Research Article

Genetic basis of ruminant headgear and rapid antler regeneration

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Science  21 Jun 2019:
Vol. 364, Issue 6446, eaav6335
DOI: 10.1126/science.aav6335
  • Neural crest cellular origin of ruminant headgear and the tight control of rapid antler regeneration and low cancer risk in cervids.

    (Left) Phylogenomic relationships of the six ruminant families. Anatomic features of family-specific headgear are depicted, showing that headgear of ruminants share tissue and cellular origins. (Upper right) The gene expression profile of antler correlates more strongly with osteocarcinoma than with normal bone tissue. (Lower right) The balance between rapid antler regeneration, which depends on genes in the oncogenic pathway, and reduced cancer risk, which may involve adaptive evolution of tumor suppressor genes.

  • Fig. 1 Phylogenomic placement of species without headgear in the Ruminantia and Cervidae.

    (Left) The phylogenomic relationships of the six ruminant families from (2). (Right) Maximum-likelihood tree for the nine studied cervid species obtained using 3,316,385 four-fold degenerate sites. The anatomic structure of headgear in each family is depicted, including the keratin sheath of Antilocapridae and Bovidae and the regenerable antler of Cervidae. The red bar indicates secondary headgear loss and the red text highlights the de novo assembled species in this study. The number of species in each family used in this study is indicated in parentheses. Sources and credits for species photos are listed in table S26.

  • Fig. 2 Gene recruitment and cellular origin of ruminant headgear.

    (A) Genes recruited to headgear from different organs. Bone, skin, testis, brain, and others are marked as orange, purple, yellow, green, and various shades of gray, respectively. (B) Diagram of neural crest cell genes involved in headgear development. The HOXD gene cluster is depicted as the hypothesized master regulator of headgear. Genes annotated in the neural crest cell migration and differentiation pathway are labeled with different colors to indicate positively selected genes (PSGs), HCEs, fetal horn bud DEGs, and genes related to abnormal horn development. The solid arrows represent known neural crest cell pathways. The dashed arrows indicate the pathway known to be related to other cell types that has not been recorded in neural crest cells. (C) Diagram of the headgear of the ruminant ancestor, mainly containing bone, skin, and nerve tissues.

  • Fig. 3 Oncogenesis and neurogenesis pathways involved in rapid antler regeneration.

    (A and D) Positively selected genes in cervids (blue), cervid-specific HCE-associated genes (yellow), and antler-specific expression genes (green) in axon guidance (A) and oncogenesis (D) pathways. (B) Annual antler regeneration cycle. Antlers are shed in winter and regenerate in spring, growing most rapidly in summer. Antlers then calcify and shed their velvet in autumn. (C) The anatomy of the antler. The source and credit for the red deer photo are listed in table S26.

  • Fig. 4 Examples of positively selected tumor suppressor genes in cervids.

    (A) Gene models showing cervid-specific mutations of two positively selected tumor suppressor genes, PML and ADAMTS18. PML has the strongest selection signals detected in cervids (likelihood ratio test, P value = 1.63 × 10−6) (table S21). (B) Genes positively selected in the p53 signaling pathway of cervids. Selected p53 cofactors are highlighted with yellow hexagons, and selected regulators are marked with green ovals.

Supplementary Materials

  • Genetic basis of ruminant headgear and rapid antler regeneration

    Yu Wang, Chenzhou Zhang, Nini Wang, Zhipeng Li, Rasmus Heller, Rong Liu, Yue Zhao, Jiangang Han, Xiangyu Pan, Zhuqing Zheng, Xueqin Dai, Ceshi Chen, Mingle Dou, Shujun Peng, Xianqing Chen, Jing Liu, Ming Li, Kun Wang, Chang Liu, Zeshan Lin, Lei Chen, Fei Hao, Wenbo Zhu, Chengchuang Song, Chen Zhao, Chengli Zheng, Jianming Wang, Shengwei Hu, Cunyuan Li, Hui Yang, Lin Jiang, Guangyu Li, Mingjun Liu, Tad S. Sonstegard, Guojie Zhang, Yu Jiang, Wen Wang, Qiang Qiu

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Materials and Methods
    • Figs. S1 to S18
    • Tables S1, S7, S11 to S14, S17, S20, S21, S24 to S26
    • Captions for Tables S2 to S6, S8 to S10, S15, S16, S18, S19, S22, S23
    • References
    Tables S2 to S6, S8 to S10, S15, S16, S18, S19, S22, S23

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