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Plant Cell. Nov 1998; 10(11): 1833–1846.
PMCID: PMC143952

Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection.

Abstract

Disease resistance genes in plants are often found in complex multigene families. The largest known cluster of disease resistance specificities in lettuce contains the RGC2 family of genes. We compared the sequences of nine full-length genomic copies of RGC2 representing the diversity in the cluster to determine the structure of genes within this family and to examine the evolution of its members. The transcribed regions range from at least 7.0 to 13.1 kb, and the cDNAs contain deduced open reading frames of approximately 5. 5 kb. The predicted RGC2 proteins contain a nucleotide binding site and irregular leucine-rich repeats (LRRs) that are characteristic of resistance genes cloned from other species. Unique features of the RGC2 gene products include a bipartite LRR region with >40 repeats. At least eight members of this family are transcribed. The level of sequence diversity between family members varied in different regions of the gene. The ratio of nonsynonymous (Ka) to synonymous (Ks) nucleotide substitutions was lowest in the region encoding the nucleotide binding site, which is the presumed effector domain of the protein. The LRR-encoding region showed an alternating pattern of conservation and hypervariability. This alternating pattern of variation was also found in all comparisons within families of resistance genes cloned from other species. The Ka /Ks ratios indicate that diversifying selection has resulted in increased variation at these codons. The patterns of variation support the predicted structure of LRR regions with solvent-exposed hypervariable residues that are potentially involved in binding pathogen-derived ligands.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Anderson PA, Okubara PA, Arroyo-Garcia R, Meyers BC, Michelmore RW. Molecular analysis of irradiation-induced and spontaneous deletion mutants at a disease resistance locus in Lactuca sativa. Mol Gen Genet. 1996 Jun 12;251(3):316–325. [PubMed]
  • Anderson PA, Lawrence GJ, Morrish BC, Ayliffe MA, Finnegan EJ, Ellis JG. Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell. 1997 Apr;9(4):641–651. [PMC free article] [PubMed]
  • Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP. Signaling in plant-microbe interactions. Science. 1997 May 2;276(5313):726–733. [PubMed]
  • Bennetzen JL. The contributions of retroelements to plant genome organization, function and evolution. Trends Microbiol. 1996 Sep;4(9):347–353. [PubMed]
  • Bent AF. Plant Disease Resistance Genes: Function Meets Structure. Plant Cell. 1996 Oct;8(10):1757–1771. [PMC free article] [PubMed]
  • Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science. 1994 Sep 23;265(5180):1856–1860. [PubMed]
  • Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirkse W, Van Staveren M, Stiekema W, et al. Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature. 1998 Jan 29;391(6666):485–488. [PubMed]
  • Brook JD, McCurrach ME, Harley HG, Buckler AJ, Church D, Aburatani H, Hunter K, Stanton VP, Thirion JP, Hudson T, et al. Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3' end of a transcript encoding a protein kinase family member. Cell. 1992 Feb 21;68(4):799–808. [PubMed]
  • Crute IR, Pink DAC. Genetics and Utilization of Pathogen Resistance in Plants. Plant Cell. 1996 Oct;8(10):1747–1755. [PMC free article] [PubMed]
  • Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JD. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell. 1996 Feb 9;84(3):451–459. [PubMed]
  • Edwards A, Civitello A, Hammond HA, Caskey CT. DNA typing and genetic mapping with trimeric and tetrameric tandem repeats. Am J Hum Genet. 1991 Oct;49(4):746–756. [PMC free article] [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, Lawrence G, Ayliffe M, Anderson P, Collins N, Finnegan J, Frost D, Luck J, Pryor T. Advances in the molecular genetic analysis of the flax-flax rust interaction. Annu Rev Phytopathol. 1997;35:271–291. [PubMed]
  • Endo T, Ikeo K, Gojobori T. Large-scale search for genes on which positive selection may operate. Mol Biol Evol. 1996 May;13(5):685–690. [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]
  • Fu YH, Kuhl DP, Pizzuti A, Pieretti M, Sutcliffe JS, Richards S, Verkerk AJ, Holden JJ, Fenwick RG, Jr, Warren ST, et al. Variation of the CGG repeat at the fragile X site results in genetic instability: resolution of the Sherman paradox. Cell. 1991 Dec 20;67(6):1047–1058. [PubMed]
  • Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangl JL. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science. 1995 Aug 11;269(5225):843–846. [PubMed]
  • Hagiwara K, Harris CC. 'Long distance sequencer' method; a novel strategy for large DNA sequencing projects. Nucleic Acids Res. 1996 Jun 15;24(12):2460–2461. [PMC free article] [PubMed]
  • Hammond-Kosack Kim E, Jones Jonathan D G. PLANT DISEASE RESISTANCE GENES. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):575–607. [PubMed]
  • Hebsgaard SM, Korning PG, Tolstrup N, Engelbrecht J, Rouzé P, Brunak S. Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. Nucleic Acids Res. 1996 Sep 1;24(17):3439–3452. [PMC free article] [PubMed]
  • Hughes AL, Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. [PubMed]
  • Hulbert SH. Structure and evolution of the rp1 complex conferring rust resistance in maize. Annu Rev Phytopathol. 1997;35:293–310. [PubMed]
  • Jones A, Davies HM, Voelker TA. Palmitoyl-acyl carrier protein (ACP) thioesterase and the evolutionary origin of plant acyl-ACP thioesterases. Plant Cell. 1995 Mar;7(3):359–371. [PMC free article] [PubMed]
  • Kajava AV, Vassart G, Wodak SJ. Modeling of the three-dimensional structure of proteins with the typical leucine-rich repeats. Structure. 1995 Sep 15;3(9):867–877. [PubMed]
  • Kobe B, Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci. 1994 Oct;19(10):415–421. [PubMed]
  • Kobe B, Deisenhofer J. A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature. 1995 Mar 9;374(6518):183–186. [PubMed]
  • Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG. The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell. 1995 Aug;7(8):1195–1206. [PMC free article] [PubMed]
  • Li WH. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol. 1993 Jan;36(1):96–99. [PubMed]
  • Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO, Zhang Z, Michelmore RW. The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell. 1998 Nov;10(11):1817–1832. [PMC free article] [PubMed]
  • Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell. 1998 Aug;10(8):1307–1319. [PMC free article] [PubMed]
  • Mindrinos M, Katagiri F, Yu GL, Ausubel FM. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell. 1994 Sep 23;78(6):1089–1099. [PubMed]
  • Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. [PubMed]
  • Nei M, Gu X, Sitnikova T. Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7799–7806. [PMC free article] [PubMed]
  • Okubara PA, Arroyo-Garcia R, Shen KA, Mazier M, Meyers BC, Ochoa OE, Kim S, Yang CH, Michelmore RW. A transgenic mutant of Lactuca sativa (lettuce) with a T-DNA tightly linked to loss of downy mildew resistance. Mol Plant Microbe Interact. 1997 Nov;10(8):970–977. [PubMed]
  • Ori N, Eshed Y, Paran I, Presting G, Aviv D, Tanksley S, Zamir D, Fluhr R. The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell. 1997 Apr;9(4):521–532. [PMC free article] [PubMed]
  • Parker JE, Coleman MJ, Szabò V, Frost LN, Schmidt R, van der Biezen EA, Moores T, Dean C, Daniels MJ, Jones JD. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell. 1997 Jun;9(6):879–894. [PMC free article] [PubMed]
  • Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BB, Jones JD. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell. 1997 Dec 12;91(6):821–832. [PubMed]
  • Richter TE, Pryor TJ, Bennetzen JL, Hulbert SH. New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics. 1995 Sep;141(1):373–381. [PMC free article] [PubMed]
  • Salmeron JM, Oldroyd GE, Rommens CM, Scofield SR, Kim HS, Lavelle DT, Dahlbeck D, Staskawicz BJ. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell. 1996 Jul 12;86(1):123–133. [PubMed]
  • SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, et al. Nested retrotransposons in the intergenic regions of the maize genome. Science. 1996 Nov 1;274(5288):765–768. [PubMed]
  • Shen KA, Meyers BC, Islam-Faridi MN, Chin DB, Stelly DM, Michelmore RW. Resistance gene candidates identified by PCR with degenerate oligonucleotide primers map to clusters of resistance genes in lettuce. Mol Plant Microbe Interact. 1998 Aug;11(8):815–823. [PubMed]
  • Shepherd KW, Mayo GM. Genes conferring specific plant disease resistance. Science. 1972 Jan 28;175(4020):375–380. [PubMed]
  • Song WY, Pi LY, Wang GL, Gardner J, Holsten T, Ronald PC. Evolution of the rice Xa21 disease resistance gene family. Plant Cell. 1997 Aug;9(8):1279–1287. [PMC free article] [PubMed]
  • Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JD. Molecular genetics of plant disease resistance. Science. 1995 May 5;268(5211):661–667. [PubMed]
  • Sudupak MA, Bennetzen JL, Hulbert SH. Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize. Genetics. 1993 Jan;133(1):119–125. [PMC free article] [PubMed]
  • Tanaka T, Nei M. Positive darwinian selection observed at the variable-region genes of immunoglobulins. Mol Biol Evol. 1989 Sep;6(5):447–459. [PubMed]
  • Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, Hatzixanthis K, Jones JD. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell. 1997 Dec;9(12):2209–2224. [PMC free article] [PubMed]
  • Traut TW. The functions and consensus motifs of nine types of peptide segments that form different types of nucleotide-binding sites. Eur J Biochem. 1994 May 15;222(1):9–19. [PubMed]
  • Wang GL, Ruan DL, Song WY, Sideris S, Chen L, Pi LY, Zhang S, Zhang Z, Fauquet C, Gaut BS, et al. Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell. 1998 May;10(5):765–779. [PMC free article] [PubMed]
  • Wessler SR, Bureau TE, White SE. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Dev. 1995 Dec;5(6):814–821. [PubMed]
  • Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kurata N, Yano M, Iwata N, Sasaki T. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1663–1668. [PMC free article] [PubMed]
  • Zhang J, Kumar S, Nei M. Small-sample tests of episodic adaptive evolution: a case study of primate lysozymes. Mol Biol Evol. 1997 Dec;14(12):1335–1338. [PubMed]

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