• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Mar 2004; 166(3): 1419–1436.
PMCID: PMC1470761

Functional divergence in tandemly duplicated Arabidopsis thaliana trypsin inhibitor genes.

Abstract

In multigene families, variation among loci and alleles can contribute to trait evolution. We explored patterns of functional and genetic variation in six duplicated Arabidopsis thaliana trypsin inhibitor (ATTI) loci. We demonstrate significant variation in constitutive and herbivore-induced transcription among ATTI loci that show, on average, 65% sequence divergence. Significant variation in ATTI expression was also found between two molecularly defined haplotype classes. Population genetic analyses for 17 accessions of A. thaliana showed that six ATTI loci arranged in tandem within 10 kb varied 10-fold in nucleotide diversity, from 0.0009 to 0.0110, and identified a minimum of six recombination events throughout the tandem array. We observed a significant peak in nucleotide and indel polymorphism spanning ATTI loci in the interior of the array, due primarily to divergence between the two haplotype classes. Significant deviation from the neutral equilibrium model for individual genes was interpreted within the context of intergene linkage disequilibrium and correlated patterns of functional differentiation. In contrast to the outcrosser Arabidopsis lyrata for which recombination is observed even within ATTI loci, our data suggest that response to selection was slowed in the inbreeding, annual A. thaliana because of interference among functionally divergent ATTI loci.

Full Text

The Full Text of this article is available as a PDF (364K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bittner-Eddy PD, Crute IR, Holub EB, Beynon JL. RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 2000 Jan;21(2):177–188. [PubMed]
  • Blanc Guillaume, Hokamp Karsten, Wolfe Kenneth H. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res. 2003 Feb;13(2):137–144. [PMC free article] [PubMed]
  • Broadway RM. Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. J Insect Physiol. 1997 Sep;43(9):855–874. [PubMed]
  • Ceci Luigi R, Volpicella Mariateresa, Rahbé Yvan, Gallerani Raffaele, Beekwilder Jules, Jongsma Maarten A. Selection by phage display of a variant mustard trypsin inhibitor toxic against aphids. Plant J. 2003 Feb;33(3):557–566. [PubMed]
  • Ceci LR, Spoto N, de Virgilio M, Gallerani R. The gene coding for the mustard trypsin inhibitor-2 is discontinuous and wound-inducible. FEBS Lett. 1995 May 8;364(2):179–181. [PubMed]
  • Ceciliani F, Bortolotti F, Menegatti E, Ronchi S, Ascenzi P, Palmieri S. Purification, inhibitory properties, amino acid sequence and identification of the reactive site of a new serine proteinase inhibitor from oil-rape (Brassica napus) seed. FEBS Lett. 1994 Apr 4;342(2):221–224. [PubMed]
  • Charlesworth Deborah. Effects of inbreeding on the genetic diversity of populations. Philos Trans R Soc Lond B Biol Sci. 2003 Jun 29;358(1434):1051–1070. [PMC free article] [PubMed]
  • Clauss MJ, Mitchell-Olds T. Population genetics of tandem trypsin inhibitor genes in Arabidopsis species with contrasting ecology and life history. Mol Ecol. 2003 May;12(5):1287–1299. [PubMed]
  • Collins Nicholas C, Thordal-Christensen Hans, Lipka Volker, Bau Stephan, Kombrink Erich, Qiu Jin-Long, Hückelhoven Ralph, Stein Mónica, Freialdenhoven Andreas, Somerville Shauna C, et al. SNARE-protein-mediated disease resistance at the plant cell wall. Nature. 2003 Oct 30;425(6961):973–977. [PubMed]
  • Comeron Josep M, Kreitman Martin. Population, evolutionary and genomic consequences of interference selection. Genetics. 2002 May;161(1):389–410. [PMC free article] [PubMed]
  • De Leo F, Bonade-Bottino MA, Ceci LR, Gallerani R, Jouanin L. Opposite effects on spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants . Plant Physiol. 1998 Nov;118(3):997–1004. [PMC free article] [PubMed]
  • De Leo F, Bonadé-Bottino M, Ceci LR, Gallerani R, Jouanin L. Effects of a mustard trypsin inhibitor expressed in different plants on three lepidopteran pests. Insect Biochem Mol Biol. 2001 Apr 27;31(6-7):593–602. [PubMed]
  • Duda TF, Jr, Palumbi SR. Evolutionary diversification of multigene families: allelic selection of toxins in predatory cone snails. Mol Biol Evol. 2000 Sep;17(9):1286–1293. [PubMed]
  • Ellis JG, Lawrence GJ, Finnegan EJ, Anderson PA. Contrasting complexity of two rust resistance loci in flax. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4185–4188. [PMC free article] [PubMed]
  • Ellis J, Dodds P, Pryor T. Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol. 2000 Aug;3(4):278–284. [PubMed]
  • Ascenzi P, Ruoppolo M, Amoresano A, Pucci P, Consonni R, Zetta L, Pascarella S, Bortolotti F, Menegatti E. Characterization of low-molecular-mass trypsin isoinhibitors from oil-rape (Brassica napus var. oleifera) seed. Eur J Biochem. 1999 Apr;261(1):275–284. [PubMed]
  • Fay JC, Wu CI. Hitchhiking under positive Darwinian selection. Genetics. 2000 Jul;155(3):1405–1413. [PMC free article] [PubMed]
  • Fay Justin C, Wyckoff Gerald J, Wu Chung-I. Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature. 2002 Feb 28;415(6875):1024–1026. [PubMed]
  • Baines John F, Chen Ying, Das Aparup, Stephan Wolfgang. DNA sequence variation at a duplicated gene: excess of replacement polymorphism and extensive haplotype structure in the Drosophila melanogaster bicoid region. Mol Biol Evol. 2002 Jul;19(7):989–998. [PubMed]
  • Ferrari Simone, Vairo Donatella, Ausubel Frederick M, Cervone Felice, De Lorenzo Giulia. Tandemly duplicated Arabidopsis genes that encode polygalacturonase-inhibiting proteins are regulated coordinately by different signal transduction pathways in response to fungal infection. Plant Cell. 2003 Jan;15(1):93–106. [PMC free article] [PubMed]
  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999 Apr;151(4):1531–1545. [PMC free article] [PubMed]
  • Betancourt Andrea J, Presgraves Daven C. Linkage limits the power of natural selection in Drosophila. Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13616–13620. [PMC free article] [PubMed]
  • Ford Michael J. Applications of selective neutrality tests to molecular ecology. Mol Ecol. 2002 Aug;11(8):1245–1262. [PubMed]
  • Frohman MA, Dush MK, Martin GR. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. [PMC free article] [PubMed]
  • Kuittinen H, Aguadé M. Nucleotide variation at the CHALCONE ISOMERASE locus in Arabidopsis thaliana. Genetics. 2000 Jun;155(2):863–872. [PMC free article] [PubMed]
  • Green TR, Ryan CA. Wound-Induced Proteinase Inhibitor in Plant Leaves: A Possible Defense Mechanism against Insects. Science. 1972 Feb 18;175(4023):776–777. [PubMed]
  • Ling MH, Qi HY, Chi CW. Protein, cDNA, and genomic DNA sequences of the towel gourd trypsin inhibitor. A squash family inhibitor. J Biol Chem. 1993 Jan 15;268(2):810–814. [PubMed]
  • Gu Zhenglong, Cavalcanti Andre, Chen Feng-Chi, Bouman Peter, Li Wen-Hsiung. Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol. 2002 Mar;19(3):256–262. [PubMed]
  • Long AD, Lyman RF, Langley CH, Mackay TF. Two sites in the Delta gene region contribute to naturally occurring variation in bristle number in Drosophila melanogaster. Genetics. 1998 Jun;149(2):999–1017. [PMC free article] [PubMed]
  • Hanfstingl U, Berry A, Kellogg EA, Costa JT, 3rd, Rüdiger W, Ausubel FM. Haplotypic divergence coupled with lack of diversity at the Arabidopsis thaliana alcohol dehydrogenase locus: roles for both balancing and directional selection? Genetics. 1994 Nov;138(3):811–828. [PMC free article] [PubMed]
  • Lynch Michael, Conery John S. The evolutionary demography of duplicate genes. J Struct Funct Genomics. 2003;3(1-4):35–44. [PubMed]
  • Haruta M, Major IT, Christopher ME, Patton JJ, Constabel CP. A Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.): cloning, functional expression, and induction by wounding and herbivory. Plant Mol Biol. 2001 Jun;46(3):347–359. [PubMed]
  • Lynch M, O'Hely M, Walsh B, Force A. The probability of preservation of a newly arisen gene duplicate. Genetics. 2001 Dec;159(4):1789–1804. [PMC free article] [PubMed]
  • Haubold Bernhard, Kroymann Jürgen, Ratzka Andreas, Mitchell-Olds Thomas, Wiehe Thomas. Recombination and gene conversion in a 170-kb genomic region of Arabidopsis thaliana. Genetics. 2002 Jul;161(3):1269–1278. [PMC free article] [PubMed]
  • Mauricio Rodney, Stahl Eli A, Korves Tonia, Tian Dacheng, Kreitman Martin, Bergelson Joy. Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics. 2003 Feb;163(2):735–746. [PMC free article] [PubMed]
  • Hauser MT, Harr B, Schlötterer C. Trichome distribution in Arabidopsis thaliana and its close relative Arabidopsis lyrata: molecular analysis of the candidate gene GLABROUS1. Mol Biol Evol. 2001 Sep;18(9):1754–1763. [PubMed]
  • McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. [PubMed]
  • Menegatti E, Tedeschi G, Ronchi S, Bortolotti F, Ascenzi P, Thomas RM, Bolognesi M, Palmieri S. Purification, inhibitory properties and amino acid sequence of a new serine proteinase inhibitor from white mustard (Sinapis alba L.) seed. FEBS Lett. 1992 Apr 13;301(1):10–14. [PubMed]
  • Meyers BC, Shen KA, Rohani P, Gaut BS, Michelmore RW. Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell. 1998 Nov;10(11):1833–1846. [PMC free article] [PubMed]
  • Miralles R, Gerrish PJ, Moya A, Elena SF. Clonal interference and the evolution of RNA viruses. Science. 1999 Sep 10;285(5434):1745–1747. [PubMed]
  • Hudson RR. Estimating the recombination parameter of a finite population model without selection. Genet Res. 1987 Dec;50(3):245–250. [PubMed]
  • Mondragón-Palomino Mariana, Meyers Blake C, Michelmore Richard W, Gaut Brandon S. Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Res. 2002 Sep;12(9):1305–1315. [PMC free article] [PubMed]
  • Hudson RR, Kaplan NL. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 1985 Sep;111(1):147–164. [PMC free article] [PubMed]
  • Hudson RR, Kreitman M, Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. [PMC free article] [PubMed]
  • Navarro Arcadio, Barton Nick H. The effects of multilocus balancing selection on neutral variability. Genetics. 2002 Jun;161(2):849–863. [PMC free article] [PubMed]
  • Bolter C, Jongsma MA. The adaptation of insects to plant protease inhibitors. J Insect Physiol. 1997 Oct;43(10):885–895. [PubMed]
  • Nordborg Magnus, Innan Hideki. The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population. Genetics. 2003 Mar;163(3):1201–1213. [PMC free article] [PubMed]
  • Jongsma MA, Bakker PL, Peters J, Bosch D, Stiekema WJ. Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):8041–8045. [PMC free article] [PubMed]
  • Nordborg Magnus, Borevitz Justin O, Bergelson Joy, Berry Charles C, Chory Joanne, Hagenblad Jenny, Kreitman Martin, Maloof Julin N, Noyes Tina, Oefner Peter J, et al. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet. 2002 Feb;30(2):190–193. [PubMed]
  • Kawabe A, Miyashita NT. DNA variation in the basic chitinase locus (ChiB) region of the wild plant Arabidopsis thaliana. Genetics. 1999 Nov;153(3):1445–1453. [PMC free article] [PubMed]
  • Kawabe A, Innan H, Terauchi R, Miyashita NT. Nucleotide polymorphism in the acidic chitinase locus (ChiA) region of the wild plant Arabidopsis thaliana. Mol Biol Evol. 1997 Dec;14(12):1303–1315. [PubMed]
  • Olsen Kenneth M, Womack Andrew, Garrett Ashley R, Suddith Jane I, Purugganan Michael D. Contrasting evolutionary forces in the Arabidopsis thaliana floral developmental pathway. Genetics. 2002 Apr;160(4):1641–1650. [PMC free article] [PubMed]
  • Kim Y, Stephan W. Joint effects of genetic hitchhiking and background selection on neutral variation. Genetics. 2000 Jul;155(3):1415–1427. [PMC free article] [PubMed]
  • Parsch J, Meiklejohn CD, Hartl DL. Patterns of DNA sequence variation suggest the recent action of positive selection in the janus-ocnus region of Drosophila simulans. Genetics. 2001 Oct;159(2):647–657. [PMC free article] [PubMed]
  • Kim Yuseob, Stephan Wolfgang. Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics. 2002 Feb;160(2):765–777. [PMC free article] [PubMed]
  • Pautot V, Holzer FM, Walling LL. Differential expression of tomato proteinase inhibitor I and II genes during bacterial pathogen invasion and wounding. Mol Plant Microbe Interact. 1991 May-Jun;4(3):284–292. [PubMed]
  • Kim Yuseob, Stephan Wolfgang. Selective sweeps in the presence of interference among partially linked loci. Genetics. 2003 May;164(1):389–398. [PMC free article] [PubMed]
  • Kirby DA, Stephan W. Multi-locus selection and the structure of variation at the white gene of Drosophila melanogaster. Genetics. 1996 Oct;144(2):635–645. [PMC free article] [PubMed]
  • Polticelli F, Ascenzi P, Bolognesi M, Honig B. Structural determinants of trypsin affinity and specificity for cationic inhibitors. Protein Sci. 1999 Dec;8(12):2621–2629. [PMC free article] [PubMed]
  • Koch M, Haubold B, Mitchell-Olds T. Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. Am J Bot. 2001 Mar;88(3):534–544. [PubMed]
  • Ramos-Onsins Sebastián E, Stranger Barbara E, Mitchell-Olds Thomas, Aguadé Montserrat. Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics. 2004 Jan;166(1):373–388. [PMC free article] [PubMed]
  • Rask L, Andréasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J. Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol. 2000 Jan;42(1):93–113. [PubMed]
  • Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature. 2003 May 1;423(6935):74–77. [PubMed]
  • Rozas J, Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. [PubMed]
  • Tiffin P, Gaut BS. Molecular evolution of the wound-induced serine protease inhibitor wip1 in Zea and related genera. Mol Biol Evol. 2001 Nov;18(11):2092–2101. [PubMed]
  • Ruoppolo M, Amoresano A, Pucci P, Pascarella S, Polticelli F, Trovato M, Menegatti E, Ascenzi P. Characterization of five new low-molecular-mass trypsin inhibitors from white mustard (Sinapis alba L.) seed. Eur J Biochem. 2000 Nov;267(21):6486–6492. [PubMed]
  • Van der Hoorn Renier A L, De Wit Pierre J G M, Joosten Matthieu H A J. Balancing selection favors guarding resistance proteins. Trends Plant Sci. 2002 Feb;7(2):67–71. [PubMed]
  • Volpicella M, Schipper A, Jongsma MA, Spoto N, Gallerani R, Ceci LR. Characterization of recombinant mustard trypsin inhibitor 2 (MTI2) expressed in Pichia pastoris. FEBS Lett. 2000 Feb 25;468(2-3):137–141. [PubMed]
  • Savolainen O, Langley CH, Lazzaro BP, Fr H. Contrasting patterns of nucleotide polymorphism at the alcohol dehydrogenase locus in the outcrossing Arabidopsis lyrata and the selfing Arabidopsis thaliana. Mol Biol Evol. 2000 Apr;17(4):645–655. [PubMed]
  • Volpicella Mariateresa, Ceci Luigi R, Cordewener Jan, America Twan, Gallerani Raffaele, Bode Wolfram, Jongsma Maarten A, Beekwilder Jules. Properties of purified gut trypsin from Helicoverpa zea, adapted to proteinase inhibitors. Eur J Biochem. 2003 Jan;270(1):10–19. [PubMed]
  • Walsh Bruce. Population-genetic models of the fates of duplicate genes. Genetica. 2003 Jul;118(2-3):279–294. [PubMed]
  • Shepard Kristen A, Purugganan Michael D. Molecular population genetics of the Arabidopsis CLAVATA2 region. The genomic scale of variation and selection in a selfing species. Genetics. 2003 Mar;163(3):1083–1095. [PMC free article] [PubMed]
  • Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. [PubMed]
  • Wright Stephen I, Lauga Beatrice, Charlesworth Deborah. Subdivision and haplotype structure in natural populations of Arabidopsis lyrata. Mol Ecol. 2003 May;12(5):1247–1263. [PubMed]
  • Zang X, Maizels RM. Serine proteinase inhibitors from nematodes and the arms race between host and pathogen. Trends Biochem Sci. 2001 Mar;26(3):191–197. [PubMed]
  • Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. [PMC free article] [PubMed]
  • Telang Manasi, Srinivasan Ajay, Patankar Aparna, Harsulkar Abhay, Joshi Vijay, Damle Archana, Deshpande Vasanti, Sainani Mohini, Ranjekar Prabhakar, Gupta Gorakh, et al. Bitter gourd proteinase inhibitors: potential growth inhibitors of Helicoverpa armigera and Spodoptera litura. Phytochemistry. 2003 Jul;63(6):643–652. [PubMed]
  • Zhang Jianzhi, Zhang Ya-ping, Rosenberg Helene F. Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. Nat Genet. 2002 Apr;30(4):411–415. [PubMed]
  • Zhang Liqing, Peek Andrew S, Dunams Detiger, Gaut Brandon S. Population genetics of duplicated disease-defense genes, hm1 and hm2, in maize (Zea mays ssp. mays L.) and its wild ancestor (Zea mays ssp. parviglumis). Genetics. 2002 Oct;162(2):851–860. [PMC free article] [PubMed]
  • Templeton AR, Hollocher H, Johnston JS. The molecular through ecological genetics of abnormal abdomen in Drosophila mercatorum. V. Female phenotypic expression on natural genetic backgrounds and in natural environments. Genetics. 1993 Jun;134(2):475–485. [PMC free article] [PubMed]
  • Zhao Qin, Chae Young Kee, Markley John L. NMR solution structure of ATTp, an Arabidopsis thaliana trypsin inhibitor. Biochemistry. 2002 Oct 15;41(41):12284–12296. [PubMed]
  • Tian Dacheng, Araki Hitoshi, Stahl Eli, Bergelson Joy, Kreitman Martin. Signature of balancing selection in Arabidopsis. Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11525–11530. [PMC free article] [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...