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To cite this version:
Qiyan Mao, Thomas Lecuit. Evo–Devo: Universal Toll Pass for the Extension Highway?. Current
Biology - CB, Elsevier, 2016, 26 (14), pp.R680 - R683. �10.1016/j.cub.2016.05.063�. �hal-01692750�
region. Because of the repulsive nature of spatial adaptation, adaptation to such an expanded region could produce a perceptual shrinkage of a subsequently viewed object. However, as with the depth adaptation explanation above, this cannot explain the opposite direction of effects for the test textures and test objects.
Separate Mechanisms for Coding Density and Object Size
How do Hisakaet al.[6]explain their shrinkage results? They opine that perceived distance is computed by summing neural signals that each express a unit of length along the path from one point to another in the image. Adaptation to a dense texture might reduce the perceptual length associated with the length of the unit, akin to the way that contrast adaptation reduces the
apparent contrast of subsequently viewed stimuli[11].
Whatever the cause of the shrinkage, it is the fact that it goes in the opposite direction to the texture density aftereffect that is the intriguing and challenging part of Hisakataet al.’s[6]study. A possible clue to the resolution of this paradox lies in existing models of texture density coding[12–15]. These models all assume that there is an initial stage in which the markings on a textured surface are
‘picked up’ by arrays of neurons, such as simple cells in the visual cortex, that are sensitive to the markings’ positions, sizes and orientations. Although the details of the models vary as to what comes next, all share the idea that subsequent neural processes convert those responses via a cascade of filtering operations into an explicit representation of density (or relative density). During this process, information about the positions of individual texture markings is lost. In other words the resulting density signal is agnostic to the local position
information that gives rise to it. If this view of density coding is correct, something altogether different must be going on when the visual system estimates the separation between parts of an object, as the paradox revealed by Hisakaet al.
implies.
Although we do not yet have a definitive explanation for the object shrinkage from texture density
adaptation demonstrated by Hisakata et al.[6], their study will doubtless set in motion a new line of inquiry into the encoding of spatial relationships in human vision.
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Evo–Devo: Universal Toll Pass for the Extension Highway?
Qiyan Mao and Thomas Lecuit
Aix-Marseille Universite´, CNRS, IBDM UMR7288, Campus de Luminy, case 907. 13009, Marseille, France
Correspondence:[email protected] http://dx.doi.org/10.1016/j.cub.2016.05.063
The distinction between long-germ and short-germ insects is a classic one in evo-devo, yet a common genetic mechanism may underlie germband extension in all insects, even all arthropods.
When Gerhard Krause coined[1](and Klaus Sander later elaborated[2]) the terms long-, intermediate- or short-germ to classify insect embryos, he was referring to the proportion of segments determined prior to gastrulation. Long- germ insects, such as the fruit fly
Drosophila melanogaster, specify most of their segments simultaneously at the blastoderm stage, before gastrulation partitions the ectoderm, mesoderm and endoderm. By contrast, short-germ insects start gastrulation with only a few segments, and then add segments more R680 Current Biology26, R667–R688, July 25, 2016ª2016 Published by Elsevier Ltd.
progressively from an undifferentiated
‘growth zone’ at the posterior end[3].
Taken at face value, one may think that long- and short-germ insects must use quite distinct mechanisms to elongate their anteroposterior body axis: the former extend a preset amount of germband tissue via convergent- extension cell movements[4–6], while the latter incorporate more tissue into the germband via cell proliferation[7]. In vertebrates, both processes contribute to axis extension[8]. However, the pattern and extent of cell proliferation in insect growth zones do not appear consistent with a proliferation-driven segmentation model[3]. Moreover, recent findings suggest that in a short-germ insect, the beetleTribolium castaneum, germband extension by the growth zone may rely on cell rearrangements too [9,10]. In light of this, one may speculate that a common cell movement-based mechanism for germband extension is employed in all insects. But how do we know if this is the case?
One way of testing this is to look for a common molecular mechanism of germband extension in a diverse range of insects. In a recentCurrent Biologypaper, Bentonet al.[11]
looked within and beyond insects, and argue that the last common ancestor of all arthropods may have utilized a set of Toll receptors to instruct germband extension, similar to the situation in Drosophila[12].
InDrosophila,it has long been established that the gene network that controls segmentation — in particular, the pair-rule genes — also drives germband extension[4–6]. Genetic links between the upstream pair-rule transcription factors and the planar cell polarization of the germband epithelial cells required for convergent extension recently emerged[12]. The Toll receptors, Toll-2, Toll-6, and Toll-8, which are expressed in characteristic stripe patterns, are downstream targets of the pair-rule geneeven-skippedand required for germband epithelium planar cell polarization and cell intercalation (Figure 1B, D, E)[12]. These Toll receptors belong to a distinct subgroup of Toll genes better known for their roles
in cell adhesion and communication than in innate immunity[13–15]. Given that Toll receptors are of an ancient origin dating back to the last common ancestor of all eumetazoans[14], it is plausible that homologous Toll receptors exist in other insects and non-insect arthropods.
However, theDrosophilasegmentation network is considered to be highly derived with respect to the ancestral mode [3,7]. Is the control of the Toll receptors by the segmentation network just another fruit fly innovation[16]? Or, is this an ancient feature of the system?
The quickest way of finding out is to look for striped expression of the Toll receptor homologues in various arthropod species.
Bentonet al.[11]did exactly that. With a strategically sampled dataset
composed of three other holometabolus insects (the short-germ beetleTribolium castaneum, the intermediate-germ milkweed bugOncopeltus fasciatus, and the long-germ waspNasonia vitripennis), one hemimetabolus insect (the short- germ cricketGryllus bimaculatus), one
amphipod crustacean (Parhyale hawaiensis), one myriapod (the centipedeStrigamia maritima) and one chelicerate (the common house spider Parasteatoda tepidariorum) (Figure 1A), the authors reconstructed the
phylogenetic relationships of Toll homologues in these species.
Several Toll homologues from each species clustered with the pair-rule regulated Toll-2, 6, and 8 ofDrosophila.The authors gave this clade of Toll receptors a whimsical name Loto (Long-Toll), since its members are characterized by more leucine rich repeats, extracellular motifs
predicted to mediate intercellular adhesion and communication[14].
Most strikingly, at least one Loto gene from each surveyed
species shows a stripy expression pattern (Figure 1C). This suggests that Loto genes are regulated by the segmentation network.
However, are they actually required for germband extension? The authors
LCA A
D Fruit fly Flour Wasp
beetle
Milkweed bug
Cricket Centipede Spider
B
C
Loto stripes “Loto code”
E
Cell intercalation Amphipod
crustacean
Current Biology
Figure 1. Toll expression and function in arthropods.
(A) Phylogeny of the eight arthropod species analyzed by Bentonet al.[11]. From left to right:
Drosophila melanogaster,Nasonia vitripennis, Tribolium castaneum,Oncopeltus fasciatus,Gryllus bimaculatus, Parhyale hawaiensis, Strigamia maritime, Parasteatoda tepidariorum. LCA: last common ancestor of all arthropods. (B, C) Schematics of aDrosophilaembryo at the blastoderm stage (B) and aTriboliumembryo at the onset of germband extension (C) showing two Loto genes expressed in distinct stripes. Boxes span a blastoderm parasegment in each embryo. (D) Schematic of two Loto genes shown at the cellular resolution, which corresponds to boxes in (B, C). (E) Schematics of a group of intercalating blastoderm cells, with shades of grey denoting different cell rows.
Current Biology26, R667–R688, July 25, 2016 R681
decided to functionally test Loto genes in two distantly related species, the beetleTriboliumand the spider Parasteatoda,where convergent extension is known to drive germband extension[9,10,17]. Satisfyingly, combined knockdown of two Loto members in each species causes severely shortened or widened germbands, a telltale sign of convergent extension defects. This is further demonstrated at the cellular level in the anterior segments of Triboliumduring germband
condensation, where cell intercalation (Figure 1E) is defective upon Loto RNAi. Taken together, the authors postulate that segmentally expressed Loto genes might constitute an ancestral axis extension mechanism dating back to the last common ancestor of all arthropods.
It has been proposed that the segment polarity genes that specify segment boundaries, such asengrailed, winglessandhedgehog, characterize a
‘phylotypic stage’ of arthropod embryonic development, as they are remarkably conserved across all arthropods, despite great variations in the upstream segmentation network[7].
If indeed the Loto genes, as proposed by Bentonet al.[11], encode an ancient mechanism for segment extension downstream of the segmentation network, then we should extend the phylotypic stage concept to include not only segment boundary formation but also axis extension within any given segment. In this new light, one may start to envision the segment as a truly autonomous building block of the arthropod body plan, with a built-in mechanism to drive its own
morphogenesis once it is specified[18].
This leads to the fascinating question of how this building block may have evolved at the dawn of segmented animals.
As pointed out by the authors[11], some technical limitations call for cautious interpretation of some of the data. Direct observation of cell intercalation defects upon Loto RNAi was only feasible in the anterior-most blastodermal segments ofTribolium during germband condensation. These segments are specified prior to
gastrulation, and thus are not part of the growth zoneper se. The fact that germband extension is severely affected in growth zone segments suggests that Tolls might have a common function in cell intercalation in both the blastodermal and the growth zone segments [9,10,19].
However, direct observation of cell movements in the growth zone is lacking.
Therefore, it will be important to elucidate whether and, if so, how Lotos regulate cell intercalation within the growth zone. Along the same line, direct evidence for the role of Lotos in regulating cell behavior during Parasteatodagermband extension will greatly enhance the mechanistic validity of the proposed ancient ‘morphogenetic module’.
The study by Bentonet al.[11]opens up several future lines of inquiry. First, in other arthropod groups, such as crustaceans and centipedes, what roles do the Loto genes play during
segmentation and axis elongation?
Second, as the Toll genes predate the diversification of all bilaterians, do they play a role in axis extension in non- arthropods too? If we walk away from arthropods and look into another group of segmented protostomes belonging to the superphylum Lophotrochozoa, the annelids, where pair-rule genes may not be involved in segmentation[20], do we expect to see Lotos at play downstream of a heterologous segmentation network? Last but not least, the proposed model for Loto function inDrosophila describes a precise combinatorial positional code[12]. In light of the likely conserved function of Tolls in a diverse range of species and tissue contexts, an important
future question is how such a code would work? What are the molecular mechanisms linking Toll receptors and intracellular planar polarity? Answers to these questions will provide greater insights into the evolution and mechanism of Toll genes in embryonic morphogenesis[14].
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1.Krause, G. (1939). Die Eitypen der Insekten (Thieme).
2.Sander, K. (1976). Specification of the basic body pattern, In Insect Embryogenesis,vol. 12 (Elsevier), pp. 125–238.
3.Chipman, A.D. (2015). Hexapoda:
comparative aspects of early development. In Evolutionary Developmental Biology of Invertebrates 5 (Vienna: Springer Vienna), pp. 93–110.
4.Irvine, K.D., and Wieschaus, E. (1994). Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development120, 827–841.
5.Zallen, J.A., and Wieschaus, E. (2004).
Patterned gene Expression directs bipolar planar polarity in Drosophila. Dev. Cell6, 343–355.
6.Bertet, C., Sulak, L., and Lecuit, T. (2004).
Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature429, 667–671.
7.Peel, A.D., Chipman, A.D., and Akam, M. (2005).
Arthropod segmentation: beyond the Drosophila paradigm. Nat. Rev. Genet.6, 905–916.
8.Steventon, B., Duarte, F., Lagadec, R., Mazan, S., Nicolas, J.-F., and Hirsinger, E. (2016).
Species-specific contribution of volumetric growth and tissue convergence to posterior body elongation in vertebrates. Development 143, 1732–1741.
9.Nakamoto, A., Hester, S.D., Constantinou, S.J., Blaine, W.G., Tewksbury, A.B., Matei, M.T., Nagy, L.M., and Williams, T.A. (2015).
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10.Sarrazin, A.F., Peel, A.D., and Averof, M.
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(2016). Toll genes have an ancestral role in axis elongation. Curr. Biol.26, 1609–
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(2014). A positional Toll receptor code directs convergent extension in Drosophila. Nature 515, 523–527.
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(1994). The Drosophila 18 wheeler is required for morphogenesis and has striking similarities to Toll. Development120, 885–899.
R682 Current Biology26, R667–R688, July 25, 2016
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20.Seaver, E.C., Yamaguchi, E., Richards, G.S., and Meyer, N.P. (2012). Expression of the pair-rule gene homologs runt , Pax3/7, even-skipped-1 and even-skipped-2 during larval and juvenile development of the polychaete annelid Capitella teleta
does not support a role in segmentation.
EvoDevo3, 8.
CRISPR–Cas: Spacer Diversity Determines the Efficiency of Defense
Anna Lopatina and Rotem Sorek*
Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 76100, Israel
*Correspondence:[email protected] http://dx.doi.org/10.1016/j.cub.2016.05.034
Bacterial CRISPR–Cas systems acquire short sequences, called spacers, from viruses and plasmids, leading to adaptive immunity. The diversity of spacers within natural bacterial populations is very high. New data now explain how spacer diversity strengthens resistance of the bacterial population to phage infection.
Viruses that infect bacteria (phages) shape bacterial population abundance and community structure in numerous habitats worldwide. The continuous evolutionary arms race between bacteria and phages resulted in the appearance of a broad range of defense mechanisms in bacteria and a high, mostly unexplored diversity of anti-defense strategies in phages. Bacteria have evolved two kinds of defense systems. Innate-immunity systems include restriction-modification systems[1], argonaute-based RNAi-like mechanisms[2], abortive infection[3], and other systems that serve to restrict incoming foreign DNAs[4,5]. Many bacteria also utilize CRISPR–Cas systems, which represent the adaptive defense system of prokaryotes. As part of CRISPR–Cas defense, bacteria acquire short sequences (spacers) from the genomes of phages or plasmids, and insert these spacers into the CRISPR array locus to build the immune memory.
Transcription products of newly acquired spacers are then used as molecular guides by Cas proteins to degrade complementary foreign nucleic acids.
The natural diversity of spacers within bacterial populations is known to be very high. Thousands of different spacers can be found in natural bacterial communities,
from the very simple communities in Antarctic snow samples[6]to more complex ones like the human gut microbiota[7]. This diversity leads to a population in which otherwise clonal bacteria contain different spacers against phage invaders[8]. The benefit of spacer diversity is now explained in a recent study by van Houteet al.[9], who, using experimental infection studies, have shown that phages cannot overcome CRISPR–Cas defense by point mutations in their genomes when spacer diversity in the population is sufficiently high.
van Houteet al.[9]established a co- evolutionary experimental system using Pseudomonas aeruginosaand its phage, DMS3vir, and monitored viral titers at certain time points after infection. Firstly, they showed that phages that infected bacteria lacking CRISPR–Cas persisted in the experimental system during 30 days of co-incubation, whereas phages that infected bacteria containing a type I–F CRISPR–Cas system went extinct at five days post-infection. They found that bacteria with CRISPR–Cas developed immunity through the acquisition of new spacers, whereas CRISPR-less bacteria developed immunity through mutations that led to loss or masking of the surface receptor recognized by the phage.
The authors were surprised by the rapid extinction of phages upon infection of CRISPR-containing bacteria because phages can in principle gain point mutations to rapidly escape CRISPR–Cas immunity. They suspected that spacer diversity within the population may be responsible for this effect, and therefore designed an experiment in which they generated bacterial populations with varying levels of spacer diversity:
monocultures, in which all bacteria contain a single spacer against DMS3vir, and polycultures consisting of equal mixtures of clones each carrying one distinct, but different, spacer against the phage. The authors then experimented with populations containing either 1, 6, 12, 24 or 48 clones, with each clone carrying a different individual spacer against DMS3vir. All bacterial populations were infected by DMS3vir and viral titers were monitored over time. The results were quite striking: whereas populations with low initial spacer diversity led to phage persistence and escape from CRISPR immunity, phage became extinct in those populations with high spacer diversity (Figure 1).
van Houteet al.[9]further showed that after one day of co-incubation, phages infecting the monocultures developed Current Biology26, R667–R688, July 25, 2016ª2016 Elsevier Ltd. R683
