Transcriptome dynamics of developing maize leaves and genomewide prediction of cis elements and their cognate transcription factors

Chun-Ping Yu, Chun-Chang Chen, Yao-Ming Chang, Wen-Yu Liu, Hsin-Hung Lin, Jinn-Jy Lin, Hsiang-June Chen, Yu-Ju Lu, Yi-Hsuan Wu, Mei-Yeh-Jade Lu, Chen-Hua Lu, Arthur-Chun-Chieh Shih, Maurice-Sun-Ben Ku, Shin-Han Shiu, Shu-Hsing Wu, Wen-Hsiung Li

Research output: Contribution to journalArticle

26 Citations (Scopus)

Abstract

Maize is a major crop and a model plant for studying C4 photosynthesis and leaf development. However, a genomewide regulatory network of leaf development is not yet available. This knowledge is useful for developing C3 crops to perform C4 photosynthesis for enhanced yields. Here, using 22 transcriptomes of developing maize leaves from dry seeds to 192 h post imbibition, we studied gene up- and down-regulation and functional transition during leaf development and inferred sets of strongly coexpressed genes. More significantly, we developed a method to predict transcription factor binding sites (TFBSs) and their cognate transcription factors (TFs) using genomic sequence and transcriptomic data. The method requires not only evolutionary conservation of candidate TFBSs and sets of strongly coexpressed genes but also that the genes in a gene set share the same Gene Ontology term so that they are involved in the same biological function. In addition, we developed another method to predict maize TF-TFBS pairs using known TF-TFBS pairs in Arabidopsis or rice. From these efforts, we predicted 1,340 novel TFBSs and 253 new TF-TFBS pairs in the maize genome, far exceeding the 30 TF-TFBS pairs currently known in maize. In most cases studied by both methods, the two methods gave similar predictions. In vitro tests of 12 predicted TF-TFBS interactions showed that our methods perform well. Our study has significantly expanded our knowledge on the regulatory network involved in maize leaf development.
Original languageEnglish
Pages (from-to)E2477-E2486
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number19
DOIs
Publication statusPublished - 2015
Externally publishedYes

Fingerprint

transcriptome
transcription factors
prediction
corn
binding sites
leaves
leaf development
C4 photosynthesis
genes
methodology
imbibition
crops
transcriptomics
Arabidopsis

Keywords

  • Cis binding site
  • Coexpressed genes
  • Maize transcriptomes
  • transcription factor
  • transcriptome
  • Arabidopsis
  • Article
  • binding site
  • controlled study
  • down regulation
  • gene expression
  • gene ontology
  • gene sequence
  • genetic conservation
  • genetic transcription
  • germination
  • in vitro study
  • leaf development
  • maize
  • molecular dynamics
  • multigene family
  • nonhuman
  • plant gene
  • plant leaf
  • plant seed
  • prediction
  • priority journal
  • rice
  • upregulation
  • Zea mays

Cite this

Transcriptome dynamics of developing maize leaves and genomewide prediction of cis elements and their cognate transcription factors. / Yu, Chun-Ping; Chen, Chun-Chang; Chang, Yao-Ming; Liu, Wen-Yu; Lin, Hsin-Hung; Lin, Jinn-Jy; Chen, Hsiang-June; Lu, Yu-Ju; Wu, Yi-Hsuan; Lu, Mei-Yeh-Jade; Lu, Chen-Hua; Shih, Arthur-Chun-Chieh; Ku, Maurice-Sun-Ben; Shiu, Shin-Han; Wu, Shu-Hsing; Li, Wen-Hsiung.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 19, 2015, p. E2477-E2486.

Research output: Contribution to journalArticle

Yu, C-P, Chen, C-C, Chang, Y-M, Liu, W-Y, Lin, H-H, Lin, J-J, Chen, H-J, Lu, Y-J, Wu, Y-H, Lu, M-Y-J, Lu, C-H, Shih, A-C-C, Ku, M-S-B, Shiu, S-H, Wu, S-H & Li, W-H 2015, 'Transcriptome dynamics of developing maize leaves and genomewide prediction of cis elements and their cognate transcription factors', Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 19, pp. E2477-E2486. https://doi.org/10.1073/pnas.1500605112
Yu, Chun-Ping ; Chen, Chun-Chang ; Chang, Yao-Ming ; Liu, Wen-Yu ; Lin, Hsin-Hung ; Lin, Jinn-Jy ; Chen, Hsiang-June ; Lu, Yu-Ju ; Wu, Yi-Hsuan ; Lu, Mei-Yeh-Jade ; Lu, Chen-Hua ; Shih, Arthur-Chun-Chieh ; Ku, Maurice-Sun-Ben ; Shiu, Shin-Han ; Wu, Shu-Hsing ; Li, Wen-Hsiung. / Transcriptome dynamics of developing maize leaves and genomewide prediction of cis elements and their cognate transcription factors. In: Proceedings of the National Academy of Sciences of the United States of America. 2015 ; Vol. 112, No. 19. pp. E2477-E2486.
@article{636a74323b794ac8911806d37739016f,
title = "Transcriptome dynamics of developing maize leaves and genomewide prediction of cis elements and their cognate transcription factors",
abstract = "Maize is a major crop and a model plant for studying C4 photosynthesis and leaf development. However, a genomewide regulatory network of leaf development is not yet available. This knowledge is useful for developing C3 crops to perform C4 photosynthesis for enhanced yields. Here, using 22 transcriptomes of developing maize leaves from dry seeds to 192 h post imbibition, we studied gene up- and down-regulation and functional transition during leaf development and inferred sets of strongly coexpressed genes. More significantly, we developed a method to predict transcription factor binding sites (TFBSs) and their cognate transcription factors (TFs) using genomic sequence and transcriptomic data. The method requires not only evolutionary conservation of candidate TFBSs and sets of strongly coexpressed genes but also that the genes in a gene set share the same Gene Ontology term so that they are involved in the same biological function. In addition, we developed another method to predict maize TF-TFBS pairs using known TF-TFBS pairs in Arabidopsis or rice. From these efforts, we predicted 1,340 novel TFBSs and 253 new TF-TFBS pairs in the maize genome, far exceeding the 30 TF-TFBS pairs currently known in maize. In most cases studied by both methods, the two methods gave similar predictions. In vitro tests of 12 predicted TF-TFBS interactions showed that our methods perform well. Our study has significantly expanded our knowledge on the regulatory network involved in maize leaf development.",
keywords = "Cis binding site, Coexpressed genes, Maize transcriptomes, transcription factor, transcriptome, Arabidopsis, Article, binding site, controlled study, down regulation, gene expression, gene ontology, gene sequence, genetic conservation, genetic transcription, germination, in vitro study, leaf development, maize, molecular dynamics, multigene family, nonhuman, plant gene, plant leaf, plant seed, prediction, priority journal, rice, upregulation, Zea mays",
author = "Chun-Ping Yu and Chun-Chang Chen and Yao-Ming Chang and Wen-Yu Liu and Hsin-Hung Lin and Jinn-Jy Lin and Hsiang-June Chen and Yu-Ju Lu and Yi-Hsuan Wu and Mei-Yeh-Jade Lu and Chen-Hua Lu and Arthur-Chun-Chieh Shih and Maurice-Sun-Ben Ku and Shin-Han Shiu and Shu-Hsing Wu and Wen-Hsiung Li",
note = "被引用次數:4 Export Date: 21 March 2016 CODEN: PNASA 通訊地址: Shiu, S.-H.; Biotechnology Center, National Chung-Hsing UniversityTaiwan 出資詳情: 1119778, NSF, Academia Sinica 出資詳情: AS-102-SS-A13, Academia Sinica 參考文獻: B{\"u}low, L., Steffens, N.O., Galuschka, C., Schindler, M., Hehl, R., AthaMap: From in silico data to real transcription factor binding sites (2006) In Silico Biol, 6 (3), pp. 243-252; Matys, V., TRANSFAC and its module TRANScompel: Transcriptional gene regulation in eukaryotes (2006) Nucleic Acids Res, 34, pp. D108-D110. , Database issue; Mathelier, A., JASPAR 2014: An extensively expanded and updated openaccess database of transcription factor binding profiles (2014) Nucleic Acids Res, 42 (Database issue), pp. D142-D147; Li, P., The developmental dynamics of the maize leaf transcriptome (2010) Nat Genet, 42 (12), pp. 1060-1067; Chang, Y.M., Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis (2012) Plant Physiol, 160 (1), pp. 165-177; Liu, W.Y., Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination (2013) Proc Natl Acad Sci USA, 110 (10), pp. 3979-3984; Wang, P., Kelly, S., Fouracre, J.P., Langdale, J.A., Genome-wide transcript analysis of early maize leaf development reveals gene cohorts associated with the differentiation of C4 Kranz anatomy (2013) Plant J, 75 (4), pp. 656-670; Wang, L., Comparative analyses of C<inf>4</inf> and C<inf>3</inf> photosynthesis in developing leaves of maize and rice (2014) Nat Biotechnol, 32 (11), pp. 1158-1165; Chen, J., Dynamic transcriptome landscape of maize embryo and endosperm development (2014) Plant Physiol, 166 (1), pp. 252-264; Bewley, J.D., Seed germination and dormancy (1997) Plant Cell, 9 (7), pp. 1055-1066; Kucera, B., Cohn, M.A., Leubner-Metzger, G., Plant hormone interactions during seed dormancy release and germination (2005) Seed Sci Res, 15 (4), pp. 281-307; Weitbrecht, K., M{\"u}ller, K., Leubner-Metzger, G., First off the mark: Early seed germination (2011) J Exp Bot, 62 (10), pp. 3289-3309; Ohashi-Ito, K., Fukuda, H., Transcriptional regulation of vascular cell fates (2010) Curr Opin Plant Biol, 13 (6), pp. 670-676; Cui, H., Kong, D., Liu, X., Hao, Y., Scarecrow, scr-like 23 and short-root control bundle sheath cell fate and function in arabidopsis thaliana (2014) Plant J, 78 (2), pp. 319-327; Slewinski, T.L., Anderson, A.A., Zhang, C., Turgeon, R., Scarecrow plays a role in establishing Kranz anatomy in maize leaves (2012) Plant Cell Physiol, 53 (12), pp. 2030-2037; Slewinski, T.L., Zhang, C., Turgeon, R., Structural and functional heterogeneity in phloem loading and transport (2013) Front Plant Sci, 4, p. 244; Fouracre, J.P., Ando, S., Langdale, J.A., Cracking the Kranz enigma with systems biology (2014) J Exp Bot, 65 (13), pp. 3327-3339; Halliday, K.J., Mart{\'i}nez-Garc{\'i}a, J.F., Josse, E.M., Integration of light and auxin signaling (2009) Cold Spring Harb Perspect Biol, 1 (6); Sassi, M., Wang, J., Ruberti, I., Vernoux, T., Xu, J., Shedding light on auxin movement: Light-regulation of polar auxin transport in the photocontrol of plant development (2013) Plant Signal Behav, 8 (3); Strayer, C., Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog (2000) Science, 289 (5480), pp. 768-771; Yazaki, J., Transcriptional profiling of genes responsive to abscisic acid and gibberellin in rice: Phenotyping and comparative analysis between rice and Arabidopsis (2004) Physiol Genomics, 17 (2), pp. 87-100; Elliott, R.C., Aintegumenta, an apetala2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth (1996) Plant Cell, 8 (2), pp. 155-168; Horiguchi, G., Kim, G.T., Tsukaya, H., The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana (2005) Plant J, 43 (1), pp. 68-78; Baima, S., The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana (1995) Development, 121 (12), pp. 4171-4182; Ohashi-Ito, K., Oguchi, M., Kojima, M., Sakakibara, H., Fukuda, H., Auxin-associated initiation of vascular cell differentiation by LONESOME HIGHWAY (2013) Development, 140 (4), pp. 765-769; Zhou, J., Wang, X., Lee, J.Y., Lee, J.Y., Cell-to-cell movement of two interacting AThook factors in Arabidopsis root vascular tissue patterning (2013) Plant Cell, 25 (1), pp. 187-201; Okada, K., Ueda, J., Komaki, M.K., Bell, C.J., Shimura, Y., Requirement of the auxin polar transport system in early stages of arabidopsis floral bud formation (1991) Plant Cell, 3 (7), pp. 677-684; Jones, A.M., Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1 (1998) Science, 282 (5391), pp. 1114-1117; Blakeslee, J.J., Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis (2007) Plant Cell, 19 (1), pp. 131-147; Guo, X., Lu, W., Ma, Y., Qin, Q., Hou, S., The big gene is required for auxin-mediated organ growth in arabidopsis (2013) Planta, 237 (4), pp. 1135-1147; Shikata, M., Koyama, T., Mitsuda, N., Ohme-Takagi, M., Arabidopsis SBP-box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase (2009) Plant Cell Physiol, 50 (12), pp. 2133-2145; Nakano, T., Suzuki, K., Fujimura, T., Shinshi, H., Genome-wide analysis of the ERF gene family in Arabidopsis and rice (2006) Plant Physiol, 140 (2), pp. 411-432; Walsh, J., Waters, C.A., Freeling, M., The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary (1998) Genes Dev, 12 (2), pp. 208-218; Silveira, A.B., The Arabidopsis AtbZIP9 protein fused to the VP16 transcriptional activation domain alters leaf and vascular development (2007) Plant Sci, 172 (6), pp. 1148-1156; Corr{\^e}a, L.G., The role of bZIP transcription factors in green plant evolution: Adaptive features emerging from four founder genes (2008) PLoS ONE, 3 (8); Li, Z., Thomas, T.L., PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in arabidopsis (1998) Plant Cell, 10 (3), pp. 383-398; Wang, D., Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice (2008) BMC Genomics, 9, p. 44; Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., Tasaka, M., Genes involved in organ separation in Arabidopsis: An analysis of the cup-shaped cotyledon mutant (1997) Plant Cell, 9 (6), pp. 841-857; Xie, Q., Frugis, G., Colgan, D., Chua, N.H., Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development (2000) Genes Dev, 14 (23), pp. 3024-3036; Xu, B., Contribution of NAC transcription factors to plant adaptation to land (2014) Science, 343 (6178), pp. 1505-1508; Scharf, K.D., Berberich, T., Ebersberger, I., Nover, L., The plant heat stress transcription factor (Hsf) family: Structure, function and evolution (2012) Biochim Biophys Acta, 1819 (2), pp. 104-119; Petricka, J.J., Clay, N.K., Nelson, T.M., Vein patterning screens and the defectively organized tributaries mutants in arabidopsis thaliana (2008) Plant J, 56 (2), pp. 251-263; Castilhos, G., Lazzarotto, F., Spagnolo-Fonini, L., Bodanese-Zanettini, M.H., Margis-Pinheiro, M., Possible roles of basic helix-loop-helix transcription factors in adaptation to drought (2014) Plant Sci, 223, pp. 1-7; Kwak, K.J., Kim, J.Y., Kim, Y.O., Kang, H., Characterization of transgenic Arabidopsis plants overexpressing high mobility group B proteins under high salinity, drought or cold stress (2007) Plant Cell Physiol, 48 (2), pp. 221-231; Lildballe, D.L., The expression level of the chromatin-associated HMGB1 protein influences growth, stress tolerance, and transcriptome in Arabidopsis (2008) J Mol Biol, 384 (1), pp. 9-21; Wang, Z.Y., Tobin, E.M., Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression (1998) Cell, 93 (7), pp. 1207-1217; Du, H., Genome-wide identification and evolutionary and expression analyses of MYB-related genes in land plants (2013) DNA Res, 20 (5), pp. 437-448; Swaminathan, K., Peterson, K., Jack, T., The plant B3 superfamily (2008) Trends Plant Sci, 13 (12), pp. 647-655; Brooks, L., 3rd, Microdissection of shoot meristem functional domains (2009) PLoS Genet, 5 (5); Hoecker, U., Vasil, I.K., McCarty, D.R., Integrated control of seed maturation and germination programs by activator and repressor functions of Viviparous-1 of maize (1995) Genes Dev, 9 (20), pp. 2459-2469; Dubos, C., MYB transcription factors in Arabidopsis (2010) Trends Plant Sci, 15 (10), pp. 573-581; Cao, D., Hussain, A., Cheng, H., Peng, J., Loss of function of four DELLA genes leads to light- and gibberellin-independent seed germination in Arabidopsis (2005) Planta, 223 (1), pp. 105-113; Ariel, F.D., Manavella, P.A., Dezar, C.A., Chan, R.L., The true story of the HD-Zip family (2007) Trends Plant Sci, 12 (9), pp. 419-426; Johannesson, H., Wang, Y., Hanson, J., Engstr{\"o}m, P., The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings (2003) Plant Mol Biol, 51 (5), pp. 719-729; Griffiths, S., Dunford, R.P., Coupland, G., Laurie, D.A., The evolution of CONSTANSlike gene families in barley, rice, and Arabidopsis (2003) Plant Physiol, 131 (4), pp. 1855-1867; Kumagai, T., The common function of a novel subfamily of B-Box zinc finger proteins with reference to circadian-associated events in Arabidopsis thaliana (2008) Biosci Biotechnol Biochem, 72 (6), pp. 1539-1549; Husbands, A., Bell, E.M., Shuai, B., Smith, H.M., Springer, P.S., LATERAL ORGAN BOUNDARIES defines a new family of DNA-binding transcription factors and can interact with specific bHLH proteins (2007) Nucleic Acids Res, 35 (19), pp. 6663-6671; Preston, J.C., Hileman, L.C., Functional evolution in the plant squamosa-pro-moter binding protein-like (SPL) gene family (2013) Front Plant Sci, 4, p. 80; Bowman, J.L., The YABBY gene family and abaxial cell fate (2000) Curr Opin Plant Biol, 3 (1), pp. 17-22; Mart{\'i}n-Trillo, M., Cubas, P., TCP genes: A family snapshot ten years later (2010) Trends Plant Sci, 15 (1), pp. 31-39; Serikawa, K.A., Martinez-Laborda, A., Kim, H.S., Zambryski, P.C., Localization of expression of KNAT3, a class 2 knotted1-like gene (1997) Plant J, 11 (4), pp. 853-861; Hamant, O., Pautot, V., Plant development: A TALE story (2010) C R Biol, 333 (4), pp. 371-381; Kim, D., BLH1 and KNAT3 modulate ABA responses during germination and early seedling development in Arabidopsis (2013) Plant J, 75 (5), pp. 755-766; Lijavetzky, D., Carbonero, P., Vicente-Carbajosa, J., Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families (2003) BMC Evol Biol, 3, p. 17; Epple, P., Mack, A.A., Morris, V.R., Dangl, J.L., Antagonistic control of oxidative stressinduced cell death in Arabidopsis by two related, plant-specific zinc finger proteins (2003) Proc Natl Acad Sci USA, 100 (11), pp. 6831-6836; Van Der Graaff, E., Laux, T., Rensing, S.A., The WUS homeobox-containing (WOX) protein family (2009) Genome Biol, 10 (12), pp. 248.1-248.9; Nakamichi, N., PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock (2010) Plant Cell, 22 (3), pp. 594-605; Franco-Zorrilla, J.M., DNA-binding specificities of plant transcription factors and their potential to define target genes (2014) Proc Natl Acad Sci USA, 111 (6), pp. 2367-2372; Weirauch, M.T., Determination and inference of eukaryotic transcription factor sequence specificity (2014) Cell, 158 (6), pp. 1431-1443; Mahony, S., Auron, P.E., Benos, P.V., DNA familial binding profiles made easy: Comparison of various motif alignment and clustering strategies (2007) PLOS Comput Biol, 3 (3), p. e61; Lin, J.J., Yu, C.P., Chang, Y.M., Chen, S.C., Li, W.H., Maize and millet transcription factors annotated using comparative genomic and transcriptomic data (2014) BMC Genomics, 15, p. 818; Thimm, O., MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes (2004) Plant J, 37 (6), pp. 914-939; Subramanian, A., Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles (2005) Proc Natl Acad Sci USA, 102 (43), pp. 15545-15550; Tsang, J.S., Ebert, M.S., Van Oudenaarden, A., Genome-wide dissection of microRNA functions and cotargeting networks using gene set signatures (2010) Mol Cell, 38 (1), pp. 140-153; Benjamini, Y., Hochberg, Y., Controlling the false discovery rate - A practical and powerful approach to multiple testing (1995) J Roy Stat Soc B Met, 57 (1), pp. 289-300; Bailey, T.L., Elkan, C., Fitting a mixture model by expectation maximization to discover motifs in biopolymers (1994) Proc Int Conf Intell Syst Mol Biol, 2, pp. 28-36; Heyndrickx, K.S., Van De Velde, J., Wang, C., Weigel, D., Vandepoele, K., A functional and evolutionary perspective on transcription factor binding in arabidopsis thaliana (2014) Plant Cell, 26 (10), pp. 3894-3910; Lin, Z., Wu, W.S., Liang, H., Woo, Y., Li, W.H., The spatial distribution of cis regulatory elements in yeast promoters and its implications for transcriptional regulation (2010) BMC Genomics, 11, p. 581; Schnable, J.C., Freeling, M., Lyons, E., Genome-wide analysis of syntenic gene deletion in the grasses (2012) Genome Biol Evol, 4 (3), pp. 265-277; Grant, C.E., Bailey, T.L., Noble, W.S., FIMO: Scanning for occurrences of a given motif (2011) Bioinformatics, 27 (7), pp. 1017-1018; Edgar, R.C., MUSCLE: Multiple sequence alignment with high accuracy and high throughput (2004) Nucleic Acids Res, 32 (5), pp. 1792-1797; Gupta, S., Stamatoyannopoulos, J.A., Bailey, T.L., Noble, W.S., Quantifying similarity between motifs (2007) Genome Biol, 8 (2), pp. R24.1-R24.9",
year = "2015",
doi = "10.1073/pnas.1500605112",
language = "English",
volume = "112",
pages = "E2477--E2486",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "National Academy of Sciences",
number = "19",

}

TY - JOUR

T1 - Transcriptome dynamics of developing maize leaves and genomewide prediction of cis elements and their cognate transcription factors

AU - Yu, Chun-Ping

AU - Chen, Chun-Chang

AU - Chang, Yao-Ming

AU - Liu, Wen-Yu

AU - Lin, Hsin-Hung

AU - Lin, Jinn-Jy

AU - Chen, Hsiang-June

AU - Lu, Yu-Ju

AU - Wu, Yi-Hsuan

AU - Lu, Mei-Yeh-Jade

AU - Lu, Chen-Hua

AU - Shih, Arthur-Chun-Chieh

AU - Ku, Maurice-Sun-Ben

AU - Shiu, Shin-Han

AU - Wu, Shu-Hsing

AU - Li, Wen-Hsiung

N1 - 被引用次數:4 Export Date: 21 March 2016 CODEN: PNASA 通訊地址: Shiu, S.-H.; Biotechnology Center, National Chung-Hsing UniversityTaiwan 出資詳情: 1119778, NSF, Academia Sinica 出資詳情: AS-102-SS-A13, Academia Sinica 參考文獻: Bülow, L., Steffens, N.O., Galuschka, C., Schindler, M., Hehl, R., AthaMap: From in silico data to real transcription factor binding sites (2006) In Silico Biol, 6 (3), pp. 243-252; Matys, V., TRANSFAC and its module TRANScompel: Transcriptional gene regulation in eukaryotes (2006) Nucleic Acids Res, 34, pp. D108-D110. , Database issue; Mathelier, A., JASPAR 2014: An extensively expanded and updated openaccess database of transcription factor binding profiles (2014) Nucleic Acids Res, 42 (Database issue), pp. D142-D147; Li, P., The developmental dynamics of the maize leaf transcriptome (2010) Nat Genet, 42 (12), pp. 1060-1067; Chang, Y.M., Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis (2012) Plant Physiol, 160 (1), pp. 165-177; Liu, W.Y., Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination (2013) Proc Natl Acad Sci USA, 110 (10), pp. 3979-3984; Wang, P., Kelly, S., Fouracre, J.P., Langdale, J.A., Genome-wide transcript analysis of early maize leaf development reveals gene cohorts associated with the differentiation of C4 Kranz anatomy (2013) Plant J, 75 (4), pp. 656-670; Wang, L., Comparative analyses of C<inf>4</inf> and C<inf>3</inf> photosynthesis in developing leaves of maize and rice (2014) Nat Biotechnol, 32 (11), pp. 1158-1165; Chen, J., Dynamic transcriptome landscape of maize embryo and endosperm development (2014) Plant Physiol, 166 (1), pp. 252-264; Bewley, J.D., Seed germination and dormancy (1997) Plant Cell, 9 (7), pp. 1055-1066; Kucera, B., Cohn, M.A., Leubner-Metzger, G., Plant hormone interactions during seed dormancy release and germination (2005) Seed Sci Res, 15 (4), pp. 281-307; Weitbrecht, K., Müller, K., Leubner-Metzger, G., First off the mark: Early seed germination (2011) J Exp Bot, 62 (10), pp. 3289-3309; Ohashi-Ito, K., Fukuda, H., Transcriptional regulation of vascular cell fates (2010) Curr Opin Plant Biol, 13 (6), pp. 670-676; Cui, H., Kong, D., Liu, X., Hao, Y., Scarecrow, scr-like 23 and short-root control bundle sheath cell fate and function in arabidopsis thaliana (2014) Plant J, 78 (2), pp. 319-327; Slewinski, T.L., Anderson, A.A., Zhang, C., Turgeon, R., Scarecrow plays a role in establishing Kranz anatomy in maize leaves (2012) Plant Cell Physiol, 53 (12), pp. 2030-2037; Slewinski, T.L., Zhang, C., Turgeon, R., Structural and functional heterogeneity in phloem loading and transport (2013) Front Plant Sci, 4, p. 244; Fouracre, J.P., Ando, S., Langdale, J.A., Cracking the Kranz enigma with systems biology (2014) J Exp Bot, 65 (13), pp. 3327-3339; Halliday, K.J., Martínez-García, J.F., Josse, E.M., Integration of light and auxin signaling (2009) Cold Spring Harb Perspect Biol, 1 (6); Sassi, M., Wang, J., Ruberti, I., Vernoux, T., Xu, J., Shedding light on auxin movement: Light-regulation of polar auxin transport in the photocontrol of plant development (2013) Plant Signal Behav, 8 (3); Strayer, C., Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog (2000) Science, 289 (5480), pp. 768-771; Yazaki, J., Transcriptional profiling of genes responsive to abscisic acid and gibberellin in rice: Phenotyping and comparative analysis between rice and Arabidopsis (2004) Physiol Genomics, 17 (2), pp. 87-100; Elliott, R.C., Aintegumenta, an apetala2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth (1996) Plant Cell, 8 (2), pp. 155-168; Horiguchi, G., Kim, G.T., Tsukaya, H., The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana (2005) Plant J, 43 (1), pp. 68-78; Baima, S., The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana (1995) Development, 121 (12), pp. 4171-4182; Ohashi-Ito, K., Oguchi, M., Kojima, M., Sakakibara, H., Fukuda, H., Auxin-associated initiation of vascular cell differentiation by LONESOME HIGHWAY (2013) Development, 140 (4), pp. 765-769; Zhou, J., Wang, X., Lee, J.Y., Lee, J.Y., Cell-to-cell movement of two interacting AThook factors in Arabidopsis root vascular tissue patterning (2013) Plant Cell, 25 (1), pp. 187-201; Okada, K., Ueda, J., Komaki, M.K., Bell, C.J., Shimura, Y., Requirement of the auxin polar transport system in early stages of arabidopsis floral bud formation (1991) Plant Cell, 3 (7), pp. 677-684; Jones, A.M., Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1 (1998) Science, 282 (5391), pp. 1114-1117; Blakeslee, J.J., Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis (2007) Plant Cell, 19 (1), pp. 131-147; Guo, X., Lu, W., Ma, Y., Qin, Q., Hou, S., The big gene is required for auxin-mediated organ growth in arabidopsis (2013) Planta, 237 (4), pp. 1135-1147; Shikata, M., Koyama, T., Mitsuda, N., Ohme-Takagi, M., Arabidopsis SBP-box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase (2009) Plant Cell Physiol, 50 (12), pp. 2133-2145; Nakano, T., Suzuki, K., Fujimura, T., Shinshi, H., Genome-wide analysis of the ERF gene family in Arabidopsis and rice (2006) Plant Physiol, 140 (2), pp. 411-432; Walsh, J., Waters, C.A., Freeling, M., The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary (1998) Genes Dev, 12 (2), pp. 208-218; Silveira, A.B., The Arabidopsis AtbZIP9 protein fused to the VP16 transcriptional activation domain alters leaf and vascular development (2007) Plant Sci, 172 (6), pp. 1148-1156; Corrêa, L.G., The role of bZIP transcription factors in green plant evolution: Adaptive features emerging from four founder genes (2008) PLoS ONE, 3 (8); Li, Z., Thomas, T.L., PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in arabidopsis (1998) Plant Cell, 10 (3), pp. 383-398; Wang, D., Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice (2008) BMC Genomics, 9, p. 44; Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., Tasaka, M., Genes involved in organ separation in Arabidopsis: An analysis of the cup-shaped cotyledon mutant (1997) Plant Cell, 9 (6), pp. 841-857; Xie, Q., Frugis, G., Colgan, D., Chua, N.H., Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development (2000) Genes Dev, 14 (23), pp. 3024-3036; Xu, B., Contribution of NAC transcription factors to plant adaptation to land (2014) Science, 343 (6178), pp. 1505-1508; Scharf, K.D., Berberich, T., Ebersberger, I., Nover, L., The plant heat stress transcription factor (Hsf) family: Structure, function and evolution (2012) Biochim Biophys Acta, 1819 (2), pp. 104-119; Petricka, J.J., Clay, N.K., Nelson, T.M., Vein patterning screens and the defectively organized tributaries mutants in arabidopsis thaliana (2008) Plant J, 56 (2), pp. 251-263; Castilhos, G., Lazzarotto, F., Spagnolo-Fonini, L., Bodanese-Zanettini, M.H., Margis-Pinheiro, M., Possible roles of basic helix-loop-helix transcription factors in adaptation to drought (2014) Plant Sci, 223, pp. 1-7; Kwak, K.J., Kim, J.Y., Kim, Y.O., Kang, H., Characterization of transgenic Arabidopsis plants overexpressing high mobility group B proteins under high salinity, drought or cold stress (2007) Plant Cell Physiol, 48 (2), pp. 221-231; Lildballe, D.L., The expression level of the chromatin-associated HMGB1 protein influences growth, stress tolerance, and transcriptome in Arabidopsis (2008) J Mol Biol, 384 (1), pp. 9-21; Wang, Z.Y., Tobin, E.M., Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression (1998) Cell, 93 (7), pp. 1207-1217; Du, H., Genome-wide identification and evolutionary and expression analyses of MYB-related genes in land plants (2013) DNA Res, 20 (5), pp. 437-448; Swaminathan, K., Peterson, K., Jack, T., The plant B3 superfamily (2008) Trends Plant Sci, 13 (12), pp. 647-655; Brooks, L., 3rd, Microdissection of shoot meristem functional domains (2009) PLoS Genet, 5 (5); Hoecker, U., Vasil, I.K., McCarty, D.R., Integrated control of seed maturation and germination programs by activator and repressor functions of Viviparous-1 of maize (1995) Genes Dev, 9 (20), pp. 2459-2469; Dubos, C., MYB transcription factors in Arabidopsis (2010) Trends Plant Sci, 15 (10), pp. 573-581; Cao, D., Hussain, A., Cheng, H., Peng, J., Loss of function of four DELLA genes leads to light- and gibberellin-independent seed germination in Arabidopsis (2005) Planta, 223 (1), pp. 105-113; Ariel, F.D., Manavella, P.A., Dezar, C.A., Chan, R.L., The true story of the HD-Zip family (2007) Trends Plant Sci, 12 (9), pp. 419-426; Johannesson, H., Wang, Y., Hanson, J., Engström, P., The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings (2003) Plant Mol Biol, 51 (5), pp. 719-729; Griffiths, S., Dunford, R.P., Coupland, G., Laurie, D.A., The evolution of CONSTANSlike gene families in barley, rice, and Arabidopsis (2003) Plant Physiol, 131 (4), pp. 1855-1867; Kumagai, T., The common function of a novel subfamily of B-Box zinc finger proteins with reference to circadian-associated events in Arabidopsis thaliana (2008) Biosci Biotechnol Biochem, 72 (6), pp. 1539-1549; Husbands, A., Bell, E.M., Shuai, B., Smith, H.M., Springer, P.S., LATERAL ORGAN BOUNDARIES defines a new family of DNA-binding transcription factors and can interact with specific bHLH proteins (2007) Nucleic Acids Res, 35 (19), pp. 6663-6671; Preston, J.C., Hileman, L.C., Functional evolution in the plant squamosa-pro-moter binding protein-like (SPL) gene family (2013) Front Plant Sci, 4, p. 80; Bowman, J.L., The YABBY gene family and abaxial cell fate (2000) Curr Opin Plant Biol, 3 (1), pp. 17-22; Martín-Trillo, M., Cubas, P., TCP genes: A family snapshot ten years later (2010) Trends Plant Sci, 15 (1), pp. 31-39; Serikawa, K.A., Martinez-Laborda, A., Kim, H.S., Zambryski, P.C., Localization of expression of KNAT3, a class 2 knotted1-like gene (1997) Plant J, 11 (4), pp. 853-861; Hamant, O., Pautot, V., Plant development: A TALE story (2010) C R Biol, 333 (4), pp. 371-381; Kim, D., BLH1 and KNAT3 modulate ABA responses during germination and early seedling development in Arabidopsis (2013) Plant J, 75 (5), pp. 755-766; Lijavetzky, D., Carbonero, P., Vicente-Carbajosa, J., Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families (2003) BMC Evol Biol, 3, p. 17; Epple, P., Mack, A.A., Morris, V.R., Dangl, J.L., Antagonistic control of oxidative stressinduced cell death in Arabidopsis by two related, plant-specific zinc finger proteins (2003) Proc Natl Acad Sci USA, 100 (11), pp. 6831-6836; Van Der Graaff, E., Laux, T., Rensing, S.A., The WUS homeobox-containing (WOX) protein family (2009) Genome Biol, 10 (12), pp. 248.1-248.9; Nakamichi, N., PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock (2010) Plant Cell, 22 (3), pp. 594-605; Franco-Zorrilla, J.M., DNA-binding specificities of plant transcription factors and their potential to define target genes (2014) Proc Natl Acad Sci USA, 111 (6), pp. 2367-2372; Weirauch, M.T., Determination and inference of eukaryotic transcription factor sequence specificity (2014) Cell, 158 (6), pp. 1431-1443; Mahony, S., Auron, P.E., Benos, P.V., DNA familial binding profiles made easy: Comparison of various motif alignment and clustering strategies (2007) PLOS Comput Biol, 3 (3), p. e61; Lin, J.J., Yu, C.P., Chang, Y.M., Chen, S.C., Li, W.H., Maize and millet transcription factors annotated using comparative genomic and transcriptomic data (2014) BMC Genomics, 15, p. 818; Thimm, O., MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes (2004) Plant J, 37 (6), pp. 914-939; Subramanian, A., Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles (2005) Proc Natl Acad Sci USA, 102 (43), pp. 15545-15550; Tsang, J.S., Ebert, M.S., Van Oudenaarden, A., Genome-wide dissection of microRNA functions and cotargeting networks using gene set signatures (2010) Mol Cell, 38 (1), pp. 140-153; Benjamini, Y., Hochberg, Y., Controlling the false discovery rate - A practical and powerful approach to multiple testing (1995) J Roy Stat Soc B Met, 57 (1), pp. 289-300; Bailey, T.L., Elkan, C., Fitting a mixture model by expectation maximization to discover motifs in biopolymers (1994) Proc Int Conf Intell Syst Mol Biol, 2, pp. 28-36; Heyndrickx, K.S., Van De Velde, J., Wang, C., Weigel, D., Vandepoele, K., A functional and evolutionary perspective on transcription factor binding in arabidopsis thaliana (2014) Plant Cell, 26 (10), pp. 3894-3910; Lin, Z., Wu, W.S., Liang, H., Woo, Y., Li, W.H., The spatial distribution of cis regulatory elements in yeast promoters and its implications for transcriptional regulation (2010) BMC Genomics, 11, p. 581; Schnable, J.C., Freeling, M., Lyons, E., Genome-wide analysis of syntenic gene deletion in the grasses (2012) Genome Biol Evol, 4 (3), pp. 265-277; Grant, C.E., Bailey, T.L., Noble, W.S., FIMO: Scanning for occurrences of a given motif (2011) Bioinformatics, 27 (7), pp. 1017-1018; Edgar, R.C., MUSCLE: Multiple sequence alignment with high accuracy and high throughput (2004) Nucleic Acids Res, 32 (5), pp. 1792-1797; Gupta, S., Stamatoyannopoulos, J.A., Bailey, T.L., Noble, W.S., Quantifying similarity between motifs (2007) Genome Biol, 8 (2), pp. R24.1-R24.9

PY - 2015

Y1 - 2015

N2 - Maize is a major crop and a model plant for studying C4 photosynthesis and leaf development. However, a genomewide regulatory network of leaf development is not yet available. This knowledge is useful for developing C3 crops to perform C4 photosynthesis for enhanced yields. Here, using 22 transcriptomes of developing maize leaves from dry seeds to 192 h post imbibition, we studied gene up- and down-regulation and functional transition during leaf development and inferred sets of strongly coexpressed genes. More significantly, we developed a method to predict transcription factor binding sites (TFBSs) and their cognate transcription factors (TFs) using genomic sequence and transcriptomic data. The method requires not only evolutionary conservation of candidate TFBSs and sets of strongly coexpressed genes but also that the genes in a gene set share the same Gene Ontology term so that they are involved in the same biological function. In addition, we developed another method to predict maize TF-TFBS pairs using known TF-TFBS pairs in Arabidopsis or rice. From these efforts, we predicted 1,340 novel TFBSs and 253 new TF-TFBS pairs in the maize genome, far exceeding the 30 TF-TFBS pairs currently known in maize. In most cases studied by both methods, the two methods gave similar predictions. In vitro tests of 12 predicted TF-TFBS interactions showed that our methods perform well. Our study has significantly expanded our knowledge on the regulatory network involved in maize leaf development.

AB - Maize is a major crop and a model plant for studying C4 photosynthesis and leaf development. However, a genomewide regulatory network of leaf development is not yet available. This knowledge is useful for developing C3 crops to perform C4 photosynthesis for enhanced yields. Here, using 22 transcriptomes of developing maize leaves from dry seeds to 192 h post imbibition, we studied gene up- and down-regulation and functional transition during leaf development and inferred sets of strongly coexpressed genes. More significantly, we developed a method to predict transcription factor binding sites (TFBSs) and their cognate transcription factors (TFs) using genomic sequence and transcriptomic data. The method requires not only evolutionary conservation of candidate TFBSs and sets of strongly coexpressed genes but also that the genes in a gene set share the same Gene Ontology term so that they are involved in the same biological function. In addition, we developed another method to predict maize TF-TFBS pairs using known TF-TFBS pairs in Arabidopsis or rice. From these efforts, we predicted 1,340 novel TFBSs and 253 new TF-TFBS pairs in the maize genome, far exceeding the 30 TF-TFBS pairs currently known in maize. In most cases studied by both methods, the two methods gave similar predictions. In vitro tests of 12 predicted TF-TFBS interactions showed that our methods perform well. Our study has significantly expanded our knowledge on the regulatory network involved in maize leaf development.

KW - Cis binding site

KW - Coexpressed genes

KW - Maize transcriptomes

KW - transcription factor

KW - transcriptome

KW - Arabidopsis

KW - Article

KW - binding site

KW - controlled study

KW - down regulation

KW - gene expression

KW - gene ontology

KW - gene sequence

KW - genetic conservation

KW - genetic transcription

KW - germination

KW - in vitro study

KW - leaf development

KW - maize

KW - molecular dynamics

KW - multigene family

KW - nonhuman

KW - plant gene

KW - plant leaf

KW - plant seed

KW - prediction

KW - priority journal

KW - rice

KW - upregulation

KW - Zea mays

U2 - 10.1073/pnas.1500605112

DO - 10.1073/pnas.1500605112

M3 - Article

VL - 112

SP - E2477-E2486

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 19

ER -