Plant Molecular Biology

, Volume 59, Issue 1, pp 191–203 | Cite as

Transcription Factors in Rice: A Genome-wide Comparative Analysis between Monocots and Eudicots

  • Yuqing Xiong
  • Tieyan Liu
  • Chaoguang Tian
  • Shouhong Sun
  • Jiayang Li
  • Mingsheng Chen
Article

Abstract

It is not known how representative the Arabidopsis thaliana complement of transcription factors (TFs) is of other plants. The availability of rice (Oryza sativa) genome sequences makes possible a comparative analysis of TFs between monocots and eudicots, the two major monophyletic groups of angiosperms. Here, we identified 1611 TF genes that belong to 37 gene families in rice, comparable to the 1510 in Arabidopsis. Several gene subfamilies, but no families, were found to be lineage-specific. Phylogenetic analyses indicated that nearly half of the TF genes form clear orthologous pairs or groups, which were derived from 383 ancestral genes in the common ancestor of rice and Arabidopsis. Investigating gene duplication mechanisms revealed twelve pairs of large intragenomic duplicated blocks, which account for more than 40% of the rice genome. About 60% of the duplicated TF genes have been retained on duplicated segments. Functional conservation and diversification of TFs across monocot and eudicot lineages are discussed.

Key words

comparative genomics genome duplication TF 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

Supplemental Table1-4.doc (1.6 mb)
Supplemental Table1-4 (DOC 1.688 KB)
Supplemental Table 5.xls (442 kb)
Supplemental Table 5 (XLS 442 KB)
Supplemental Figures.doc (6.3 mb)
Supplemental Figures (DOC 6.405 KB)

References

  1. Ambrose, B.A., Lerner, D.R., Ciceri, P., Padilla, C.M., Yanofsky, M.F., Schmidt, R.J. 2000Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocotsMol. Cell5569579PubMedCrossRefGoogle Scholar
  2. Bateman, A., Birney, E., Durbin, R., Eddy, S.R., Howe, K.L., Sonnhammer, E.L. 2000The Pfam protein families databaseNucleic Acids Res28263266PubMedCrossRefGoogle Scholar
  3. Becker, A., Theissen, G. 2003The major clades of MADS-box genes and their role in the development and evolution of flowering plantsMol. Phylogenet. Evol.29464489PubMedCrossRefGoogle Scholar
  4. Benfey, P.N., Weigel, D. 2001Transcriptional networks controlling plant developmentPlant Physiol.125109111PubMedCrossRefGoogle Scholar
  5. Blanc, G., Hokamp, K., Wolfe, K.H. 2003A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genomeGenome Res.13137144PubMedCrossRefGoogle Scholar
  6. Bowman, J.L. 2000Axial patterning in leaves and other lateral organsCurr. Opin. Genet. Dev.10399404PubMedCrossRefGoogle Scholar
  7. Bowman, J.L., Eshed, Y., Baum, S.F. 2002Establishment of polarity in angiosperm lateral organsTrends Genet.18134141PubMedCrossRefGoogle Scholar
  8. Bowman, J.L., Smyth, D.R. 1999CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domainsDevelopment12623872396PubMedGoogle Scholar
  9. Chen, Q., Atkinson, A., Otsuga, D., Christensen, T., Reynolds, L., Drews, G.N. 1999The Arabidopsis FILAMENTOUS FLOWER gene is required for flower formationDevelopment12627152726PubMedGoogle Scholar
  10. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G., Thompson, J.D. 2003Multiple sequence alignment with the Clustal series of programsNucleic Acids Res.3134973500PubMedCrossRefGoogle Scholar
  11. Doebley, J., Stec, A., Hubbard, L. 1997The evolution of apical dominance in maizeNature386485488PubMedCrossRefGoogle Scholar
  12. Felsenstein, J. 1989. PHYLIP: phylogeny inference package. Cladistics S, pp. 164–166Google Scholar
  13. Feng, Q., Zhang, Y., Hao, P., Wang, S., Fu, G., Huang, Y., Li, Y., Zhu, J., Liu, Y., Hu, X., Jia, P., Zhao, Q., Ying, K., Yu, S., Tang, Y., Weng, Q., Zhang, L., Lu, Y., Mu, J., Zhang, L.S., Yu, Z., Fan, D., Liu, X., Lu, T., Li, C., Wu, Y., Sun, T., Lei, H., Li, T., Hu, H., Guan, J., Wu, M., Zhang, R., Zhou, B., Chen, Z., Chen, L., Jin, Z., Wang, R., Yin, H., Cai, Z., Ren, S., Lv, G., Gu, W., Zhu, G., Tu, Y., Jia, J., Chen, J., Kang, H., Chen, X., Shao, C., Sun, Y., Hu, Q., Zhang, X., Zhang, W., Wang, L., Ding, C., Sheng, H., Gu, J., Chen, S., Ni, L., Zhu, F., Chen, W., Lan, L., Lai, Y., Cheng, Z., Gu, M., Jiang, J., Li, J., Hong, G., Xue, Y., Han, B. 2002Sequence and analysis of rice chromosome 4Nature420316320PubMedCrossRefGoogle Scholar
  14. Galtier, N., Gouy, M., Gautier, C. 1996SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogenyComput. Appl. Biosci.12543548PubMedGoogle Scholar
  15. Goff, S.A., Ricke, D., Lan, T.H., Presting, G., Wang, R., Dunn, M., Glazebrook, J., Sessions, A., Oeller, P., Varma, H., Hadley, D., Hutchison, D., Martin, C., Katagiri, F., Lange, B.M., Moughamer, T., Xia, Y., Budworth, P., Zhong, J., Miguel, T., Paszkowski, U., Zhang, S., Colbert, M., Sun, W.L., Chen, L., Cooper, B., Park, S., Wood, T.C., Mao, L., Quail, P., Wing, R., Dean, R., Yu, Y., Zharkikh, A., Shen, R., Sahasrabudhe, S., Thomas, A., Cannings, R., Gutin, A., Pruss, D., Reid, J., Tavtigian, S., Mitchell, J., Eldredge, G., Scholl, T., Miller, R.M., Bhatnagar, S., Adey, N., Rubano, T., Tusneem, N., Robinson, R., Feldhaus, J., Macalma, T., Oliphant, A., Briggs, S. 2002A draft sequence of the rice genome (Oryza sativa L. ssp. japonica)Science29692100PubMedCrossRefGoogle Scholar
  16. Greb, T., Clarenz, O., Schafer, E., Muller, D., Herrero, R., Schmitz, G., Theres, K. 2003Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formationGenes Dev.1711751187PubMedCrossRefGoogle Scholar
  17. Griffiths, S., Dunford, R.P., Coupland, G., Laurie, D.A. 2003The evolution of CONSTANS-like gene families in barley, rice, and ArabidopsisPlant Physiol.13118551867PubMedCrossRefGoogle Scholar
  18. Heisler, M.G., Atkinson, A., Bylstra, Y.H., Walsh, R., Smyth, D.R. 2001SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH proteinDevelopment12810891098PubMedGoogle Scholar
  19. Ikeda, A., Ueguchi-Tanaka, M., Sonoda, Y., Kitano, H., Koshioka, M., Futsuhara, Y., Matsuoka, M., Yamaguchi, J. 2001Slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8Plant Cell139991010PubMedCrossRefGoogle Scholar
  20. In-depth view of structure, activity, and evolution of rice chromosome 10. 2003. Science 300: 1566–1569Google Scholar
  21. Jeong, D.H., An, S., Kang, H.G., Moon, S., Han, J.J., Park, S., Lee, H.S., An, K., An, G. 2002T-DNA insertional mutagenesis for activation tagging in ricePlant Physiol.13016361644PubMedCrossRefGoogle Scholar
  22. Juarez, M.T., Kui, J.S., Thomas, J., Heller, B.A., Timmermans, M.C. 2004MicroRNA-mediated repression of rolled leaf1 specifies maize leaf polarityNature4288488PubMedCrossRefGoogle Scholar
  23. Kerstetter, R.A., Bollman, K., Taylor, R.A., Bomblies, K., Poethig, R.S. 2001KANADI regulates organ polarity in ArabidopsisNature411706709PubMedCrossRefGoogle Scholar
  24. Kikuchi, S., Satoh, K., Nagata, T., Kawagashira, N., Doi, K., Kishimoto, N., Yazaki, J., Ishikawa, M., Yamada, H., Ooka, H., Hotta, I., Kojima, K., Namiki, T., Ohneda, E., Yahagi, W., Suzuki, K., Li, C.J., Ohtsuki, K., Shishiki, T., Otomo, Y., Murakami, K., Iida, Y., Sugano, S., Fujimura, T., Suzuki, Y., Tsunoda, Y., Kurosaki, T., Kodama, T., Masuda, H., Kobayashi, M., Xie, Q., Lu, M., Narikawa, R., Sugiyama, A., Mizuno, K., Yokomizo, S., Niikura, J., Ikeda, R., Ishibiki, J., Kawamata, M., Yoshimura, A., Miura, J., Kusumegi, T., Oka, M., Ryu, R., Ueda, M., Matsubara, K., Kawai, J., Carninci, P., Adachi, J., Aizawa, K., Arakawa, T., Fukuda, S., Hara, A., Hashizume, W., Hayatsu, N., Imotani, K., Ishii, Y., Itoh, M., Kagawa, I., Kondo, S., Konno, H., Miyazaki, A., Osato, N., Ota, Y., Saito, R., Sasaki, D., Sato, K., Shibata, K., Shinagawa, A., Shiraki, T., Yoshino, M., Hayashizaki, Y., Yasunishi, A. 2003Collection, mapping, and annotation of over 28,000 cDNA clones from japonica riceScience301376379PubMedCrossRefGoogle Scholar
  25. Kim, J.H., Choi, D., Kende, H. 2003The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in ArabidopsisPlant J.3694104PubMedCrossRefGoogle Scholar
  26. Kumar, S., Tamura, K., Jakobsen, I.B., Nei, M. 2001MEGA2: molecular evolutionary genetics analysis softwareBioinformatics1712441245PubMedCrossRefGoogle Scholar
  27. Leister, D. 2004Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance geneTrends Genet.20116122PubMedCrossRefGoogle Scholar
  28. Li, X., Qian, Q., Fu, Z., Wang, Y., Xiong, G., Zeng, D., Wang, X., Liu, X., Teng, S., Hiroshi, F., Yuan, M., Luo, D., Han, B., Li, J. 2003Control of tillering in riceNature422618621PubMedCrossRefGoogle Scholar
  29. Li, Z., Thomas, T.L. 1998PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in ArabidopsisPlant Cell10383398PubMedCrossRefGoogle Scholar
  30. McConnell, J.R., Emery, J., Eshed, Y., Bao, N., Bowman, J., Barton, M.K. 2001Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shootsNature411709713PubMedCrossRefGoogle Scholar
  31. McGinnis, W., Levine, M.S., Hafen, E., Kuroiwa, A., Gehring, W.J. 1984A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexesNature308428433PubMedCrossRefGoogle Scholar
  32. Mena, M., Ambrose, B.A., Meeley, R.B., Briggs, S.P., Yanofsky, M.F., Schmidt, R.J. 1996Diversification of C-function activity in maize flower developmentScience27415371540PubMedCrossRefGoogle Scholar
  33. Miyao, A., Tanaka, K., Murata, K., Sawaki, H., Takeda, S., Abe, K., Shinozuka, Y., Onosato, K., Hirochika, H. 2003Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genomePlant Cell1517711780PubMedCrossRefGoogle Scholar
  34. Moreno, M.A., Harper, L.C., Krueger, R.W., Dellaporta, S.L., Freeling, M. 1997liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesisGenes Dev11616628PubMedGoogle Scholar
  35. Nagasawa, N., Miyoshi, M., Sano, Y., Satoh, H., Hirano, H., Sakai, H., Nagato, Y. 2003SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in riceDevelopment130705718PubMedCrossRefGoogle Scholar
  36. Parenicova, L., Folter, S., Kieffer, M., Horner, D.S., Favalli, C., Busscher, J., Cook, H.E., Ingram, R.M., Kater, M.M., Davies, B., Angenent, G.C., Colombo, L. 2003Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS worldPlant Cell1515381551PubMedCrossRefGoogle Scholar
  37. Peng, J., Richards, D.E., Hartley, N.M., Murphy, G.P., Devos, K.M., Flintham, J.E., Beales, J., Fish, L.J., Worland, A.J., Pelica, F., Sudhakar, D., Christou, P., Snape, J.W., Gale, M.D., Harberd, N.P. 1999‘Green revolution’ genes encode mutant gibberellin response modulatorsNature400256261PubMedCrossRefGoogle Scholar
  38. Rajani, S., Sundaresan, V. 2001The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscenceCurr. Biol.1119141922PubMedCrossRefGoogle Scholar
  39. Riechmann, J.L., Heard, J., Martin, G., Reuber, L., Jiang, C., Keddie, J., Adam, L., Pineda, O., Ratcliffe, O.J., Samaha, R.R., Creelman, R., Pilgrim, M., Broun, P., Zhang, J.Z., Ghandehari, D., Sherman, B.K., Yu, G. 2000Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotesScience29021052110PubMedCrossRefGoogle Scholar
  40. Riechmann, J.L. 2002Meyerowitz CsaE,  eds. Transcriptional regulation: a genomic overviewAmerian Society of Plant BiologistsRockvilleGoogle Scholar
  41. Riechmann, J.L., Meyerowitz, E.M. 1997MADS domain proteins in plant developmentBiol. Chem.37810791101PubMedCrossRefGoogle Scholar
  42. Salamov, A.A., Solovyev, V.V. 2000Ab initio gene finding in Drosophila genomic DNAGenome Res.10516522PubMedCrossRefGoogle Scholar
  43. Sasaki, T., Matsumoto, T., Yamamoto, K., Sakata, K., Baba, T., Katayose, Y., Wu, J., Niimura, Y., Cheng, Z., Nagamura, Y., Antonio, B.A., Kanamori, H., Hosokawa, S., Masukawa, M., Arikawa, K., Chiden, Y., Hayashi, M., Okamoto, M., Ando, T., Aoki, H., Arita, K., Hamada, M., Harada, C., Hijishita, S., Honda, M., Ichikawa, Y., Idonuma, A., Iijima, M., Ikeda, M., Ikeno, M., Ito, S., Ito, T., Ito, Y., Iwabuchi, A., Kamiya, K., Karasawa, W., Katagiri, S., Kikuta, A., Kobayashi, N., Kono, I., Machita, K., Maehara, T., Mizuno, H., Mizubayashi, T., Mukai, Y., Nagasaki, H., Nakashima, M., Nakama, Y., Nakamichi, Y., Nakamura, M., Namiki, N., Negishi, M., Ohta, I., Ono, N., Saji, S., Sakai, K., Shibata, M., Shimokawa, T., Shomura, A., Song, J., Takazaki, Y., Terasawa, K., Tsuji, K., Waki, K., Yamagata, H., Yamane, H., Yoshiki, S., Yoshihara, R., Yukawa, K., Zhong, H., Iwama, H., Endo, T., Ito, H., Hahn, J.H., Kim, H.I., Eun, M.Y., Yano, M., Jiang, J., Gojobori, T. 2002The genome sequence and structure of rice chromosome 1Nature420312316PubMedCrossRefGoogle Scholar
  44. Sawa, S., Watanabe, K., Goto, K., Liu, Y.G., Shibata, D., Kanaya, E., Morita, E.H., Okada, K. 1999FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domainsGenes Dev.1310791088PubMedGoogle Scholar
  45. Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K., Beermann, A., Thumfahrt, J., Jurgens, G., Hulskamp, M. 2002TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in ArabidopsisEmbo. J.2150365046PubMedCrossRefGoogle Scholar
  46. Schiefelbein, J. 2003Cell-fate specification in the epidermis: a common patterning mechanism in the root and shootCurr. Opin. Plant Biol.67478PubMedCrossRefGoogle Scholar
  47. Schiefthaler, U., Balasubramanian, S., Sieber, P., Chevalier, D., Wisman, E., Schneitz, K. 1999Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thalianaProc. Natl. Acad. Sci. USA961166411669PubMedCrossRefGoogle Scholar
  48. Schumacher, K., Schmitt, T., Rossberg, M., Schmitz, G., Theres, K. 1999The lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein familyProc. Natl. Acad. Sci. USA96290295PubMedCrossRefGoogle Scholar
  49. Scott, M.P., Weiner, A.J. 1984Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of DrosophilaProc. Natl. Acad. Sci. USA8141154119PubMedCrossRefGoogle Scholar
  50. Soltis, P.S., Soltis, D.E., Chase, M.W. 1999Angiosperm phylogeny inferred from multiple genes as a tool for comparative biologyNature402402404PubMedCrossRefGoogle Scholar
  51. Soltis, P.S., Soltis, D.E., Savolainen, V., Crane, P.R., Barraclough, T.G. 2002Rate heterogeneity among lineages of tracheophytes: integration of molecular and fossil data and evidence for molecular living fossilsProc. Natl. Acad. Sci. USA9944304435PubMedCrossRefGoogle Scholar
  52. Suzuki, M., Kao, C.Y., Cocciolone, S., McCarty, D.R. 2001Maize VP1 complements Arabidopsis abi3 and confers a novel ABA/auxin interaction in rootsPlant J.28409418PubMedCrossRefGoogle Scholar
  53. Takatsuji, H. 1998Zinc-finger transcription factors in plantsCell Mol. Life Sci.54582596PubMedCrossRefGoogle Scholar
  54. Talbert, P.B., Adler, H.T., Parks, D.W., Comai, L. 1995The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thalianaDevelopment12127232735PubMedGoogle Scholar
  55. Theissen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J.T., Munster, T., Winter, K.U., Saedler, H. 2000A short history of MADS-box genes in plantsPlant Mol. Biol.42115149PubMedCrossRefGoogle Scholar
  56. Theodoris, G., Inada, N., Freeling, M. 2003Conservation and molecular dissection of ROUGH SHEATH2 and ASYMMETRIC LEAVES1 function in leaf developmentProc. Natl. Acad. Sci. USA10068376842PubMedCrossRefGoogle Scholar
  57. Tian, C., Wan, P., Sun, S., Li, J., Chen, M. 2004Genome-wide analysis of the GRAS gene family in rice and ArabidopsisPlant Mol. Biol.54519532PubMedCrossRefGoogle Scholar
  58. Tian, C., Xiong, Y., Liu, T., Sun, S., Chen., L. and Chen, M. 2005. Evidence for an ancient whole-genome duplication event in rice and other cereals. Acta Genetica Sinica (in press)Google Scholar
  59. Toledo-Ortiz, G., Huq, E., Quail, P.H. 2003The Arabidopsis basic/helix-loop-helix transcription factor familyPlant Cell1517491770PubMedCrossRefGoogle Scholar
  60. Vandenbussche, M., Zethof, J., Royaert, S., Weterings, K., Gerats, T. 2004The duplicated B-class heterodimer model: whorl-specific effects and complex genetic interactions in Petunia hybrida flower developmentPlant Cell16741754PubMedCrossRefGoogle Scholar
  61. Wada, T., Tachibana, T., Shimura, Y., Okada, K. 1997Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPCScience27711131116PubMedCrossRefGoogle Scholar
  62. Wang, R.L., Stec, A., Hey, J., Lukens, L., Doebley, J. 1999The limits of selection during maize domesticationNature398236239PubMedCrossRefGoogle Scholar
  63. Wikstrom, N., Savolainen, V., Chase, M.W. 2001Evolution of the angiosperms: calibrating the family treeProc. R. Soc. Lond. B. Biol. Sci.26822112220CrossRefGoogle Scholar
  64. Wolfe, K.H., Gouy, M., Yang, Y.W., Sharp, P.M., Li, W.H. 1989Date of the monocot-dicot divergence estimated from chloroplast DNA sequence dataProc. Natl. Acad. Sci. USA8662016205PubMedCrossRefGoogle Scholar
  65. Yamaguchi, T., Nagasawa, N., Kawasaki, S., Matsuoka, M., Nagato, Y., Hirano, H.Y. 2004The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativaPlant Cell16500509PubMedCrossRefGoogle Scholar
  66. Yang, W.C., Ye, D., Xu, J., Sundaresan, V. 1999The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear proteinGenes Dev.1321082117PubMedGoogle Scholar
  67. Yu, J., Hu, S., Wang, J., Wong, G.K., Li, S., Liu, B., Deng, Y., Dai, L., Zhou, Y., Zhang, X., Cao, M., Liu, J., Sun, J., Tang, J., Chen, Y., Huang, X., Lin, W., Ye, C., Tong, W., Cong, L., Geng, J., Han, Y., Li, L., Li, W., Hu, G., Li, J., Liu, Z., Qi, Q., Li, T., Wang, X., Lu, H., Wu, T., Zhu, M., Ni, P., Han, H., Dong, W., Ren, X., Feng, X., Cui, P., Li, X., Wang, H., Xu, X., Zhai, W., Xu, Z., Zhang, J., He, S., Xu, J., Zhang, K., Zheng, X., Dong, J., Zeng, W., Tao, L., Ye, J., Tan, J., Chen, X., He, J., Liu, D., Tian, W., Tian, C., Xia, H., Bao, Q., Li, G., Gao, H., Cao, T., Zhao, W., Li, P., Chen, W., Zhang, Y., Hu, J., Liu, S., Yang, J., Zhang, G., Xiong, Y., Li, Z., Mao, L., Zhou, C., Zhu, Z., Chen, R., Hao, B., Zheng, W., Chen, S., Guo, W., Tao, M., Zhu, L., Yuan, L., Yang, H. 2002A draft sequence of the rice genome (Oryza sativa L. ssp. indica)Science2967992PubMedCrossRefGoogle Scholar
  68. Yuan, Q., Ouyang, S., Liu, J., Suh, B., Cheung, F., Sultana, R., Lee, D., Quackenbush, J., Buell, C.R. 2003The TIGR rice genome annotation resource: annotating the rice genome and creating resources for plant biologistsNucleic Acids Res.31229233PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Yuqing Xiong
    • 1
  • Tieyan Liu
    • 1
  • Chaoguang Tian
    • 1
  • Shouhong Sun
    • 1
  • Jiayang Li
    • 1
  • Mingsheng Chen
    • 1
  1. 1.Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingChina

Personalised recommendations