Quail-duck chimeras reveal spatiotemporal plasticity in molecular and histogenic programs of cranial feather development.
The avian feather complex represents a vivid example of how a developmental module composed of highly integrated molecular and histogenic programs can become rapidly elaborated during the course of evolution. Mechanisms that facilitate this evolutionary diversification may involve the maintenance of plasticity in developmental processes that underlie feather morphogenesis. Feathers arise as discrete buds of mesenchyme and epithelium, which are two embryonic tissues that respectively form dermis and epidermis of the integument. Epithelial-mesenchymal signaling interactions generate feather buds that are neatly arrayed in space and time. The dermis provides spatiotemporal patterning information to the epidermis but precise cellular and molecular mechanisms for generating species-specific differences in feather pattern remain obscure. In the present study, we exploit the quail-duck chimeric system to test the extent to which the dermis regulates the expression of genes required for feather development. Quail and duck have distinct feather patterns and divergent growth rates, and we exchange pre-migratory neural crest cells destined to form the craniofacial dermis between them. We find that donor dermis induces host epidermis to form feather buds according to the spatial pattern and timetable of the donor species by altering the expression of members and targets of the Bone Morphogenetic Protein, Sonic Hedgehog and Delta/Notch pathways. Overall, we demonstrate that there is a great deal of spatiotemporal plasticity inherent in the molecular and histogenic programs of feather development, a property that may have played a generative and regulatory role throughout the evolution of birds.
Eames
B Frank
BF
Department of Orthopaedic Surgery, University of California at San Francisco, 533 Parnassus Avenue, U-453, San Francisco, CA 94143-0514, USA.
Schneider
Richard A
RA
D000818:Animals; D019485:Bone Morphogenetic Proteins / Q000096:biosynthesis / Q000235:genetics; D002678:Chimera / Q000196:embryology*; D004372:Ducks / Q000196:embryology*; D005241:Feathers / Q000196:embryology*; D018507:Gene Expression Regulation, Developmental / Q000502:physiology; D006257:Head / Q000196:embryology; D053823:Hedgehog Proteins; D047908:Intracellular Signaling Peptides and Proteins; D008565:Membrane Proteins / Q000096:biosynthesis / Q000235:genetics; D009432:Neural Crest / Q000196:embryology; D011784:Quail / Q000196:embryology*; D051880:Receptors, Notch; D015534:Trans-Activators / Q000096:biosynthesis / Q000235:genetics
D019485:Bone Morphogenetic Proteins; D053823:Hedgehog Proteins; D047908:Intracellular Signaling Peptides and Proteins; D008565:Membrane Proteins; D051880:Receptors, Notch; D015534:Trans-Activators; C064045:delta protein
Curr Top Dev Biol. 1987;22:209-34
2443312
Mech Dev. 2001 Feb;100(2):233-44
11165480
Dev Biol. 2004 Jan 1;265(1):219-33
14697365
Int J Dev Biol. 1995 Apr;39(2):357-71
7545414
Science. 2003 Jan 24;299(5606):565-8
12543976
J Craniofac Genet Dev Biol Suppl. 1986;2:15-31
3491109
Anat Rec. 1979 Jul;194(3):469-75
475011
J Exp Zool B Mol Dev Evol. 2003 Aug 15;298(1):73-90
12949770
Dev Biol. 1999 Apr 15;208(2):441-55
10191057
Mech Dev. 1997 Oct;67(2):111-23
9392510
Int J Dev Biol. 2004;48(2-3):137-48
15272378
Development. 2003 May;130(9):1749-58
12642481
Mech Dev. 2004 Feb;121(2):157-71
15037317
J Embryol Exp Morphol. 1973 Dec;30(3):587-603
4772387
Evol Dev. 2004 Jan-Feb;6(1):32-40
15108816
Int J Dev Biol. 2003;47(7-8):613-21
14756337
J Exp Zool. 2002 Aug 15;294(2):160-76
12210117
Int J Dev Biol. 2004;48(2-3):93-101
15272374
Dev Biol. 1998 Apr 1;196(1):11-23
9527877
Dev Biol. 2000 Dec 1;228(1):73-85
11087627
J Morphol. 1951 Jan;88(1):49-92
24539719
J Embryol Exp Morphol. 1963 Dec;11:765-89
14081994
Int J Dev Biol. 2004;48(2-3):103-6
15272375
J Exp Zool. 1977 Apr;200(1):107-24
870614
J Embryol Exp Morphol. 1967 Dec;18(3):389-400
5583445
Mech Dev. 1999 Aug;86(1-2):51-62
10446265
Nature. 2002 Nov 21;420(6913):308-12
12442169
J Invest Dermatol. 1996 Dec;107(6):797-803
8941663
Dev Biol. 1972 Feb;27(2):244-71
5019938
Dev Biol. 1984 Oct;105(2):343-50
6479443
Development. 1998 Feb;125(4):767-75
9435296
Development. 1999 Jun;126(12):2577-87
10331970
Dev Dyn. 1998 Dec;213(4):386-97
9853960
Dev Biol. 2003 Oct 15;262(2):195-205
14550785
Eur J Dermatol. 2001 Jul-Aug;11(4):286-92
11399531
Mech Dev. 1998 Mar;72(1-2):159-68
9533960
Development. 2000 Nov;127(21):4611-7
11023864
Development. 1988;103 Suppl:155-69
3250849
Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10246-9
8816784
Dev Biol. 1980 Jul;78(1):47-62
7399143
Development. 1987 Mar;99(3):341-51
3653006
Mech Dev. 2002 Aug;116(1-2):39-49
12128204
Dev Biol. 1998 Dec 15;204(2):420-31
9882480
Dev Biol. 1983 Mar;96(1):144-65
6825950
Development. 1992 Jan;114(1):1-15
1576952
Int J Dev Biol. 2004;48(2-3):107-15
15272376
Arch Oral Biol. 1994 Jul;39(7):551-62
7945013
Arch Oral Biol. 1978;23(12):1157-61
287433
Dev Dyn. 1996 Oct;207(2):157-70
8906419
Development. 2004 Jul;131(14):3333-43
15201222
Mech Dev. 1998 Jul;75(1-2):3-28
9739099
Dev Biol. 2000 Mar 1;219(1):98-114
10677258
Int J Dev Biol. 2002 Mar;46(2):243-53
11934153
J Embryol Exp Morphol. 1982 Apr;68:127-36
7108417
J Neurobiol. 1993 Feb;24(2):146-61
8445384
Biochem Biophys Res Commun. 1995 Jan 5;206(1):33-9
7818537
Development. 1988;103 Suppl:101-13
3250847
Anat Rec. 1980 Jul;197(3):305-15
7436007
Dev Dyn. 2004 Dec;231(4):741-9
15532057
Biochem Biophys Res Commun. 1995 Jun 6;211(1):123-9
7779076
J Cell Sci Suppl. 1988;10:195-230
3077937
Mech Dev. 2002 Jan;110(1-2):51-60
11744368
Microsc Res Tech. 1997 Aug 15;38(4):452-65
9297695
Histol Histopathol. 1995 Jan;10(1):223-37
7756740
Development. 1999 Aug;126(16):3509-21
10409498
Mech Dev. 2001 Feb;100(2):331-3
11165492
Dev Biol. 1982 Jan;89(1):13-24
7054004
Arch Pathol Lab Med. 1991 Feb;115(2):115-9
1992974
Anat Embryol (Berl). 1986;174(2):195-205
3526977
Cell Tissue Res. 1987 Jul;249(1):31-7
3621295
Dev Dyn. 1998 Aug;212(4):533-9
9707326
Dev Biol. 1998 Sep 1;201(1):1-12
9733569
Int J Dev Biol. 2004;48(2-3):181-91
15272383
Dev Biol. 1965 Aug;12(1):131-53
5833108
Dev Biol. 1978 Dec;67(2):296-312
738529
Dev Biol. 1997 Aug 1;188(1):181-7
9245521
J Invest Dermatol. 1996 Oct;107(4):639-46
8823374
Int J Dev Biol. 1999 Mar;43(2):95-110
10235385
Cell Tissue Res. 1999 Apr;296(1):103-9
10199970
Development. 1999 Nov;126(22):4997-5009
10529418
J Embryol Exp Morphol. 1970 Aug;24(1):73-94
5487160
Prog Clin Biol Res. 1993;383B:645-54
8115380
J Craniofac Genet Dev Biol. 1990;10(3):241-61
2262536
Dev Cell. 2003 Feb;4(2):231-40
12586066
Development. 2002 Feb;129(4):1061-73
11861488
FASEB J. 1994 Jul;8(10):699-706
8050668
Development. 1999 Jan;126(1):63-73
9834186
J Embryol Exp Morphol. 1980 Apr;56:269-81
7400746
Methods Cell Biol. 1996;51:23-59
8722469
Cell Mol Life Sci. 2000 Nov;57(12):1672-81
11130174
Development. 1998 Oct;125(19):3775-87
9729486
Dev Biol. 1985 Jun;109(2):259-67
3996749
Dev Biol. 1992 Dec;154(2):299-308
1426640
Development. 2001 Jul;128(14):2755-67
11526081
Dev Dyn. 1996 Jan;205(1):82-91
8770554
J Invest Dermatol. 2003 Jan;120(1):20-6
12535194
J Embryol Exp Morphol. 1983 Apr;74:261-73
6886598