Sequence of a complete chicken BG haplotype shows dynamic expansion and contraction of two gene lineages with particular expression patterns

Jan Salomonsen; John A. Chattaway; Andrew C. Y. Chan; Aimée Parker; Samuel Huguet; Denise A. Marston; Sally L. Rogers; Zhiguang Wu; Adrian L. Smith; Karen Staines; Colin Butter; Patricia Riegert; Olli Vainio; Line Nielsen; Bernd Kaspers; Darren K. Griffin; Fengtang Yang; Rima Zoorob; Francois Guillemot; Charles Auffray; Stephan Beck; Karsten Skjødt; Jim Kaufman

doi:10.1371/journal.pgen.1004417

Sequence of a complete chicken BG haplotype shows dynamic expansion and contraction of two gene lineages with particular expression patterns

Jan Salomonsen, John A. Chattaway, Andrew C. Y. Chan, Aimée Parker, Samuel Huguet, Denise A. Marston, Sally L. Rogers, Zhiguang Wu, Adrian L. Smith, Karen Staines, Colin Butter, Patricia Riegert, Olli Vainio, Line Nielsen, Bernd Kaspers, Darren K. Griffin, Fengtang Yang, Rima Zoorob, Francois Guillemot, Charles AuffrayStephan Beck, Karsten Skjødt, Jim Kaufman

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Abstract

Many genes important in immunity are found as multigene families. The butyrophilin genes are members of the B7 family, playing diverse roles in co-regulation and perhaps in antigen presentation. In humans, a fixed number of butyrophilin genes are found in and around the major histocompatibility complex (MHC), and show striking association with particular autoimmune diseases. In chickens, BG genes encode homologues with somewhat different domain organisation. Only a few BG genes have been characterised, one involved in actin-myosin interaction in the intestinal brush border, and another implicated in resistance to viral diseases. We characterise all BG genes in B12 chickens, finding a multigene family organised as tandem repeats in the BG region outside the MHC, a single gene in the MHC (the BF-BL region), and another single gene on a different chromosome. There is a precise cell and tissue expression for each gene, but overall there are two kinds, those expressed by haemopoietic cells and those expressed in tissues (presumably non-haemopoietic cells), correlating with two different kinds of promoters and 5′ untranslated regions (5′UTR). However, the multigene family in the BG region contains many hybrid genes, suggesting recombination and/or deletion as major evolutionary forces. We identify BG genes in the chicken whole genome shotgun sequence, as well as by comparison to other haplotypes by fibre fluorescence in situ hybridisation, confirming dynamic expansion and contraction within the BG region. Thus, the BG genes in chickens are undergoing much more rapid evolution compared to their homologues in mammals, for reasons yet to be understood.

Original language	English
Article number	e1004417
Journal	P L o S Genetics
Volume	10
Issue number	6
Number of pages	21
ISSN	1553-7390
DOIs	https://doi.org/10.1371/journal.pgen.1004417
Publication status	Published - Jun 2014

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Sequence of a complete chicken BG haplotype shows dynamic expansion and contraction of two gene lineages with particular expression patternsFinal published version, 1.86 MB

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Salomonsen, J., Chattaway, J. A., Chan, A. C. Y., Parker, A., Huguet, S., Marston, D. A., Rogers, S. L., Wu, Z., Smith, A. L., Staines, K., Butter, C., Riegert, P., Vainio, O., Nielsen, L., Kaspers, B., Griffin, D. K., Yang, F., Zoorob, R., Guillemot, F., ... Kaufman, J. (2014). Sequence of a complete chicken BG haplotype shows dynamic expansion and contraction of two gene lineages with particular expression patterns. P L o S Genetics, 10(6), [e1004417]. https://doi.org/10.1371/journal.pgen.1004417

Salomonsen, J, Chattaway, JA, Chan, ACY, Parker, A, Huguet, S, Marston, DA, Rogers, SL, Wu, Z, Smith, AL, Staines, K, Butter, C, Riegert, P, Vainio, O, Nielsen, L, Kaspers, B, Griffin, DK, Yang, F, Zoorob, R, Guillemot, F, Auffray, C, Beck, S, Skjødt, K & Kaufman, J 2014, 'Sequence of a complete chicken BG haplotype shows dynamic expansion and contraction of two gene lineages with particular expression patterns', P L o S Genetics, vol. 10, no. 6, e1004417. https://doi.org/10.1371/journal.pgen.1004417

@article{828c45577fe340ea87cea51d891e8048,

title = "Sequence of a complete chicken BG haplotype shows dynamic expansion and contraction of two gene lineages with particular expression patterns",

abstract = "Many genes important in immunity are found as multigene families. The butyrophilin genes are members of the B7 family, playing diverse roles in co-regulation and perhaps in antigen presentation. In humans, a fixed number of butyrophilin genes are found in and around the major histocompatibility complex (MHC), and show striking association with particular autoimmune diseases. In chickens, BG genes encode homologues with somewhat different domain organisation. Only a few BG genes have been characterised, one involved in actin-myosin interaction in the intestinal brush border, and another implicated in resistance to viral diseases. We characterise all BG genes in B12 chickens, finding a multigene family organised as tandem repeats in the BG region outside the MHC, a single gene in the MHC (the BF-BL region), and another single gene on a different chromosome. There is a precise cell and tissue expression for each gene, but overall there are two kinds, those expressed by haemopoietic cells and those expressed in tissues (presumably non-haemopoietic cells), correlating with two different kinds of promoters and 5′ untranslated regions (5′UTR). However, the multigene family in the BG region contains many hybrid genes, suggesting recombination and/or deletion as major evolutionary forces. We identify BG genes in the chicken whole genome shotgun sequence, as well as by comparison to other haplotypes by fibre fluorescence in situ hybridisation, confirming dynamic expansion and contraction within the BG region. Thus, the BG genes in chickens are undergoing much more rapid evolution compared to their homologues in mammals, for reasons yet to be understood.",

author = "Jan Salomonsen and Chattaway, {John A.} and Chan, {Andrew C. Y.} and Aim{\'e}e Parker and Samuel Huguet and Marston, {Denise A.} and Rogers, {Sally L.} and Zhiguang Wu and Smith, {Adrian L.} and Karen Staines and Colin Butter and Patricia Riegert and Olli Vainio and Line Nielsen and Bernd Kaspers and Griffin, {Darren K.} and Fengtang Yang and Rima Zoorob and Francois Guillemot and Charles Auffray and Stephan Beck and Karsten Skj{\o}dt and Jim Kaufman",

year = "2014",

month = jun,

doi = "10.1371/journal.pgen.1004417",

language = "English",

volume = "10",

journal = "P L o S Genetics",

issn = "1553-7390",

publisher = "Public Library of Science",

number = "6",

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TY - JOUR

T1 - Sequence of a complete chicken BG haplotype shows dynamic expansion and contraction of two gene lineages with particular expression patterns

AU - Salomonsen, Jan

AU - Chattaway, John A.

AU - Chan, Andrew C. Y.

AU - Parker, Aimée

AU - Huguet, Samuel

AU - Marston, Denise A.

AU - Rogers, Sally L.

AU - Wu, Zhiguang

AU - Smith, Adrian L.

AU - Staines, Karen

AU - Butter, Colin

AU - Riegert, Patricia

AU - Vainio, Olli

AU - Nielsen, Line

AU - Kaspers, Bernd

AU - Griffin, Darren K.

AU - Yang, Fengtang

AU - Zoorob, Rima

AU - Guillemot, Francois

AU - Auffray, Charles

AU - Beck, Stephan

AU - Skjødt, Karsten

AU - Kaufman, Jim

PY - 2014/6

Y1 - 2014/6

N2 - Many genes important in immunity are found as multigene families. The butyrophilin genes are members of the B7 family, playing diverse roles in co-regulation and perhaps in antigen presentation. In humans, a fixed number of butyrophilin genes are found in and around the major histocompatibility complex (MHC), and show striking association with particular autoimmune diseases. In chickens, BG genes encode homologues with somewhat different domain organisation. Only a few BG genes have been characterised, one involved in actin-myosin interaction in the intestinal brush border, and another implicated in resistance to viral diseases. We characterise all BG genes in B12 chickens, finding a multigene family organised as tandem repeats in the BG region outside the MHC, a single gene in the MHC (the BF-BL region), and another single gene on a different chromosome. There is a precise cell and tissue expression for each gene, but overall there are two kinds, those expressed by haemopoietic cells and those expressed in tissues (presumably non-haemopoietic cells), correlating with two different kinds of promoters and 5′ untranslated regions (5′UTR). However, the multigene family in the BG region contains many hybrid genes, suggesting recombination and/or deletion as major evolutionary forces. We identify BG genes in the chicken whole genome shotgun sequence, as well as by comparison to other haplotypes by fibre fluorescence in situ hybridisation, confirming dynamic expansion and contraction within the BG region. Thus, the BG genes in chickens are undergoing much more rapid evolution compared to their homologues in mammals, for reasons yet to be understood.

AB - Many genes important in immunity are found as multigene families. The butyrophilin genes are members of the B7 family, playing diverse roles in co-regulation and perhaps in antigen presentation. In humans, a fixed number of butyrophilin genes are found in and around the major histocompatibility complex (MHC), and show striking association with particular autoimmune diseases. In chickens, BG genes encode homologues with somewhat different domain organisation. Only a few BG genes have been characterised, one involved in actin-myosin interaction in the intestinal brush border, and another implicated in resistance to viral diseases. We characterise all BG genes in B12 chickens, finding a multigene family organised as tandem repeats in the BG region outside the MHC, a single gene in the MHC (the BF-BL region), and another single gene on a different chromosome. There is a precise cell and tissue expression for each gene, but overall there are two kinds, those expressed by haemopoietic cells and those expressed in tissues (presumably non-haemopoietic cells), correlating with two different kinds of promoters and 5′ untranslated regions (5′UTR). However, the multigene family in the BG region contains many hybrid genes, suggesting recombination and/or deletion as major evolutionary forces. We identify BG genes in the chicken whole genome shotgun sequence, as well as by comparison to other haplotypes by fibre fluorescence in situ hybridisation, confirming dynamic expansion and contraction within the BG region. Thus, the BG genes in chickens are undergoing much more rapid evolution compared to their homologues in mammals, for reasons yet to be understood.

U2 - 10.1371/journal.pgen.1004417

DO - 10.1371/journal.pgen.1004417

M3 - Journal article

SN - 1553-7390

VL - 10

JO - P L o S Genetics

JF - P L o S Genetics

IS - 6

M1 - e1004417

ER -

Sequence of a complete chicken BG haplotype shows dynamic expansion and contraction of two gene lineages with particular expression patterns

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