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Divergent functions of orthologous NAC transcription factors in wheat and rice

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Abstract

The wheat GPC-B1 gene located on chromosome 6B is an early regulator of senescence and affects remobilization of protein and minerals to the grain. GPC-B1 is a NAC transcription factor and has a paralogous copy on chromosome 2B in wheat, GPC-B2. The closest rice homolog to both wheat GPC genes is Os07g37920 which is located on rice chromosome 7 and is colinear with GPC-B2. Since rice is a diploid species with a sequenced genome, we initiated the study of Os07g37920 to develop a simpler model to study senescence and mineral remobilization in cereals. We developed eleven independent RNA interference transgenic rice lines (Os07g37920-RNAi) and 10 over-expressing transgenic lines (Os07g37920-OE), but none of them showed differences in senescence. Transgenic Os07g37920-RNAi rice plants had reduced proportions of viable pollen grains and were male-sterile, but were able to produce seeds by cross pollination. Analysis of the flower morphology of the transgenic rice plants showed that anthers failed to dehisce. Transgenic Os07g37920-OE lines showed no sterility or anther dehiscence problems. Os07g37920 transcript levels were higher in stamens compared to leaves and significantly reduced in the transgenic Os07g37920-RNAi plants. Wheat GPC genes showed the opposite transcription profile (higher transcript levels in leaves than in flowers) and plants carrying knock-out mutations of all GPC-1 and GPC-2 genes exhibited delayed senescence but normal anther dehiscence and fertility. These results indicate a functional divergence of the homologous wheat and rice NAC genes and suggest the need for separate studies of the function and targets of these transcription factors in wheat and rice.

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References

  • Alvarado V, Tag A, Thomas T (2011) A cis regulatory element in the TAPNAC promoter directs tapetal gene expression. Plant Mol Biol 75:129–139

    Google Scholar 

  • Balazadeh S, Riaño-Pachón DM, Mueller-Roeber B (2008) Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol 10:63–75. doi:10.1111/j.1438-8677.2008.00088.x

    Article  PubMed  Google Scholar 

  • Balazadeh S, Kwasniewski M, Caldana C, Mehrnia M, Zanor MI, Xue G-P, Mueller-Roeber B (2011) ORS1, an H2O2-Responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol Plant 4:346–360. doi:10.1093/mp/ssq080

    Article  PubMed  CAS  Google Scholar 

  • Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, Zhang CJ, Morris K, Jenner C, Jackson S, Thomas B, Tabrett A, Legaie R, Moore JD, Wild DL, Ott S, Rand D, Beynon J, Denby K, Mead A, Buchanan-Wollaston V (2011) High-resolution temporal profiling of transcripts during arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23:873–894. doi:10.1105/tpc.111.083345

    Article  PubMed  CAS  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signaling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585

    Article  PubMed  CAS  Google Scholar 

  • Cantu D, Pearce SP, Distelfeld A, Christiansen MW, Uauy C, Akhunov E, Fahima T, Dubcovsky J (2011) Effect of the down-regulation of the high Grain Protein Content (GPC) genes on the wheat transcriptome during monocarpic senescence. BMC Genomics 12:492

    Article  PubMed  CAS  Google Scholar 

  • Conley EJ, Nduati V, Gonzalez-Hernandez JL, Mesfin A, Trudeau-Spanjers M, Chao S, Lazo GR, Hummel DD, Anderson OD, Qi LL, Gill BS, Echalier B, Linkiewicz AM, Dubcovsky J, Akhunov ED, Dyorak J, Peng JH, Lapitan NLV, Pathan MS, Nguyen HT, Ma XF, Miftahudin, Gustafson JP, Greene RA, Sorrells ME, Hossain G, Kalavacharla V, Kianian SF, Sidhu K, Dijbirligi M, Gill KS, Choi DW, Fenton RD, Close TJ, McGuire PE, Qualset CO, Anderson JA (2004) A 2600-locus chromosome bin map of wheat homoeologous group 2 reveals interstitial gene-rich islands and colinearity with rice. Genetics 168:625–637

    Article  PubMed  CAS  Google Scholar 

  • Distelfeld A, Cakmak I, Peleg Z, Ozturk L, Yazici AM, Budak H, Saranga Y, Fahima T (2007) Multiple QTL-effects of wheat Gpc-B1 locus on grain protein and micronutrient concentrations. Physiol Plantarum 129:635–643. doi:10.1111/j.1399-3054.2006.00841.x

    Article  CAS  Google Scholar 

  • Distelfeld A, Tranquilli G, Li C, Yan L, Dubcovsky J (2009) Genetic and molecular characterization of the VRN2 loci in tetraploid wheat. Plant Physiol 149:245–257

    Article  PubMed  CAS  Google Scholar 

  • Ernst HA, Olsen AN, Skriver K, Larsen S, Lo Leggio L (2004) Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep 5:297–303

    Article  PubMed  CAS  Google Scholar 

  • Fang YJ, You J, Xie KB, Xie WB, Xiong LZ (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics 280:547–563

    Article  PubMed  CAS  Google Scholar 

  • Guo YF, Gan SS (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27:521–549

    Article  CAS  Google Scholar 

  • Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53:927–937. doi:10.1093/jexbot/53.370.927

    Article  PubMed  Google Scholar 

  • Joppa L, Cantrell R (1990) Chromosomal location of genes for grain protein content in wild tetraploid wheat. Crop Sci 30:1059–1064

    Article  CAS  Google Scholar 

  • Kariya K (1989) Sterility caused by cooling treatment at the flowering stage in rice plants. Jpn J Crop Sci 58:96–102

    Article  Google Scholar 

  • Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG (2009) Trifurcate feed-forward regulation of age-dependent cell death involving mir164 in Arabidopsis. Science 323:1053–1057. doi:10.1126/science.1166386

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \(2^{-\Delta\Delta {C_{\text T}}}\) method. Methods 25:402–408

  • Matile P, Hortensteiner S, Thomas H, Krautler B (1996) Chlorophyll breakdown in senescent leaves. Plant Physiol 112:1403–1409. doi:10.1104/pp.112.4.1403

    PubMed  CAS  Google Scholar 

  • Mester D, Ronin Y, Minkov D, Nevo E, Korol A (2003) Constructing large-scale genetic maps using an evolutionary strategy algorithm. Genetics 165:2269–2282

    PubMed  CAS  Google Scholar 

  • Miki D, Itoh R, Shimamoto K (2005) RNA silencing of single and multiple members in a gene family of rice. Plant Physiol 138:1903–1913

    Article  PubMed  CAS  Google Scholar 

  • Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44. doi:10.1016/j.gene.2010.06.008

    Article  PubMed  CAS  Google Scholar 

  • Olsen AN, Ernst HA, Lo Leggio L, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    Article  PubMed  CAS  Google Scholar 

  • Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239

    Article  PubMed  CAS  Google Scholar 

  • Peleg Z, Saranga Y, Suprunova T, Ronin Y, Roder MS, Kilian A, Korol AB, Fahima T (2008) High-density genetic map of durum wheat x wild emmer wheat based on SSR and DArT markers. Theor Appl Genet 117:103–115. doi:10.1007/s00122-008-0756-9

    Article  PubMed  CAS  Google Scholar 

  • Rohila JS, Chen M, Cerny R, Fromm ME (2004) Improved tandem affinity purification tag and methods for isolation of protein heterocomplexes from plants. Plant J 38:172–181

    Article  PubMed  CAS  Google Scholar 

  • Sablowski RWM, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103

    Article  PubMed  CAS  Google Scholar 

  • Slade A, Fuerstenberg S, Loeffler D, Steine M, Facciotti D (2005) A reverse genetic, non transgenic approach to wheat crop improvement by TILLING. Nat Biotechnol 23:75–81

    Article  PubMed  CAS  Google Scholar 

  • Sourdille P, Singh S, Cadalen T, Brown-Guedira GL, Gay G, Qi L, Gill BS, Dufour P, Murigneux A, Bernard M (2004) Microsatellite-based deletion bin system for the establishment of genetic-physical map relationships in wheat (Triticum aestivum L.). Funct Integr Genomics 4:12–25

    Article  PubMed  CAS  Google Scholar 

  • Sperotto R, Ricachenevsky F, Duarte G, Boff T, Lopes K, Sperb E, Grusak M, Fett J (2009) Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230:985–1002

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis software (MEGA). Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ, Clustal W (1994) Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Uauy C, Brevis JC, Dubcovsky J (2006a) The high grain protein content gene Gpc-B1 accelerates senescence and has pleiotropic effects on protein content in wheat. J Exp Bot 57:2785–2794

    Article  PubMed  CAS  Google Scholar 

  • Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006b) A NAC gene regulating senescence improves grain protein, zinc and irons content in wheat. Science 314:1298–1300

    Article  PubMed  CAS  Google Scholar 

  • Uauy C, Paraiso F, Colasuonno P, Tran RK, Tsai H, Berardi S, Comai L, Dubcovsky J (2009) A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol 9:115. doi:10.1186/1471-2229-9-115

    Article  PubMed  Google Scholar 

  • Yoshida S (2003) Molecular regulation of leaf senescence. Curr Opin Plant Biol 6:79–84

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This project was supported by the National Research Initiative Competitive Grant no. 2008-35318-18654 from the USDA National Institute of Food and Agriculture and by the United States—Israel Binational Science Foundation (BSF) grant number 2007194. The authors would like to thank Dayna Loeffler, Michael N. Steine, Anna Amen and Cate McGuire of Arcadia Biosciences for mutation discovery and Cindy Miguita and Mei-Yee Lau of UC Davis for excellent technical assistance.

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Correspondence to Jorge Dubcovsky.

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Distelfeld, A., Pearce, S.P., Avni, R. et al. Divergent functions of orthologous NAC transcription factors in wheat and rice. Plant Mol Biol 78, 515–524 (2012). https://doi.org/10.1007/s11103-012-9881-6

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