Skip to main content
Log in

Characterization of oil palm MADS box genes in relation to the mantled flower abnormality

  • Published:
Plant Cell, Tissue and Organ Culture Aims and scope Submit manuscript

Abstract

In vitro propagation of oil palm (Elaeis guineensis Jacq.) frequently induces a somaclonal variant called ‘mantled’ abnormality, in which the stamens of both male and female flowers are transformed into carpels. This leads to a reduced yield or complete loss of the harvest of palm oil. The high frequency of the abnormality in independent lines and the high reversal rate suggest that it is due to an epigenetic change. The type of morphological changes suggest that it involves homeotic MADS box genes that regulate the identity of the flower whorls. We have isolated a number of MADS box genes from oil palm inflorescences by a MADS box-directed mRNA display approach. The isolated partial cDNAs included genes that were likely to function at the initial stages of flowering as well as genes that may function in determination of the inflorescence and the identity of the flower whorls. For four genes that were homologous to genes known to affect the reproductive parts of the flower, full length cDNAs were isolated. These were a B-type MADS box gene which may function in the determination of stamen formation, a C-type gene expected to be involved in stamen and carpel formation, and two putative SEP genes which act in concert with the A-, B- and C-type MADS box gene in determining flower whorl formation. The B-type gene EgMADS16 was functionally characterized as a PISTILLATA orthologue; it was able to complement an Arabidopsis thaliana pi mutant. Whether EgMADS16, or any of the other EgMADS genes, are functionally involved in the mantled condition remains to be established.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

SEP:

SEPALLATA

EgMADS:

Elaeis guineensis Jacq. MADS box gene

AG:

AGAMOUS

PI:

PISTILLATA

References

  • Altschul SF, Gish W, Miller W, Myers MW, Lipman DJ, (1990) Basic local alignment search tool J. Mol. Biol. 215: 403–410

    Article  PubMed  CAS  Google Scholar 

  • Adam H, Jouannic S, Morcillo F, Richaud F, Duval Y & Tregear JW (2006) MADS box genes in oil palm (Elaeis guineensis): patterns in the evolution of the SQUAMOSA, DEFICIENS, GLOBOSA, AGAMOUS and SEPALLATA subfamilies. J. Mol. Evol. 62: 15–31

    Google Scholar 

  • Angenent GC, Colombo L, (1996) Molecular control of ovule development Trends Plant Sci. 1: 228–232

    Google Scholar 

  • Basri MW, Siti Nor Akmar A & Henson IE (2004) Oil Palm – Achievements and Potential. In: New directions for a diverse planet, Proceedings of the 4th International Crop Science Congress, 26 Sep–1 Oct 2004, Brisbane, Australia. http://www.cropscience.org.au/icsc2004/pdf/187_wahidmb.pdf

  • Becker A, Theissen G, (2003) The major clades of MADS-box genes and their role in development and evolution of flowering plants Mol. Phylogenet. Evol. 29: 464–489

    Article  PubMed  CAS  Google Scholar 

  • Bonhomme F, Kurz B, Melzer S, Bernier G, Jacqmard A, (2000) Cytokinin and gibberellin activate SaMADSA, a gene apparently involved in regulation of the floral transition in Sinapis albaPlant J. 24: 103–111

    Article  PubMed  CAS  Google Scholar 

  • Borner R, Kampmann G, Chandler J, Gleißner R, Wisman E, Apel K, Melzer S, (2000) A MADS domain gene involved in the transition to flowering in Arabidopsis Plant J. 24: 591–599

    Article  PubMed  CAS  Google Scholar 

  • Boss PK, Sensi E, Hua C, Davies C, Thomas MR, (2002) Cloning and characterization of grapevine (Vitis vinifera L.) MADS box genes expressed during inflorescence and berry development Plant Sci. 162: 887–895

    Article  CAS  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM, (1989) Genes directing flower development in Arabidopsis Plant Cell 1: 37–52

    Article  PubMed  CAS  Google Scholar 

  • Chung YY, Kim SR, Finkel D, Yanofsky MF, An G, (1994) Early flowering and reduced apical dominance result from ectopic expression of a rice MADS box gene Plant Mol. Biol. 26: 657–665

    Article  PubMed  CAS  Google Scholar 

  • Chung YY, Kim SR, Kang HG, Noh YS, Park MC, Finkel DF, An G, (1995) Characterization of two rice MADS box genes homologous to GLOBOSAPlant Sci. 109: 45–56

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF, (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thalianaPlant J. 16: 735–743

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Meyerowitz EM, (1991) The war of the whorls: genetic interactions controlling flower development Nature 353: 31–37

    Article  PubMed  CAS  Google Scholar 

  • Colombo L, Franken J, Koetje E, Van Went J, Dons HJM, Angenent GC, Van Tunen AJ, (1995) The petunia MADS box gene FBP11 determines ovule identity Plant Cell 7: 1859–1868

    Article  PubMed  CAS  Google Scholar 

  • Corley RHV, Lee CH, Law IH, Wong CY, (1986) Abnormal flower development in oil palm clones Planter (Kuala Lumpur) 62: 233–240

    Google Scholar 

  • Duval Y, Besse I, Verdeil JL, Maldiney R, (1995) Study on the induction of the floral morphogenesis abnormality in oil palm during the in vitro regeneration process. In: Rao N, Henson IE, Rajanaidu N, (Eds). Proc. of the 1993 ISOPB Intl. Symp. On Recent Development in Oil Palm Tissue Culture and Biotechnology Palm Oil Research Institute of Malaysia, Bangi, Malaysia (pp. 64–76)

    Google Scholar 

  • Eeuwens CJ, Lord S, Donough CR, Rao V, Vallejo G, Nelson S, (2002) Effects of tissue culture conditions during embryoid multiplication on the incidence of “mantled” flowering in clonally propagated oil palm Plant Cell Tissue Organ Cult. 70: 311–323

    Article  CAS  Google Scholar 

  • Ferrario S, Immink RGH, Shchennikova A, Busscher-Lange J, Angenent GC, (2003) The MADS box gene FBP2 is required for SEPALLATA function in Petunia Plant Cell 15: 914–925

    Article  PubMed  CAS  Google Scholar 

  • Fischer A, Saedler H, Theissen G, (1995) Restriction fragment length polymorphism-coupled domain-directed differential display: A highly efficient technique for expression analysis of multigene families Proc. Natl. Acad. Sci. USA 92: 5331–5335

    Article  PubMed  CAS  Google Scholar 

  • Flanagan CA, Ma H, (1994) Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant Arabidopsis flowers Plant Mol. Biol. 26: 581–595

    Article  PubMed  CAS  Google Scholar 

  • Greco R, Stagi L, Colombo L, Angenent GC, Sari-Gorla M, Pe ME, (1997) MADS box genes expressed in developing inflorescence of rice and sorghum Mol. Gen. Genet. 253: 615–623

    Article  PubMed  CAS  Google Scholar 

  • Gustafson-Brown C, Savidge B, Yanofsky MF, (1994) Regulation of the floral homeotic gene APETALA1 Cell 76: 131–143

    Article  PubMed  CAS  Google Scholar 

  • Heuer S, Hansen S, Bantin J, Brettschneider R, Kranz E, Lörz H, Dresselhaus T, (2001) The maize MADS box gene ZmMADS3 affects node number and spikelet development and is co-expressed with ZmMADS1 during flower development, in egg cells, and early embryogenesis Plant Physiol. 127: 33–45

    Article  PubMed  CAS  Google Scholar 

  • Immink RGH, Gadella TWJ Jr., Ferrario S, Busscher M, Angenent GC, (2002) Analysis of MADS box protein–protein interactions in living plant cells Proc. Nat. Acad. Sci. USA 99: 2416–2421

    Article  PubMed  CAS  Google Scholar 

  • Jaligot E, Beulé T, Rival A, (2002) Methylation-sensitive RFLPs: characterisation of two oil palm markers showing somaclonal variation-associated polymorphism Theor. Appl. Genet. 104: 1263–1269

    Article  PubMed  CAS  Google Scholar 

  • Jones LH, (1974) Propagation of clonal oil palms by tissue culture Oil Palm News 17: 1–8

    Google Scholar 

  • Kaeppler SM, Phillips RL, (1993) Tissue culture-induced DNA methylation variation in maize Proc. Natl. Acad. Sci. USA 90: 8773–8776

    Article  PubMed  CAS  Google Scholar 

  • Kaeppler SM , Kaeppler HF, Rhee Y, (2000) Epigenetic aspects of somaclonal variation in plants Plant Mol. Biol. 43: 179–188

    Article  PubMed  CAS  Google Scholar 

  • Kramer EM, Dorit RL, Irish VF, (1998) Molecular evolution of genes controlling petal and stamen development: Duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages Genetics 149: 765–783

    PubMed  CAS  Google Scholar 

  • Kubis SE, Castilho AMMF, Vershinin AV, Heslop-Harrison JS, (2003) Retroelements, transposons and methylation status in the genome of oil palm (Elaeis guineensis) and the relationship to somaclonal variation Plant Mol. Biol. 52: 69–79

    Article  PubMed  CAS  Google Scholar 

  • Kyozuka J, Kobayashi T, Morita M, Shimamoto K, (2000) Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes Plant Cell Physiol. 41: 710–718

    PubMed  CAS  Google Scholar 

  • Li QZ, Li XG, Bai SN, Lu WL, Zhang XS, (2001) Isolation and expression of HAP2, a homolog of AP2 in Hyacinthus orientalis Dev. Reprod. Biol. 10: 69–75

    CAS  Google Scholar 

  • Li QZ, Li XG, Bai SN, Lu WL, Zhang XS, (2002) Isolation of HAG1 and its regulation by plant hormones during in vitro floral organogenesis in Hyacinthus orientalis L Planta 215: 533–540

    Article  PubMed  CAS  Google Scholar 

  • Lu ZX, Wu M, Loh CS, Yeong CY, Goh CJ, (1993) Nucleotide sequence of a flower-specific MADS box cDNA clone from orchid Plant Mol. Biol. 23: 901–904

    Article  PubMed  CAS  Google Scholar 

  • Malcomber ST, Kellogg EA, (2004) Heterogeneous expression patterns and separate roles of the SEPALLATA gene LEAFY HULL STERILE1 in grasses Plant Cell 16: 1692–1706

    Article  PubMed  CAS  Google Scholar 

  • Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF, (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1Nature 360: 273–277

    Article  PubMed  CAS  Google Scholar 

  • Mandel T, Lutzinger I, Kuhlemeier C, (1994) A ubiquitously expressed MADS-box gene from Nicotiana tabacumPlant Mol. Biol. 25: 319–321

    Article  PubMed  CAS  Google Scholar 

  • Mandel MA, Yanofsky MF, (1995) The Arabidopsis AGL8 MADS-box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1 Plant Cell 7: 1763–1771

    Article  PubMed  CAS  Google Scholar 

  • Mandel MA, Yanofsky MF, (1998) The Arabidopsis AGL9 MADS box gene is expressed in young flower primordia Sex. Plant Reprod. 11: 22–28

    Article  CAS  Google Scholar 

  • Matthes M, Singh R, Cheah S-C, Karp A, (2001) Variation in oil palm (Elaeis guineensis Jacq.) tissue culture-derived regenerants revealed by AFLPs with methylation-sensitive enzymes Theor. Appl. Genet. 102: 971–979

    Article  CAS  Google Scholar 

  • Mena M, Mandel MA, Lerner R, Yanofsky MF, Schmidt RJ, (1995) A characterization of the MADS-box gene family in maize Plant J. 8: 845–854

    PubMed  CAS  Google Scholar 

  • Murai K, Murai R, Ogihara Y, (1997) Wheat MADS box genes, a multigene family dispersed throughout the genome Genes Genet. Syst. 72: 317–321

    Article  PubMed  CAS  Google Scholar 

  • Münster T, Miyoshi M, Sano Y, Satoh H, Hirano H, Sakai H, Nagato Y, (2001) Characterisation of three GLOBOSA-like MADS-box genes from maize: evidence for ancient paralogy in one class of floral homeotic B-function genes of grasses Gene 262: 1–13

    Article  PubMed  Google Scholar 

  • Ng M, Yanofsky MF, (2001) Function and evolution of the plant MADS-box gene family Nat. Rev. Genet. 2: 186–195

    Article  PubMed  CAS  Google Scholar 

  • Okamuro JK, Szeto W, Lotys-Prass C, Jofuku KD, (1997) Photo and hormonal control of meristem identity in the Arabidopsis flower mutants apetala2 and apetala1 Plant Cell 9: 37–47

    Article  PubMed  CAS  Google Scholar 

  • Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF, (2000) B and C floral organ identity functions require SEPALLATA MADS box genes Nature 405: 200–203

    Article  PubMed  CAS  Google Scholar 

  • Pnueli L, Hareven D, Broday L, Hurwitz C, Lifschitz E, (1994) The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers Plant Cell 6: 175–186

    Article  PubMed  CAS  Google Scholar 

  • Purugganan MD, Rounsley SD, Schmidt RJ, Yanofsky MF, (1995) Molecular evolution of flower development: Diversification of the plant MADS box regulatory gene family Genetics 140: 354–356

    Google Scholar 

  • Rabéchault H, Martin JP, (1976) Multiplication vegetative du palmier à huile (Elaeis guineensis Jacq.) à l’aide de cultures de tissues foliaires CR. Acad. Sci. Paris 238: 1735–1737

    Google Scholar 

  • Rounsley SD, Ditta GS, Yanofsky MF, (1995) Diverse roles for MADS box genes in Arabidopsis development Plant Cell 7: 1259–1269

    Article  PubMed  CAS  Google Scholar 

  • Savidge B, Rounsley SD, Yanofsky MF, (1995) Temporal relationships between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes Plant Cell 7: 721–733

    Article  PubMed  CAS  Google Scholar 

  • Schmidt RJ, Veit B, Mandel MA, Mena M, Hake S, Yanofsky MF, (1993) Identification and molecular characterization of ZAG1 the maize homolog of the Arabidopsis floral homeotic gene AGAMOUSPlant Cell 5: 729–737

    Article  PubMed  CAS  Google Scholar 

  • Schultz DJ, Craig R, Cox-Foster DL, Mumma RO, Medford JI, (1994) RNA isolation from recalcitrant plant tissue Plant Mol. Biol. Rep. 12: 310–316

    Article  CAS  Google Scholar 

  • Smulders MJM, Rus-Kortekaas W, Vosman B, (1995) Tissue culture-induced DNA methylation polymorphisms in repetitive DNA of tomato calli and regenerated plants Theor. Appl. Genet. 91: 1257–1264

    Article  CAS  Google Scholar 

  • Theissen G, Strater T, Fischer A, Saedler H, (1995) Structural characterization, chromosomal localization and phylogenetic evaluation of two pairs of AGAMOUS-like MADS-box genes from maize Gene 156: 155–166

    Article  PubMed  CAS  Google Scholar 

  • Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Munster T, Winter K-U, Saedler H, (2000) A short history of MADS box genes in plants Plant Mol. Biol. 42: 115–149

    Article  PubMed  CAS  Google Scholar 

  • Theissen G, (2001) Development of floral organ identity: stories from the MADS house Curr. Opin. Plant Biol. 4: 75–85

    Article  PubMed  CAS  Google Scholar 

  • Van der Linden CG, Vosman B, Smulders MJM, (2002) Cloning and characterization of four apple MADS box genes isolated from vegetative tissue J. Exp. Bot. 53: 1025–1036

    Article  PubMed  Google Scholar 

  • Van Engelen FA, Molthoff JW, Conner AJ, Nap JP, Pereira A, Stiekema WJ, (1995) pBINPLUS: an improved plant transformation vector based on pBIN19 Transgenic Res. 4: 288–290

    Article  PubMed  Google Scholar 

  • Van Heel WA, Breure CJ, Menendez T, (1987) The early development of inflorescences and flowers of the oil palm (Elaeis guineensis Jacq.) seen through the scanning electron microscope Blumea 32: 67–78

    Google Scholar 

  • Weigel D, Meyerowitz EM, (1994) The ABCs of floral homeotic genes Cell 78: 203–209

    Article  PubMed  CAS  Google Scholar 

  • Whipple CJ, Ciceri P, Padilla CM, Ambrose BA, Bandong SL, Schmidt RJ, (2004) Conservation of B-class floral homeotic gene function between maize and ArabidopsisDevelopment 131: 6083–6091

    Article  PubMed  CAS  Google Scholar 

  • Wong G, Tan CC, Soh AC, (1997) Large scale propagation of oil palm clones – experiences todate Acta Hort. (ISHS) 447: 649–658

    Google Scholar 

  • Xiao H, Wang Y, Liu D, Wang W, Li X, Zhao X, Xu J, Zhai W, Zhu L, (2003) Functional analysis of the rice AP3 homologue OsMADS16 by RNA interference Plant Mol. Biol. 52: 957–966

    Article  PubMed  CAS  Google Scholar 

  • Zachgo S, Silva EDA, Motte P, Troebner W, Saedler H, Schwarz Sommer Z, (1995) Functional analysis of the Antirrhinum flora homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant Development 121: 2861–2875

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank the Director-General of the Malaysian Palm Oil Board for allowing us to publish this work. Ineke Rus-Kortekaas is gratefully acknowledged for expert technical assistance, and Azizah Mokri and Roslan Ngadio for assistance with sample collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C.G. Van der Linden.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alwee, S.S., Van der Linden, C., Van der Schoot, J. et al. Characterization of oil palm MADS box genes in relation to the mantled flower abnormality. Plant Cell Tiss Organ Cult 85, 331–344 (2006). https://doi.org/10.1007/s11240-006-9084-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-006-9084-4

Keywords

Navigation