Skip to main content
SpringerLink
Log in

Light-regulated overexpression of an Arabidopsis phytochrome A gene in rice alters plant architecture and increases grain yield

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The phytochromes are a family of red/far-red light absorbing photoreceptors that control plant developmental and metabolic processes in response to changes in the light environment. We report here the overexpression of Arabidopsis thaliana PHYTOCHROME A (PHYA) gene in a commercially important indica rice variety (Oryza sativa L. Pusa Basmati-1). The expression of the transgene was driven by the light-regulated and tissue-specific rice rbcS promoter. Several independent homozygous sixth generation (T5) transgenic lines were characterized and shown to accumulate relatively high levels of PHYA protein in the light. Under both far-red and red light, PHYA-overexpressing lines showed inhibition of the coleoptile extension in comparison to non-transgenic seedlings. Furthermore, compared with non-transgenic rice plants, mature transgenic plants showed significant reduction in plant height, internode length and internode diameter (including differences in cell size and number), and produced an increased number of panicles per plant. Under greenhouse conditions, rice grain yield was 6–21% higher in three PHYA-overexpressing lines than in non-transgenic plants. These results demonstrate the potential of manipulating light signal-transduction pathways to minimize the problems of lodging in basmati/aromatic rice and to enhance grain productivity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

FR:

Far-red light

PBNT:

Pusa Basmati-1

Pfr:

Far-red-absorbing form of phytochrome

PHYA :

Phytochrome A gene

phyA :

Phytochrome A mutant

PHYA:

Phytochrome A apoprotein

phyA:

Phytochrome A holoprotein

PHYB :

Phytochrome B gene

Pr:

Red-absorbing form of phytochrome

R:

Red light

R:FR:

Quantum ratio of red to far-red light

References

  • Aggarwal RK, Shenoy V, Ramadevi J, Rajkumar R, Singh L (2002) Molecular characterization of some Indian Basmati and other elite rice genotypes using fluorescent-AFLP. Theor Appl Genet 105:680–690

    Article  PubMed  CAS  Google Scholar 

  • Ballare CL (2001) Arabidopsis mutants and other model systems in plant physiological ecology. Trends Plant Sci 6:99

    Article  PubMed  CAS  Google Scholar 

  • Boccalandro HE, Ploschuk EL, Yanovsky MJ, Sanchez RA, Gatz C, Casal JJ (2003) Increased phytochrome B alleviates density effects on tuber yield of field potato crops. Plant Physiol 133:1539–1546

    Article  PubMed  CAS  Google Scholar 

  • Boylan MT, Quail PH (1989) Oat phytochrome is biologically active in transgenic tomatoes. Plant Cell 1:765–773

    Article  PubMed  CAS  Google Scholar 

  • Boylan MT, Quail PH (1991) Phytochrome A overexpression inhibits hypocotyl elongation in transgenic Arabidopsis. Proc Natl Acad Sci USA 88:10806–10810

    Article  PubMed  CAS  Google Scholar 

  • Casal JJ (1996) Phytochrome A enhances the promotion of hypocotyl growth caused by reductions in levels of phytochrome B in its far-red-light-absorbing form in light-grown Arabidopsis thaliana. Plant Physiol 112:965–973

    Article  PubMed  CAS  Google Scholar 

  • Clack T, Mathews S, Sharrock R (1994) The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Mol Biol 25:413–427

    Article  PubMed  CAS  Google Scholar 

  • Clough RC, Vierstra RD (1997) Phytochrome degradation. Plant Cell Environ 20:713–721

    Article  CAS  Google Scholar 

  • Clough RC, Casal JJ, Jordan ET, Christou P, Vierstra RD (1995) Expression of a functional oat phytochrome A in transgenic rice. Plant Physiol 109:1039–1045

    Article  PubMed  CAS  Google Scholar 

  • Davis SJ, Bhoo SH, Durski AM, Walker JM, Vierstra RD (2001) The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiol 126:656–669

    Article  PubMed  CAS  Google Scholar 

  • Dehesh K, Tepperman J, Christensen AH, Quail PH (1991) PHYB is evolutionarily conserved and constitutively expressed in rice seedling shoots. Mol Gen Genet 225:305–313

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Garg AK, Kim J-K, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903

    Article  PubMed  CAS  Google Scholar 

  • Halliday KJ, Thomas B, Whitelam GC (1997) Expression of heterologous phytochrome A, B or C in transgenic tobacco plants alters vegetative development and flowering time. Plant J 12:1079–1090

    Article  PubMed  CAS  Google Scholar 

  • Halliday KJ, Bolle C, Chua NH, Whitelam GC (1999) Overexpression of rice phytochrome A partially complements phytochrome B deficiency in Arabidopsis. Planta 207:401–409

    Article  PubMed  CAS  Google Scholar 

  • Hirschfeld M, Tepperman JM, Clack T, Quail PQ, Sharrock RA (1998) Coordination of phytochrome levels in phyB mutants of Arabidopsis as revealed by apoprotein-specific monoclonal antibodies. Genetics 149:523–535

    PubMed  CAS  Google Scholar 

  • Izawa T, Oikawa T, Tokutomi S, Okuno K, Shimamoto K (2000) Phytochromes confer the photoperiodic control of flowering in rice (a short-day plant). Plant J 22:391–399

    Article  PubMed  CAS  Google Scholar 

  • Johnson E, Bradley M, Harberd NP, Whitelam GC (1994) Photoresponses of light-grown phyA mutants of Arabidopsis. Plant Physiol 105:141–149

    Article  PubMed  CAS  Google Scholar 

  • Jordan ET, Hatfield PM, Hondred D, Talon M, Zeevaart JAD, Vierstra RD (1995) Phytochrome A overexpression in transgenic tobacco: Correlation of dwarf phenotype with high concentrations of phytochrome in vascular tissue and attenuated gibberellin levels. Plant Physiol 107:797–805

    Article  PubMed  CAS  Google Scholar 

  • Kay SA, Nagatani A, Keith B, Deak M, Furuya M, Chua N-H (1989) Rice phytochrome is biologically active in transgenic tobacco. Plant Cell 1:775–782

    Article  PubMed  CAS  Google Scholar 

  • Keller JM, Shanklin J, Vierstra RD, Hershey HP (1989) Expression of a functional monocotyledonous phytochrome gene in transgenic tobacco plants. EMBO J 8:1005–1012

    PubMed  CAS  Google Scholar 

  • Khush GS, dela Cruz N (2001) Developing Basmati rices with high yield potential. In: Chaudhary RC, Tran DV, Duffy R (eds) Speciality rices of the world: breeding production and marketing. Science Publishers, NH, pp 15–18

    Google Scholar 

  • Komari T, Hiei Y, Saito Y, Murai N, Kumashiro T (1996) Vectors carrying two separate T-DNAs for co-transformation of higher plants mediated by Agrobacterium tumefaciens and segregation of transformants free from selection markers. Plant J 10:165–174

    Article  PubMed  CAS  Google Scholar 

  • Kong SG, Lee DS, Kwak SN, Kim JK, Sohn JK, Kim IS (2004) Characterization of sunlight-grown transgenic rice plants expressing Arabidopsis phytochrome A. Mol Breed 14:35–45

    Article  CAS  Google Scholar 

  • Kyozuka J, McElroy D, Hayakawa T, Xie Y, Wu R, Shimamoto K (1993) Light-regulated and cell-specific expression of tomato rbcS-gusA and rice rbcS-gusA fusion genes in transgenic rice. Plant Physiol 102: 991–1000

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • McCormac AC, Cherry JR, Hershey HP, Vierstra RD, Smith H (1991) Photobiology of tobacco altered by expression of oat phytochrome. Planta 185:162–170

    Article  CAS  Google Scholar 

  • McCormac AC, Wagner D, Boylan MT, Quail PH, Smith H, Whitelam GC (1993) Photoresponses of transgenic Arabidopsis seedlings expressing introduced phytochrome B-encoding cDNAs: evidence that phytochrome A and phytochrome B have distinct photoregulatory functions. Plant J 4:19–27

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nagaraju J, Kathirvel M, Kumar RR, Siddiq EA, Hasnain SE (2002) Genetic analysis of traditional and evolved Basmati and non-Basmati rice varieties by using fluorescence-based ISSR-PCR and SSR markers. Proc Natl Acad Sci USA 99:5836–5841

    Article  PubMed  CAS  Google Scholar 

  • Nagatani A, Reed JW, Chory J (1993) Isolation and initial characterization of Arabidopsis mutants that are deficient in phytochrome A. Plant Physiol 102:269–277

    PubMed  CAS  Google Scholar 

  • Nagatani A, Kay SA, Deak M, Chua N-H, Furuya M (1991) Rice type I phytochrome regulates hypocotyl elongation in transgenic tobacco seedlings. Proc Natl Acad Sci USA 88:5207–5211

    Article  PubMed  CAS  Google Scholar 

  • Olsen JE, Juntilla O, Nilsen J, Eriksson ME, Martinussen I, Olsson O, Sandberg G, Moritz T (1997) Ectopic expression of oat phytochrome A in hybrid aspen changes critical day length for growth and prevents cold acclimation. Plant J 12:1339–1350

    Article  CAS  Google Scholar 

  • Parks BM, Quail PH (1993) hy8, a new class of Arabidopsis long hypocotyl mutants deficient in functional phytochrome A. Plant Cell 5:39–48

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rani NS, Krishnaiah K (2001) Current status and future prospects for improvement of aromatic rices in India. In: Chaudhary RC, Tran DV, Duffy R (eds) Speciality rices of the world: breeding production and marketing. Science Publishers, NH, pp 49–78

    Google Scholar 

  • Reed JW, Nagpal P, Poole DS, Furuya M, Chory J (1993) Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5:147–157

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sawers RJ, Sheehan MJ, Brutnell TP (2005) Cereal phytochromes: targets of selection, targets for manipulation? Trends Plant Sci 10:138–43

    PubMed  CAS  Google Scholar 

  • Sharrock R A, Clack T (2002) Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol 130:442–456

    Article  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 Dev 3:1745–1757

    Article  PubMed  CAS  Google Scholar 

  • Shlumukov LR, Barro F, Barcelo P, Lazzeri P, Smith H (2001) Establishment of far-red high irradiance responses in wheat through transgenic expression of an oat phytochrome A gene. Plant Cell Environ 24:703–712

    Article  CAS  Google Scholar 

  • Singh RK, Khush GS, Singh US, Singh AK, Singh S (2000) Breeding aromatic rice for high yield, improved aroma and grain quality. In: Singh RK, Singh US, Khush GS (eds) Aromatic rices. Science Publishers, NH pp 71–105

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Takano M, Kanegae H, Shinomura T, Miyao A, Hirochika H, Furuya M (2001) Isolation and characterization of rice phytochrome A mutants. Plant Cell 13:521–534

    Article  PubMed  CAS  Google Scholar 

  • Terry MJ (1997) Phytochrome chromophore-deficient mutants. Plant Cell Environ 20:740–745

    Article  CAS  Google Scholar 

  • Thiele A, Herold M, Lenk I, Quail PH, Gatz C (1999) Heterologous expression of Arabidopsis phytochrome B in transgenic potato influences photosynthetic performance and tuber development. Plant Physiol 120:73–81

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Tepperman J, Quail PH (1991) Overexpression of phytochrome B induces a short hypocotyl phenotype in transgenic Arabidopsis. Plant Cell 3:1275–1288

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Deng, XW (2003) Phytochrome A-regulated signaling network and photomorphogenesis. Trends Plant Sci 8:172–178

    Article  PubMed  CAS  Google Scholar 

  • Whitelam GC, Johnson E, Peng J, Carol P, Anderson ML, Cowl JS, Harberd NP (1993) phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5:757–768

    Article  PubMed  CAS  Google Scholar 

  • Yanovsky MJ, Alconada-Magliano TM, Mazzella MA, Gatz C, Thomas B, Casal J (1998) Phytochrome A affects stem growth, anthocyanin synthesis, sucrose-phosphate-synthase activity and neighbour detection in sunlight-grown potato. Planta 205:235–241

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Peter H. Quail (University of California, Berkeley and the USDA Plant Gene Expression Center, Albany, CA) for his generous gift of Arabidopsis PHYA cDNA and two monoclonal antibodies (1.9B5A, 073D). We thank Drs. Andre T. Jagendorf, Thomas G. Owens, Maureen Hanson and Tim L. Setter (all from Cornell University) for critical review of the manuscript. We also thank Mike Stoko, Laura Fabrizio, Joan Lee, Julie Batley, Jenny Lee, Carole Dougherty and Anita Aluisio for technical assistance.

Author information

Authors and Affiliations

  1. Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York, 14853, USA

    Ajay K. Garg & Ray J. Wu

  2. Boyce Thompson Institute, Cornell University, Ithaca, New York, 14853, USA

    Ruairidh J. H. Sawers, Haiyang Wang & Thomas P. Brutnell

  3. Division of Bioscience and Bioinformatics, Myongji University, Yongin, 449-728, Korea

    Ju-Kon Kim

  4. Department of Genetics, University of Wisconsin-Madison, Madison, WI, 53706, USA

    Joseph M. Walker & Richard D. Vierstra

  5. Department of Plant Biology, Cornell University, Ithaca, New York, 14853, USA

    Mandayam V. Parthasarathy

Authors
  1. Ajay K. Garg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruairidh J. H. Sawers
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haiyang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ju-Kon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joseph M. Walker
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thomas P. Brutnell
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mandayam V. Parthasarathy
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Richard D. Vierstra
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ray J. Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ray J. Wu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Garg, A.K., Sawers, R.J.H., Wang, H. et al. Light-regulated overexpression of an Arabidopsis phytochrome A gene in rice alters plant architecture and increases grain yield. Planta 223, 627–636 (2006). https://doi.org/10.1007/s00425-005-0101-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-0101-3

Keywords

Search

Navigation