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Animal Asymmetry View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Magazine R473 Cytoplasmic transport of the BBSome Primer PCM-1 Rab8GDP Animal asymmetry Rabin8 A. Richard Palmer Rab8GTP For decades morphological BBS8 BBS4 asymmetries have evoked curiosity BBIP10 Docking and fusion of vesicles and wonder (Figure 1). Although BBS1 with the base of the cilium BBS2 largely studied by natural history connoisseurs, many wonderful stories emerged: for instance, lopsided BBS7 BBS9 flatfish that lie on one side of their body and have both eyes on the BBS5 other; the narwhal’s spectacular, sinistrally- coiled and left-sided tusk; Leptin receptor Velella velella, the by-the-wind sailor that drifts on the ocean surface and Sensing of fat stores has right- and left-sailing forms; the and weight-lowering response Current Biology ability of oppositely coiled snails to mate — sometimes it’s easy and sometimes it’s not; male theridiid Figure 1. Molecular interactions of the BBSome. See text for details. spiders that rip off one palp and eat it, leaving only one for mating; male problems and defects in mucus What remains to be explored? fiddler crabs with a massive claw (up clearance that are characteristic of Nearly everything! What are the to 40% of body weight) that is used primary cilliary dyskinesia, a disorder membrane proteins that require for signaling and fighting. of motile cilia. the BBSome for their trafficking? Morphological asymmetry is Does the BBSome function only in one of those exceedingly rare Anything related to signaling? This trafficking to cilia or is it also involved characteristics of animals (and is one of the most exciting aspects of in IFT or trafficking out of cilia? protists and plants) that has evolved primary cilium biology and BBSome What is the molecular activity of the independently many times (Table 1). function. In the ear of bbs knockout BBSome? Does it have any enzymatic In a 1932 compilation not since animals, hair cells frequently fail to activity? What is the function of the equaled, Wilhelm Ludwig tallied align with one another, a characteristic BBS proteins that do not belong to all known examples and kinds of of defective planar cell polarity (PCP). the BBSome? In particular, does animal asymmetries: large, small, Although cilia are now known to be BBS3/Arl6 function in vesicular bilateral, helical, morphological essential for PCP in vertebrates, no trafficking? How and where is the and behavioral. But little general one knows the identity of the relevant BBSome assembled? Do the type II insight emerged from this Herculean signals sensed and transduced by chaperonin-like BBS proteins BBS6, exercise other than an attempt cilia. Do cilia sense a morphogen BBS10 and BBS12 play a role in to standardize terminology, some gradient that instructs polarity within the folding or assembly of BBSome speculations on common causes, the plane of the epithelium? Or are subunits? and a nearly 100-page screed on cilia facilitating planar cell polarization handed behavior in humans and established at cell–cell contacts by Where can I find out more? other primates, a subject that, Fliegauf, M., Benzing, T., and Omran, H. (2007). relaying a permissive signal? On the When cilia go bad: cilia defects and ciliopathies. astonishingly, remains poorly obesity front, bbs mutant mice are Nat. Rev. Mol. Cell. Biol. 8, 880–893. understood even today. Nachury, M.V., Loktev, A.V., Zhang, Q., Westlake, unable to transduce leptin signals in C.J., Peränen, J., Merdes, A., Slusarski, D.C., specialized hypothalamic neurons that Scheller, R.H., Bazan, J.F., et al. (2007). A core A simplified perspective control feeding behavior. Since the complex of BBS proteins cooperates with the on morphological asymmetry GTPase Rab8 to promote ciliary membrane leptin receptor was found to interact biogenesis. Cell 129, 1201–1213. Despite the great diversity of with a BBSome subunit, it has been Pazour, G.J., and Bloodgood, R.A. (2008). Targeting asymmetrical forms, a focus proteins to the ciliary membrane. Curr. Top. Dev. hypothesized that the leptin receptor Biol. 85, 115–149. solely on direction of asymmetry may get trafficked to cilia by the Seo, S., Guo, D.F., Bugge, K., Morgan, D.A., renders broad-scale comparative BBSome. However, to this date, no one Rahmouni, K., and Sheffield, V.C. (2009). studies of asymmetry variation Requirement of Bardet-Biedl syndrome proteins has succeeded in visualizing the leptin for leptin receptor signaling. Hum. Mol. Genet. tractable. This is because the receptor in cilia of the relevant neuronal 18, 1323–1331. development and evolution of a cell types. Nonetheless, the discovery simple and well- defined qualitative that IFT dysfunction also causes Department of Molecular and Cellular trait — direction of asymmetry — can Physiology, Stanford University School unregulated weight gains in mice of Medicine, 279 Campus Drive, Stanford, be easily compared among makes the ciliary hypothesis of leptin CA 94305-5345, USA. organisms with very different body signaling extremely appealing. *E-mail: [email protected] plans. If only direction is considered, Current Biology Vol 19 No 12 R474 two-allele polymorphism, a result made somewhat puzzling by the fact that either dextral or sinistral may be dominant. In flatfish, eye-side inheritance has only been studied in starry flounder, a rare polymorphic species whose eye-side frequencies depart significantly from random. Eye side is clearly heritable, but, curiously, only about 70%. Some odd observations in cultivated flatfish raise eyebrows even further. Despite the rarity of reversed individuals in nature, flatfish in cultivation exhibit up to 20% reversal, suggesting that eye- side determination remains sensitive to environmental effects. Another peculiar mode of inheritance involves an internal, anatomical asymmetry. Like all vertebrates, mice have an asymmetrical, left-sided heart. Curiously, heart side is random in iv mutant mice, regardless of the parents’ direction of asymmetry. Figure 1. Examples of morphological asymmetries in different animal groups. Therefore, unlike snails, the two (A) Bothus lunatus, a flatfish whose eyes lie on the left side of the head (photo by Arthur Anker). alleles are not for left and right, but (B) Amphidromus heerianus, a polymorphic snail having both dextral (left image) and sinistral (right image) forms (photo by Bill Frank). (C) Chama lazarus, a bivalve that cements one valve to for left and random. the substratum, in this case, the left one (photo by George Sangiouloglou). (D) Pandora inaequiv- alvis, a bivalve that lies horizontally near the sediment-water interface on either the right or left Random asymmetry: inheritance valve (photo with permission from www.femorale.com). (E) Torquirhynchia, a brachiopod where A more consistent, albeit surprising, the dorsal (upper) and ventral (lower) valves are raised on one side (right side of valve in this pattern of inheritance emerges from image) at random (reproduced with permission from Fürsich, F. T. and T. Palmer (1984). Commis- studies of random asymmetries sural asymmetry in brachiopods. Lethaia 17, 251–265. With permission from Wiley-Blackwell). (F) Verruca sp., a peculiar group of barnacles with only two movable opercular plates, the re- (Table 1, Figure 1). Because maining two (right or left at random) are fused into the rigid ring of lateral wall plates. (G) Circeis dextral and sinistral forms are amoricana, a coiled tube-building polychaete (Spirorbinae); tubes attach to the substratum along equally common in such species, the dorsal or ventral side so the worm’s body bends to the right or left (photo by Tara Macdon- tests for inheritance are easier to ald). (H) Spirographis, a feather-duster type polychaete worm with a coiled tentacle fan (photo conduct. Remarkably, among 13 by Cristophe Quintin). (I) Loxia leucoptera, a crossbill finch where the upper mandible crosses animal studies only one suggested randomly to the left or right of the lower one (to the left here) (photo by Frode Falkenberg, www. cyberbirding.no). (J) Neotrypaea californiensis, a large male thalassinid mud shrimp with a greatly that direction of asymmetry was enlarged right claw (photo by Greg Jensen). inherited, and doubts remain about that exception. Add to this even three types of conspicuous What role do genes and environment more results from plants — in 15 of asymmetry typically occur within play in the evolutionary origin of 16 cases direction is not inherited — species: dextral (all individuals morphological asymmetry (i.e., in and a broad generalization emerges. right- sided or dextrally coiled), the breaking of symmetry during With only one exception — albeit sinistral (all individuals left-sided development when morphological a highly informative one (see or sinistrally coiled) or random (half asymmetries first appear below) — direction of asymmetry of the individuals are right/dextral evolutionarily)? is not inherited in cases of random and half are left/sinistral; sometimes asymmetry. called antisymmetry). An even Fixed asymmetry: inheritance In cases of random asymmetry, simpler grouping is: fixed asymmetry Fixed asymmetries occur in many therefore, right-sided and left-sided (all individuals asymmetrical in groups (Figure 1, Table 1), and may are conspicuous phenotypic variants the same direction, regardless of be either right-sided (dextral) or that almost always lack a genetic direction) and random asymmetry. left-sided (sinistral). In most such basis. This lack of a heritable basis One or more of these kinds of species, reversed individuals occur to direction of asymmetry raises asymmetry occur in the external form occasionally. These variants permit some fascinating questions about of many animal groups (Table 1), as breeding studies to test whether how right and left forms develop. they do in internal organs. direction of asymmetry is controlled Perhaps direction is entirely Two questions emerge: of what by a few or many genes. The answer stochastic, or random influences significance is the observation that is mixed.
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