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An expression analysis of 57 transcription factors derived from ESTs of developing seeds in Maize (Zea mays)

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Abstract

Maize seeds are an important source of food, animal feed, and industrial raw materials. To understand global gene expression and regulation during maize seed development, a normalized cDNA library, covering most of the developmental stages of maize seeds, was constructed. Sequencing analysis of 10,848 randomly selected clones identified 6,630 unique ESTs. Among them, 57 putative transcription factors (TFs) were identified. The TFs belong to seven different super-families, specifically 17 Zinc-finger, 13 bZIP, 8 bHLH, 6 MADS, 7 MYB, 3 Homedomain, and 3 AP2/EREBP. The spatial and temporal expression of the TFs was analyzed by semi-quantitative RT-PCR with representative tissue types and seeds at different developmental stages, revealing their diverse expression patterns and expression levels. One-third (19) of the maize TFs was found their putative orthologs in Arabidopsis. Similar expression patterns were observed in both maize and Arabidopsis for the majority of orthologous pairs (15 out of 19), suggesting their conserved functions during seed development. In conclusion, the systematic analysis of maize seed TFs has provided valuable insight into transcriptional regulation during maize seed development.

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Abbreviations

DAP:

Days after pollination

TF:

Transcription factor

Y2H:

Yeast two-hybrid

References

  • Alexandrov NN, Brover VV, Freidin S, Troukhan ME, Tatarinova TV, Zhang H, Swaller TJ, Lu YP, Bouck J, Flavell RB, Feldmann KA (2009) Insights into corn genes derived from large-scale cDNA sequencing. Plant Mol Biol 69:179–194

    Article  CAS  PubMed  Google Scholar 

  • Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12:419–426

    Article  CAS  PubMed  Google Scholar 

  • Arruda P, Kemper EL, Papes F, Leite A (2000) Regulation of lysine catabolism in higher plants. Trends Plant Sci 5:324–330

    Article  CAS  PubMed  Google Scholar 

  • Baumann K, Perez-Rodriguez M, Bradley D, Venail J, Bailey P, Jin H, Koes R, Roberts K, Martin C (2007) Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134:1691–1701

    Article  CAS  PubMed  Google Scholar 

  • Berger F (1999) Endosperm development. Curr Opin Plant Biol 2:28–32

    Article  CAS  PubMed  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL, Custers JB, van Lookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  CAS  PubMed  Google Scholar 

  • Carpita NC, McCann MC (2008) Maize and sorghum: genetic resources for bioenergy grasses. Trends Plant Sci 13:415–420

    Article  CAS  PubMed  Google Scholar 

  • Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585

    Article  CAS  PubMed  Google Scholar 

  • Chaudhury AM, Craig S, Dennis E, Peacock WJ (1998) Ovule and embryo development, apomixis and fertilization. Curr Opin Plant Biol 1:26–31

    Article  CAS  PubMed  Google Scholar 

  • Chaudhury AM, Koltunow A, Payne T, Luo M, Tucker MR, Dennis ES, Peacock WJ (2001) Control of early seed development. Annu Rev Cell Dev Biol 17:677–699

    Article  CAS  PubMed  Google Scholar 

  • Cooper B, Clarke JD, Budworth P, Kreps J, Hutchison D, Park S, Guimil S, Dunn M, Luginbuhl P, Ellero C, Goff SA, Glazebrook J (2003) A network of rice genes associated with stress response and seed development. Proc Natl Acad Sci USA 100:4945–4950

    Article  CAS  PubMed  Google Scholar 

  • Day RC, Herridge RP, Ambrose BA, Macknight RC (2008) Transcriptome analysis of proliferating Arabidopsis endosperm reveals biological implications for the control of syncytial division, cytokinin signaling, and gene expression regulation. Plant Physiol 148:1964–1984

    Article  CAS  PubMed  Google Scholar 

  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194

    CAS  PubMed  Google Scholar 

  • Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185

    CAS  Google Scholar 

  • Feng L, Zhu J, Wang G, Tang Y, Chen H, Jin W, Wang F, Mei B, Xu Z, Song R (2009) Expressional profiling study revealed unique expressional patterns and dramatic expressional divergence of maize alpha-zein super gene family. Plant Mol Biol 69:649–659

    Article  CAS  PubMed  Google Scholar 

  • Fontanet P, Vicient CM (2008) Maize embryogenesis. Methods Mol Biol 427:17–29

    Article  CAS  PubMed  Google Scholar 

  • Gao G, Zhong Y, Guo A, Zhu Q, Tang W, Zheng W, Gu X, Wei L, Luo J (2006) DRTF: a database of rice transcription factors. Bioinformatics 22:1286–1287

    Article  CAS  PubMed  Google Scholar 

  • Giroux MJ, Boyer C, Feix G, Hannah LC (1994) Coordinated transcriptional regulation of storage product genes in the maize endosperm. Plant Physiol 106:713–722

    CAS  PubMed  Google Scholar 

  • Gomez-Mena C, de Folter S, Costa MM, Angenent GC, Sablowski R (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132:429–438

    Article  CAS  PubMed  Google Scholar 

  • Grabowska A, Wisniewska A, Tagashira N, Malepszy S, Filipecki M (2009) Characterization of CsSEF1 gene encoding putative CCCH-type zinc finger protein expressed during cucumber somatic embryogenesis. J Plant Physiol 166:310–323

    Article  CAS  PubMed  Google Scholar 

  • Grotewold E, Chamberlin M, Snook M, Siame B, Butler L, Swenson J, Maddock S, Clair GS, Bowen B (1998) Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell 10:721–740

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Rupe MA, Danilevskaya ON, Yang X, Hu Z (2003) Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. Plant J 36:30–44

    Article  CAS  PubMed  Google Scholar 

  • Guo A, He K, Liu D, Bai S, Gu X, Wei L, Luo J (2005) DATF: a database of Arabidopsis transcription factors. Bioinformatics 21:2568–2569

    Article  CAS  PubMed  Google Scholar 

  • Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R, Eilbeck K, Lewis S, Marshall B, Mungall C, Richter J, Rubin GM, Blake JA, Bult C, Dolan M, Drabkin H, Eppig JT, Hill DP, Ni L, Ringwald M, Balakrishnan R, Cherry JM, Christie KR, Costanzo MC, Dwight SS, Engel S, Fisk DG, Hirschman JE, Hong EL, Nash RS, Sethuraman A, Theesfeld CL, Botstein D, Dolinski K, Feierbach B, Berardini T, Mundodi S, Rhee SY, Apweiler R, Barrell D, Camon E, Dimmer E, Lee V, Chisholm R, Gaudet P, Kibbe W, Kishore R, Schwarz EM, Sternberg P, Gwinn M, Hannick L, Wortman J, Berriman M, Wood V, de la Cruz N, Tonellato P, Jaiswal P, Seigfried T, White R (2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261

    Article  CAS  PubMed  Google Scholar 

  • Hunter BG, Beatty MK, Singletary GW, Hamaker BR, Dilkes BP, Larkins BA, Jung R (2002) Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell 14:2591–2612

    Article  CAS  PubMed  Google Scholar 

  • Immink RG, Nougalli Tonaco IA, de Folter S, Shchennikova A, van Dijk AD, Busscher-Lange J, Borst JW, Angenent GC (2009) SEPALLATA3: The “glue” for MADS box transcription factor complex formation. Genome Biol 10:R24

    Article  PubMed  Google Scholar 

  • Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y, Hattori T, Miyao A, Hirochika H, Ashikari M, Matsuoka M (2004) Loss-of-function mutations of the rice GAMYB gene impair alpha-amylase expression in aleurone and flower development. Plant Cell 16:33–44

    Article  CAS  PubMed  Google Scholar 

  • Kang IH, Steffen JG, Portereiko MF, Lloyd A, Drews GN (2008) The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20:635–647

    Article  CAS  PubMed  Google Scholar 

  • Kiesselbach TA (1998) The structure and reproduction of corn. 50th Anniversary Edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

  • Lai J, Dey N, Kim CS, Bharti AK, Rudd S, Mayer KF, Larkins BA, Becraft P, Messing J (2004) Characterization of the maize endosperm transcriptome and its comparison to the rice genome. Genome Res 14:1932–1937

    Article  PubMed  Google Scholar 

  • Lehti-Shiu MD, Adamczyk BJ, Fernandez DE (2005) Expression of MADS-box genes during the embryonic phase in Arabidopsis. Plant Mol Biol 58:89–107

    Article  CAS  PubMed  Google Scholar 

  • Li X, Duan X, Jiang H, Sun Y, Tang Y, Yuan Z, Guo Jingkang, Liang W, Chen L, Yin J, Ma H, Wang J, Zhang D (2006) Genome-wide analysis of basic/helix–loop–helix transcription factor family in rice and Arabidopsis. Plant Physiol 141:1167–1184

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Fu J, Gu D, Liu W, Liu T, Peng Y, Wang J, Wang G (2008) Genome-wide analysis of gene expression profiles during the kernel development of maize (Zea mays L.). Genomics 91:378–387

    Article  CAS  PubMed  Google Scholar 

  • Lohmer S, Maddaloni M, Motto M, Di Fonzo N, Hartings H, Salamini F, Thompson RD (1991) The maize regulatory locus Opaque-2 encodes a DNA-binding protein which activates the transcription of the b-32 gene. EMBO J 10:617–624

    CAS  PubMed  Google Scholar 

  • Mechin V, Balliau T, Chateau-Joubert S, Davanture M, Langella O, Negroni L, Prioul JL, Thevenot C, Zivy M, Damerval C (2004) A two-dimensional proteome map of maize endosperm. Phytochemistry 65:1609–1618

    Article  CAS  PubMed  Google Scholar 

  • Mechin V, Thevenot C, Le Guilloux M, Prioul JL, Damerval C (2007) Developmental analysis of maize endosperm proteome suggests a pivotal role for pyruvate orthophosphate dikinase. Plant Physiol 143:1203–1219

    Article  CAS  PubMed  Google Scholar 

  • Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947

    Article  CAS  PubMed  Google Scholar 

  • Neuffer MG, Sheridan WF (1980) Defective kernel mutants of maize. I. Genetic and lethality studies. Genetics 95:929–944

    PubMed  Google Scholar 

  • Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS box gene family. Nat Rev Genet 2:186–195

    Article  CAS  PubMed  Google Scholar 

  • Ohto MA, Fischer RL, Goldberg RB, Nakamura K, Harada JJ (2005) Control of seed mass by APETALA2. Proc Natl Acad Sci USA 102:3123–3128

    Article  CAS  PubMed  Google Scholar 

  • Olsen OA (2001) Endosperm development: cellularization and cell fate specification. Annu Rev Plant Physiol Plant Mol Biol 52:233–267

    Article  CAS  PubMed  Google Scholar 

  • Olsen OA (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16(suppl):S214–S227

    Article  CAS  PubMed  Google Scholar 

  • Penfield S, Josse EM, Kannangara R, Gilday AD, Halliday KJ, Graham IA (2005) Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr Biol 15:1998–2006

    Article  CAS  PubMed  Google Scholar 

  • Portereiko MF, Lloyd A, Steffen JG, Punwani JA, Otsuga D, Drews GN (2006) AGL80 is required for central cell and endosperm development in Arabidopsis. Plant Cell 18:1862–1872

    Article  CAS  PubMed  Google Scholar 

  • Prioul JL, Mechin V, Lessard P, Thevenot C, Grimmer M, Chateau-Joubert S, Coates S, Hartings H, Kloiber-Maitz M, Murigneux A, Sarda X, Damerval C, Edwards KJ (2008) A joint transcriptomic, proteomic and metabolic analysis of maize endosperm development and starch filling. Plant Biotechnol J 6:855–869

    Google Scholar 

  • Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D (2004) The effect of alpha-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134:1598–1613

    Article  CAS  PubMed  Google Scholar 

  • Rampey RA, Woodward AW, Hobbs BN, Tierney MP, Lahner B, Salt DE, Bartel B (2006) An Arabidopsis basic helix–loop–helix leucine zipper protein modulates metal homeostasis and auxin conjugate responsiveness. Genetics 174:1841–1857

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, ZC, Jiang, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu GL (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

  • Sabelli PA, Larkins BA (2009) The development of endosperm in grasses. Plant Physiol 149:14–26

    Article  CAS  PubMed  Google Scholar 

  • Schmidt RJ, Ketudat M, Aukerman MJ, Hoschek G (1992) Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kD zein genes. Plant Cell 4:689–700

    Article  CAS  PubMed  Google Scholar 

  • Soderlund C, Descour A, Kudrna D, Bomhoff M, Boyd L, Currie J, Angelova A, Collura K, Wissotski M, Ashley E, Morrow D, Fernandes J, Walbot V, Yu Y (2009) Sequencing, mapping, and analysis of 27, 455 maize full-length cDNAs. PLoS Genet 5:e1000740

    Article  PubMed  Google Scholar 

  • Sreenivasulu N, Radchuk V, Strickert M, Miersch O, Weschke W, Wobus U (2006) Gene expression patterns reveal tissue-specific signaling networks controlling programmed cell death and ABA-regulated maturation in developing barley seeds. Plant J 47:310–327

    Article  CAS  PubMed  Google Scholar 

  • Sridhar VV, Surendrarao A, Liu Z (2006) APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133:3159–3166

    Article  CAS  PubMed  Google Scholar 

  • Takatsuji H (1999) Zinc-finger proteins: the classical zinc finger emerges in contemporary plant science. Plant Mol Biol 39:1073–1078

    Article  CAS  PubMed  Google Scholar 

  • Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278:631–637

    Article  CAS  PubMed  Google Scholar 

  • Verza NC, TR ES, Neto GC, Nogueira FT, Fisch PH, de Rosa VE Jr, Rebello MM, Vettore AL, da Silva FR, Arruda P (2005) Endosperm-preferred expression of maize genes as revealed by transcriptome-wide analysis of expressed sequence tags. Plant Mol Biol 59:363–374

    Google Scholar 

  • Wang G, Gao Y, Yang L, Shi J (2007) Identification and analysis of differentially expressed genes in differentiating xylem of Chinese fir (Cunninghamia lanceolata) by suppression subtractive hybridization. Genome 50:1141–1155

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, Gao T, Guo H, Xie Q (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19:1912–1929

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Binbin Huang and Liangliang Zhou for technical support with sequencing analysis. This work was supported by National Natural Sciences Foundation of China (30671303, 30900900), Fok Ying Tung Education Foundation (101024), Ministry of Education of China (NCET-06-0435, 206048), Ministry of Science and Technology of China (2006AA10Z148, 2006AA10A107, 2009CB118400), Science and Technology Commission of Shanghai Municipality (05PJ14049, 05QMX1424, 09DZ2271800), and Education Commission of Shanghai Municipality (05ZZ02), Shanghai Education Foundation (04SG40).

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Correspondence to Rentao Song.

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Communicated by M. Jordan.

G. Wang and H. Wang have contributed equally to this work.

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Wang, G., Wang, H., Zhu, J. et al. An expression analysis of 57 transcription factors derived from ESTs of developing seeds in Maize (Zea mays). Plant Cell Rep 29, 545–559 (2010). https://doi.org/10.1007/s00299-010-0843-7

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