image indicates the direction from which each light ray came, but there is no unambiguous information about the distance of the object which emitted that light. Nevertheless, even in such a simple system, depth can be deduced from cues such as shading, texture gradients, and perspective. Over the centuries, artists have learnt how to mimic these so as to produce the illusion of depth on the flat surface of a painting. However, these cues
require assumptions about the world, and when these are violated, the results can be misleading (Figure 1). Distance can, however, be solved for directly if one is able to compare two different light-rays emanating from the same point. This requires sampling the
adaptive genetic changes. Curr. Biol. 17, 1241–1247. 19. Christin, P.-A., Salamin, N., Muasya, M., Roalson, E.H., Russier, F., and Besnard, G. (2008). Evolutionary switch and genetic convergence on rbcL following the evolution of C4 photosynthesis. Mol. Biol. Evol. 25, 2361–2368. 20. Riera-Lizarazu, O., Rines, H.W., and Phillips, R.L. (1996). Cytological and molecular characterization of oat x maize partial hybrids. Theor. Appl. Genet. 93, 123–135.
School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA. E-mail: [email protected] DOI: 10.1016/j.cub.2012.01.043
optic array at multiple locations: not one pinhole camera, but several (Figure 2). Our visual systems do this in several ways. For example, we may move our heads so as to sample the optic array at different locations over time. This motion parallax is exploited by birds when they bob their heads back and forth. Second, our two eyes sample the optic array simultaneously at two different locations about 6 cm apart, enabling us to extract the disparity between an object’s image-position in the two eyes. Third, our pupils are not pinholes but have
Figure 1. Giant Boy: Ames Room at the Edinburgh World of Illusions. The room is trapezoidal; the woman is much further from the viewer than the child, and so subtends a similar angle on the retina even though she is much taller. Our brains interpret the perspective information on the false assumption that the room is rectangular. The child therefore appears enormous. Photo by Erika Fanselow.