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Reduced tillering in Basmati rice T-DNA insertional mutant OsTEF1 associates with differential expression of stress related genes and transcription factors

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Abstract

A T-DNA insertional mutant OsTEF1 of rice gives 60–80% reduced tillering, retarded growth of seminal roots, and sensitivity to salt stress compared to wild type Basmati 370. The insertion occurred in a gene encoding a transcription elongation factor homologous to yeast elf1, on chromosome 2 of rice. Detailed transcriptomic profiling of OsTEF1 revealed that mutation in the transcription elongation factor differentially regulates the expression of more than 100 genes with known function and finely regulates tillering process in rice by inducing the expression of cytochrome P450. Along with different transcription factors, several stress associated genes were also affected due to a single insertion. In silico analysis of the TEF1 protein showed high conservation among different organisms. This transcription elongation factor predicted to interact with other proteins that directly or indirectly positively regulate tillering in rice.

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References

  • Aguilar-Martıínez JA, Poza-Carrión C, Cubas P (2007) Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19:458–472

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka J (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51:1019–1029

    Article  PubMed  CAS  Google Scholar 

  • Basha OP (2008) Mapping and cloning of oligoculm Osoc and seedling lethal Ossl insertional mutants in basmati. Dissertation, Indian Institute of Technology Roorkee

  • Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16:553–563

    Article  PubMed  CAS  Google Scholar 

  • Beveridge CA, Ross JJ, Murfet IC (1996) Branching in pea (action of genes RMS3 and RMS4). Plant Physiol 110:859–865

    PubMed  CAS  Google Scholar 

  • Beveridge CA, Symons GM, Turnbull CGN (2000) Auxin inhibition of decapitation-induced branching is dependent on graft-transmissible signals regulated by genes Rms1 and Rms2. Plant Physiol 123:689–697

    Article  PubMed  CAS  Google Scholar 

  • Booker J, Sieberer T, Wright W, Williamson L, Willett B, Strinberg P, Turnbull C, Murali S, Goddard P, Leyse O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8:443–449

    Article  PubMed  CAS  Google Scholar 

  • Borovskii GV, Stupnikova IV, Antipina AI, Vladirimova SV, Voinikov VK (2002) Accumulation of dehydrin-like proteins in the mitochondria of cereals in response to cold, freezing, drought and ABA treatment. BMC Plant Biol 2(5):1–7. doi:10.1186/1471-2229-2-5

    Google Scholar 

  • Cao Y, Song S, Goodman RM, Zheng Z (2006) Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. Plant Physiol 163:1167–1178. doi:10.1016/j.jplph.2005.11.004

    Article  CAS  Google Scholar 

  • Catterou M, Dubois F, Smets R, Vaniet S, Kichey T, Onckelen HV, Sangwan-Norreel BS, Sangwan RS (2002) Hoc: an Arabidopsis mutant overproducing cytokinins and expressing high in vitro organogenic capacity. Plant J 30:273–287

    Article  PubMed  CAS  Google Scholar 

  • Cazzonelli CI, Cuttriss AJ, Cossetto SB, Pye W, Crisp P, Whelan J, Finnegan EJ, Tumbull C, Pogson BJ (2009) Regulation of carotenoid composition and shoot branching in Arabidopsis by a chromatin modifying histone methyltransferase, SDG8. Plant Cell 21:39–53

    Article  PubMed  CAS  Google Scholar 

  • Chen M, Wang QY, Cheng XG, Xu ZS, Li LC, Ye XG, Xia LQ, Ma YZ (2007) GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem Biophys Res Commun 353:299–305

    Article  PubMed  CAS  Google Scholar 

  • Cline MG (1996) Exogenous auxin effect on lateral bud outgrowth in decapitated shoots. Ann Bot 78:255–266

    Article  CAS  Google Scholar 

  • Dai X, Xu Y, Ma Q, Xu W, Wang T, Xue Y, Chong K (2007) Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol 143:1739–1751

    Article  PubMed  CAS  Google Scholar 

  • Dhaliwal HS, Das A, Singh A, Gupta VK (2001) Isolation of insertional mutants in indica rice using Ds transposable element of maize. Rice Genet Newslett 18:98–99

    Google Scholar 

  • Doebley J, Stec A, Gustus C (1995) Teosinte branched 1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–346

    PubMed  CAS  Google Scholar 

  • Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Mol Cell Biol 12:211–221. doi:10.1038/nrm3088

    CAS  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    Article  PubMed  CAS  Google Scholar 

  • Grasser KD (2005) Emerging role for transcript elongation in plant development. Trends Plant Sci 10:484–490

    Article  PubMed  CAS  Google Scholar 

  • Greb T, Clarenz O, Schäfer E, Müller D, Herrero R, Schmitz G, Theres K (2003) Molecular analysis of the lateral suppressor gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17:1175–1187

    Article  PubMed  CAS  Google Scholar 

  • Gupta SK, Rai AK, Kanwar SS, Chand D, Singh NK, Sharma TR (2012) The single functional blast resistance gene Pi54 activates a complex defence mechanism in rice. J Exp Bot 63:757–772

    Article  PubMed  CAS  Google Scholar 

  • Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT (2002) Heterology expression of the Arabidopsis C-Repeat/Dehydration Response Element Binding Factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 129:1086–1094

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Wang JF, Wang QH, Zhang HS (2005) Identification of a rice zinc finger protein whose expression is transiently induced by drought, cold but not by salinity and abscisic acid. DNA Seq 16:130–136

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Yang X, Wang MM, Tang HJ, Ding LY, Shen Y, Zhang HS (2007) A novel rice C2H2-type zinc finger protein lacking DLN-box/EAR-motif plays a role in salt tolerance. Biochim Biophys Acta 1769:220–227

    PubMed  CAS  Google Scholar 

  • Hunter T (2000) Signaling—2000 and beyond. Cell 100:113–127

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46:79–86

    Article  PubMed  CAS  Google Scholar 

  • Islam MS, Wang MH (2009) Expression of dehydration responsive element-binding protein-3 (DREB3) under different abiotic stresses in tomato. BMB reports

  • Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47(1):141–153

    Article  PubMed  CAS  Google Scholar 

  • Kapulnik Y, Delaux PM, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Séjalon-Delmas N, Combier JP, Bécard G, Belausov E, Beeckman T, Dor E, Hershenhorn J, Koltai H (2011) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216. doi:10.1007/s00425-010-1310-y

    Article  PubMed  CAS  Google Scholar 

  • Keller T, Abbott J, Moritz T, Doerner P (2006) Arabidopsis REGULATOR OF AXILLARY MERISTEMS1 controls a leaf axil stem cell niche and modulates vegetative development. Plant Cell 18:598–611

    Article  PubMed  CAS  Google Scholar 

  • Komatsu K, Maekawa M, Ujiie S, Satake Y, Furutani I, Okamoto H, Shimamoto K, Kyozuka J (2003) LAX and SPA: major regulators of shoot branching in rice. Proc Natl Acad Sci U S A 100:11765–11770

    Article  PubMed  CAS  Google Scholar 

  • Krogan NJ, Dover J, Wood A, Schneider J, Heidt J, Boateng MA, Dean K, Ryan OW, Golshani A, Johnston M, Greenblatt JF, Shilatifard A (2003a) The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol Cell 11:721–729

    Article  PubMed  CAS  Google Scholar 

  • Krogan NJ, Kim M, Tong A, Golshani A, Cagney G, Canadien V, Richards DP, Beattie BK, Emili A, Boone C, Shilatifard A, Buratowski S, Greenblatt J (2003b) Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol Cell Biol 23:4207–4218

    Article  PubMed  CAS  Google Scholar 

  • Kubinski K, Zielinski R, Hellman U, Mazur E, Szyszka R (2006) Yeast elf1 factor is phosphorylated and interacts with protein kinase CK2. J Biochem Mol Biol 39(3):311–318

    Article  PubMed  CAS  Google Scholar 

  • 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 (2003) Control of tillering in rice. Nature 422:618–621

    Article  PubMed  CAS  Google Scholar 

  • Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, Chong K (2007) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 226(4):1007–1016. doi:10.1007/s00425-007-0548-5

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Ma Q, Dai X, Xu Y, Guo J, Liu Y, Chen N, Xiao J, Zhang D, Xu Z, Zhang X, Chong K (2009) Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiol 150:244–256

    Article  PubMed  CAS  Google Scholar 

  • Malik V, Wu R (2005) Transcription factor AtMyb2 increased salt-stress tolerance in rice, (Oryza sativa L.). Rice Genet Newslett 22:63

    Google Scholar 

  • Mao C, Ding W, Wu Y, Yu J, He X, Shou H, Wu P (2007) Overexpression of a NAC-domain protein promotes shoot branching in rice. New Phytol 176:288–298

    Article  PubMed  CAS  Google Scholar 

  • Marchler-Bauer A, Anderson JB, DeWeese-Scott C, Fedorova ND, Geer LY, He S, Hurwitz DI, Jackson JD, Jacobs AR, Lanczycki CJ, Liebert CA, Liu C, Madej T, Marchler GH, Mazumder R, Nikolskaya AN, Panchenko AR, Rao BS, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Vasudevan S, Wang Y, Yamashita RA, Yin JJ, Bryant SH (2003) CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res 31:383–387

    Article  PubMed  CAS  Google Scholar 

  • Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993

    Article  PubMed  CAS  Google Scholar 

  • McSteen P (2009) Hormonal regulation of branching in grasses. Plant Physiol 149:46–55

    Article  PubMed  CAS  Google Scholar 

  • McSteen P, Leyser O (2005) Shoot branching. Annu Rev Plant Biol 56:353–374

    Article  PubMed  CAS  Google Scholar 

  • Minakuchi K, Komeoka H, Yasuno N, Umehara M, Luo L, Kobayashi K, Hanada A, Ueno K, Asami T, Yamaguchi S, Kyozuka J (2010) FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51(7):1127–1135. doi:10.1093/pcp/pcq083

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci U S A 101(16):6309–6314. doi:10.1073_pnas.0401572101

    Article  PubMed  CAS  Google Scholar 

  • Nelissen H, Boccardi TM, Himanen K, Lijsebettens MV (2007) Impact of core histone modifications on transcriptional regulation and plant growth. Crit Rev Plant Sci 26:243–263

    Article  CAS  Google Scholar 

  • Ongaro V, Leyser O (2008) Hormonal control of shoot branching. J Exp Bot 59:67–74

    Article  PubMed  CAS  Google Scholar 

  • Prather D, Krogan NJ, Emili A, Greenblatt JF, Winston F (2005) Identification and characterization of Elf1, a conserved transcription elongation factor in Saccharomyces cerevisiae. Mol Cell Biol 25:10122–10135

    Article  PubMed  CAS  Google Scholar 

  • Proudfoot NJ, Furger A, Dye MJ (2002) Integrating mRNA processing with transcription. Cell 108(4):501–512

    Article  PubMed  CAS  Google Scholar 

  • Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45(8):1042–1052

    Article  PubMed  CAS  Google Scholar 

  • Rai AK, Kumar SP, Gupta SK, Gautam N, Singh NK, Sharma TR (2011) Functional complementation of rice blast resistance gene Pi-k h (Pi54) conferring resistance to diverse strains of Magnaporthe oryzae. J Plant Biochem Biotechnol 20:55–65

    Article  CAS  Google Scholar 

  • Reintanz B, Lehnen M, Reichelt M, Gershenzon J, Kowalczyk M, Sandberg G, Godde M, Uhl R, Palme K (2001) Bus, a Bushy Arabidopsis CYP79F1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell 13:351–367

    Article  PubMed  CAS  Google Scholar 

  • Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K (1999) The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci U S A 96:290–295

    Article  PubMed  CAS  Google Scholar 

  • Schmitz G, Tillmann E, Carriero F, Fiore C, Cellini F, Theres K (2002) The tomato Blind gene encodes a MYB transcription factor that controls the formation of lateral meristems. Proc Natl Acad Sci U S A 99:1064–1069

    Article  PubMed  CAS  Google Scholar 

  • Sentoku N, Sato Y, Kurata N, Ito Y, Kitano H, Matsuoka M (1999) Regional expression of the rice KN1-Type Homeobox Gene family during embryo, shoot and flower development. Plant Cell 11:1651–1663

    Article  PubMed  CAS  Google Scholar 

  • Singh AK, Ansari MW, Pareek A, Singla-Pareek SL (2008) Raising salinity tolerant rice: recent progress and future perspectives. Physiol Mol Biol Plants 14(1&2):137–154

    Article  CAS  Google Scholar 

  • Skirpan A, Culler AH, Gallavotti A, Jackson D, Cohen JD, McSteen P (2009) BARREN INFLORESCENCE2 interaction with ZmPIN1a suggests a role in auxin transport during maize inflorescence development. Plant Cell Physiol 50:652–657

    Article  PubMed  CAS  Google Scholar 

  • Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (2005) The decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17:746–759

    Article  PubMed  CAS  Google Scholar 

  • Song Y, Wang L, Xiong L (2009) Comprehensive expression profiling analysis of OsIAA gene family in developmental processes and in response to phytohormone and stress treatments. Planta 229:577–591. doi:10.1007/s00425-008-0853-7

    Article  PubMed  CAS  Google Scholar 

  • Sorefan K, Booker J, Haurogne K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, Leyser O (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17:1469–1474

    Article  PubMed  CAS  Google Scholar 

  • Squazzo SL, Costa PJ, Lindstrom DL, Kumer KE, Simic R, Jennings JL, Link AJ, Arndt KM, Hartzog GA (2002) The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J 21:1764–1774

    Article  PubMed  CAS  Google Scholar 

  • Stirnberg P, Chatfield SP, Leyser HM (1999) AXR1 acts after lateral bud formation to inhibit lateral bud growth in Arabidopsis. Plant Physiol 121:839–847

    Article  PubMed  CAS  Google Scholar 

  • Su YH, Liu YB, Zhang XS (2011) Auxin–cytokinin interaction regulates meristem development. Mol Plant 1–10. doi:10.1093/mp/ssr007

  • Svejstrup JQ (2004) The RNA polymerase II transcription cycle: cycling through chromatin. Biochim Biophys Acta 1677:64–73

    PubMed  CAS  Google Scholar 

  • Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33:513–520

    Article  PubMed  CAS  Google Scholar 

  • Talbert PB, Adler HT, Parks DW, Comai L (1995) The revoluta gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 121:2723–2735

    PubMed  CAS  Google Scholar 

  • Tantikanjana T, Yong JW, Letham DS, Griffith M, Hussain M, Ljung K, Sandberg G, Sundaresan V (2001) Control of axillary bud initiation and shoot architecture in Arabidopsis through the Supershoot gene. Genes Dev 15:1577–1588

    Article  PubMed  CAS  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Pan Y, Zhao X, Zhu L, Fu B, Li Z (2011) Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genomics 12:149

    Article  PubMed  Google Scholar 

  • Wang Y, Li J (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59:253–279

    Article  PubMed  CAS  Google Scholar 

  • Xiang J, Lin J, Tang D, Zhou B, Guo M, He R, Huang X, Zhao X, Liu X (2010) A DHHC-type zinc finger protein gene regulates shoot branching in Arabidopsis. Afr J Biotechnol 9:7759–7766

    CAS  Google Scholar 

  • Zou J, Zhang S, Zhang W, Li G, Chen Z, Zhai W, Zhao X, Pan X, Xie Q, Zhu L (2006) The rice high-tillering DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J 48:687–698

    Article  PubMed  CAS  Google Scholar 

  • Zubko E, Adams CJ, Machaekova I, Malbeck J, Scollan C, Meyer P (2002) Activation tagging identifies a gene from Petunia hybrida responsible for the production of active cytokinins in plants. Plant J 29:797–808

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to the Department of Biotechnology, Government of India for funding the project. The authors are thankful to Niraj Kumar of Xplorigen Technologies for help in making graphics. The first author is also thankful to the Ministry of Human Resources and Development (MHRD) for the financial aid provided.

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Correspondence to H. S. Dhaliwal.

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Supplementary Table 1

List of 116 differentially expressed genes in the OsTEF1 mutant (DOCX 24.3 kb)

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Paul, P., Awasthi, A., Rai, A.K. et al. Reduced tillering in Basmati rice T-DNA insertional mutant OsTEF1 associates with differential expression of stress related genes and transcription factors. Funct Integr Genomics 12, 291–304 (2012). https://doi.org/10.1007/s10142-012-0264-5

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