Skip to main content
SpringerLink
Log in

Isolation and Characterization of Circadian Clock Genes in the Biofuel Plant Pongamia (Millettia pinnata)

  • Published:
BioEnergy Research Aims and scope Submit manuscript

Abstract

The increasing human population has led to an inevitable increase in global energy demands. In the recent decades, biofuels have emerged as one of the potential solutions to the world’s insatiable energy needs while reducing the high reliance on fossil fuels. Pongamia (Millettia pinnata), a nitrogen-fixing tree legume, has shown a great promise as an oil source for the production of biofuel with economical and environmental benefits. The generation of pongamia-derived biofuel is dependent on the success of flowering and seed development. However, molecular control of floral initiation pathways in pongamia remains largely unexplored. Photoperiod pathway has been reported to be one of the major checkpoints of plant flowering time and flower initiation. The circadian clock pathway, a part of the photoperiod pathways, is one of the key regulators of flowering time. Here, we report the identification of four pongamia circadian clock genes (ELF4, LCL1, PRR7, and TOC1) through the mapping of the pongamia transcriptome short-paired reads library, by using soybean circadian clock genes as the reference sequences. Furthermore, multiple alignments and phylogenetic analyses suggested that pongamia clock genes are conserved among legume crops such as soybean, Medicago, and garden pea. Gene expression studies highlight that pongamia circadian clock genes are diurnally regulated under long-day conditions. Thus, this study reports the isolation and characterization of circadian clock genes in pongamia and enhances our understanding of the molecular mechanism of flowering control in pongamia.

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
Fig. 5

Similar content being viewed by others

References

  1. BP Statistical Review of World Energy 2013 (2013) http://www.bp.com/en/global/corporate/about-bp/energy-economics/statistical-review-of-world-energy.html. Accessed 20 June 2014

  2. McMichael AJ, Powles JW, Butler CD, Uauy R (2007) Food, livestock production, energy, climate change, and health. Lancet 370(9594):1253–1263

    PubMed  Google Scholar 

  3. Murray J, King D (2012) Climate policy: oil’s tipping point has passed. Nature 481(7382):433–435. doi:10.1038/481433a

    CAS  PubMed  Google Scholar 

  4. Murphy HT, O’Connell DA, Seaton G, Raison RJ, Rodriguez LC, Braid AL, Kriticos DJ, Jovanovic T, Abadi A, Betar M (2012) A common view of the opportunities, challenges, and research actions for pongamia in Australia. Bioenergy Res 5(3):778–800

    Google Scholar 

  5. Biswas B, Scott PT, Gresshoff PM (2011) Tree legumes as feedstock for sustainable biofuel production: opportunities and challenges. J Plant Physiol 168(16):1877–1884. doi:10.1016/j.jplph.2011.05.015

    CAS  PubMed  Google Scholar 

  6. Jensen ES, Peoples MB, Boddey RM, Gresshoff PM, Hauggaard-Nielsen H, Alves BJ, Morrison MJ (2012) Legumes for mitigation of climate change and the provision of feedstock for biofuels and biorefineries. A review. Agron Sustain Dev 32(2):329–364

    CAS  Google Scholar 

  7. Scott PT, Pregelj L, Chen N, Hadler JS, Djordjevic MA, Gresshoff PM (2008) Pongamia pinnata: an untapped resource for the biofuels industry of the future. Bioenergy Res 1(1):2–11

    Google Scholar 

  8. Tomar O, Gupta R (1985) Performance of some forest tree species in saline soils under shallow and saline water-table conditions. Plant Soil 87(3):329–335

    Google Scholar 

  9. Patil S, Hebbara M, Devarnavadagi S (1996) Screening of multipurpose trees for saline vertisols and their bioameliorative effects. Ann Arid Zone 35(1):57–60

    Google Scholar 

  10. Arpiwi NL, Yan G, Barbour EL, Plummer JA, Watkin E (2012) Phenotypic and genotypic characterisation of root nodule bacteria nodulating Millettia pinnata (L.) Panigrahi, a biodiesel tree. Plant Soil:1–15

  11. Kant P, Wu S (2011) The extraordinary collapse of Jatropha as a global biofuel. Environ Sci Technol 45(17):7114–7115. doi:10.1021/es201943v

    CAS  PubMed  Google Scholar 

  12. Kazakoff SH, Gresshoff PM, Scott PT (2011) Pongamia pinnata, a sustainable feedstock for biodiesel production. Energy crops Royal Society of Chemistry, London, pp 233–254

    Google Scholar 

  13. Coupland G (1997) Regulation of flowering by photoperiod in Arabidopsis. Plant Cell Environ 20(6):785–789

    Google Scholar 

  14. Abou-Elwafa SF, Büttner B, Chia T, Schulze-Buxloh G, Hohmann U, Mutasa-Göttgens E, Jung C, Müller AE (2011) Conservation and divergence of autonomous pathway genes in the flowering regulatory network of Beta vulgaris. J Exp Bot 62(10):3359–3374. doi:10.1093/jxb/erq321

    PubMed Central  CAS  PubMed  Google Scholar 

  15. Cober ER, Tanner JW, Voldeng HD (1996) Genetic control of photoperiod response in early-maturing, near-isogenic soybean lines. Crop Sci 36(3):601–605

    Google Scholar 

  16. Faure S, Turner AS, Gruszka D, Christodoulou V, Davis SJ, von Korff M, Laurie DA (2012) Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. Proc Natl Acad Sci U S A 109(21):8328–8333. doi:10.1073/pnas.1120496109

    PubMed Central  CAS  PubMed  Google Scholar 

  17. Hsu JC, Hamner KC (1967) Studies of the involvement of an endogenous rhythm in the photoperiodic response of Hyoscyamus niger. Plant Physiol 42(5):725–730

    PubMed Central  CAS  PubMed  Google Scholar 

  18. Takahashi Y, Shomura A, Sasaki T, Yano M (2001) Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc Natl Acad Sci U S A 98(14):7922–7927

    PubMed Central  CAS  PubMed  Google Scholar 

  19. Weller JL, Liew LC, Hecht VFG, Rajandran V, Laurie RE, Ridge S, Wenden B, Vander Schoor JK, Jaminon O, Blassiau C, Dalmais M, Rameau C, Bendahmane A, Macknight RC, Lejeune-Hénaut I (2012) A conserved molecular basis for photoperiod adaptation in two temperate legumes. Proc Natl Acad Sci U S A 109:21158–21163. doi:10.1073/pnas.1207943110

    PubMed Central  CAS  PubMed  Google Scholar 

  20. Kukade SA, Tidke JA (2013) Studies on pollination and reproductive biology of Pongamia pinnata l. (fabaceae). Indian J Fundam Appl Life Sci 3(1):149–155

    Google Scholar 

  21. Jiang Q, Yen S-H, Stiller J, Edwards D, Scott PT, Gresshoff PM (2012) Genetic, biochemical, and morphological diversity of the legume biofuel tree Pongamia pinnata. J Plant Genome Sci 1(3):54–67

    Google Scholar 

  22. Kazakoff SH, Imelfort M, Edwards D, Koehorst J, Biswas B, Batley J, Scott PT, Gresshoff PM (2012) Capturing the biofuel wellhead and powerhouse: the chloroplast and mitochondrial genomes of the leguminous feedstock tree Pongamia pinnata. PLoS One 7(12):e51687

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Gardner M, Hubbard K, Hotta C, Dodd A, Webb A (2006) How plants tell the time. Biochem J 397:15–24

    PubMed Central  CAS  PubMed  Google Scholar 

  24. Nagel DH, Kay SA (2012) Complexity in the wiring and regulation of plant circadian networks. Curr Biol 22(16):R648–657. doi:10.1016/j.cub.2012.07.025

    PubMed Central  CAS  PubMed  Google Scholar 

  25. Stratmann T, Más P (2008) Chromatin, photoperiod and the Arabidopsis circadian clock: a question of time. In: Seminars in cell & developmental biology, vol 6. Elsevier, pp 554–559

  26. Nakahata Y, Grimaldi B, Sahar S, Hirayama J, Sassone-Corsi P (2007) Signaling to the circadian clock: plasticity by chromatin remodeling. Curr Opin Cell Biol 19(2):230–237

    CAS  PubMed  Google Scholar 

  27. Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Sci Signal 309(5734):630

    CAS  Google Scholar 

  28. Green RM, Tingay S, Wang Z-Y, Tobin EM (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol 129(2):576–584

    PubMed Central  CAS  PubMed  Google Scholar 

  29. Michael TP, Salome PA, Yu HJ, Spencer TR, Sharp EL, McPeek MA, Alonso JM, Ecker JR, McClung CR (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302(5647):1049–1053

    CAS  PubMed  Google Scholar 

  30. Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD (2004) Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc Natl Acad Sci U S A 101:15670–15675

    PubMed Central  CAS  PubMed  Google Scholar 

  31. Faure S, Turner AS, Gruszka D, Christodoulou V, Davis SJ, von Korff M, Laurie DA (2012) Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1120496109

    Google Scholar 

  32. Slotte T, Holm K, McIntyre LM, Lagercrantz U, Lascoux M (2007) Differential expression of genes important for adaptation in Capsella bursa-pastoris (Brassicaceae). Plant Physiol 145(1):160–173. doi:10.1104/pp. 107.102632

    PubMed Central  CAS  PubMed  Google Scholar 

  33. Jung CH, Wong CE, Singh MB, Bhalla PL (2012) Comparative genomic analysis of soybean flowering genes. PLoS One 7(6):e38250. doi:10.1371/journal.pone.0038250

    PubMed Central  CAS  PubMed  Google Scholar 

  34. Wong CE, Singh MB, Bhalla PL (2013) The dynamics of soybean leaf and shoot apical meristem transcriptome undergoing floral initiation process. PLoS ONE 8(6):e65319

    PubMed Central  CAS  PubMed  Google Scholar 

  35. Jiang B, Yue Y, Gao Y, Ma L, Sun S, Wu C, Hou W, Lam H-M, Han T (2013) GmFT2a polymorphism and maturity diversity in soybeans. PLoS ONE 8(10):e77474

    PubMed Central  CAS  PubMed  Google Scholar 

  36. Na X, Jian B, Yao W, Wu C, Hou W, Jiang B, Bi Y, Han T (2013) Cloning and functional analysis of the flowering gene GmSOC1-like, a putative SUPPRESSOR OF OVEREXPRESSION CO1/AGAMOUS-LIKE 20 (SOC1/AGL20) ortholog in soybean. Plant Cell Rep:1–11

  37. Wong CE, Khor SY, Bhalla PL, Singh MB (2011) Novel spatial expression of soybean WUSCHEL in the incipient floral primordia. Planta 233:553–560

    CAS  PubMed  Google Scholar 

  38. Wong CE, Singh MB, Bhalla PL (2013) Spatial expression of CLAVATA3 in the shoot apical meristem suggests it is not a stem cell marker in soybean. J Exp Bot 64(18):5641–5649. doi:10.1093/jxb/ert341

    PubMed Central  CAS  PubMed  Google Scholar 

  39. Wong CE, Singh MB, Bhalla PL (2013) Novel members of the AGAMOUS LIKE 6 subfamily of MIKCC-type MADS-box genes in soybean. BMC Plant Biol 13(1):105

    PubMed Central  PubMed  Google Scholar 

  40. Wu F, Price BW, Haider W, Seufferheld G, Nelson R, Hanzawa Y (2014) Functional and evolutionary characterization of the CONSTANS gene family in short-day photoperiodic flowering in soybean. PLoS One 9(1):e85754

    PubMed Central  PubMed  Google Scholar 

  41. Xia Z, Watanabe S, Yamada T, Tsubokura Y, Nakashima H, Zhai H, Anai T, Sato S, Yamazaki T, Lü S, Wu H, Tabata S, Harada K (2012) Positional cloning and characterization reveal the molecular basis for soybean maturity locus E1 that regulates photoperiodic flowering. Proc Natl Acad Sci U S A 109(32):E2155–E2164. doi:10.1073/pnas.1117982109

    PubMed Central  CAS  PubMed  Google Scholar 

  42. Zhang Q, Li H, Li R, Hu R, Fan C, Chena F, Wang Z, Liu X, Fu Y, Lin C (2008) Association of the circadian rhythmic expression of GmCRY1a with a latitudinal cline in photoperiodic flowering of soybean. Proc Natl Acad Sci U S A 105:21028–21033

    PubMed Central  CAS  PubMed  Google Scholar 

  43. Liew LC, Singh MB, Bhalla PL (2013) An RNA-Seq transcriptome analysis of histone modifiers and RNA silencing genes in soybean during floral initiation process. PLoS One 8(10):e77502

    PubMed Central  CAS  PubMed  Google Scholar 

  44. Gepts P, Beavis WD, Brummer EC, Shoemaker RC, Stalker HT, Weeden NF, Young ND (2005) Legumes as a model plant family. Genomics for food and feed report of the cross-legume advances through genomics conference. Plant Physiol 137(4):1228–1235

    PubMed Central  CAS  PubMed  Google Scholar 

  45. Huang J, Lu X, Yan H, Chen S, Zhang W, Huang R, Zheng Y (2012) Transcriptome characterization and sequencing-based identification of salt-responsive genes in Millettia pinnata, a semi-mangrove plant. DNA Res 19(2):195–207. doi:10.1093/dnares/dss004

    PubMed Central  CAS  PubMed  Google Scholar 

  46. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(Database issue):D1178–1186. doi:10.1093/nar/gkr944

    PubMed Central  CAS  PubMed  Google Scholar 

  47. Drummond A, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, A W (2013) Geneious v6 (http://www.geneious.com/) Biomatters Ltd, Auckland, New Zealand

  48. Rogers SO, Bendich AJ (1994) Extraction of total cellular DNA from plants, algae and fungi. In: Plant molecular biology manual. Springer, pp 183–190

  49. Southern E (2006) Southern blotting. Nat Protoc 1(2):518–525

    CAS  PubMed  Google Scholar 

  50. Thibivilliers S, Joshi T, Campbell K, Scheffler B, Xu D, Cooper B, Nguyen H, Stacey G (2009) Generation of Phaseolus vulgaris ESTs and investigation of their regulation upon Uromyces appendiculatus infection. BMC Plant Biol 9(1):46

    PubMed Central  PubMed  Google Scholar 

  51. Libault M, Thibivilliers S, Bilgin D, Radwan O, Benitez M, Clough S, Stacey G (2008) Identification of four soybean reference genes for gene expression normalization. Plant Genome 1(1):44–54

    CAS  Google Scholar 

  52. Pokhilko A, Fernández AP, Edwards KD, Southern MM, Halliday KJ, Millar AJ (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol Syst Biol 8:574

    PubMed Central  PubMed  Google Scholar 

  53. Doyle MR, Davis SJ, Bastow RM, McWatters HG, Kozma-Bognár L, Nagy F, Millar AJ, Amasino RM (2002) The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 419(6902):74–77

    CAS  PubMed  Google Scholar 

  54. Alabadi D, Yanovsky MJ, Más P, Harmer SL, Kay SA (2002) Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis. Curr Biol 12(9):757–761

    CAS  PubMed  Google Scholar 

  55. Alabadi D, Oyama T, Yanovsky MJ, Harmon FG, Mas P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Sci Signal 293(5531):880

    CAS  Google Scholar 

  56. Farré EM, Harmer SL, Harmon FG, Yanovsky MJ, Kay SA (2005) Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr Biol 15(1):47–54

    PubMed  Google Scholar 

  57. Khanna R, Kikis EA, Quail PH (2003) Early flowering 4 functions in phytochrome B-regulated seedling de-etiolation. Plant Physiol 133(4):1530–1538

    PubMed Central  CAS  PubMed  Google Scholar 

  58. Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay SA (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475(7356):398–402

    PubMed Central  CAS  PubMed  Google Scholar 

  59. Kikis EA, Khanna R, Quail PH (2005) ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. Plant J 44(2):300–313

    CAS  PubMed  Google Scholar 

  60. Kolmos E, Nowak M, Werner M, Fischer K, Schwarz G, Mathews S, Schoof H, Nagy F, Bujnicki JM, Davis SJ (2009) Integrating ELF4 into the circadian system through combined structural and functional studies. HFSP J 3(5):350–366

    PubMed Central  CAS  PubMed  Google Scholar 

  61. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, Coupland G (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93(7):1219–1229

    CAS  PubMed  Google Scholar 

  62. Wang Z-Y, Tobin EM (1998) Constitutive expression of the circadian clock associated 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93(7):1207–1218

    CAS  PubMed  Google Scholar 

  63. Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song H-R, Carré IA, Coupland G (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2(5):629–641

    CAS  PubMed  Google Scholar 

  64. Green RM, Tobin EM (2002) The role of CCA1 and LHY in the plant circadian clock. Dev Cell 2(5):516–518

    CAS  PubMed  Google Scholar 

  65. Thakare D, Kumudini S, Dinkins RD (2010) Expression of flowering-time genes in soybean E1 near-isogenic lines under short and long day conditions. Planta 231(4):951–963. doi:10.1007/s00425-010-1100-6

    CAS  PubMed  Google Scholar 

  66. Liu H, Wang H, Gao P, Xu J, Xu T, Wang J, Wang B, Lin C, Fu YF (2009) Analysis of clock gene homologs using unifoliolates as target organs in soybean (Glycine max). J Plant Physiol 166(3):278–289. doi:10.1016/j.jplph.2008.06.003

    CAS  PubMed  Google Scholar 

  67. Liew LC, Hecht V, Laurie RE, Knowles CL, Vander Schoor JK, Macknight RC, Weller JL (2009) DIE NEUTRALIS and LATE BLOOMER 1 contribute to regulation of the pea circadian clock. Plant Cell 21:3198–3211. doi:10.1105/tpc.109.067223

    PubMed Central  CAS  PubMed  Google Scholar 

  68. Liu H, Wang H, Gao P, Xü J, Xü T, Wang J, Wang B, Lin C, Fu Y-F (2009) Analysis of clock gene homologs using unifoliolates as target organs in soybean (Glycine max). J Plant Physiol 166(3):278–289

    CAS  PubMed  Google Scholar 

  69. Murakami M, Tago Y, Yamashino T, Mizuno T (2007) Comparative overviews of clock-associated genes of Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol 48(1):110–121

    CAS  PubMed  Google Scholar 

  70. Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Más P, Panda S, Kreps JA, Kay SA (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Sci Signal 289(5480):768

    CAS  Google Scholar 

  71. Matsushika A, Makino S, Kojima M, Mizuno T (2000) Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: insight into the plant circadian clock. Plant Cell Physiol 41(9):1002–1012

    CAS  PubMed  Google Scholar 

  72. Imamura A, Hanaki N, Umeda H, Nakamura A, Suzuki T, Ueguchi C, Mizuno T (1998) Response regulators implicated in His-to-Asp phosphotransfer signaling in Arabidopsis. Proc Natl Acad Sci U S A 95(5):2691–2696

    PubMed Central  CAS  PubMed  Google Scholar 

  73. Mizuno T (2004) Plant response regulators implicated in signal transduction and circadian rhythm. Curr Opin Plant Biol 7(5):499–505

    CAS  PubMed  Google Scholar 

  74. Robert LS, Robson F, Sharpe A, Lydiate D, Coupland G (1998) Conserved structure and function of the Arabidopsis flowering time gene CONSTANS in Brassica napus. Plant Mol Biol 37(5):763–772

    CAS  PubMed  Google Scholar 

  75. Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448(7151):358–361. doi:10.1038/nature05946

    CAS  PubMed  Google Scholar 

  76. Niwa Y, Yamashino T, Mizuno T (2009) The circadian clock regulates the photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant Cell Physiol 50(4):838–854

    CAS  PubMed  Google Scholar 

  77. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53(2):312–323

    CAS  PubMed  Google Scholar 

  78. Carré IA, Kim JY (2002) MYB transcription factors in the Arabidopsis circadian clock. J Exp Bot 53(374):1551–1557

    PubMed  Google Scholar 

  79. Saikumar P, Murali R, Reddy EP (1990) Role of tryptophan repeats and flanking amino acids in Myb-DNA interactions. Proc Natl Acad Sci U S A 87(21):8452–8456

    PubMed Central  CAS  PubMed  Google Scholar 

  80. Nakamichi N, Kiba T, Henriques R, Mizuno T, Chua N-H, Sakakibara H (2010) Pseudo-response regulators 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. Plant Cell 22(3):594–605

    PubMed Central  CAS  PubMed  Google Scholar 

  81. Asakura Y, Hagino T, Ohta Y, Aoki K, Yonekura-Sakakibara K, Deji A, Yamaya T, Sugiyama T, Sakakibara H (2003) Molecular characterization of His-Asp phosphorelay signaling factors in maize leaves: implications of the signal divergence by cytokinin-inducible response regulators in the cytosol and the nuclei. Plant Mol Biol 52(2):331–341

    CAS  PubMed  Google Scholar 

  82. Carre I, Veflingstad S (2013) Emerging design principles in the Arabidopsis circadian clock. Semin Cell Dev Biol 24 (5): Academic Press, 2013

  83. Makino S, Kiba T, Imamura A, Hanaki N, Nakamura A, Suzuki T, Taniguchi M, Ueguchi C, Sugiyama T, Mizuno T (2000) Genes encoding pseudo-response regulators: insight into His-to-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana. Plant Cell Physiol 41(6):791–803

    CAS  PubMed  Google Scholar 

  84. Gendron JM, Pruneda-Paz JL, Doherty CJ, Gross AM, Kang SE, Kay SA (2012) Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proc Natl Acad Sci U S A 109(8):3167–3172

    PubMed Central  CAS  PubMed  Google Scholar 

  85. Dixon LE, Knox K, Kozma-Bognar L, Southern MM, Pokhilko A, Millar AJ (2011) Temporal repression of core circadian genes is mediated through early flowering 3 in Arabidopsis. Curr Biol 21(2):120–125

    PubMed Central  CAS  PubMed  Google Scholar 

  86. Hazen SP, Schultz TF, Pruneda-Paz JL, Borevitz JO, Ecker JR, Kay SA (2005) Lux arrhythmo encodes a Myb domain protein essential for circadian rhythms. Proc Natl Acad Sci U S A 102(29):10387–10392

    PubMed Central  CAS  PubMed  Google Scholar 

  87. Li G, Siddiqui H, Teng Y, Lin R, X-y W, Li J, Lau O-S, Ouyang X, Dai M, Wan J (2011) Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis. Nat Cell Biol 13(5):616–622

    CAS  PubMed  Google Scholar 

  88. Helfer A, Nusinow DA, Chow BY, Gehrke AR, Bulyk ML, Kay SA (2011) Lux arrhythmo encodes a nighttime repressor of circadian gene expression in the Arabidopsis core clock. Curr Biol 21(2):126–133

    PubMed Central  CAS  PubMed  Google Scholar 

  89. Liew LC, Hecht V, Sussmilch FC, Weller JL (2014) The pea photoperiod response gene STERILE NODES is an ortholog of LUX ARRHYTHMO. Plant Physiol 165(2):648–657

    PubMed Central  CAS  PubMed  Google Scholar 

  90. Huang W, Pérez-García P, Pokhilko A, Millar A, Antoshechkin I, Riechmann J, Mas P (2012) Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Sci Signal 336(6077):75

    CAS  Google Scholar 

  91. Khan S, Rowe SC, Harmon FG (2010) Coordination of the maize transcriptome by a conserved circadian clock. BMC Plant Biol 10(1):126

    PubMed Central  PubMed  Google Scholar 

  92. Turner A, Beales J, Faure S, Dunford R, Laurie D (2005) The pseudo-response regulator ppd-h1 provides adaptation to photoperiod in barley. Science 310(5750):1031–1034

    CAS  PubMed  Google Scholar 

  93. Beales J, Turner A, Griffiths S, Snape JW, Laurie DA (2007) A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet 115(5):721–733

    CAS  PubMed  Google Scholar 

  94. Shaw LM, Turner AS, Laurie DA (2012) The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat (Triticum aestivum). Plant J 71(1):71–84

    CAS  PubMed  Google Scholar 

  95. Chen A, Li C, Hu W, Lau MY, Lin H, Rockwell NC, Martin SS, Jernstedt JA, Lagarias JC, Dubcovsky J (2014) PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod. Proc Natl Acad Sci U S A 111(28):10037–10044

    PubMed Central  CAS  PubMed  Google Scholar 

  96. Jung C, Müller AE (2009) Flowering time control and applications in plant breeding. Trends Plant Sci 14:563–573

    CAS  PubMed  Google Scholar 

  97. Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40(6):761–767

    CAS  PubMed  Google Scholar 

  98. Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18(8):926–936

    PubMed Central  CAS  PubMed  Google Scholar 

  99. Takahashi Y, Teshima KM, Yokoi S, Innan H, Shimamoto K (2009) Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc Natl Acad Sci U S A 106(11):4555–4560. doi:10.1073/pnas.0812092106

    PubMed Central  CAS  PubMed  Google Scholar 

  100. Zhao J, Huang X, Ouyang X, Chen W, Du A, Zhu L, Wang S, Deng XW, Li S (2012) OsELF3-1, an ortholog of Arabidopsis EARLY FLOWERING 3, regulates rice circadian rhythm and photoperiodic flowering. PLoS ONE 7(8):e43705. doi:10.1371/journal.pone.0043705

    PubMed Central  CAS  PubMed  Google Scholar 

  101. Hudson KA (2010) The circadian clock-controlled transcriptome of developing soybean seeds. Plant Genome 3(1):3–13. doi:10.3835/plantgenome2009.08.0025

    CAS  Google Scholar 

  102. Preuss SB, Meister R, Xu Q, Urwin CP, Tripodi FA, Screen SE, Anil VS, Zhu S, Morrell JA, Liu G (2012) Expression of the Arabidopsis thaliana BBX32 gene in soybean increases grain yield. PLoS ONE 7(2):e30717

    PubMed Central  CAS  PubMed  Google Scholar 

  103. Hecht V, Knowles CL, Vander Schoor JK, Liew LC, Jones SE, Lambert MJM, Weller JL (2007) Pea LATE BLOOMER1 is a GIGANTEA ortholog with roles in photoperiodic flowering, deetiolation, and transcriptional regulation of circadian clock gene homologs. Plant Physiol 144(2):648–661

    PubMed Central  CAS  PubMed  Google Scholar 

  104. Raju AS, Rao SP (2006) Explosive pollen release and pollination as a function of nectar-feeding activity of certain bees in the biodiesel plant, Pongamia pinnata (L.) Pierre (Fabaceae). Curr Sci (Bangalore) 90(7):960–967

    Google Scholar 

  105. Pesti J (1976) Daily fluctuations in the sugar content of nectar and periodicity of secretion in the Compositae. Acta Agron Acad Sci Hung 25(5):17

    Google Scholar 

  106. Gimenes M, Benedito-Silva A, Marques M (1996) Circadian rhythms of pollen and nectar collection by bees on the flowers of Ludwigia elegans (Onagraceae). Biol Rhythm Res 27(3):281–290

    Google Scholar 

  107. Radhika V, Kost C, Mithöfer A, Boland W (2010) Regulation of extrafloral nectar secretion by jasmonates in lima bean is light dependent. Proc Natl Acad Sci 107(40):17228–17233

    PubMed Central  CAS  PubMed  Google Scholar 

  108. Farré EM (2012) The regulation of plant growth by the circadian clock. Plant Biol (Stuttg) 14(3):401–410. doi:10.1111/j.1438-8677.2011.00548.x

    Google Scholar 

  109. Devlin PF (2002) Signs of the time: environmental input to the circadian clock. J Exp Bot 53(374):1535–1550

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Australian Research Council in the form of the ARC Centre of Excellence for Integrative Legume Research (CE0348212) and the McKenzie Postdoctoral Fellowship (LCL) by the University of Melbourne.

Author information

Authors and Affiliations

  1. Plant Molecular Biology and Biotechnology Laboratory, ARC Centre of Excellence for Integrative Legume Research, Melbourne School of Land and Environment, The University of Melbourne, Parkville, VIC, 3010, Australia

    Harry P. Winarto, Lim Chee Liew, Mohan B. Singh & Prem L. Bhalla

  2. Centre for Integrative Legume Research, School of Agriculture and Food Sciences, The University of Queensland, St. Lucia, Brisbane, QLD, 4072, Australia

    Peter M. Gresshoff & Paul T. Scott

Authors
  1. Harry P. Winarto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lim Chee Liew
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter M. Gresshoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul T. Scott
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohan B. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Prem L. Bhalla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Prem L. Bhalla.

Additional information

Harry P. Winarto and Lim Chee Liew contributed equally to the article.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 15kb)

ESM 2

(DOCX 79kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Winarto, H.P., Liew, L.C., Gresshoff, P.M. et al. Isolation and Characterization of Circadian Clock Genes in the Biofuel Plant Pongamia (Millettia pinnata). Bioenerg. Res. 8, 760–774 (2015). https://doi.org/10.1007/s12155-014-9556-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12155-014-9556-z

Keywords

Search

Navigation