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Molecular Evolution of a Small Gene Family of Wound Inducible Kunitz Trypsin Inhibitors in Populus

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Abstract

Maximum likelihood models of codon substitutions were used to analyze the molecular evolution of a Kunitz trypsin inhibitor (KTI) gene family in Populus and Salix. The methods support previous assertions that the KTI genes comprise a rapidly evolving gene family. Models that allow for codon specific estimates of the ratio of nonsynonymous to synonymous substitutions (ω) among sites detect positive Darwinian selection at several sites in the KTI protein. In addition, branch-specific maximum likelihood models show that there is significant heterogeneity in ω among branches of the KTI phylogeny. In particular, ω is substantially higher following duplication than speciation. There is also evidence for significant rate heterogeneity following gene duplication, suggesting different evolutionary rates in newly arisen gene duplicates. The results indicate uneven evolutionary rates both between sites in the KTI protein and among different lineages in the KTI phylogeny, which is incompatible with a neutral model of sequence evolution.

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References

  • Agrawal S, Tuzun S, Bent E (1999) Inducible plant defenses against pathogens and herbivores: Biochemistry, ecology, and agriculture. Am Phytopathol Soc Press, St. Paul, MN

    Google Scholar 

  • Anisimova M, Bielawski JP, Yang Z (2001) Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol 18(8):1585–1592

    PubMed  CAS  Google Scholar 

  • Bergelson J, Dwyer G, Emerson JJ (2001) Models and data on plant-enemy coevolution. Annu Rev Genet 35:469–499

    Article  PubMed  CAS  Google Scholar 

  • Bradshaw HD, Hollick JB, Parsons TJ, Clarke HR, Gordon MP (1990) Systemically wound-responsive genes in poplar trees encode proteins similar to sweet potato sporamins and legume Kunitz trypsin inhibitors. Plant Mol Biol 14:51–59

    Article  PubMed  CAS  Google Scholar 

  • Christopher ME, Miranda M, Major IT, Constabel CP (2004) Gene expression profiling of systemically wound-induced defenses in hybrid poplar. Planta 219:936–947

    Article  PubMed  CAS  Google Scholar 

  • Clauss MJ, Mitchell-Olds TM (2004) Functional divergence in tandemly duplicated Arabidopsis thaliana trypsin inhibitor genes. Genetics 166:1419–1436

    Article  PubMed  CAS  Google Scholar 

  • Constabel CP (1999) A Survay of Herbivore-Inducible Defensive Proteins and Phytochemicals. In: Agrawal S, Tuzun S, Bent E (eds) Inducible plant defenses against pathogens and herbivores: Biochemistry, ecology, and agriculture. Am Phytopathol Soc Press, St. Paul, MN, pp 137–166

    Google Scholar 

  • De Meester P, Brick P, Lloyd LF, Blow DM, Onesti S (1998) Structure of the Kunitz-type Soybean trypsin inhibitor (STI): implications for the interactions between members of the STI family and tissue-plasminogen activator. Acta Crystallogr D54:589–597

    Google Scholar 

  • Grzesiak A, Helland R, Smalas AO, Krowarsch D, Dadlez M, Otlewski J (2000) Substitutions at the P- position in BPTI strongly affect the association energy with serine proteinases. J Mol Biol 301:205–217

    Article  PubMed  CAS  Google Scholar 

  • Gu Z, Cavalcanti A, Chen F, Bouman P, Li W (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19:256–262

    PubMed  CAS  Google Scholar 

  • Haq SK, Atif SM, Khan RH (2004) Protein proteinase inhibitors in combat against insects, pests and pathogens: natural and engineered phytoprotection. Arch Biochem Biophys 431:145–159

    Article  PubMed  CAS  Google Scholar 

  • Haruta M, Major IT, Christopher ME, Patton JJ, Constable CP (2001) A Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.): cloning, functional expression and induction by wounding and herbivory. Plant Mol Biol 46:347–359

    Article  PubMed  CAS  Google Scholar 

  • Heitz T, Geoffroy P, Fritig B, Legrand M (1999) The PR-6 family: proteinase inhibitors in plant-microbe and plant-insect interactions. In: Datta SK, Muthukrishan S (eds) Pathogenesis-related proteins in plants. CRC Press, Boca Raton, FL, pp 131–155

    Google Scholar 

  • Hughes AL (1994) The evolution of functionally novel proteins after gene duplication. Proc R Soc Lond B Biol Sci 256:119–124

    CAS  Google Scholar 

  • Ingvarsson PK (2005) Molecular population genetics of herbivore-induced protease inhibitor genes in European Aspen (Populus tremula, L., Salicaceae). Mol Biol Evol 22(9):1802–1812

    Article  PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responces to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • Kellenberger C, Ferrat G, Leone P, Darbon H, Roussel A (2003) Selective inhibition of trypsins by insect peptides: Role of P6-P10 loop. Biochemistry 42:13605–13612

    Article  PubMed  CAS  Google Scholar 

  • Lazzaro BP, Sceurman BK, Clar AG (2004) Genetic basis of natural variation in D-melanogaster antibacterial immunity. Science 303:1873–1876

    Article  PubMed  CAS  Google Scholar 

  • Lee SI, Lee SH, Koo JC, Chun HJ, Lim CO, Mun JH, Song YH, Cho MJ (1999) Soybean Kunitz trypsin inhibitor (SKTI) confers resistance to the brown planthopper (Nilaparvata lugens Stal) in transgenic rice. Mol Breed 5:1–9

    Article  Google Scholar 

  • Leister D (2004) Tandem and segmental duplication and recombination in the evolution of plant disease resistance genes. Trends Genet 20:116–122

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Connery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, O’Hely M, Walsh B, Force A (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159:1789–1804

    PubMed  CAS  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134

    Article  PubMed  CAS  Google Scholar 

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes evolve by divergent selection and a birth-death process. Genome Res 8:1113–1130

    PubMed  CAS  Google Scholar 

  • Mondragon-Palomino M, Meyers BC, Michelmore RW, Gaut BS (2002) Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Res 12:1305–1315

    Article  PubMed  CAS  Google Scholar 

  • Moore RC, Purugganan MD (2003) The early stages of duplicate gene evolution. Proc Natl Acad Sci USA 100:15682–15687

    Article  PubMed  CAS  Google Scholar 

  • Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122–128

    Article  PubMed  CAS  Google Scholar 

  • Nielsen J, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Prot Eng 10:1–6

    Article  CAS  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer-Verlag, Berlin

    Google Scholar 

  • Ravichandran S, Sen U, Chakrabarti C, Dattagupta JK (1999) Cryocrystallography of a Kunitz-type serine protease inhibitor: the 90 K structure of winged bean chymotrypsin inhibitor (WCI) at 2.13 Å resolution. Acta Crystallogr D 55:1814–1821

    Article  PubMed  CAS  Google Scholar 

  • Ryan CA (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu Rev Phytopath 28:425–449

    Article  CAS  Google Scholar 

  • Saarikoski P, Clapham D, von Arnold S (1996) A wound-inducible gene from Salix viminalis coding for a trypsin inhibitor. Plant Mol Biol 31:465–478

    Article  PubMed  CAS  Google Scholar 

  • Schein M, Yang Z, Mitchell-Olds T, Schmid KJ (2004) Rapid evolution of a pollen-specific oleosin-like gene family from Arabidopsis thaliana and closely related species. Mol Biol Evol 21(4):659–669

    Article  PubMed  CAS  Google Scholar 

  • Song HK, Suh SW (1998) Kunitz-type soybean trypsin inhibitor revisited: Refined structure of its complex with porcine trypsin reveals an insight into the interaction between a homologous inhibitor from Erythrina caffra and tissue-type plasminogen activator. J Mol Biol 275:347–363

    Article  PubMed  CAS  Google Scholar 

  • Swanson WJ, Vaquier V (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–144

    Article  PubMed  CAS  Google Scholar 

  • Swanson WJ, Neilsen R, Yang Q (2003) Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20(1):18–20

    PubMed  CAS  Google Scholar 

  • Tajima F (1993) Simple methods for testing molecular clock hypothesis. Genetics 135:599–607

    PubMed  CAS  Google Scholar 

  • Tiffin P, Gaut BS (2001) Molecular evolution of the wound-induced serine protease inhibitor wip1 in Zea and related genera. Mol Biol Evol 18:2092–2101

    PubMed  CAS  Google Scholar 

  • Walsh JB (1995) How often do duplicated genes evolve new functions? Genetics 139:421–428

    PubMed  CAS  Google Scholar 

  • Yang Z (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15(5):568–573

    PubMed  CAS  Google Scholar 

  • Yang Z, Nielsen R (1998) Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol 46(4):409–418

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Nielsen R (2002) Codon-substitution models for detecting molecular adaptation at individualnsites along specific lineages. Mol Biol Evol 19(6):908–917

    PubMed  CAS  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Krabbe Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    PubMed  CAS  Google Scholar 

  • Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by a grant from the Swedish Research Council (Vetenskapsrådet) to P.K.I. We are grateful to two anonymous reviewers for providing comments that substantially improved the paper.

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  1. Umeå Plant Science Centre, Department of Ecology and Environmental Science, Umeå University, SE-90187, Umeå, Sweden

    Nina M. Talyzina & Pär K. Ingvarsson

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  1. Nina M. Talyzina
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  2. Pär K. Ingvarsson
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Correspondence to Pär K. Ingvarsson.

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[Reviewing Editor: Dr. Willie J. Swanson]

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Talyzina, N.M., Ingvarsson, P.K. Molecular Evolution of a Small Gene Family of Wound Inducible Kunitz Trypsin Inhibitors in Populus. J Mol Evol 63, 108–119 (2006). https://doi.org/10.1007/s00239-005-0249-2

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  • DOI: https://doi.org/10.1007/s00239-005-0249-2

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