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TaNF-YB3 is involved in the regulation of photosynthesis genes in Triticum aestivum

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Abstract

Nuclear factor Y (NF-Y) transcription factor is a heterotrimer comprised of three subunits: NF-YA, NF-YB and NF-YC. Each of the three subunits in plants is encoded by multiple genes with differential expression profiles, implying the functional specialisation of NF-Y subunit members in plants. In this study, we investigated the roles of NF-YB members in the light-mediated regulation of photosynthesis genes. We identified two NF-YB members from Triticum aestivum (TaNF-YB3 & 7) which were markedly upregulated by light in the leaves and seedling shoots using quantitative RT-PCR. A genome-wide coexpression analysis of multiple Affymetrix Wheat Genome Array datasets revealed that TaNF-YB3-coexpressed transcripts were highly enriched with the Gene Ontology term photosynthesis. Transgenic wheat lines constitutively overexpressing TaNF-YB3 had a significant increase in the leaf chlorophyll content, photosynthesis rate and early growth rate. Quantitative RT-PCR analysis showed that the expression levels of a number of TaNF-YB3-coexpressed transcripts were elevated in the transgenic wheat lines. The mRNA level of TaGluTR encoding glutamyl-tRNA reductase, which catalyses the rate-limiting step of the chlorophyll biosynthesis pathway, was significantly increased in the leaves of the transgenic wheat. Significant increases in the expression level in the transgenic plant leaves were also observed for four photosynthetic apparatus genes encoding chlorophyll a/b-binding proteins (Lhca4 and Lhcb4) and photosystem I reaction centre subunits (subunit K and subunit N), as well as for a gene coding for chloroplast ATP synthase γ subunit. These results indicate that TaNF-YB3 is involved in the positive regulation of a number of photosynthesis genes in wheat.

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References

  • Bae G, Choi G (2008) Decoding of light signals by plant phytochromes and their interacting proteins. Annu Rev Plant Biol 59:281–311

    Article  PubMed  CAS  Google Scholar 

  • Cai X, Ballif J, Endo S, Davis E, Liang M, Chen D, DeWald D, Kreps J, Zhu T, Wu Y (2007) A putative CCAAT-binding transcription factor is a regulator of flowering timing in Arabidopsis. Plant Physiol 145:98–105

    Article  PubMed  CAS  Google Scholar 

  • Casal JJ, Yanovsky MJ (2005) Regulation of gene expression by light. Int J Dev Biol 49:501–511

    Article  PubMed  CAS  Google Scholar 

  • Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38:87–117

    Article  PubMed  CAS  Google Scholar 

  • Chen NZ, Zhang XQ, Wei PC, Chen QJ, Ren F, Chen J, Wang XC (2007) AtHAP3b plays a crucial role in the regulation of flowering time in Arabidopsis during osmotic stress. J Biochem Mol Biol 40:1083–1089

    Article  PubMed  CAS  Google Scholar 

  • Christensen AH, Quail PH (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res 5:213–218

    Article  PubMed  CAS  Google Scholar 

  • Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45

    Article  PubMed  CAS  Google Scholar 

  • Clément C, Mischler P, Burrus M, Audran J-C (1997) Characteristics of the photosynthetic apparatus and CO2-fixation in the flower bud of Lilium. II. Anther. Int J Plant Sci 158:801–810

    Article  Google Scholar 

  • Crismani W, Baumann U, Sutton T, Shirley N, Webster T, Spangenberg G, Langridge P, Able JA (2006) Microarray expression analysis of meiosis and microsporogenesis in hexaploid bread wheat. BMC Genomics 7:267

    Article  PubMed  Google Scholar 

  • Devlin PF, Christie JM, Terry MJ (2007) Many hands make light work. J Exp Bot 58:3071–3077

    Article  PubMed  CAS  Google Scholar 

  • Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Boil 12:178–184

    Article  CAS  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) AgriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38(Suppl_2):W64–W70

    Article  PubMed  CAS  Google Scholar 

  • Goslings D, Meskauskiene R, Kim C, Lee KP, Nater M, Apel M (2004) Concurrent interactions of heme and FLU with Glu tRNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark- and light-grown Arabidopsis plants. Plant J 40:957–967

    Article  PubMed  CAS  Google Scholar 

  • Gusmaroli G, Tonelli C, Mantovani R (2001) Regulation of the CCAAT-binding NF-Y subunits in Arabidopsis thaliana. Gene 264:173–185

    Article  PubMed  CAS  Google Scholar 

  • Gusmaroli G, Tonelli C, Mantovani R (2002) Regulation of novel members of the Arabidopsis thaliana CCAAT-binding nuclear factor Y subunits. Gene 283:41–48

    Article  PubMed  CAS  Google Scholar 

  • Ilag LL, Kumar AM, Soll D (1994) Light regulation of chlorophyll biosynthesis at the level of 5-aminolevulinate formation in Arabidopsis. Plant Cell 6:265–275

    Article  PubMed  CAS  Google Scholar 

  • Inohara N, Iwamoto A, Moriyama Y, Shimomura S, Maeda M, Futai M (1991) Two genes, atpC1 and atpC2, for the γ subunit of Arabidopsis thaliana chloroplast ATP synthase. J Biol Chem 266:7333–7338

    PubMed  CAS  Google Scholar 

  • Jiao Y, Ma L, Strickland E, Deng XW (2005) Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. Plant Cell 17:3239–3256

    Article  PubMed  CAS  Google Scholar 

  • Jordan MC, Somers DJ, Banks TW (2007) Identifying regions of the wheat genome controlling seed development by mapping expression quantitative trait loci. Plant Biotech J 5:442–453

    Article  CAS  Google Scholar 

  • Kumimoto RW, Adam L, Hymus GJ, Repetti PP, Reuber TL, Marion CM, Hempel FD, Ratcliffe OJ (2008) The nuclear factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis. Planta 228:709–723

    Article  PubMed  CAS  Google Scholar 

  • Kumimoto RW, Zhang Y, Siefers N, Holt BF 3rd (2010) NF-YC3, NF-YC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. Plant J 63:379–391

    CAS  Google Scholar 

  • Kusnetsov V, Landsberger M, Meurer J, Oelmuller R (1999) The assembly of the CAAT-box binding complex at a photosynthesis gene promoter is regulated by light, cytokinin, and the stage of the plastids. J Biol Chem 274:36009–36014

    Article  PubMed  CAS  Google Scholar 

  • Lefebvre S, Lawson T, Fryer M, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 138:451–460

    Article  PubMed  CAS  Google Scholar 

  • Li QH, Yang HQ (2007) Cryptochrome signaling in plants. Photochem Photobiol 83:94–101

    Article  PubMed  CAS  Google Scholar 

  • Li WX, Oono Y, Zhu J, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251

    Article  PubMed  CAS  Google Scholar 

  • Liu J-X, Howell SH (2010) bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell 22:782–796

    Article  PubMed  CAS  Google Scholar 

  • Lotan T, Ohto M, Yee KM, West MA, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    Article  PubMed  CAS  Google Scholar 

  • Mantovani R (1998) A survey of 178 NF-Y binding CCAAT boxes. Nucleic Acids Res 26:1135–1143

    Article  PubMed  CAS  Google Scholar 

  • Mantovani R (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene 239:15–27

    Article  PubMed  CAS  Google Scholar 

  • Matsuoka M, Kano-Murakami Y, Tanaka Y, Ozeki Y, Yamamoto N (1988) Classification and nucleotide sequence of cDNA encoding the small subunit of ribulose-1,5-bisphosphate carboxylase from rice. Plant Cell Physiol 29:1015–1022

    CAS  Google Scholar 

  • Mir-Mahmoodi T, Soleimanzadeh H (2009) Relationship between rapid canopy closure and grain yield in wheat. Asian J Plant Sci 8:250–253

    Article  Google Scholar 

  • Miyoshi K, Ito Y, Serizawa A, Kurata N (2003) OsHAP3 genes regulate chloroplast biogenesis in rice. Plant J 36:532–540

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki M, Tanaka R, Grimm B, Masuda T, Moulin M, Smith AG, Tanaka A, Terry MJ (2010) The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci. doi:10.1016/j.tplants.2010.05.012

    PubMed  Google Scholar 

  • Mott IW, Wang RRC (2007) Comparative transcriptome analysis of salt-tolerant wheat germplasm lines using wheat genome arrays. Plant Sci 173:327–339

    Article  CAS  Google Scholar 

  • Nogaj LA, Srivastava A, van Lis R, Beale SI (2005) Cellular levels of glutamyl-tRNA reductase and glutamate-1-semialdehyde aminotransferase do not control chlorophyll synthesis in Chlamydomonas reinhardtii. Plant Physiol 139:389–396

    Article  PubMed  CAS  Google Scholar 

  • Parkinson H, Kapushesky M, Kolesnikov N, Rustici G, Shojatalab M, Abeygunawardena N, Berube H, Dylag M, Emam I, Farne A, Holloway E, Lukk M, Malone J, Mani R, Pilicheva E, Rayner TF, Rezwan F, Sharma A, Williams E, Bradley XZ, Adamusiak T, Brandizi M, Burdett T, Coulson R, Krestyaninova M, Kurnosov P, Maguire E, Neogi SG, Rocca-Serra P, Sansone SA, Sklyar N, Zhao M, Sarkans U, Brazma A (2009) ArrayExpress update—from an archive of functional genomics experiments to the atlas of gene expression. Nucl Acids Res 37:D868–D872

    Article  PubMed  CAS  Google Scholar 

  • Patel M, Johnson JS, Brettell RIS, Jacobsen J, Xue GP (2000) Transgenic barley expressing a fungal xylanase gene in the endosperm of the developing grains. Mol Breed 6:113–124

    Article  CAS  Google Scholar 

  • Pellegrineschi A, Noguera LM, Skovmand B, Brito RM, Velazquez L, Salgado MM, Hernandez R, Warburton M, Hoisington D (2002) Identification of highly transformable wheat genotypes for mass production of fertile transgenic plants. Genome 45:421–430

    Article  PubMed  CAS  Google Scholar 

  • Peter E, Grimm B (2009) GUN4 is required for posttranslational control of plant tetrapyrrole biosynthesis. Mol Plant 2:1198–1210

    Article  PubMed  CAS  Google Scholar 

  • Qin D, Wu H, Peng H, Yao Y, Ni Z, Li Z, Zhou C, Sun Q (2008) Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using wheat genome array. BMC Genomics 9:432

    Article  PubMed  Google Scholar 

  • Reynolds M, Foulkes MJ, Slafer GA, Berry P, Parry MAJ, Snape JW, Angus WJ (2009) Raising yield potential in wheat. J Exp Bot 60:1899–1918

    Article  PubMed  CAS  Google Scholar 

  • Richards RA (2000) Selectable traits to increase crop photosynthesis and yield of grain crops. J Exp Bot 51:447–458

    Article  PubMed  CAS  Google Scholar 

  • Siefers N, Dang KK, Kumimoto RW, Bynum WE, Tayrose G, Holt BF 3rd (2009) Tissue-specific expression patterns of Arabidopsis NF-Y transcription factors suggest potential for extensive combinatorial complexity. Plant Physiol 149:625–641

    Article  PubMed  CAS  Google Scholar 

  • Soltani A, Galeshi S (2002) Importance of rapid canopy closure for wheat production in a temperate sub-humid environment: experimentation and simulation. Field Crop Res 77:17–30

    Article  Google Scholar 

  • Stephenson TJ, McIntyre CL, Collet C, Xue GP (2007) Genome-wide identification and expression analysis of the NF-Y family of transcription factors in Triticum aestivum. Plant Mol Biol 65:77–92

    Article  PubMed  CAS  Google Scholar 

  • Stephenson TJ, McIntyre CL, Collet C, Xue GP (2010) TaNF-YC11, one of the light-upregulated NF-YC members in Triticum aestivum, is co-regulated with photosynthesis-related genes. Funct Integr Genomics 10:265–276

    Article  PubMed  CAS  Google Scholar 

  • Tanaka A, Makino A (2009) Photosynthetic research in plant science. Plant Cell Physiol 50:681–683

    Article  PubMed  CAS  Google Scholar 

  • Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:248–255

    Article  PubMed  CAS  Google Scholar 

  • Testa A, Donati G, Yan P, Romani F, Huang TH, Vigano MA, Mantovani R (2005) Chromatin immunoprecipitation (ChIP) on chip experiments uncover a widespread distribution of NF-Y binding CCAAT sites outside of core promoters. J Biol Chem 280:13606–13615

    Article  PubMed  CAS  Google Scholar 

  • Thirumurugan T, Ito Y, Kubo T, Serizawa A, Kurata N (2008) Identification, characterization and interaction of HAP family genes in rice. Mol Genet Genomics 279:279–289

    Article  PubMed  CAS  Google Scholar 

  • Vickers CE, Xue GP, Gresshoff PM (2003) A synthetic xylanase as reporter in plants. Plant Cell Rep 22:135–140

    Article  PubMed  CAS  Google Scholar 

  • Wan Y, Poole RL, Huttly AK, Toscano-Underwood C, Feeney K, Welham S, Gooding MJ, Mills C, Edwards KJ, Shewry PR, Mitchell RA (2008) Transcriptome analysis of grain development in hexaploid wheat. BMC Genomics 9:121

    Article  PubMed  Google Scholar 

  • Warpeha KM, Upadhyay S, Yeh J, Adamiak J, Hawkins SI, Lapik YR, Anderson MB, Kaufman LS (2007) The GCR1, GPA1, PRN1, NF-Y signal chain mediates both blue light and abscisic acid responses in Arabidopsis. Plant Physiol 143:1590–1600

    Article  PubMed  CAS  Google Scholar 

  • Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, Coupland G (2006) CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 18:2971–2984

    Article  PubMed  CAS  Google Scholar 

  • Xue GP, Loveridge CW (2004) HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. Plant J 37:326–339

    Article  PubMed  CAS  Google Scholar 

  • Xue GP, Bower NI, McIntyre CL, Riding GA, Kazan K, Shorter R (2006) TaNAC69 from the NAC superfamily of transcription factors is up-regulated by abiotic stresses in wheat and recognises two consensus DNA-binding sequences. Func Plant Biol 33:43–57

    Article  CAS  Google Scholar 

  • Xue GP, McIntyre CL, Glassop D, Shorter R (2008a) Use of expression analysis to dissect alterations in carbohydrate metabolism in wheat leaves during drought stress. Plant Mol Biol 67:197–214

    Article  PubMed  CAS  Google Scholar 

  • Xue GP, McIntyre CL, Jenkins CL, Glassop D, van Herwaarden AF, Shorter R (2008b) Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiol 146:441–454

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto A, Kagaya Y, Toyoshima R, Kagaya M, Takeda S, Hattori T (2009) Arabidopsis NF-YB subunits LEC1 and LEC1-LIKE activate transcription by interacting with seed-specific ABRE-binding factors. Plant J 58:843–856

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Forno D, Cock J (1971) Laboratory manual for physiological studies of rice, 2nd edn. International Rice Research Institute, Los Banos

    Google Scholar 

  • Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Australian Grains Research & Development Corporation. We would like to thank Dr. Maryse Bourgault for her help in the measurement of photosynthetic rate.

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Correspondence to Gang-Ping Xue.

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Stephenson, T.J., McIntyre, C.L., Collet, C. et al. TaNF-YB3 is involved in the regulation of photosynthesis genes in Triticum aestivum. Funct Integr Genomics 11, 327–340 (2011). https://doi.org/10.1007/s10142-011-0212-9

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