, Volume 139, Issue 11–12, pp 1465–1475

Adaptive evolution of Xa21 homologs in Gramineae



The XA21 protein has broad spectrum resistance against Xanthomonas oryzae pv. oryzae. Although Xa21-mediated immunity is well characterized, little is known about the origin and evolutionary history of this gene in grasses. Therefore, we analyzed all Xa21 gene homologs in eight whole-genome sequenced rice lines, as well as in four gramineous genomes, rice, Brachypodium, sorghum and maize; using Arabidopsis Xa21 homologs as outgroups, 17, 7, 7 and 3 Xa21 homologs were detected in these four grasses, respectively. Synteny and phylogenetic analysis showed that frequent gene translocation, duplication and/or loss, have occurred at Xa21 homologous loci, suggesting that they have undergone or are undergoing rapid generation of copy number variations. Within the rice species, the high level of nucleotide diversity between Xa21-like orthologs showed a strong association with the presence/absence haplotypes, suggesting that the genetic structure of rice lines plays an important role in the variations between these Xa21-like orthologs. Strongly positive selection was detected in the core region of the leucine-rich repeat domains of the Xa21 subclade among the rice lines, indicating that the rapid gene diversification of Xa21 homologs may be a strategy for a given species to adapt to the changing spectrum of species-specific pathogens.


Xa21 Adaptive evolution Syntenic block Positive selection 

Supplementary material

10709_2012_9645_MOESM1_ESM.doc (2.2 mb)
Supplementary material 1 (DOC 2229 kb)


  1. Albert M, Jehle AK, Mueller K, Eisele C, Lipschis M, Felix G (2010) Arabidopsis thaliana pattern recognition receptors for bacterial elongation factor Tu and flagellin can be combined to form functional chimeric receptors. J Biol Chem 285(25):19035–19042PubMedCrossRefGoogle Scholar
  2. Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6(10):973–979PubMedCrossRefGoogle Scholar
  3. Becraft PW, Stinard PS, McCarty DR (1996) CRINKLY4: A TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273(5280):1406–1409PubMedCrossRefGoogle Scholar
  4. Chen Q, Han Z, Jiang H, Tian D, Yang S (2010) Strong positive selection drives rapid diversification of R-genes in Arabidopsis relatives. J Mol Evol 70:137–148CrossRefGoogle Scholar
  5. Danna CH, Millet YA, Koller T, Han SW, Bent AF, Ronald PC, Ausubel FM (2011) The Arabidopsis flagellin receptor FLS2 mediates the perception of Xanthomonas Ax21 secreted peptides. Proc Natl Acad Sci USA 108(22):9286–9291PubMedCrossRefGoogle Scholar
  6. DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7(12):1243–1249PubMedCrossRefGoogle Scholar
  7. Ding J, Cheng HL, Jin XQ, Araki H, Yang YH, Tian DC (2007) Contrasting patterns of evolution between allelic groups at a single locus in Arabidopsis. Genetica 129(3):235–242PubMedCrossRefGoogle Scholar
  8. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103(23):8888–8893PubMedCrossRefGoogle Scholar
  9. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797PubMedCrossRefGoogle Scholar
  10. Ellis JG, Lawrence GJ, Luck JE, Dodds PN (1999) Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11(3):495–506PubMedCrossRefGoogle Scholar
  11. Fantl WJ, Johnson DE, Williams LT (1993) Signaling by receptor tyrosine kinases. Annu Rev Biochem 62:453–481PubMedCrossRefGoogle Scholar
  12. Gaut BS (2002) Evolutionary dynamics of grass genomes. New Phytol 154(1):15–28CrossRefGoogle Scholar
  13. Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5(6):1003–1011PubMedCrossRefGoogle Scholar
  14. Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Lin Z, Buckler ES, Qian Q, Zhang QF, Li J, Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42(11):961–967PubMedCrossRefGoogle Scholar
  15. Initiative TheArabidopsisGenome (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796–815CrossRefGoogle Scholar
  16. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436(7052):793–800CrossRefGoogle Scholar
  17. Jiang HY, Wang CC, Ping L, Yang SH, Tian DC (2007) Pattern of LRR nucleotide variation in plant resistance genes. Plant Sci 173(2):253–261CrossRefGoogle Scholar
  18. Kuang H, Woo SS, Meyers BC, Nevo E, Michelmore RW (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16(11):2870–2894PubMedCrossRefGoogle Scholar
  19. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16(12):3496–3507PubMedCrossRefGoogle Scholar
  20. Lee SW, Han SW, Sririyanum M, Park CJ, Seo YS, Ronald PC (2009) A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 326(5954):850–853PubMedCrossRefGoogle Scholar
  21. Leung H (2008) Stressed genomics—bringing relief to rice fields. Curr Opin Plant Biol 11(2):201–208PubMedCrossRefGoogle Scholar
  22. Li JM, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90(5):929–938PubMedCrossRefGoogle Scholar
  23. Li J, Ding J, Zhang W, Zhang YL, Tang P, Chen JQ, Tian DC, Yang SH (2010) Unique evolutionary pattern of numbers of gramineous NBS-LRR genes. Mol Genet Genomics 283(5):427–438PubMedCrossRefGoogle Scholar
  24. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452PubMedCrossRefGoogle Scholar
  25. Lynch M, Crease TJ (1990) The analysis of population survey data on DNA sequence variation. Mol Biol Evol 7(4):377–394PubMedGoogle Scholar
  26. Mew TW (1987) Current status and future-prospects of research on bacterial-blight of rice. Annu Rev Phytopathol 25:359–382CrossRefGoogle Scholar
  27. Park CJ, Peng Y, Chen XW, Dardick C, Ruan DL, Bart R, Canlas PE, Ronald PC (2008) Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21-mediated innate immunity. PLoS Biol 6(9):1910–1926CrossRefGoogle Scholar
  28. Park CJ, Han SW, Chen XW, Ronald PC (2010) Elucidation of XA21-mediated innate immunity. Cell Microbiol 12(8):1017–1025PubMedCrossRefGoogle Scholar
  29. Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BB, Jones JD (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91(6):821–832PubMedCrossRefGoogle Scholar
  30. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob ur R, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556PubMedCrossRefGoogle Scholar
  31. Ronald PC, Albano B, Tabien R, Abenes L, Wu KS, Mccouch S, Tanksley SD (1992) Genetic and physical analysis of the rice bacterial-blight disease resistance locus, Xa21. Mol Gen Genet 236(1):113–120PubMedGoogle Scholar
  32. Schnable PS, Ware D, Fulton RS, Stein JC, Wei FS, Pasternak S, Liang CZ, Zhang JW, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du FY, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen WZ, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He RF, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin JK, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren LY, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han YJ, Lee H, Li PH, Lisch DR, Liu SZ, Liu ZJ, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang LX, Yu Y, Zhang LF, Zhou SG, Zhu Q, Bennetzen JL, Dawe RK, Jiang JM, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115PubMedCrossRefGoogle Scholar
  33. Shiu SH, Karlowski WM, Pan RS, Tzeng YH, Mayer KFX, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16(5):1220–1234PubMedCrossRefGoogle Scholar
  34. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270(5243):1804–1806PubMedCrossRefGoogle Scholar
  35. Song WY, Pi LY, Wang GL, Gardner J, Holsten T, Ronald PC (1997) Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9(8):1279–1287PubMedCrossRefGoogle Scholar
  36. Song WY, Wang YS, Pi LY, Chen XH, Chakrabarty PK, Jiang J, De Leon AL, Liu GZ, Li LC, Benny U, Oard J, Ronald PC (2006) Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18(12):3635–3646PubMedCrossRefGoogle Scholar
  37. Stein JC, Dixit R, Nasrallah ME, Nasrallah JB (1996) SRK, the stigma-specific S locus receptor kinase of Brassica, is targeted to the plasma membrane in transgenic tobacco. Plant Cell 8(3):429–445PubMedCrossRefGoogle Scholar
  38. Takai R, Isogai A, Takayama S, Che FS (2008) Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Mol Plant Microbe Interact 21(12):1635–1642PubMedCrossRefGoogle Scholar
  39. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739Google Scholar
  40. Tang T, Lu J, Huang J, He J, McCouch SR, Shen Y, Kai Z, Purugganan MD, Shi S, Wu CI (2006) Genomic variation in rice: genesis of highly polymorphic linkage blocks during domestication. PLoS Genet 2(11):e199PubMedCrossRefGoogle Scholar
  41. Tang P, Zhang Y, Sun XQ, Tian DC, Yang SH, Ding J (2010) Disease resistance signature of the leucine-rich repeat receptor-like kinase genes in four plant species. Plant Sci 179(4):399–406CrossRefGoogle Scholar
  42. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y (1996) The arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8(4):735–746PubMedCrossRefGoogle Scholar
  43. Wang GL, Song WY, Ruan DL, Sideris S, Ronald PC (1996) The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv oryzae isolates in transgenic plants. Mol Plant Microbe In 9(9):850–855CrossRefGoogle Scholar
  44. Wang GL, Ruan DL, Song WY, Sideris S, Chen LL, Pi LY, Zhang SP, Zhang Z, Fauquet C, Gaut BS, Whalen MC, Ronald PC (1998) 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 10(5):765–779PubMedCrossRefGoogle Scholar
  45. Wang J, Tan S, Zhang L, Li P, Tian D (2011) Co-variation among major classes of LRR-encoding genes in two pairs of plant species. J Mol Evol 72(5–6):498–509PubMedCrossRefGoogle Scholar
  46. Xu WH, Wang YS, Liu GZ, Chen XH, Tinjuangjun P, Pi LY, Song WY (2006) The autophosphorylated Ser686, Thr688, and Ser689 residues in the intracellular juxtamembrane domain of XA21 are implicated in stability control of rice receptor-like kinase. Plant J 45(5):740–751PubMedCrossRefGoogle Scholar
  47. Yue JX, Meyers BC, Chen JQ, Tian D, Yang S (2012) Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol 193(4):1049–1063PubMedCrossRefGoogle Scholar
  48. Zhang YL, Wang J, Zhang XH, Chen JQ, Yang SH, Tian DC (2009) Genetic signature of rice domestication shown by a variety of genes. J Mol Evol 68(4):393–402PubMedCrossRefGoogle Scholar
  49. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125(4):749–760PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.State Key Laboratory of Pharmaceutical Biotechnology, School of Life SciencesNanjing UniversityNanjingChina
  2. 2.Department of BiologyNanjing UniversityNanjingChina

Personalised recommendations