Loss of fish actinotrichia proteins and the fin-to-limb transition.
The early development of teleost paired fins is strikingly similar to that of tetrapod limb buds and is controlled by similar mechanisms. One early morphological divergence between pectoral fins and limbs is in the fate of the apical ectodermal ridge (AER), the distal epidermis that rims the bud. Whereas the AER of tetrapods regresses after specification of the skeletal progenitors, the AER of teleost fishes forms a fold that elongates. Formation of the fin fold is accompanied by the synthesis of two rows of rigid, unmineralized fibrils called actinotrichia, which keep the fold straight and guide the migration of mesenchymal cells within the fold. The actinotrichia are made of elastoidin, the components of which, apart from collagen, are unknown. Here we show that two zebrafish proteins, which we name actinodin 1 and 2 (And1 and And2), are essential structural components of elastoidin. The presence of actinodin sequences in several teleost fishes and in the elephant shark (Callorhinchus milii, which occupies a basal phylogenetic position), but not in tetrapods, suggests that these genes have been lost during tetrapod species evolution. Double gene knockdown of and1 and and2 in zebrafish embryos results in the absence of actinotrichia and impaired fin folds. Gene expression profiles in embryos lacking and1 and and2 function are consistent with pectoral fin truncation and may offer a potential explanation for the polydactyly observed in early tetrapod fossils. We propose that the loss of both actinodins and actinotrichia during evolution may have led to the loss of lepidotrichia and may have contributed to the fin-to-limb transition.
Zhang
Jing
J
CAREG, Department of Biology, University of Ottawa, Ottawa, Ontario K1N 6N5, Canada.
Wagh
Purva
P
Guay
Danielle
D
Sanchez-Pulido
Luis
L
Padhi
Bhaja K
BK
Korzh
Vladimir
V
Andrade-Navarro
Miguel A
MA
Akimenko
Marie-Andrée
MA
D000825:Animal Structures / Q000033:anatomy & histology* / Q000196:embryology / Q000502:physiology*; D000818:Animals; D005075:Biological Evolution; D003094:Collagen / Q000737:chemistry / Q000378:metabolism; D004475:Ectoderm / Q000196:embryology / Q000378:metabolism; D004625:Embryo, Nonmammalian / Q000033:anatomy & histology / Q000196:embryology / Q000378:metabolism; D019143:Evolution, Molecular; D005121:Extremities / Q000033:anatomy & histology / Q000196:embryology / Q000502:physiology*; D029941:Fish Proteins / Q000172:deficiency* / Q000235:genetics / Q000378:metabolism; D020869:Gene Expression Profiling; D018507:Gene Expression Regulation, Developmental; D055785:Gene Knockdown Techniques; D018878:Limb Buds / Q000033:anatomy & histology / Q000196:embryology / Q000378:metabolism; D008954:Models, Biological; D010802:Phylogeny; D015027:Zebrafish / Q000033:anatomy & histology* / Q000196:embryology / Q000235:genetics / Q000378:metabolism*; D029961:Zebrafish Proteins / Q000172:deficiency / Q000235:genetics / Q000378:metabolism
D029941:Fish Proteins; D029961:Zebrafish Proteins; C551359:actinodin 1, zebrafish; C551360:actinodin 2, zebrafish; C028849:elastoidin; D003094:Collagen