Skip to main content
Log in

Genomics and relative expression analysis identifies key genes associated with high female to male flower ratio in Jatropha curcas L.

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Jatropha curcas, has been projected as a major source of biodiesel due to high seed oil content (42 %). A major roadblock for commercialization of Jatropha-based biodiesel is low seed yield per inflorescence, which is affected by low female to male flower ratio (1:25–30). Molecular dissection of female flower development by analyzing genes involved in phase transitions and floral organ development is, therefore, crucial for increasing seed yield. Expression analysis of 42 genes implicated in floral organ development and sex determination was done at six floral developmental stages of a J. curcas genotype (IC561235) with inherently higher female to male flower ratio (1:8–10). Relative expression analysis of these genes was done on low ratio genotype. Genes TFL1, SUP, AP1, CRY2, CUC2, CKX1, TAA1 and PIN1 were associated with reproductive phase transition. Further, genes CUC2, TAA1, CKX1 and PIN1 were associated with female flowering while SUP and CRY2 in female flower transition. Relative expression of these genes with respect to low female flower ratio genotype showed up to ~7 folds increase in transcript abundance of SUP, TAA1, CRY2 and CKX1 genes in intermediate buds but not a significant increase (~1.25 folds) in female flowers, thereby suggesting that these genes possibly play a significant role in increased transition towards female flowering by promoting abortion of male flower primordia. The outcome of study has implications in feedstock improvement of J. curcas through functional validation and eventual utilization of key genes associated with female flowering.

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

Access this article

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. Akbar E, Yaakob Z, Kamarudin S, Ismail M (2009) Characteristics and Composition of Jatropha curcas oil seed from Malaysia and its potential as Biodiesel Feedstock. Eur J Sci Res 29:396–403

    Google Scholar 

  2. Luo C-W, Li K, Chen Y, Y-y S (2007) Floral display and breeding system of Jatropha curcas L. For Stud China 9:114–119. doi:10.1007/s11632-007-0017-z

    Article  Google Scholar 

  3. Wu J, Liu Y, Tang L, Zhang F, Chen F (2010) A study on structural features in early flower development of Jatropha curcas L. and the classification of its inflorescences. Afr J Agric Res 6:275–284

    Google Scholar 

  4. Abdelgadir HA, Jager AK, Johnson SD, Van Staden J (2010) Influence of plant growth regulators on flowering, fruiting, seed oil content, and oil quality of Jatropha curcas. S Afr J Sci 76:440–446

    CAS  Google Scholar 

  5. Liu HFF, Kirchoff BK, Wu GJJ, Liao JPP (2007) Microsporogenesis and male gametogenesis in Jatropha curcas L. (Euphorbiaceae). J Torrey Bot Soc 134:335–343

    Article  Google Scholar 

  6. Mathooko FM, Mwaniki MW, Nakatsuka A, Shiomi S et al (1999) Expression characteristics of CS-ACS1, CS-ACS2 and CS-ACS3, three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in cucumber (Cucumis sativus L.) fruit under carbon dioxide stress. Plant Cell Physiol 40:164–172

    Article  CAS  PubMed  Google Scholar 

  7. Boualem A, Fergany M, Fernandez R, Troadec C et al (2008) A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons. Science 321:836–838. doi:10.1126/science.1159023

    Article  CAS  PubMed  Google Scholar 

  8. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191. doi:10.1016/j.cell.2008.01.047

    Article  CAS  PubMed  Google Scholar 

  9. Siddiqi I, Ganesh G, Grossniklaus U, Subbiah V (2000) The dyad gene is required for progression through female meiosis in Arabidopsis. Development 127:197–207

    CAS  PubMed  Google Scholar 

  10. Higuchi M, Pischke MS, Mahonen AP, Miyawaki K et al (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci 101:8821–8826. doi:10.1073/pnas.0402887101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kamiuchi Y, Yamamoto K, Furutani M, Tasaka M, Aida M (2014) The CUC1 and CUC2 genes promote carpel margin meristem formation during Arabidopsis gynoecium development. Front Plant Sci 5:165. doi:10.3389/fpls.2014.00165

    Article  PubMed  PubMed Central  Google Scholar 

  12. Ceccato L, Masiero S, Roy DS, Bencivenga S et al (2013) Maternal control of PIN1 is required for female gametophyte development in Arabidopsis. PLoS One 8(6):e66148. doi:10.1371/journal.pone.0066148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Li C, Luo L, Fu Q, Niu L, Xu ZF (2014) Isolation and functional characterization of JcFT, a FLOWERING LOCUS T (FT) homologous gene from the biofuel plant Jatropha curcas. BMC Plant Biol 14:125. doi:10.1186/1471-2229-14-125

    Article  PubMed  PubMed Central  Google Scholar 

  14. Pan BZ, Xu ZF (2010) Benzyladenine treatment significantly increases the seed yield of the biofuel plant Jatropha curcas. J Plant Growth Regul 30:166–174. doi:10.1007/s00344-010-9179-3

    Article  Google Scholar 

  15. Chen MS, Pan BZ, Wang GJ, Ni J, Niu L, Xu ZF (2014) Analysis of the transcriptional responses in inflorescence buds of Jatropha curcas exposed to cytokinin treatment. BMC Plant Biol 14:318. doi:10.1186/s12870-014-0318-z

    Article  PubMed  PubMed Central  Google Scholar 

  16. Pan BZ, Chen MS, Ni J, Xu ZF (2014) Transcriptome of the inflorescence meristems of the biofuel plant Jatropha curcas treated with cytokinin. BMC Genom 15:974. doi:10.1186/1471-2164-15-974

    Article  Google Scholar 

  17. http://www.kazusa.or.jp/e/resources/database.html

  18. http://www.softberry.com/berry.phtml

  19. http://primer3plus.com/

  20. Sangha JS, Gu K, Kaur J, Yin Z (2010) An improved method for RNA isolation and cDNA library construction from immature seeds of Jatropha curcas L. BMC Res Notes 3:126. doi:10.1186/1756-0500-3-126

    Article  PubMed  PubMed Central  Google Scholar 

  21. Zhang L, He LL, Fu QT, Xu ZF (2013) Selection of reliable reference genes for gene expression studies in the biofuel plant Jatropha curcas using real-time quantitative PCR. Int J Mol Sci 14:24338–24354. doi:10.3390/ijms141224338

    Article  PubMed  PubMed Central  Google Scholar 

  22. http://www.dna.affrc.go.jp/PLACE

  23. Galbiati F, Sinha Roy D, Simonini S, Cucinotta M et al (2013) An integrative model of the control of ovule primordia formation. Plant J 12:1–10. doi:10.1111/tpj.12309

    Google Scholar 

  24. Mohamed R, Wang CT, Shevchenko CM, Dye SJ et al (2010) Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J 62:674–688. doi:10.1111/j.1365-313X.2010.04185.x

    Article  CAS  PubMed  Google Scholar 

  25. Igasaki T, Watanabe Y, Nishiguchi M, Kotoda N (2008) The FLOWERING LOCUS T/TERMINAL FLOWER 1 Family in Lombardy Poplar. Plant Cell Physiol 49:291–300. doi:10.1093/pcp/pcn010

    Article  CAS  PubMed  Google Scholar 

  26. Zeng HY, Lu YT, Yang XM et al (2015) Ectopic expression of the BoTFL1-like gene of Bambusa oldhamii delays blossoming in Arabidopsis thaliana and rescues the tfl1 mutant phenotype. Genet Mol Res 14:9306–9317. doi:10.4238/2015.August.10.11

    Article  CAS  PubMed  Google Scholar 

  27. Conti L, Bradley D (2007) TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. Plant cell 19(767–78):78. doi:10.1105/tpc.106.049767

    Google Scholar 

  28. Kaufmann K, Wellmer F, Muiño JM, Ferrier T, Wuest SE, Kumar V, Serrano-Mislata A, Madueño F, Krajewski P, Meyerowitz EM, Angenent GC, Riechmann JL (2010) Orchestration of floral initiation by APETALA1. Science 328:85–89. doi:10.1126/science.1185244

    Article  CAS  PubMed  Google Scholar 

  29. Kazama Y, Fujiwara MT, Koizumi A, Nishihara K et al (2009) A SUPERMAN-like gene is exclusively expressed in female flowers of the dioecious plant Silene latifolia. Plant Cell Physiol 50:1127–1141. doi:10.1093/pcp/pcp064

    Article  CAS  PubMed  Google Scholar 

  30. Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun TP (2004) Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019. doi:10.1104/pp.104.039578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ishida T, Aida M, Takada S, Tasaka M (2000) Involvement of CUP-SHAPED COTYLEDON Genes in gynoecium and ovule development in Arabidopsis thaliana. Plant Cell Physiol 41:60–67

    Article  CAS  PubMed  Google Scholar 

  32. Zluvova J, Nicolas M, Berger A, Negrutiu I, Monéger F (2006) Premature arrest of the male flower meristem precedes sexual dimorphism in the dioecious plant Silene latifolia. Proc Natl Acad Sci 103:18854–18859. doi:10.1073/pnas.0606622103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Huang S, Cerny RC, Qi Y, Bhat D et al (2003) Transgenic Studies on the involvement of cytokinin and gibberellin in male development. Plant Physiol 131:1270–1282. doi:10.1104/pp.102.018598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Irish VF, Sussex IM (1990) Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2:741–753. doi:10.1105/tpc.2.8.741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Barak M, Trebitsh T (2007) A developmentally regulated GTP binding tyrosine phosphorylated protein A-like cDNA in cucumber (Cucumis sativus L.). Plant Mol Biol 65:829–837. doi:10.1007/s11103-007-9246-8

    Article  CAS  PubMed  Google Scholar 

  36. Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37:128–138. doi:10.1046/j.1365-313X.2003.01945.x

    Article  CAS  PubMed  Google Scholar 

  37. Li XG, Su YH, Zhao XY, Li W, Gao XQ, Zhang XS (2010) Cytokinin overproduction-caused alteration of flower development is partially mediated by CUC2 and CUC3 in Arabidopsis. Gene 450:109–120. doi:10.1016/j.gene.2009.11.003

    Article  CAS  PubMed  Google Scholar 

  38. Cucinotta M, Colombo L, Roig-Villanova I (2014) Ovule development, a new model for lateral organ formation. Front Plant Sci 5:117. doi:10.3389/fpls.2014.00117

    Article  PubMed  PubMed Central  Google Scholar 

  39. Bencivenga S, Simonini S, Benková E, Colombo L (2012) The transcription factors BEL1 and SPL are required for cytokinin and auxin signaling during ovule development in Arabidopsis. Plant Cell 24:2886–2897. doi:10.1105/tpc.112.100164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Sakai H, Krizek BA, Jacobsen SE, Meyerowitz EM (2000) Regulation of SUP expression identifies multiple regulators involved in Arabidopsis floral meristem development. Plant Cell 12:1607–1618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Ramireddy E, Brenner WG, Pfeifer A, Heyl A, Schmülling T (2013) In planta analysis of a cis-regulatory cytokinin response motif in Arabidopsis and identification of a novel enhancer sequence. Plant Cell Physiol 54:1079–1092. doi:10.1093/pcp/pct060

    Article  CAS  PubMed  Google Scholar 

  42. Bao Y, Dharmawardhana P, Arias RS, Allen MB, Ma C, Strauss SH (2009) WUS and STM-based reporter genes for studying meristem development in poplar. Plant Cell Rep 28:947–962. doi:10.1007/s00299-009-0685-3

    Article  CAS  PubMed  Google Scholar 

  43. Reiser L, Modrusan Z, Margossian L, Samach A, Ohad N, Haughn GW, Fisher RK (1995) The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell 83:735–742. doi:10.1016/0092-8674(95)90186-8

    Article  CAS  PubMed  Google Scholar 

  44. Filichkin SA, Leonard JM, Monteros A, Liu PP, Nonogaki H (2004) A novel endo-beta-mannanase gene in tomato LeMAN5 is associated with anther and pollen development. Plant Physiol 134:1080–1087. doi:10.1104/pp.103.035998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Zhang ZL, Xie Z, Zou X, Casaretto J, Ho TH, Shen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134:1500–1513. doi:10.1104/pp.103.034967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Tatematsu K, Ward S, Leyser O, Kamiya Y, Nambara E (2005) Identification of selements that regulate gene expression during initiation of axillary bud outgrowth in Arabidopsis. Plant Physiol 138:757–766. doi:10.1104/pp.104.057984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604. doi:10.1105/tpc.011650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78. doi:10.1105/tpc.006130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Hepworth SR, Valverde F, Ravenscroft D, Mouradov A, Coupland G (2002) Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J 21:4327–4337. doi:10.1093/emboj/cdf432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Hong RL, Hamaguchi L, Busch MA, Weigel D (2003) Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing. Plant Cell 15:1296–1309. doi:10.1105/tpc.009548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Sutoh K, Yamauchi D (2003) Two cis-acting elements necessary and sufficient for gibberellin-upregulated proteinase expression in rice seeds. Plant J 34:636–645

    Article  Google Scholar 

  52. Perry SE, Lehti MD, Fernandez DE (1991) The MADS-domain protein AGAMOUS-like 15 accumulates in embryonic tissues with diverse origins. Plant Physiol 120:121–129

    Article  Google Scholar 

  53. Okushima Y, Mitina I, Quach HL, Theologis A (2005) AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 43:29–46. doi:10.1111/j.1365-313X.2005.02426.x

    Article  CAS  PubMed  Google Scholar 

  54. Cremer F, Lonnig WE, Saedler H, Huijser P (2001) The delayed terminal flower phenotype is caused by a conditional mutation in the CENTRORADIALIS Gene of Snapdragon. Plant Physiol 126:1031–1041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Deng Y, Dong H, Mu J, Ren B et al (2010) Arabidopsis histidine kinase CKI1 acts upstream of histidine phosphotransfer proteins to regulate female gametophyte development and vegetative growth. Plant Cell 22:1232–1248. doi:10.1105/tpc.108.065128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations. Plant Cell 15:2532–2550. doi:10.1105/tpc.014928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418

    CAS  PubMed  Google Scholar 

  58. Ahmad M, Cashmore AR (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–166

    Article  CAS  PubMed  Google Scholar 

  59. Liu H, Yu X, Li K, Klejnot J, Yang H, Lisiero D, Lin C (2008) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322:1535–1539. doi:10.1126/science.1163927

    Article  CAS  PubMed  Google Scholar 

  60. Manzano S, Martínez C, Gómez P, Garrido D, Jamilena M (2010) Cloning and characterisation of two CTR1-like genes in Cucurbita pepo: regulation of their expression during male and female flower development. Sex Plant Reprod 23:301–313. doi:10.1007/s00497-010-0140-1

    Article  CAS  PubMed  Google Scholar 

  61. Takei k, Yamaya, T, and Sakakibara,H (2004) Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-Zeatin. JBC Papers in Press 279:41866–41872. doi:10.1074/jbc.M406337200

  62. Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191–2209. doi:10.1105/tpc.010192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Ju C, Yoon GM, Shemansky JM, Lin DY et al (2012) CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc Natl Acad Sci 109:19486–19491. doi:10.1073/pnas.1214848109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Ando S, Sato Y, Kamachi S, Sakai S (2001) Isolation of a MADS-box gene (ERAF17) and correlation of its expression with the induction of formation of female flowers by ethylene in cucumber plants (Cucumis sativus L.). Planta 213:943–952. doi:10.1007/s004250100571

    Article  CAS  PubMed  Google Scholar 

  65. Hall BP, Shakeel SN, Amir M et al (2012) Histidine kinase activity of the ethylene receptor ETR1 facilitates the ethylene response in Arabidopsis. Plant Physiol 159:682–695. doi:10.1104/pp.112.196790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859

    Article  CAS  PubMed  Google Scholar 

  67. Kasahara RD, Portereiko MF, Sandaklie-NikolovaL Rabiger DS, Drews GN (2005) MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 17:2981–2992. doi:10.1105/tpc.105.034603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Talbert PB, Adler HT, Parks DW, Comai L (1995) The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 21:2723–2735

    Google Scholar 

  69. Preston JC, Hileman LC (2011) SQUAMOSA-PROMOTER BINDING PROTEIN 1 initiates flowering in Antirrhinum majus through the activation of meristem identity genes. Plant J 62:704–712. doi:10.1111/j.1365-313X.2010.04184.x

    Article  Google Scholar 

  70. Ray A, Lang JD, Golden T, Ray S (1996) SHORT INTEGUMENT (SIN1), a gene required for ovule development in Arabidopsis, also controls flowering time. Development 122:2631–2638

    CAS  PubMed  Google Scholar 

  71. Groszmann M, Paicu T, Alvarez JP, Swain SM, Smyth DR (2011) SPATULA and ALCATRAZ, are partially redundant, functionally diverging bHLH genes required for Arabidopsis gynoecium and fruit development. Plant J 68:816–829. doi:10.1111/j.1365-313X.2011.04732.x

    Article  CAS  PubMed  Google Scholar 

  72. Motte P, Saedler H, Schwarz-Sommer Z (1998) STYLOSA and FISTULATA: regulatory components of the homeotic control of Antirrhinum floral organogenesis. Development 125:71–84

    CAS  PubMed  Google Scholar 

  73. Sablowski R (2009) Cytokinin and WUSCHEL tie the knot around plant stem cells. Proc Natl Acad Sci 106:6016–16017. doi:10.1073/pnas.0909300106

    Article  Google Scholar 

Download references

Acknowledgments

The authors are thankful to the Department of Biotechnology, Govt. of India for providing financial support to RSC in the form of R&D project on Jatropha curcas. The authors are thankful to Dr. Sreekrishna Chanumolu for assisting in PCA analysis and Mr. Archit Sood for suggesting J. curcas genotype IC561235.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rajinder Singh Chauhan.

Ethics declarations

Conflict of Interest

The authors declare that they do not have any conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gangwar, M., Sood, H. & Chauhan, R.S. Genomics and relative expression analysis identifies key genes associated with high female to male flower ratio in Jatropha curcas L.. Mol Biol Rep 43, 305–322 (2016). https://doi.org/10.1007/s11033-016-3953-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-016-3953-7

Keywords

Navigation