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A Role for buttonhead in the Early Head and Trunk Development in the Beetle Tribolium castaneum

  • Jeon, Haewon (Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • O, Jiyun (Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • Jin, Sil (Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • Lim, Jinsung (Division of Life Science, Gyeongsang National University) ;
  • Choe, Chong Pyo (Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University)
  • Received : 2019.01.09
  • Accepted : 2019.02.22
  • Published : 2019.03.31

Abstract

The head gap gene buttonhead (btd) is required for the patterning of head segments in the early Drosophila embryo. Mutant phenotypes of btd display a gap-like phenotype in which antennal, intercalary, mandibular and the anterior portion of the maxillary segments are eliminated. In agreement with the phenotypes, btd is expressed in a stripe covering the head segments at the blastoderm stage. During the early phase of the germband extension, btd is expressed in stripes with single segmental periodicity, which is required for the formation of the peripheral nervous system. In contrast to the key role of btd in Drosophila embryonic development, it has been suggested that Tribolium ortholog of btd (Tc-btd) is dispensable for embryonic head development. In order for better understanding of the requirement of Tc-btd in the early Tribolium embryo, we re-analyzed the expression patterns and functions of Tc-btd during embryonic segmentation. Tc-btd is expressed in segmental stripes at the stages of blastoderm and germband elongation. Up to 28.3% of embryos in which Tc-btd is knocked down displays the loss of antennal, mandibular and the pregnathal regions in the head, with abdominal segments being disrupted in the trunk. Our findings suggest that Tc-btd is required for the head and trunk development in the early Tribolium embryo.

Keywords

References

  1. Birkan M, Schaeper ND, Chipman AD (2011) Early patterning and blastodermal fate map of the head in the milkweed bug Oncopeltus fasciatus. Evol Dev 13:436-447. https://doi.org/10.1111/j.1525-142X.2011.00497.x
  2. Brown SJ, Patel NH, Denell RE (1994) Embryonic expression of the single Tribolium engrailed homolog. Dev Genet 15:7-18. https://doi.org/10.1002/dvg.1020150103
  3. Bucher G, Scholten J, Klingler M (2002) Parental RNAi in Tribolium (Coleoptera). Curr Biol 12:R85-86. https://doi.org/10.1016/S0960-9822(01)00651-0
  4. Cepeda RE, Pardo RV, Macaya CC, Sarrazin AF (2017) Contribution of cell proliferation to axial elongation in the red flour beetle Tribolium castaneum. PLOS ONE 12:e0186159. https://doi.org/10.1371/journal.pone.0186159
  5. Choe CP, Brown SJ (2007) Evolutionary flexibility of pairrule patterning revealed by functional analysis of secondary pair-rule genes, paired and sloppy-paired in the short-germ insect, Tribolium castaneum. Dev Biol 302:281-294. https://doi.org/10.1016/j.ydbio.2006.09.037
  6. Choe CP, Miller SC, Brown SJ (2006) A pair-rule gene circuit defines segments sequentially in the short-germ insect Tribolium castaneum. Proc Natl Acad Sci USA 103:6560-6564. https://doi.org/10.1073/pnas.0510440103
  7. Chouard T (2008) Darwin 200: Beneath the surface. Nature 456:300-303. https://doi.org/10.1038/456300a
  8. Cohen SM, Jurgens G (1990) Mediation of Drosophila head development by gap-like segmentation genes. Nature 346:482-485. https://doi.org/10.1038/346482a0
  9. Dalton D, Chadwick R, McGinnis W (1989) Expression and embryonic function of empty spiracles: A Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev 3:1940-1956. https://doi.org/10.1101/gad.3.12a.1940
  10. El-Sherif E, Averof M, Brown SJ (2012) A segmentation clock operating in blastoderm and germband stages of Tribolium development. Development 139:4341-4346. https://doi.org/10.1242/dev.085126
  11. Finkelstein R, Perrimon N (1990) The orthodenticle gene is regulated by bicoid and torso and specifies Drosophila head development. Nature 346:485-488. https://doi.org/10.1038/346485a0
  12. Gao Q, Finkelstein R (1998) Targeting gene expression to the head: The Drosophila orthodenticle gene is a direct target of the Bicoid morphogen. Development 125:4185-4193. https://doi.org/10.1242/dev.125.21.4185
  13. Kim EJ, Lee JM, Jung HS (2013) Fus expression patterns in developing tooth. Dev Reprod 17:215-220. https://doi.org/10.12717/DR.2013.17.3.215
  14. Kitzmann P, Schwirz J, Schmitt-Engel C, Bucher G (2013) RNAi phenotypes are influenced by the genetic background of the injected strain. BMC Genomics 14:5. https://doi.org/10.1186/1471-2164-14-5
  15. Lefort V, Longueville JE, Gascuel O (2017) SMS: Smart model selection in PhyML. Mol Biol Evol 34:2422-2424. https://doi.org/10.1093/molbev/msx149
  16. Patel NH, Condron BG, Zinn K (1994) Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367:429-434. https://doi.org/10.1038/367429a0
  17. Rogers BT, Kaufman TC (1996) Structure of the insect head as revealed by the EN protein pattern in developing embryos. Development 122:3419-3432. https://doi.org/10.1242/dev.122.11.3419
  18. Rogers BT, Kaufman TC (1997) Structure of the insect head in ontogeny and phylogeny: A view from Drosophila. Int Rev Cytol 174:1-84. https://doi.org/10.1016/S0074-7696(08)62115-4
  19. Sarrazin AF, Peel AD, Averof M (2012) A segmentation clock with two-segment periodicity in insects. Science 336:338-341. https://doi.org/10.1126/science.1218256
  20. Schinko JB, Kreuzer N, Offen N, Posnien N, Wimmer EA, Bucher G (2008) Divergent functions of orthodenticle, empty spiracles and buttonhead in early head patterning of the beetle Tribolium castaneum (Coleoptera). Dev Biol 317:600-613. https://doi.org/10.1016/j.ydbio.2008.03.005
  21. Schroder R (2003) The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422:621-625. https://doi.org/10.1038/nature01536
  22. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. https://doi.org/10.1038/msb.2011.75
  23. Snodgrass RE (1935) Principles of Insect Morphology. McGRaw Hill, New York.
  24. St Johnston D, Nusslein-Volhard C (1992) The origin of pattern and polarity in the Drosophila embryo. Cell 68:201-219. https://doi.org/10.1016/0092-8674(92)90466-P
  25. Stauber M, Jackle H, Schmidt-Ott U (1999) The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc Natl Acad Sci USA 96:3786-3789. https://doi.org/10.1073/pnas.96.7.3786
  26. Walldorf U, Gehring WJ (1992) Empty spiracles, a gap gene containing a homeobox involved in Drosophila head development. EMBO J 11:2247-2259. https://doi.org/10.1002/j.1460-2075.1992.tb05284.x
  27. Wimmer EA, Frommer G, Purnell BA, Jackle H (1996) Buttonhead and D-Sp1: A novel Drosophila gene pair. Mech Dev 59:53-62. https://doi.org/10.1016/0925-4773(96)00575-8
  28. Wimmer EA, Jackle H, Pfeifle C, Cohen SM (1993) A Drosophila homologue of human Sp1 is a head-specific segmentation gene. Nature 366:690-694. https://doi.org/10.1038/366690a0
  29. Wimmer EA, Simpson-Brose M, Cohen SM, Desplan C, Jackle H (1995) Trans- and cis-acting requirements for blastodermal expression of the head gap gene buttonhead. Mech Dev 53:235-245. https://doi.org/10.1016/0925-4773(95)00439-8