title: Global expression differences and tissue specific expression differences in rice evolution result in two contrasting types of differentially expressed genes.
abstract: BACKGROUND
  Since the development of transcriptome analysis systems, many expression evolution studies characterized evolutionary forces acting on gene expression, without explicit discrimination between global expression differences and tissue specific expression differences. However, different types of gene expression alteration should have different effects on an organism, the evolutionary forces that act on them might be different, and different types of genes might show different types of differential expression between species. To confirm this, we studied differentially expressed (DE) genes among closely related groups that have extensive gene expression atlases, and clarified characteristics of different types of DE genes including the identification of regulating loci for differential expression using expression quantitative loci (eQTL) analysis data.
  
  
  RESULTS
  We detected differentially expressed (DE) genes between rice subspecies in five homologous tissues that were verified using japonica and indica transcriptome atlases in public databases. Using the transcriptome atlases, we classified DE genes into two types, global DE genes and changed-tissues DE genes. Global type DE genes were not expressed in any tissues in the atlas of one subspecies, however changed-tissues type DE genes were expressed in both subspecies with different tissue specificity. For the five tissues in the two japonica-indica combinations, 4.6 ± 0.8 and 5.9 ± 1.5 % of highly expressed genes were global and changed-tissues DE genes, respectively. Changed-tissues DE genes varied in number between tissues, increasing linearly with the abundance of tissue specifically expressed genes in the tissue. Molecular evolution of global DE genes was rapid, unlike that of changed-tissues DE genes. Based on gene ontology, global and changed-tissues DE genes were different, having no common GO terms. Expression differences of most global DE genes were regulated by cis-eQTLs. Expression evolution of changed-tissues DE genes was rapid in tissue specifically expressed genes and those rapidly evolved changed-tissues DE genes were regulated not by cis-eQTLs, but by complicated trans-eQTLs.
  
  
  CONCLUSIONS
  Global DE genes and changed-tissues DE genes had contrasting characteristics. The two contrasting types of DE genes provide possible explanations for the previous controversial conclusions about the relationships between molecular evolution and expression evolution of genes in different species, and the relationship between expression breadth and expression conservation in evolution.
authors.affiliation: Plant Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, 411-8540, Japan. yhoriuch@nig.ac.jp.|Transdisciplinary Research Integration Center, Research Organization of Information and Systems, Hulic Kamiyacho 2 F, 4-3-13 Toranomon, Minatoku, Tokyo, 105-0001, Japan. yhoriuch@nig.ac.jp.
authors.forename: Youko
authors.initials: Y
authors.lastname: Horiuchi
authors.affiliation: Plant Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, 411-8540, Japan. yharushi@nig.ac.jp.|Transdisciplinary Research Integration Center, Research Organization of Information and Systems, Hulic Kamiyacho 2 F, 4-3-13 Toranomon, Minatoku, Tokyo, 105-0001, Japan. yharushi@nig.ac.jp.
authors.forename: Yoshiaki
authors.initials: Y
authors.lastname: Harushima
authors.affiliation: Department of Mathematical Analysis and Statistical Inference, The Institute of Statistical Mathematics, 10-3 Midori-cho, Tachikawa, Tokyo, 190-8562, Japan. fujisawa@ism.ac.jp.|SOKENDAI (The Graduate University for Advanced Studies), 1560-35 Kamiyamaguchi, Hayama, Miura District, Kanagawa Prefecture, 240-0115, Japan. fujisawa@ism.ac.jp.
authors.forename: Hironori
authors.initials: H
authors.lastname: Fujisawa
authors.affiliation: Plant Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, 411-8540, Japan. tm@nig.ac.jp.|Present address: Genome Informatics Laboratory, Center for Information Biology, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, 411-8540, Japan. tm@nig.ac.jp.
authors.forename: Takako
authors.initials: T
authors.lastname: Mochizuki
authors.affiliation: Plant Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, 411-8540, Japan. masfujit@nig.ac.jp.
authors.forename: Masahiro
authors.initials: M
authors.lastname: Fujita
authors.affiliation: Plant Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, 411-8540, Japan. hajime.ohyanagi@kaust.edu.sa.|Mitsubishi Space Software Co Ltd, Tsukuba Mitsui Building 14 F, 1-6-1 Takezono, Tsukuba, Ibaraki, 305-0032, Japan. hajime.ohyanagi@kaust.edu.sa.|Present address: Computational Bioscience Research Center, King Abdullah University of Science and Technology, 4700 KAUST, Thuwal, 23955-6900, Kingdom of Saudi Arabia. hajime.ohyanagi@kaust.edu.sa.
authors.forename: Hajime
authors.initials: H
authors.lastname: Ohyanagi
authors.affiliation: Plant Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Yata 1111, Mishima, Shizuoka, 411-8540, Japan. nkurata@nig.ac.jp.|SOKENDAI (The Graduate University for Advanced Studies), 1560-35 Kamiyamaguchi, Hayama, Miura District, Kanagawa Prefecture, 240-0115, Japan. nkurata@nig.ac.jp.
authors.forename: Nori
authors.initials: N
authors.lastname: Kurata
mesh_terms: D030541:Databases, Genetic; D019143:Evolution, Molecular; D020869:Gene Expression Profiling / Q000379:methods*; D018506:Gene Expression Regulation, Plant; D063990:Gene Ontology; D017343:Genes, Plant; D009928:Organ Specificity; D012275:Oryza / Q000145:classification / Q000235:genetics*; D040641:Quantitative Trait Loci