Massive Gene Losses in Asian Cultivated Rice Unveiled by Comparative Genome Analysis

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2010 Feb 20

PMID 20167122

Citations 20

Authors

Hiroaki Sakai

Takeshi Itoh

Affiliations

Soon will be listed here.

Abstract

Background: Rice is one of the most important food crops in the world. With increasing world demand for food crops, there is an urgent need to develop new cultivars that have enhanced performance with regard to yield, disease resistance, and so on. Wild rice is expected to provide useful genetic resources that could improve the present cultivated species. However, the quantity and quality of these unexplored resources remain unclear. Recent accumulation of the genomic information of both cultivated and wild rice species allows for their comparison at the molecular level. Here, we compared the genome sequence of Oryza sativa ssp. japonica with sets of bacterial artificial chromosome end sequences (BESs) from two wild rice species, O. rufipogon and O. nivara, and an African rice species, O. glaberrima.

Results: We found that about four to five percent of the BESs of the two wild rice species and about seven percent of the African rice could not be mapped to the japonica genome, suggesting that a substantial number of genes have been lost in the japonica rice lineage; however, their close relatives still possess their counterpart genes. We estimated that during evolution, O. sativa has lost at least one thousand genes that are still preserved in the genomes of the other species. In addition, our BLASTX searches against the non-redundant protein sequence database showed that disease resistance-related proteins were significantly overrepresented in the close relative-specific genomic portions. In total, 235 unmapped BESs of the three relatives matched 83 non-redundant proteins that contained a disease resistance protein domain, most of which corresponded to an NBS-LRR domain.

Conclusion: We found that the O. sativa lineage appears to have recently experienced massive gene losses following divergence from its wild ancestor. Our results imply that the domestication process accelerated large-scale genomic deletions in the lineage of Asian cultivated rice and that the close relatives of cultivated rice have the potential to restore the lost traits.

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References

Leister D . Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet. 2004; 20(3):116-22. DOI: 10.1016/j.tig.2004.01.007. View

Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R . InterProScan: protein domains identifier. Nucleic Acids Res. 2005; 33(Web Server issue):W116-20. PMC: 1160203. DOI: 10.1093/nar/gki442. View

Gale M, Devos K . Plant comparative genetics after 10 years. Science. 1998; 282(5389):656-9. DOI: 10.1126/science.282.5389.656. View

Khush G . Origin, dispersal, cultivation and variation of rice. Plant Mol Biol. 1997; 35(1-2):25-34. View

Tian D, Traw M, Chen J, Kreitman M, Bergelson J . Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature. 2003; 423(6935):74-7. DOI: 10.1038/nature01588. View

Nei M, Rooney A . Concerted and birth-and-death evolution of multigene families. Annu Rev Genet. 2005; 39:121-52. PMC: 1464479. DOI: 10.1146/annurev.genet.39.073003.112240. View

Shang J, Tao Y, Chen X, Zou Y, Lei C, Wang J . Identification of a new rice blast resistance gene, Pid3, by genomewide comparison of paired nucleotide-binding site--leucine-rich repeat genes and their pseudogene alleles between the two sequenced rice genomes. Genetics. 2009; 182(4):1303-11. PMC: 2728867. DOI: 10.1534/genetics.109.102871. View

Itoh T, Takemoto K, Mori H, Gojobori T . Evolutionary instability of operon structures disclosed by sequence comparisons of complete microbial genomes. Mol Biol Evol. 1999; 16(3):332-46. DOI: 10.1093/oxfordjournals.molbev.a026114. View

Wang Z, Yano M, Yamanouchi U, Iwamoto M, Monna L, Hayasaka H . The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J. 1999; 19(1):55-64. DOI: 10.1046/j.1365-313x.1999.00498.x. View

10.

Khush G . Challenges for meeting the global food and nutrient needs in the new millennium. Proc Nutr Soc. 2001; 60(1):15-26. DOI: 10.1079/pns200075. View

11.

Lu T, Yu S, Fan D, Mu J, Shangguan Y, Wang Z . Collection and comparative analysis of 1888 full-length cDNAs from wild rice Oryza rufipogon Griff. W1943. DNA Res. 2008; 15(5):285-95. PMC: 2575888. DOI: 10.1093/dnares/dsn018. View

12.

Tian F, Li D, Fu Q, Zhu Z, Fu Y, Wang X . Construction of introgression lines carrying wild rice (Oryza rufipogon Griff.) segments in cultivated rice (Oryza sativa L.) background and characterization of introgressed segments associated with yield-related traits. Theor Appl Genet. 2005; 112(3):570-80. DOI: 10.1007/s00122-005-0165-2. View

13.

Roze D, Lenormand T . Self-fertilization and the evolution of recombination. Genetics. 2005; 170(2):841-57. PMC: 1450426. DOI: 10.1534/genetics.104.036384. View

14.

Chin D, Arroyo-Garcia R, Ochoa O, Kesseli R, Lavelle D, Michelmore R . Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). Genetics. 2001; 157(2):831-49. PMC: 1461523. DOI: 10.1093/genetics/157.2.831. View

15.

Matsuya A, Sakate R, Kawahara Y, Koyanagi K, Sato Y, Fujii Y . Evola: Ortholog database of all human genes in H-InvDB with manual curation of phylogenetic trees. Nucleic Acids Res. 2007; 36(Database issue):D787-92. PMC: 2238928. DOI: 10.1093/nar/gkm878. View

16.

Ma J, Bennetzen J . Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A. 2004; 101(34):12404-10. PMC: 515075. DOI: 10.1073/pnas.0403715101. View

17.

Mullins M, Hilu W . Sequence variation in the gene encoding the 10-kDa prolamin in Oryza (Poaceae). I. Phylogenetic Implications. Theor Appl Genet. 2003; 105(6-7):841-846. DOI: 10.1007/s00122-002-1056-4. View

18.

Caicedo A, Williamson S, Hernandez R, Boyko A, Fledel-Alon A, York T . Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet. 2007; 3(9):1745-56. PMC: 1994709. DOI: 10.1371/journal.pgen.0030163. View

19.

Itoh T, Tanaka T, Barrero R, Yamasaki C, Fujii Y, Hilton P . Curated genome annotation of Oryza sativa ssp. japonica and comparative genome analysis with Arabidopsis thaliana. Genome Res. 2007; 17(2):175-83. PMC: 1781349. DOI: 10.1101/gr.5509507. View

20.

Eichler E, Sankoff D . Structural dynamics of eukaryotic chromosome evolution. Science. 2003; 301(5634):793-7. DOI: 10.1126/science.1086132. View