EvoDevo | |
Developmental coupling of larval and adult stages in a complex life cycle: insights from limb regeneration in the flour beetle, Tribolium castaneum | |
Yuichiro Suzuki1  Elaine R Kim1  Christie C Sze1  Alison K Lee1  | |
[1] Department of Biological Sciences, Wellesley College, 106 Central St., Wellesley, MA 02481, USA | |
关键词: Blastema; Patterning; Tribolium castaneum; Abrupt; Spineless; Dachshund; Distal-less; Limb regeneration; | |
Others : 806402 DOI : 10.1186/2041-9139-4-20 |
|
received in 2013-03-20, accepted in 2013-06-04, 发布年份 2013 | |
【 摘 要 】
Background
A complex life cycle, such as complete metamorphosis, is a key innovation that can promote diversification of species. The evolution of a morphologically distinct larval stage is thought to have enabled insects to occupy broader ecological niches and become the most diverse metazoan taxon, yet the extent to which larval and adult morphologies can evolve independently remains unknown. Perturbation of larval limb regeneration allows us to generate larval legs and antennae with altered limb morphologies, which may be used to explore the developmental continuity that might exist between larval and adult appendages. In this study, we determined the roles of several appendage patterning transcription factors, abrupt (ab), dachshund (dac), Distal-less (Dll), and spineless (ss), in the red flour beetle, Tribolium castaneum, during larval appendage regeneration. The functions of these genes in regenerating and non-regenerating limbs were compared using RNA interference.
Results
During limb regeneration, dac and ss were necessary to re-pattern the same larval structures as those patterned during embryogenesis. Removal of these two genes led to larval appendage patterning defects that were carried over to the adult legs. Surprisingly, even though maternal knockdown of ab had minimal effects on limb allocation and patterning in the embryo, it was necessary for blastema growth, an earlier phase of regeneration. Finally, knockdown of Dll prevented the blastema-like bumps from re-differentiating into appendages.
Conclusions
Our results suggest that, similar to vertebrates, the re-patterning phase of Tribolium larval limb regeneration relies on the same genes that are used during embryonic limb patterning. Thus, the re-patterning phase of regeneration is likely to be regulated by taxon-specific patterning mechanisms. Furthermore, Ab and Dll appear to play important roles during blastema proliferation and re-differentiation, respectively. Finally, our results show that continuity exists between larval and adult limb patterning, and that larval and adult leg morphologies may be developmentally coupled. Thus, the evolution of imaginal discs may have been a key step towards completely removing any developmental constraints that existed between larval and adult phenotypes.
【 授权许可】
2013 Lee et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20140708093023482.pdf | 3937KB | download | |
Figure 7. | 36KB | Image | download |
Figure 6. | 94KB | Image | download |
Figure 5. | 145KB | Image | download |
Figure 4. | 166KB | Image | download |
Figure 3. | 101KB | Image | download |
Figure 2. | 162KB | Image | download |
Figure 1. | 106KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
【 参考文献 】
- [1]Moran NA: Adaptation and constraint in the complex life-cycles of animals. Annu Rev Ecol Syst 1994, 25:573-600.
- [2]Truman JW, Riddiford LM: The origins of insect metamorphosis. Nature 1999, 401:447-452.
- [3]Siegel JG, Fristrom JW: The biochemistry of imaginal disc development. In The genetics and biology of Drosophila vol. 2A. Edited by Ashburner M, Wright TRF. New York: Academic Press; 1978.
- [4]Tanaka K, Truman JW: Development of the adult leg epidermis in Manduca sexta: contribution of different larval cell populations. Dev Genes Evol 2005, 215:78-89.
- [5]Truman JW, Riddiford LM: Endocrine insights into the evolution of metamorphosis in insects. Annu Rev Entomol 2002, 47:467-500.
- [6]Nagel RH: Metathetely in larvae of the confused flour beetle (Tribolium confusum Duval). Ann Entomol Soc Am 1934, 27:425-428.
- [7]Truman J, Riddiford L: The morphostatic actions of juvenile hormone. Insect Biochem Mol Biol 2007, 37:761-831.
- [8]Angelini DR, Kikuchi M, Jockusch EL: Genetic patterning in the adult capitate antenna of the beetle Tribolium castaneum. Dev Biol 2009, 327:240-251.
- [9]Angelini DR, Smith FW, Jockusch EL: Extent with modification: leg patterning in the beetle Tribolium castaneum and the evolution of serial homologs. G3 (Bethesda) 2012, 2:235-248.
- [10]Shippy TD, Yeager SJ, Denell RE: The Tribolium spineless ortholog specifies both larval and adult antennal identity. Dev Genes Evol 2009, 219:45-51.
- [11]Namigai EKO, Suzuki Y: Functional conservation and divergence of BMP ligands in limb development and lipid homeostasis of holometabolous insects. Evol Dev 2012, 14:296-310.
- [12]Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, Gibbs R, Bucher G, Friedrich M, Grimmelikhuijzen CJ, Klingler M, Lorenzen M, Richards S, Roth S, Schröder R, Tautz D, Zdobnov EM, Muzny D, Gibbs RA, Weinstock GM, Attaway T, Bell S, Buhay CJ, Chandrabose MN, Chavez D, Clerk-Blankenburg KP, Cree A, Dao M, Davis C, Chacko J: The genome of the model beetle and pest Tribolium castaneum. Nature 2008, 452:949-955.
- [13]Tomoyasu Y, Denell RE: Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Dev Genes Evol 2004, 214:575-578.
- [14]Shah M, Namigai E, Suzuki Y: The role of canonical Wnt signaling in leg regeneration and metamorphosis in the red flour beetle Tribolium castaneum. Mech Dev 2011, 128:342-400.
- [15]Prpic NM, Wigand B, Damen WG, Klingler M: Expression of dachshund in wild-type and Distal-less mutant Tribolium corroborates serial homologies in insect appendages. Dev Genes Evol 2001, 211:467-477.
- [16]Mardon G, Solomon NM: Rubin GM: dachshundencodes a nuclear protein required for normal eye and leg development inDrosophila. Development 1994, 120:3473-3486.
- [17]Tanaka K, Truman JW: Molecular patterning mechanism underlying metamorphosis of the thoracic leg in Manduca sexta. Dev Biol 2007, 305:539-550.
- [18]Suzuki Y, Squires DC, Riddiford LM: Larval leg integrity is maintained by Distal-less and is required for proper timing of metamorphosis in the flour beetle, Tribolium castaneum. Dev Biol 2009, 326:60-67.
- [19]Cohen SM, Bronner G, Kuttner F, Jurgens G, Jackle H: Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature 1989, 338:432-434.
- [20]Bucher G, Scholten J, Klingler M: Parental RNAi in Tribolium (Coleoptera). Curr Biol 2002, 12:R85-R86.
- [21]Hu S, Fambrough D, Atashi JR, Goodman CS, Crews ST: The Drosophila abrupt gene encodes a BTB-zinc finger regulatory protein that controls the specificity of neuromuscular connections. Genes Dev 1995, 9:2936-2948.
- [22]Cook O, Biehs B, Bier E: Brinker and optomotor-blind act coordinately to initiate development of the L5 wing vein primordium in Drosophila. Development 2004, 131:2113-2124.
- [23]Biehs B, Sturtevant MA, Bier E: Boundaries in the Drosophila wing imaginal disc organize vein-specific genetic programs. Development 1998, 125:4245-4257.
- [24]Caygill EE, Johnston LA: Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs. Curr Biol 2008, 18:943-950.
- [25]Duncan DM, Burgess EA, Duncan I: Control of distal antennal identity and tarsal development in Drosophila by spineless-aristapedia, a homolog of the mammalian dioxin receptor. Genes Dev 1998, 12:1290-1303.
- [26]Emerald BS, Curtiss J, Mlodzik M, Cohen SM: Distal antenna and distal antenna related encode nuclear proteins containing pipsqueak motifs involved in antenna development in Drosophila. Development 2003, 130:1171-1180.
- [27]Struhl G: Spineless-aristapedia: a homeotic gene that does not control the development of specific compartments in Drosophila. Genetics 1982, 102:737-749.
- [28]Emmons RB, Duncan D, Duncan I: Regulation of the Drosophila distal antennal determinant spineless. Dev Biol 2007, 302:412-426.
- [29]Toegel JP, Wimmer EA, Prpic NM: Loss of spineless function transforms the Tribolium antenna into a thoracic leg with pretarsal, tibiotarsal, and femoral identity. Dev Genes Evol 2009, 219:53-58.
- [30]Hughes C, Kaufman TC: RNAi analysis of Deformed, proboscipedia and sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the hemipteran head. Development 2000, 127:3683-3694.
- [31]Bolognesi R, Farzana L, Fischer TD, Brown SJ: Multiple Wnt genes are required for segmentation in the short-germ embryo of Tribolium castaneum. Curr Biol 2008, 18:1624-1629.
- [32]Shippy TD, Guo JH, Brown SJ, Beeman RW, Denell RE: Analysis of maxillopedia expression pattern and larval cuticular phenotype in wild-type and mutant Tribolium. Genetics 2000, 155:721-731.
- [33]Beermann A, Jay DG, Beeman RW, Hulskamp M, Tautz D, Jurgens G: The short antennae gene of Tribolium is required for limb development and encodes the orthologue of the Drosophila Distal-less protein. Development 2001, 128:287-297.
- [34]Nakamura T, Mito T, Bando T, Ohuchi H, Noji S: Dissecting insect leg regeneration through RNA interference. Cell Mol Life Sci 2008, 65:64-72.
- [35]Dong PDS, Chu J, Panganiban G: Proximodistal domain specification and interactions in developing Drosophila appendages. Development 2001, 128:2365-2372.
- [36]Bergantinos C, Corominas M, Serras F: Cell death-induced regeneration in wing imaginal discs requires JNK signalling. Development 2010, 137:1169-1179.
- [37]Bosch M, Serras F, Martin-Blanco E, Baguna J: JNK signaling pathway required for wound healing in regenerating Drosophila wing imaginal discs. Dev Biol 2005, 280:73-86.
- [38]Sustar A, Schubiger G: A transient cell cycle shift in Drosophila imaginal disc cells precedes multipotency. Cell 2005, 120:383-393.
- [39]D’Jamoos CA, McMahon G, Tsonis PA: Fibroblast growth factor receptors regulate the ability for hindlimb regeneration in Xenopus laevis. Wound Repair Regen 1998, 6:388-397.
- [40]Mullen LM, Bryant SV, Torok MA, Blumberg B, Gardiner DM: Nerve dependency of regeneration: the role of distal-less and FGF signaling in amphibian limb regeneration. Development 1996, 122:3487-3497.
- [41]Lee Y, Grill S, Sanchez A, Murphy-Ryan M, Poss KD: Fgf signaling instructs position-dependent growth rate during zebrafish fin regeneration. Development 2005, 132:5173-5183.
- [42]Poss FD, Shen JX, Nechiporuk A, McMahon G, Thisse B, Thisse C, Keating MT: Roles for Fgf signaling during zebrafish fin regeneration. Dev Biol 2000, 222:347-358.
- [43]Whitehead GG, Makino S, Lien CL, Keating MT: fgf20 is essential for initiating zebrafish fin regeneration. Science 2005, 310:1957-1960.
- [44]Giampaoli S, Bucci S, Ragghianti M, Mancino G, Zhang F, Ferretti P: Expression of FGF2 in the limb blastema of two Salamandridae correlates with their regenerative capability. Proc R Soc Lond B Biol Sci 2003, 270(1530):2197-2205.
- [45]Poulin ML, Patrie KM, Botelho MJ, Tassava RA, Chiu IM: Heterogeneity in the expression of fibroblast growth-factor receptors during limb regeneration in newts (Notophthalmus-viridescens). Development 1993, 119:353-361.
- [46]Han MJ, An JY, Kim WS: Expression patterns of Fgf-8 during development and limb regeneration of the axolotl. Dev Dyn 2001, 220:40-48.
- [47]Mitten EK, Jing D, Suzuki Y: Matrix metalloproteinases (MMPs) are required for wound closure and healing during larval leg regeneration in the flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 2012, 42:854-864.
- [48]Nakamura T, Mito T, Tanaka Y, Bando T, Ohuchi H, Noji S: Involvement of canonical Wnt/Wingless signaling in the determination of the positional values within the leg segment of the cricket Gryllus bimaculatus. Develop Growth Differ 2007, 49:79-88.
- [49]Yokoyama H, Ogino H, Stoick-Cooper CL, Grainger RM, Moon RT: Wnt/beta-catenin signaling has an essential role in the initiation of limb regeneration. Dev Biol 2007, 306:170-178.
- [50]Yokoyama H: Initiation of limb regeneration: the critical steps for regenerative capacity. Develop Growth Differ 2008, 50:13-22.
- [51]Vinarsky V, Atkinson DL, Stevenson TJ, Keating MT, Odelberg SJ: Normal newt limb regeneration requires matrix metalloproteinase function. Dev Biol 2005, 279:86-98.
- [52]Shimizu H, Zhang XM, Zhang JS, Leontovich A, Fei KY, Yan L, Sarras MP: Epithelial morphogenesis in hydra requires de novo expression of extracellular matrix components and matrix metalloproteinases. Development 2002, 129:1521-1532.
- [53]Bateson W: Materials for the Study of Variation Treated with Especial Regard to Discontinuity in the Origin of Species. London: Macmillan; 1894.
- [54]Okada TS: A brief history of regeneration research - For admiring Professor Niazi’s discovery of the effect of vitamin A on regeneration. J Biosci 1996, 21:261-271.
- [55]Edwards JS, Reddy GR, Rani MU: Central projections of a homoeotic regenerate, antennapedia, in a stick insect, Carausius-morosus (Phasmida). J Neurobiol 1989, 20:101-114.
- [56]Svacha P: What are and what are not imaginal discs: reevaluation of some basic concepts (Insecta, Holometabola). Dev Biol 1992, 154:101-117.