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Structural characterization, expression analysis and evolution of the red/far-red sensing photoreceptor gene, phytochrome C (PHYC), localized on the ‘B’ genome of hexaploid wheat (Triticum aestivum L.)

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Abstract

Phytochromes are a family of red/far-red light perceiving photoreceptors.The monocot phytochrome family is represented by three members, PHYA, PHYB and PHYC. We have isolated and characterized the first PHY gene member (TaPHYC) from common wheat, Triticum aestivum var. CPAN1676. It codes for a species of the photoreceptor, phyC, which is known to be light-stable in all plants analyzed so far. A sequence of 7.2 kb has been determined, which includes 3.42 kb of coding region.This is the second full-length PHYC gene sequenced from a monocot (first was from rice). TaPHYC gene shares structural similarities with the rice PHYC containing four exons and three introns in the coding region. The 5′ UTR is 1.0-kb-long and harbors an upstream open reading frame (URF) encoding 28 aa. Southern blot analysis of TaPHYC indicates that it represents single locus in the wheat genome, although the possibility of additional loci cannot be completely ruled out. Chromosomal localization using nullisomic–tetrasomic lines of Triticum aestivum var. Chinese Spring places TaPHYC on chromosome 4B. PHYC represents a constitutively expressed gene in all the organs tested and under light/dark conditions. However, PHYC was found to be developmentally regulated showing maximal expression in 3-day-old dark-grown seedlings, which declined thereafter. In silico analysis has also been done to compare TaPHYC gene with the partial sequences known from other wheat species and cultivars. The presence of a topoisomerase gene immediately downstream of the PHYC gene, both in rice and wheat genomes, presents yet another example of synteny in cereals and its possible significance has been discussed.

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Abbreviations

ESTs:

Expressed sequence tags

PHYC:

Phytochrome C (apoprotein)

PHYC :

Phytochrome C (gene)

phyC:

Phytochrome C (holoprotein)

RACE:

Rapid amplification of cDNA ends

RT-PCR:

Reverse transcriptase-polymerase chain reaction

UTRs:

Untranslated regions

References

  • Adams RA, Xinran L, Williams DS, Newton AC (2003) Differential spatial and temporal phosphorylation of the visual receptor, rhodopsin, at two primary phosphorylation sites in mice exposed to light. Biochem J 374:537–543

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, 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  CAS  PubMed  Google Scholar 

  • Basu D, Dehesh K, Schneider-Poetsch HJ, Harrington SE, McCouch SR, Quail PH (2000) Rice PHYC gene: structure, expression, map position and evolution. Plant Mol Biol 44:27–42

    Article  CAS  PubMed  Google Scholar 

  • Beevers L, Loveys B, Pearson JA, Wareing PF (1970) Phytochrome and hormonal expansion and greening of etiolated wheat leaves. Planta 90:286–294

    Article  CAS  Google Scholar 

  • Bennetzen JL, Freeling M (1993) Grasses as a single genetic system. Trends Genet 9:259–261

    Article  CAS  PubMed  Google Scholar 

  • Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386:414–417

    Article  CAS  PubMed  Google Scholar 

  • Bhoo S, Hirano T, Jeong HY, Lee JG, Furuya M, Song PS (1997) Phytochrome photochromism probed by site-directed mutations and chromophore esterification. J Am Chem Soc 119:11717–11718

    Google Scholar 

  • Bhoo SH, Davis SJ, Walker J, Karniol B, Vierstra RD (2001) Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 414:776–779

    Article  CAS  PubMed  Google Scholar 

  • Childs KL, Miller FR, Cordonnier-Pratt MM, Pratt LH, Morgan PW, Mullet JE (1997) The Sorghum photoperiod sensitivity gene Ma3, encodes a phytochrome B. Plant Physiol 113:611–619

    Google Scholar 

  • Clack T, Mathews S, Sharrock RA (1994) The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequence and expression of PHYD and PHYE. Plant Mol Biol 25:413–417

    Article  CAS  PubMed  Google Scholar 

  • Cowl JS, Hartley N, Xie DX, Whitelam GC, Murphy GP, Harberd NP (1994) The PHYC gene of Arabidopsis. Plant Physiol 106:813–814

    Article  CAS  PubMed  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19–21

    CAS  Google Scholar 

  • Feldman M, Segal G, Abbo S, Levy A, Vega JM (1997) Rapid elimination of low-copy DNA sequences in polyploid wheat: a possible mechanism for differentiation of homoeologous chromosomes. Genetics 147:1381–1387

    Google Scholar 

  • Franklin KA, Davis SJ, Stoddart WM, Vierstra RD, Whitelam GC (2003) Mutant analyses define multiple roles for phytochrome C in Arabidopsis photomorphogenesis. Plant Cell 15:1981–1989

    Article  CAS  PubMed  Google Scholar 

  • Geballe AP (1996) Translational control mediated by upstream AUG codons. In: Hershey JWB, Mathews MB, Sonenberg N (eds) Translational Control. Cold Spring Harbor Laboratory Press, Plainview, New York, p 173

    Google Scholar 

  • Goosey L, Palecanda L, Sharrock RA (1997) Differential pattern of expression of the Arabidopsis PHYB, PHYD, and PHYE phytochrome genes. Plant Physiol 115:959–969

    Article  CAS  PubMed  Google Scholar 

  • Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589–600

    Article  CAS  PubMed  Google Scholar 

  • Hartung F, Puchta H (2000) Molecular characterization of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Res 28:1548–1554

    Article  CAS  PubMed  Google Scholar 

  • Herdman M, Coursin T, Rippka R, Houmard J, Tandeau deMarsac N (2000) A new appraisal of the prokaryotic origin of eukaryotic phytochromes. J Mol Evol 51:205–213

    CAS  PubMed  Google Scholar 

  • Hershey HP, Barker RF, Idler KB, Lissemore JL, Quail PH (1985) Analysis of cloned cDNA and genomic sequences for phytochrome: complete amino acid sequences for two gene products expressed in etiolated Avena. Nucleic Acids Res 13:8543–8558

    CAS  PubMed  Google Scholar 

  • Jellings AL, Leese BM, Leech RM (1983) Location of a chromosomal control of ribulose bisphosphate carboxylase amounts in wheat. Mol Gen Genet 192:272–274

    Article  CAS  Google Scholar 

  • Karniol B, Vierstra RD (2003) The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with photobiological properties. Proc Natl Acad Sci USA 100:2807–2812

    Article  CAS  PubMed  Google Scholar 

  • Kato K, Nakamura W, Tabiki T, Miura H, Sawada S (2001) Detection of loci controlling seed dormancy on group 4 chromosomes of wheat and comparative mapping with rice and barley genomes. Theor Appl Genet 102:980–985

    Article  CAS  Google Scholar 

  • Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalysed by Spo11, a member of widely conserved protein family. Cell 88:375–384

    Google Scholar 

  • Khurana JP, Kulshreshtha R (2003) Diversity in higher plant phytochromes and their molecular characteristics. In: Souvenir: 2nd International Congress of Plant Physiology, New Delhi, pp 128–145

  • Khurana JP, Kochhar A, Tyagi AK (1998) Photosensory perception and signal transduction in higher plants–molecular genetic analysis. Crit Rev Plant Sci 17:465–539

    Article  CAS  Google Scholar 

  • Kircher S, Gil P, Kozma-Bognar L, Fejes E, Speth V, Husselstein-Muller T, Bauer D, Adam E, Schaefer E, Nagy F (2002) Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell 14:1541–1555

    Article  CAS  PubMed  Google Scholar 

  • Kulshreshtha R (2003) Isolation and characterization of phytochrome gene family from Triticum aestivum var. CPAN1676. PhD Thesis, University of Delhi

  • Kuspira J, Unrau J (1957) Genetic analysis of certain characters in common wheat using whole chromosome substitution lines. Can J Plant Sci 37:300–326

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor

    Google Scholar 

  • Mathews S, Sharrock RA (1996) The phytochrome gene family in grasses (Poaceae): a phylogeny and evidence that grasses have a subset of the loci found in dicot angiosperms. Mol Biol Evol 13:1141–1150

    CAS  PubMed  Google Scholar 

  • Mathews S, Sharrock RA (1997) Phytochrome gene diversity. Plant Cell Environ 20:666–671

    Article  CAS  Google Scholar 

  • Mathews S, Lavin M, Sharrock RA (1995) Evolution of the phytochrome gene family and its utility for phylogenetic analysis of angiosperms. Ann Missouri Bot Gard 82:296–321

    Google Scholar 

  • Millar AJ, McGrath RB, Chua NH (1994) Phytochrome phototransduction pathways. Annu Rev Genet 28:325–349

    Article  CAS  PubMed  Google Scholar 

  • Monte E, Alonso JM, Ecker J, Zhang Y, Li X, Young J, Austin-Phillips S, Quail P (2003) Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways. Plant Cell 15:1962–1980

    Article  CAS  PubMed  Google Scholar 

  • Nagy F, Kay SA, Chua NH (1988) Analysis of gene expression in transgenic plants. In: Gelvin SB, Schilperoort RA, Verma DPS (eds) Plant Molecular Biology Manual. Kluwer Academic Publishers, Dordrecht, p B4/1-B4/29

    Google Scholar 

  • Neuhaus G, Bowler C, Hiratsuka K, Yamagata H, Chua NH (1997) Phytochrome regulated repression of gene expression requires calcium and cGMP. EMBO J 15:2554–2564

    Article  Google Scholar 

  • Ogihara Y, Shimizu, H, Hasegawa K, Tsujimoto H, Sasakuma T (1994) Chromosome assignment of four photosynthesis-related genes and their variability in wheat species. Theor Appl Genet 88:383–394

    Article  CAS  Google Scholar 

  • Ozkan H, Levy A, Feldman M (2001) Allopolyploidy induced rapid genome evolution in the wheat (Aegilops–Triticum) group. Plant Cell 13:1735–1747

    Article  CAS  PubMed  Google Scholar 

  • Parks BM, Spalding EP (1999) Sequential and coordinated action of phytochromes A and B during Arabidopsis stem growth revealed by kinetic analysis. Proc Nat Acad Sci USA 96:14142–14146

    Article  CAS  PubMed  Google Scholar 

  • Paterson AH, Lin YR, Li Z, Schertz KF, Doebley JF, Pinson SRM, Liu SC, Stansel JW, Irvine JE (1995) Convergent domestication of cereal crops by independent mutations at corresponding gene loci. Science 269:1714–1717

    CAS  Google Scholar 

  • Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3:85–93

    Article  CAS  PubMed  Google Scholar 

  • Quail PH , Boylan MT, Parks BM, Short TW, Xu Y, Wagner D (1995) Phytochromes: photosensory perception and signal transduction. Science 268:675–680

    CAS  PubMed  Google Scholar 

  • Raghuram N, Sopory SK (1995) Evidence for some common signal transduction events for opposite regulation of nitrate reductase and phytochrome-I gene expression by light. Plant Mol Biol 29:25–35

    Article  CAS  PubMed  Google Scholar 

  • Reed JW, Nagatani A, Elich TD, Fagan M, Chory J (1994) Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiol 104:1139–1149

    CAS  PubMed  Google Scholar 

  • Robson PHR, McCormac AC, Irvine AS, Smith H (1996) Genetic engineering of harvest index in tobacco through overexpression of a phytochrome gene. Nat Biotech 14:995–998

    Article  CAS  Google Scholar 

  • Sandhu D, Gill KS (2002) Gene-containing regions of wheat and the other grass genomes. Plant Physiol 128:803–811

    Article  CAS  PubMed  Google Scholar 

  • Sandhu D, Champoux JA, Bondareva SN, Gill KS (2001) Identification and physical localization of useful genes and markers to a major gene-rich region on wheat group 1S chromosomes. Genetics 157:1735–1747

    CAS  PubMed  Google Scholar 

  • Santos M (1991) An improved method for the small scale preparation of bacteriophage DNA based on phage precipitation by zinc chloride. Nucleic Acids Res 19:5443

    PubMed  Google Scholar 

  • Schäfer E., Kunkel T, Frohnmeyer H (1997) Signal transduction in the photocontrol of chalcone synthase gene expression. Plant Cell Environ 20:722–727

    Google Scholar 

  • Shaked H, Kashkush K, Ozkan H, Feldman M, Levy A (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13:1749–1759

    Article  CAS  PubMed  Google Scholar 

  • Sharrock RA, Quail PH (1989) Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution and differential expression of a plant regulatory photoreceptor family. Genes Devel 3:1745–1757

    CAS  PubMed  Google Scholar 

  • Singh NK, Raghuvanshi S, Srivastava SK, Gaur A, Pal AK, Dalal V, Singh A, Ghazi IA, Bhargav A, Yadav M, Dixit A, Batra K, Gaikwad K, Sharma TR, Mohanty A, Bharti AK, Kapur A, Gupta V, Kumar D, Vij S, Vydianathan R, Khurana P, Sharma S, McCombie WR, Messing J, Wing R, Sasaki T, Khurana P, Mohapatra T, Khurana JP, Tyagi AK (2004) Sequence analysis of the long arm of rice chromosome 11 for rice-wheat synteny. Funct Integr Genomics 4:102–117

    Article  CAS  PubMed  Google Scholar 

  • Smith H (1995) Physiological and ecological functions within the phytochrome family. Annu Rev Plant Physiol Plant Mol Biol 46:289–315

    CAS  Google Scholar 

  • Smith H (2000) Phytochrome and light signal perception by plants—an emerging synthesis. Nature 407:585–591

    Article  CAS  PubMed  Google Scholar 

  • Smith H, Whitelam GC (1997) The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant Cell Environ 20:840–844

    Google Scholar 

  • Somers DE, Quail PH (1995a) Phytochrome-mediated light regulation of PHYA- and PHYB-GUS transgenes in Arabidopsis thaliana seedlings. Plant Physiol 107:523–534

    CAS  Google Scholar 

  • Somers DE, Quail PH (1995b) Temporal and spatial expression patterns of PHYA and PHYB genes in Arabidopsis. Plant J 7:413–427

    Article  CAS  Google Scholar 

  • Somers DE, Devlin PF, Kay SA (1998) Phytochromes and cryptochromes in entrainment of the Arabidopsis circadian clock. Science 282:1488–1490

    Article  CAS  PubMed  Google Scholar 

  • Sommer D, Wells TA, Song PS (1996) A possible tyrosine phosphorylation in phytochrome A. FEBS Lett 393:161–166

    Article  CAS  PubMed  Google Scholar 

  • Song KM, Lu P, Osborn TC (1995) Rapid genome change in synthetic polyploids of Brassica and its implications for polyploidy evolution. Proc Natl Acad Sci USA 92:7719–7723

    CAS  PubMed  Google Scholar 

  • Sopory SK, Munshi M (1998) Protein kinases and phosphatases and their role in cellular signaling in plants. Crit Rev Plant Sci 17:245–318

    Article  CAS  Google Scholar 

  • Sorrells ME, Rota ML, Bermudez-Kandianis CE, Greene RA, Kantety R, Munkvold JD, Mahmoud MA, Ma X, Gustafson PJ, Qi LL, Echalier B, Gill BS, Matthews DE, Lazo GR, Chao S, Anderson OD, Edwards H, Linkiewicz AM, Dubcovsky J, Akhunov ED, Dvorak J, Zhang D, Nguyen HT, Peng J, Lapitan NLV, Gonzalez-Hernandez JL, Anderson JA, Hossain K, Kalavacharla V, Kianian SF, Choi D-W, Close TJ, Dilbirligi M, Gill KS, Steber C, Walker-Simmons MK, McGuire PE, Qualset CO (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827

    CAS  PubMed  Google Scholar 

  • Van Deynze AE, Nelson JC, Yglesias ES, Harrington SE, Braga DP, McCouch SR, Sorrells ME (1995) Comparative mapping in grasses. Wheat relationships. Mol Gen Genet 248:744–754

    PubMed  Google Scholar 

  • Wicker T, Yahiaoui N, Guyot R, Schlagenhauf E, Liu Z-D, Dubcovsky J, Keller B (2003) Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and Am genomes of wheat. Plant Cell 15:1186–1197

    Article  CAS  PubMed  Google Scholar 

  • Wu SH, Lagarias JC (2000) Defining the bilin-lyase domain: lessons from the extended phytochrome superfamily. Biochemistry 39:13487–13495

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Cheong H, Friedrichsen D, Zhao Y, Hu J, Mora-Garcia S, Chory J (2002) A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development. Proc Natl Acad Sci USA 99:10191–10196

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Dr. Peter H. Quail, USDA Plant Gene Expression Center, Albany, California, USA, for providing the clone of the oat PHYA gene, and Dr. Bikram S. Gill, Kansas State University, USA, for providing seeds of nullisomic-tetrasomic lines of Chinese Spring wheat. RK and NK acknowledge the award of Senior Research Fellowship by the University Grants Commission and the Council of Scientific and Industrial Research, New Delhi, respectively. This research work was financially supported by the Department of Biotechnology of the Government of India and the University Grants Commission, New Delhi. This work was carried out in compliance with the current laws governing genetic experimentation in India.

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Kulshreshtha, R., Kumar, N., Balyan, H.S. et al. Structural characterization, expression analysis and evolution of the red/far-red sensing photoreceptor gene, phytochrome C (PHYC), localized on the ‘B’ genome of hexaploid wheat (Triticum aestivum L.). Planta 221, 675–689 (2005). https://doi.org/10.1007/s00425-004-1473-5

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