期刊论文详细信息
BMC Genetics
Heterogeneous evolutionary rates of Pi2/9 homologs in rice
Sihai Yang1  Xiaohui Zhang1  Changjiang Guo1  Ting Xu1  Kejing Wu1 
[1] State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, 210093, China
关键词: Gene conversion;    Positive selection;    Copy number variation;    Nucleotide diversity;    Type I and Type II R-genes;    Pi2/9;   
Others  :  1121378
DOI  :  10.1186/1471-2156-13-73
 received in 2012-03-11, accepted in 2012-08-16,  发布年份 2012
PDF
【 摘 要 】

Background

The Pi2/9 locus contains multiple nucleotide binding site–leucine-rich repeat (NBS-LRR) genes in the rice genome. Although three functional R-genes have been cloned from this locus, little is known about the origin and evolutionary history of these genes. Herein, an extensive genome-wide survey of Pi2/9 homologs in rice, sorghum, Brachypodium and Arabidopsis, was conducted to explore this theme.

Results

In our study, 1, 1, 5 and 156 Pi2/9 homologs were detected in Arabidopsis, Brachypodium, sorghum and rice genomes, respectively. Two distinct evolutionary patterns of Pi2/9 homologs, Type I and Type II, were observed in rice lines. Type I Pi2/9 homologs showed evidence of rapid gene diversification, including substantial copy number variations, obscured orthologous relationships, high levels of nucleotide diversity or/and divergence, frequent sequence exchanges and strong positive selection, whereas Type II Pi2/9 homologs exhibited a fairly slow evolutionary rate. Interestingly, the three cloned R-genes from the Pi2/9 locus all belonged to the Type I genes.

Conclusions

Our data show that the Pi2/9 locus had an ancient origin predating the common ancestor of gramineous species. The existence of two types of Pi2/9 homologs suggest that diversifying evolution should be an important strategy of rice to cope with different types of pathogens. The relationship of cloned Pi2/9 genes and Type I genes also suggests that rapid gene diversification might facilitate rice to adapt quickly to the changing spectrum of the fungal pathogen M. grisea. Based on these criteria, other potential candidate genes that might confer novel resistance specificities to rice blast could be predicted.

【 授权许可】

   
2012 Wu et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150212013559268.pdf 1236KB PDF download
Figure 3. 30KB Image download
Figure 2. 47KB Image download
Figure 1. 95KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】
  • [1]Chisholm ST, Coaker G, Day B, Staskawicz BJ: Host-microbe interactions: shaping the evolution of the plant immune response. Cell 2006, 124:803-814.
  • [2]Jones JDG, Dangl JL: The plant immune system. Nature 2006, 444:323-329.
  • [3]Yue JX, Meyers BC, Chen JQ, Tian D, Yang S: Tracing the origin and evolutionary history of plant nucleotide-binding site–leucine-rich repeat (NBS-LRR) genes. New Phytol 2012, 193:1049-1063.
  • [4]Chen X, Ronald PC: Innate immunity in rice. Trends Plant Sci 2011, 16:451-459.
  • [5]Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW: Genome-wide analysis of NBS-LRR–encoding genes in Arabidopsis. Plant Cell 2003, 15:809-834.
  • [6]McHale L, Tan X, Koehl P, Michelmore RW: Plant NBS-LRR proteins: adaptable guards. Genome Biol 2006, 7:212.
  • [7]Li J, Ding J, Zhang W, Zhang Y, Tang P, Chen JQ, Tian D, Yang S: Unique evolutionary pattern of numbers of gramineous NBS–LRR genes. Mol Genet Genomics 2010, 283:427-438.
  • [8]Zhang XH, Feng Y, Cheng H, Tian DC, Yang SH, Chen JQ: Relative evolutionary rates of NBS-encoding genes revealed by soybean segmental duplication. Mol Genet Genomics 2011, 285:79-90.
  • [9]Hulbert SH, Webb CA, Smith SM, Sun Q: Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 2001, 39:285-312.
  • [10]Yang S, Gu T, Pan C, Feng Z, Ding J, Hang Y, Chen JQ, Tian D: Genetic variation of NBS-LRR class resistance genes in rice lines. Theor Appl Genet 2008, 116:165-177.
  • [11]Hulbert SH: Structure and evolution of the rp1 complex conferring rust resistance in maize. Annu Rev Phytopathol 1997, 35:293-310.
  • [12]Chen Q, Han Z, Jiang H, Tian D, Yang S: Strong positive selection drives rapid diversification of R-genes in Arabidopsis relatives. J Mol Evol 2010, 70:137-148.
  • [13]Kuang H, Caldwell KS, Meyers BC, Michelmore RW: Frequent sequence exchanges between homologs of RPP8 in Arabidopsis are not necessarily associated with genomic proximity. Plant J 2008, 54:69-80.
  • [14]Kuang H, Woo SS, Meyers BC, Nevo E, Michelmore RW: Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 2004, 16:2870-2894.
  • [15]Dai LY, Liu XL, Xiao YH, Wang GL: Recent advances in cloning and characterization of disease resistance genes in rice. J Integ Plant Biol 2007, 49:112-119.
  • [16]Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K, Hayashi N, Takahashi A, Hirochika H, Okuno K: Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 2009, 325:998.
  • [17]Shang JJ, Tao Y, Chen XW, Zou Y, Lei CL, Wang J, Li XB, Zhao XF, Zhang MJ, Lu ZK, et al.: Identification of a New Rice Blast Resistance Gene, Pid3, by Genome wide Comparison of Paired Nucleotide-Binding Site-Leucine-Rich Repeat Genes and Their Pseudogene Alleles Between the Two Sequenced Rice Genomes. Genetics 2009, 182:1303-1311.
  • [18]Qu SH, Liu GF, Zhou B, Bellizzi M, Zeng LR, Dai LY, Han B, Wang GL: The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice. Genetics 2006, 172:1901-1914.
  • [19]Zhou B, Qu SH, Liu GF, Dolan M, Sakai H, Lu GD, Bellizzi M, Wang GL: The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea. Mol Plant Microbe In 2006, 19:1216-1228.
  • [20]Dai LY, Wu J, Li XB, Wang XJ, Liu XL, Jantasuriyarat C, Kudrna D, Yu Y, Wing RA, Han B, et al.: Genomic structure and evolution of the Pi2/9 locus in wild rice species. Theor Appl Genet 2010, 121:295-309.
  • [21]Yang S, Feng Z, Zhang X, Jiang K, Jin X, Hang Y, Chen JQ, Tian D: Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol Biol 2006, 62:181-193.
  • [22]Bergelson J, Kreitman M, Stahl EA, Tian D: Evolutionary dynamics of plant R-genes. Science 2001, 292:2281.
  • [23]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 mega bases. Plant Cell 1998, 10:1817-1832.
  • [24]Zhu Q, Ge S: Phylogenetic relationships among A‐genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytol 2005, 167:249-265.
  • [25]Watterson G: On the number of segregating sites in genetical models without recombination. Theor Popul Biol 1975, 7:256-276.
  • [26]Martin GB, Bogdanove AJ, Sessa G: Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 2003, 54:23-61.
  • [27]Kuang H, Woo SS, Meyers BC, Nevo E, Michelmore RW: Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 2004, 16:2870-2894.
  • [28]Riely BK, Martin GB: Ancient origin of pathogen recognition specificity conferred by the tomato disease resistance gene Pto. Proc Natl Acad Sci USA 2059, 2001:98.
  • [29]Wei F, Wing RA, Wise RP: Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell 2002, 14:1903-1917.
  • [30]Michelmore RW, Meyers BC: Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 1998, 8:1113-1130.
  • [31]Tian D, Traw M, Chen J, Kreitman M, Bergelson J: Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 2003, 423:74-77.
  • [32]Rose LE, Bittner-Eddy PD, Langley CH, Holub EB, Michelmore RW, Beynon JL: The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 2004, 166:1517.
  • [33]Noël L, Moores TL, van der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JDG: Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 1999, 11:2099-2112.
  • [34]Ellis JG, Lawrence GJ, Luck JE, Dodds PN: Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 1999, 11:495-506.
  • [35]Ding J, Zhang W, Jing Z, Chen JQ, Tian D: Unique pattern of R-gene variation within populations in Arabidopsis. Mol Genet Genomics 2007, 277:619-629.
  • [36]Jiang H, Wang C, Ping L, Tian D, Yang S: Pattern of LRR nucleotide variation in plant resistance genes. Plant Sci 2007, 173:253-261.
  • [37]Zhang Y, Wang J, Zhang X, Chen JQ, Tian D, Yang S: Genetic signature of rice domestication shown by a variety of genes. J Mol Evol 2009, 68:393-402.
  • [38]Wulff BBH, Thomas CM, Smoker M, Grant M, Jones JDG: Domain swapping and gene shuffling identify sequences required for induction of an Avr-dependent hypersensitive response by the tomato Cf-4 and Cf-9 proteins. Plant Cell 2001, 13:255-272.
  • [39]Rairdan GJ, Moffett P: Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell 2006, 18:2082-2093.
  • [40]The International Rice Genome Sequencing Project. [http://rgp.dna.affrc.go.jp/E/IRGSP/download.html]
  • [41]Matsumoto T, Wu J, Kanamori H, Katayose Y, Fujisawa M, Namiki N, Mizuno H, Yamamoto K, Antonio BA, Baba T: The map-based sequence of the rice genome. Nature 2005, 436:793-800.
  • [42]Yu J, Hu S, Wang J, Wong GKS, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X: A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 2002, 296:79.
  • [43]Yu J, Wong GKS, Liu S, Wang J, Yang H: A comprehensive crop genome research project: the Super hybrid Rice Genome Project in China. Philos T R Soc B 2007, 362:1023-1034.
  • [44]The Beijing Genomics Institute. http://rise2.genomics.org.cn/page/rice/index.jsp
  • [45]The National Center for Genome Resources. [NCGR; http://www.ncgr.ac.cn/scientific_data.asp]
  • [46]Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z: Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 2010, 42:961-967.
  • [47]Ammiraju JSS, Luo M, Goicoechea JL, Wang W, Kudrna D, Mueller C, Talag J, Kim HR, Sisneros NB, Blackmon B: The Oryza bacterial artificial chromosome library resource: construction and analysis of 12 deep-coverage large-insert BAC libraries that represent the 10 genome types of the genus Oryza. Genome Res 2006, 16:140-147.
  • [48]The Oryza bacterial artificial chromosome library resource. http://blast.ncbi.nlm.nih.gov/Blast.cgi?PAGE=Nucleotides&PROGRAM=blastn&BLAST_SPEC=TraceArchive&BLAST_PROGRAMS=megaBlast&PAGE_TYPE=BlastSearch
  • [49]Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A: The Sorghum bicolor genome and the diversification of grasses. Nature 2009, 457:551-556.
  • [50]Vogel JP, Garvin DF, Mockler TC, Schmutz J, Rokhsar D, Bevan MW, Barry K, Lucas S, Harmon-Smith M, Lail K: Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 2010, 463:763-768.
  • [51]The Joint Genome Institute. http://genome.jgi-psf.org/Sorbi1/Sorbi1.home.html
  • [52]The Brachypodium distachyon database. http://www.brachypodium.org
  • [53]The_Arabidopsis_Genome_Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408:796-815.
  • [54]Peng SQ, Huang FY, Sun GC, Liu EM, Sun YJ, Ai RX, Zhao JX, Bai SZ, Xiao FH: Studies on Durable Resistance to Blast Disease in Different Latitudes for Rice. Sci Agric Sin 1996, 29:52-28.
  • [55]Yu Z, Mackill D, Bonman J, Tanksley S: Tagging genes for blast resistance in rice via linkage to RFLP markers. Theor Appl Genet 1991, 81:471-476.
  • [56]Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D: Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genomics 2004, 271:402-415.
  • [57]Pfam. http://pfam.janelia.org
  • [58]SMART. http://smart.embl-heidelberg.d
  • [59]SHORE. http://sourceforge.net/projects/shore/files
  • [60]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
  • [61]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
  • [62]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
  • [63]Ellis J, Dodds P, Pryor T: Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 2000, 3:278-284.
  • [64]Data monkey. http://www.datamankey.org
  • [65]Pond SL, Frost SD, Muse SV: HyPhy: hypothesis testing using phylogenies. Bioinformatics 2005, 21:676-679.
  • [66]Pond SLK, Posada D, Gravenor MB, Woelk CH, Frost SDW: Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 2006, 23:1891-1901.
  • [67]Lynch M, Crease T: The analysis of population survey data on DNA sequence variation. Mol Biol Evol 1990, 7:377-394.
  • [68]GENECONV1.81. http://www.math.wustl.edu/sawyer/geneconv
  • [69]Weir B, Hill W: Estimating F-statistics. Annu Rev Genet. 2002, 36:721-750.
  • [70]The ARLEQUIN version 3.11. http://www.lgb.unige.ch/arequin
  • [71]Hudson RR: A new statistic for detecting genetic differentiation. Genetics 2011, 2000:155.
  文献评价指标  
  下载次数:11次 浏览次数:7次