Li HUANG,Mian ZHAO,Zhenhua LUO and Hua WU.Allelic Polymorphism, Gene Duplication and Balancing Selection of MHC Class IIB Genes in the Omei Treefrog (Rhacophorus omeimontis)[J].Asian Herpetological Research(AHR),2016,7(1):1-11.[doi:10.16373/j.cnki.ahr.150053]
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Allelic Polymorphism, Gene Duplication and Balancing Selection of MHC Class IIB Genes in the Omei Treefrog (Rhacophorus omeimontis)
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Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

Issue:
2016 VoI.7 No.1
Page:
1-11
Research Field:
Publishing date:
2016-03-25

Info

Title:
Allelic Polymorphism, Gene Duplication and Balancing Selection of MHC Class IIB Genes in the Omei Treefrog (Rhacophorus omeimontis)
Author(s):
Li HUANG# Mian ZHAO# Zhenhua LUO and Hua WU*
Institute of Evolution and Ecology, International Research Centre of Ecology and Environment, School of Life Sciences, Central China Normal University, 152 Luoyulu, Hongshan District, Wuhan 430079, China
Keywords:
MHC class IIB polymorphism gene duplication balancing selection Rhacophorus omeimontis
PACS:
-
DOI:
10.16373/j.cnki.ahr.150053
Abstract:
The worldwide declines in amphibian populations have largely been caused by infectious fungi and bacteria. Given that vertebrate immunity against these extracellular pathogens is primarily functioned by the major histocompatibility complex (MHC) class II molecules, the characterization and the evolution of amphibian MHC class II genes have attracted increasing attention. The polymorphism of MHC class II genes was found to be correlated with susceptibility to fungal pathogens in many amphibian species, suggesting the importance of studies on MHC class II genes for amphibians. However, such studies on MHC class II gene evolution have rarely been conducted on amphibians in China. In this study, we chose Omei treefrog (Rhacophorus omeimontis), which lived moist environments easy for breeding bacteria, to study the polymorphism of its MHC class II genes and the underlying evolutionary mechanisms. We amplified the entire MHC class IIB exon 2 sequence in the R. omeimontis using newly designed primers. We detected 102 putative alleles in 146 individuals. The number of alleles per individual ranged from one to seven, indicating that there are at least four loci containing MHC class IIB genes in R. omeimontis. The allelic polymorphism estimated from the 102 alleles in R. omeimontis was not high compared to that estimated in other anuran species. No significant gene recombination was detected in the 102 MHC class IIB exon 2 sequences. In contrast, both gene duplication and balancing selection greatly contributed to the variability in MHC class IIB exon 2 sequences of R. omeimontis. This study lays the groundwork for the future researches to comprehensively analyze the evolution of amphibian MHC genes and to assess the role of MHC gene polymorphisms in resistance against extracellular pathogens for amphibians in China.

References:

Aguilar A., Roemer G., Debenham S., Binns M., Garcelon D., Wayne R. K. 2004. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci U S A, 101: 3490–3494
Andersson L., Mikko S. 1995. Generation of MHC class II diversity by intra- and intergenic recombination. Immunol Rev, 143: 5–12
Babik W., Pabijan M., Arntzen J. W., Cogalniceanu D., Durka W., Radwan J. 2009. Long-term survival of a urodele amphibian despite depleted major histocompatibility complex variation. Mol Ecol, 18: 769–781
Babik W., Pabijan M., Radwan J. 2008. Contrasting patterns of variation in MHC loci in the Alpine newt. Mol Ecol, 17: 2339–2355
Bai C., Garner T. W., Li Y. 2010. First evidence of Batrachochytrium dendrobatidis in China: discovery of chytridiomycosis in introduced American bullfrogs and native amphibians in the Yunnan Province, China. Ecohealth, 7: 127–134
Baker C. S., Vant M. D., Dalebout M. L., Lento G. M., O’Brien S. J., Yuhki N. 2006. Diversity and duplication of DQB and DRB-like genes of the MHC in baleen whales (suborder: Mysticeti). Immunogenetics, 58: 283–296
Balakrishnan C., Ekblom R., Volker M., et al. 2010. Gene duplication and fragmentation in the zebra finch major histocompatibility complex. BMC Biol, 8: 29
Balá? V., V?r?s J., Civi? P., et al. 2014. Assessing risk and guidance on monitoring of Batrachochytrium dendrobatidis in Europe through identification of taxonomic selectivity of infection. Conserv Biol, 28: 213–223
Bataille A., Cashins S. D., Grogan L., et al. 2015. Susceptibility of amphibians to chytridiomycosis is associated with MHC class II conformation. Proc Roy Soc B: Biol Sci, 282
Begovich A. B., McClure G. R., Suraj V. C., Helmuth R. C., Fildes N., Bugawan T.L., Erlich H.A., Klitz W. 1992. Polymorphism, recombination, and linkage disequilibrium within the HLA class II region. J Immunol, 148: 1249–1258
Berger L., Speare R., Daszak P., et al. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci U S A, 95: 9031–9036
Bernatchez L., Landry C. 2003. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol, 16: 363–377
Bollmer J. L., Dunn P. O., Whittingham L. A., Wimpee C. 2010. Extensive MHC class II B gene duplication in a passerine, the common Yellowthroat (Geothlypis trichas). J Hered, 101: 448–460
Bos D. H., DeWoody J. A. 2005. Molecular characterization of major histocompatibility complex class II alleles in wild tiger salamanders (Ambystoma tigrinum). Immunogenetics, 57: 775–781
Brown J. H., Jardetzky T. S., Gorga J. C., et al. 1993. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature, 364: 33–39
Bryja J., Galan M., Charbonnel N., Cosson J. F. 2006. Duplication, balancing selection and trans-species evolution explain the high levels of polymorphism of the DQA MHC class II gene in voles (Arvicolinae). Immunogenetics, 58: 191–202
Edwards S. V., Hedrick P. W. 1998. Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol, 13: 305–311
Fei L., Ye C. Y. 2001. The colour handbook of amphibians of Sichuan. China Forestry Publishing House, Beijing (China)
Garner T. W., Perkins M. W., Govindarajulu P., et al. 2006. The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biol Lett, 2: 455–459
Garrigan D., Hedrick P. W. 2003. Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution, 57: 1707–1722
Goldman N., Yang Z. 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol, 11: 725–736
Hauswaldt J. S., Stuckas H., Pfautsch S., Tiedemann R. 2007. Molecular characterization of MHC class II in a nonmodel anuran species, the fire-bellied toad Bombina bombina. Immunogenetics, 59: 479–491
Hughes A. L., Nei M. 1989. Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci U S A, 86: 958
Hughes A. L., Nei M. 1990. Evolutionary relationships of class II major-histocompatibility-complex genes in mammals. Mol Biol Evol, 7: 491–514
Hughes A. L., Yeager M. 1998. Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet, 32: 415–435
Jakobsen I. B., Wilson S. R., Easteal S. 1998. Patterns of reticulate evolution for the classical class I and II HLA loci. Immunogenetics, 48: 312–323
Jeffery K. J. M., Bangham C. R. M. 2000. Do infectious diseases drive MHC diversity? Microbes Infect, 2: 1335–1341
Kamath P. L., Getz W. M. 2011. Adaptive molecular evolution of the major histocompatibility complex genes, DRA and DQA, in the genus Equus. BMC Evol Biol, 11: 128
Kiemnec-Tyburczy K. M., Richmond J. Q., Savage A. E., Lips K. R., Zamudio K. R. 2012. Genetic diversity of MHC class I loci in six non-model frogs is shaped by positive selection and gene duplication. Heredity, 109: 146–155
Kiemnec-Tyburczy K. M., Richmond J. Q., Savage A. E., Zamudio K. R. 2010. Selection, trans-species polymorphism, and locus identification of major histocompatibility complex class IIbeta alleles of New World ranid frogs. Immunogenetics, 62: 741–751
Laurens V., Chapusot C., del Rosario Ordonez M., Bentrari F., Padros M. R., Tournefier A. 2001. Axolotl MHC class II beta chain: predominance of one allele and alternative splicing of the β1 domain. Eur J Immunol, 31: 506–515
Librado P., Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25: 1451–1452
Li F., Shu Y. L., Wu H. L. 2012. Polymorphism of exon 2 of MHC Class II B gene in the Chinese concave-eared torrent frog (Odorrana tormota). Biodivers Sci, 20: 184–192
Lillie M., Grueber C. E., Sutton J. T., et al. 2015. Selection on MHC class II supertypes in the New Zealand endemic Hochstetter’s frog. BMC Evol Biol, 15: 63
Lips K. R., Brem F., Brenes R., et al. 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci U S A, 103: 3165–3170
Liu Y. G., Chen Y. 2007. High-efficiency thermal asymmetric interlaced PCR for amplification of unknown flanking sequences. Biotechniques, 43: 649–656
Martin D. P., Murrell B., Golden M., Khoosal A., Muhire B. 2015. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol, 1: vev003
May S., Beebee T. J. C. 2009. Characterisation of major histocompatibility complex class II alleles in the natterjack toad, Bufo calamita. Conserv Genet Resour, 1: 415–417
May S., Zeisset I., Beebee T. J. C. 2011. Larval fitness and immunogenetic diversity in chytrid-infected and uninfected natterjack toad (Bufo calamita) populations. Conserv Genet, 12: 805–811
Morgan J. A., Vredenburg V. T., Rachowicz L. J., et al. 2007. Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. Proc Natl Acad Sci U S A, 104: 13845–13850
Murrell B., Wertheim J. O., Moola S., Weighill T., Scheffler K., Kosakovsky Pond S. L. 2012. Detecting individual sites subject to episodic diversifying selection. PLoS Genet, 8: e1002764
Nei M., Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol, 3: 418–426
Nei M., Gu X., Sitnikova T. 1997. Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci U S A, 94: 7799–7806
Nei M., Rooney A. P. 2005. Concerted and birth-and-death evolution of multigene families. Annu Rev Genet, 39: 121–152
O’Brien S. J., Evermann J. F. 1988. Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol, 3: 254–259
Ohta Y., Goetz W., Hossain M. Z., Nonaka M., Flajnik M. F. 2006. Ancestral organization of the MHC revealed in the amphibian Xenopus. J Immunol, 176: 3674–3685
Piertney S. B., Oliver M. K. 2006. The evolutionary ecology of the major histocompatibility complex. Heredity, 96: 7–21
Pond S. L. K., Frost S. D. 2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol, 22: 1208–1222
Pounds J. A., Bustamante M. R., Coloma L. A., et al. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature, 439: 161–167
Reusch T. H., Langefors ?. 2005. Inter- and intralocus recombination drive MHC class IIB gene diversification in a teleost, the three-spined stickleback Gasterosteus aculeatus. J Mol Evol, 61: 531–541
Rozen S., Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol, 132: 365–386
Sato A., Tichy H., Grant P. R., Grant B. R., Sato T., O’HUigin C. 2011. Spectrum of MHC class II variability in Darwin’s finches and their close relatives. Mol Biol Evol, 28: 1943–1956
Sato K., Flajnik M. F., Du Pasquier L., Katagiri M., Kasahara M. 1993. Evolution of the MHC: isolation of class II beta-chain cDNA clones from the amphibian Xenopus laevis. J Immunol, 150: 2831–2843
Savage A. E., Zamudio K. R. 2011. MHC genotypes associate with resistance to a frog-killing fungus. Proc Natl Acad Sci U S A, 108: 16705–16710
Schaschl H., Wandeler P., Suchentrunk F., Obexer-Ruff G., Goodman S. J. 2006. Selection and recombination drive the evolution of MHC class II DRB diversity in ungulates. Heredity, 97: 427–437
She J. X., Boehme S. A., Wang T. W., Bonhomme F., Wakeland E. K. 1991. Amplification of major histocompatibility complex class II gene diversity by intraexonic recombination. Proc Natl Acad Sci U S A, 88: 453–457
Shu Y. L., Hong P., Yang Y. W., Wu H. L. 2013. An endemic frog harbors multiple expression loci with different patterns of variation in the MHC class II B gene. J Exp Zool Part B: Mol Develop Evol, 9999: 1–10
Siddle H. V., Kreiss A., Eldridge M. D. B., et al. 2007. Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc Natl Acad Sci U S A, 104: 16221–16226
Smith S., de Bellocq J. G., Suchentrunk F., Schaschl H. 2011. Evolutionary genetics of MHC class II beta genes in the brown hare, Lepus europaeus. Immunogenetics, 63: 743–751
Sommer S. 2005. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool, 2: 16
Spurgin L. G., Richardson D. S. 2010. How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc Roy Soc B: Biol Sci, 277: 979–988
Stuart S. N., Chanson J. S., Cox N. A., et al. 2004. Status and trends of amphibian declines and extinctions worldwide. Science, 306: 1783–1786
Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol, 30: 2725–2729
Tong J. C., Bramson J., Kanduc D., Chow S., Sinha A. A., Ranganathan S. 2006. Modeling the bound conformation of Pemphigus vulgaris-associated peptides to MHC Class II DR and DQ alleles. Immunol Res, 2: 1
Wei Y., Xu K., Zhu D.Z., Chen X.F., Wang X.L. 2010. Early-spring survey for Batrachochytrium dendrobatidis in wild Rana dybowskii in Heilongjiang Province, China. Dis Aquat Organ, 92: 241–244
Xu S., Ren W., Zhou X., Zhou K., Yang G. 2010. Sequence polymorphism and geographical variation at a positively selected MHC-DRB gene in the finless porpoise (Neophocaena phocaenoides): implication for recent differentiation of the Yangtze finless porpoise? J Mol Evol, 71: 6–22
Xu T. J., Sun Y. N., Wang R. X. 2011. Allelic polymorphism, gene duplication and balancing selection of the MHC class II DAB gene of Cynoglossus semilaevis (Cynoglossidae). Genet Mol Res, 10: 53–64
Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci, 13: 555–556
Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol, 24: 1586–1591
Yang Z., Nielsen R., Goldman N., Pedersen A. M. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics, 155: 431–449
Yang Z., Wong W. S., Nielsen R. 2005. Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol, 22: 1107–1118
Yu X., Zheng R., Zhang J., Shen B., Dong B. 2014. Genetic polymorphism of major histocompatibility complex class IIB alleles and pathogen resistance in the giant spiny frog Quasipaa spinosa. Infect Genet Evol, 28: 175–182
Zeisset I., Beebee T. C. 2013. Bufo MHC class II loci with conserved introns flanking exon 2: cross-species amplification with common primers. Conserv Genet Resour, 5: 211–213
Zeisset I., Beebee T. J. 2009. Molecular characterization of major histocompatibility complex class II alleles in the common frog, Rana temporaria. Mol Ecol Resour, 9: 738–745
Zhao E. M., Adler K. 1993. Herpetology of China. Society for the Study of Amphibians and Reptiles, Oxford (Ohio)
Zhao M., Wang Y., Shen H., et al. 2013. Evolution by selection, recombination, and gene duplication in MHC class I genes of two Rhacophoridae species. BMC Evol Biol, 13: 113
Zhu R., Chen Z. Y., Wang J., et al. 2013. Extensive diversification of MHC in Chinese giant salamanders Andrias davidianus (Anda-MHC) reveals novel splice variants. Dev Comp Immunol, 42: 311–322

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Last Update: 2016-03-30