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.
Similar content being viewed by others
References
Bae G, Choi G (2008) Decoding of light signals by plant phytochromes and their interacting proteins. Annu Rev Plant Biol 59:281–311
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
Casal JJ, Yanovsky MJ (2005) Regulation of gene expression by light. Int J Dev Biol 49:501–511
Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38:87–117
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
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
Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45
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
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
Devlin PF, Christie JM, Terry MJ (2007) Many hands make light work. J Exp Bot 58:3071–3077
Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Boil 12:178–184
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
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
Gusmaroli G, Tonelli C, Mantovani R (2001) Regulation of the CCAAT-binding NF-Y subunits in Arabidopsis thaliana. Gene 264:173–185
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
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
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
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
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
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
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
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
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
Li QH, Yang HQ (2007) Cryptochrome signaling in plants. Photochem Photobiol 83:94–101
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
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
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
Mantovani R (1998) A survey of 178 NF-Y binding CCAAT boxes. Nucleic Acids Res 26:1135–1143
Mantovani R (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene 239:15–27
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
Mir-Mahmoodi T, Soleimanzadeh H (2009) Relationship between rapid canopy closure and grain yield in wheat. Asian J Plant Sci 8:250–253
Miyoshi K, Ito Y, Serizawa A, Kurata N (2003) OsHAP3 genes regulate chloroplast biogenesis in rice. Plant J 36:532–540
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
Mott IW, Wang RRC (2007) Comparative transcriptome analysis of salt-tolerant wheat germplasm lines using wheat genome arrays. Plant Sci 173:327–339
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
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
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
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
Peter E, Grimm B (2009) GUN4 is required for posttranslational control of plant tetrapyrrole biosynthesis. Mol Plant 2:1198–1210
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
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
Richards RA (2000) Selectable traits to increase crop photosynthesis and yield of grain crops. J Exp Bot 51:447–458
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
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
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
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
Tanaka A, Makino A (2009) Photosynthetic research in plant science. Plant Cell Physiol 50:681–683
Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:248–255
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
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
Vickers CE, Xue GP, Gresshoff PM (2003) A synthetic xylanase as reporter in plants. Plant Cell Rep 22:135–140
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
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
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
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
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
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
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
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
Yoshida S, Forno D, Cock J (1971) Laboratory manual for physiological studies of rice, 2nd edn. International Rice Research Institute, Los Banos
Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261
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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 63 kb)
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-011-0212-9