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Developmental changes in the composition of leaf cuticular wax of banana influenced by wax biosynthesis gene expression: a case study in Musa acuminata and Musa balbisiana

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Abstract

The composition of the cuticular wax varies from species to species as well as the developmental stage of the organ. In the present study, the variation in the pattern of accumulation of C28 and > C28 chain length of the cuticular wax compounds in the two contrasting Musa species for wax content has been examined—Musa balbisiana ‘Bee heekela’ (BB genome) (with high wax content) and Musa acuminata ssp. Burmannicoides Colla—‘Calcutta-4’ (AA genome) (with low wax content). These two species are the progenitors for the modern cultivated banana. Using GC–MS analysis, 40 different cuticular wax compounds from five different leaf developmental stages in these two musa species were identified. Around tenfold higher accumulation of C28 length compounds was found in ‘Calcutta-4’ as compared to that of ‘Bee hee kela’. In case of ‘Bee hee kela’,  > C28 length compounds were in large proportion compared to C28 length wax compounds. The qPCR analysis was carried out for the gene CUT1/CER6/KCS6 which are involved in the fatty acid elongation step of cuticular wax biosynthesis. A higher expression in the 2nd (young), 4th and 6th (old) fully expanded leaves of high wax genotype ‘Bee hee kela’ with 1.57083, 9.71512, and 1.44963 fold change, whereas a lower expression of 0.9151, 4.8785, and 1.2321 fold change in low wax genotype ‘Calcutta-4’, respectively, was observed. A negative relationship between the gene expression and C28 wax compounds’ accumulation was observed, indicating the importance of the expression of CUT1/CER6/KCS6 gene for elongation of C28 to > C28 cuticular wax compounds. The current study suggest that CUT1/CER6/KCS6 from ‘Bee heekela’ would be a good contributor for higher cuticular wax with higher > C28 compounds, thus, finally, contributing for higher leaf water retention capacity their by conferring drought tolerance helping in the future banana improvement programs.

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References

  • Albanes D, Heinonen OP, Taylor PR, Virtamo J, Edwards BK, Rautalahti M, Barrett MJ (1996) α-Tocopherol and β-carotene supplements and lung cancer incidence in the Alpha-Tocopherol, beta-carotene cancer prevention study: effects of base-line characteristics and study compliance. J Natl Cancer Inst 88(21):1560–1570

    Article  CAS  Google Scholar 

  • Bakker MI, Baas WJ, Sijm DT, Kolloffel C (1998) Leaf wax of Lactuca sativa and Plantago major. Phytochemistry 47(8):1489–1493

    Article  CAS  Google Scholar 

  • Bauer S, Schulte E, Their HP (2004) Composition of the surface wax from tomatoes. Eur Food Res Technol 219(3):223–228

    Article  CAS  Google Scholar 

  • Bernard A, Joubes J (2013) Arabidopsis cuticular waxes: advances in synthesis, export and regulation. Prog Lipid Res 52(1):110–129

    Article  CAS  Google Scholar 

  • Buschhaus C, Jetter R (2011) Composition differences between epicuticular and intracuticular wax substructures: how do plants seal their epidermal surfaces? J Exp Bot 62:841–853

    Article  CAS  Google Scholar 

  • Busta L, Hegebarth D, Kroc E, Jetter R (2017) Changes in cuticular wax coverage and composition on developing Arabidopsis leaves are influenced by wax biosynthesis gene expression levels and trichome density. Planta 245(2):297–311

    Article  CAS  Google Scholar 

  • Bustin SA (2004) Quantification of nucleic acids by PCR. In: Bustin SA (ed) A Z of quantitative PCR, IUL biotechnology series. International University Line, La Jolla, pp 3–48

    Google Scholar 

  • Chang S (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Cheesman EE (1932) Genetic and cytological studies of Musa. J Genet 26(3):291–312

    Article  Google Scholar 

  • Chen L, Zhong HY, Kuang JF, Li JG, Lu WJ, Chen JY (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234(2):377

    Article  CAS  Google Scholar 

  • Cizkova J, Hribova E, Humplíkova L, Christelova P, Suchankova P, Dolezel J (2013) Molecular analysis and genomic organization of major DNA satellites in banana (Musa spp.). PLoS One 8(1):e54808

    Article  CAS  Google Scholar 

  • D’Hont Angelique, Denoeud France, Aury Jean-Marc, Baurens Franc-Christophe, Carreel Francoise, Garsmeur Olivier, Noel Benjamin et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488(7410):213

    Article  Google Scholar 

  • Fiebig A, Mayfield JA, Miley NL, Chau S, Fischer RL, Preuss D (2000) Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell 12(10):2001–2008

    Article  CAS  Google Scholar 

  • Food and Agriculture Organization of the United Nations (FAO) (2016). http://faostat.fao.org. Accessed 25 Oct 2017

  • Gonzales R, Ruiz-Silvera C, Bleiholder H, Hack H, Meier U and Wicke H (2002) Proposal for codification of the phenological cycle of edible musaceae. In: Proceedings of XV Reunión International ACORBAT Meeting, pp. 412–417

  • Hauke V, Schreiber L (1998) Ontogenetic and seasonal development of wax composition and cuticular transpiration of ivy (Hedera helix L.) sun and shade leaves. Planta 207(1):67–75

    Article  CAS  Google Scholar 

  • Hooker TS, Millar AA, Kunst L (2002) Significance of the expression of the CER6 condensing enzyme for cuticular wax production in Arabidopsis. Plant Physiol 129(4):1568–1580

    Article  CAS  Google Scholar 

  • Jeffree CE (2006) The fine structure of the plant cuticle. In: Riederer M, Muller C (eds) Biology of the plant cuticle, vol 23. Annual Plant Reviews. Blackwell Publishing, Oxford, pp 11–125

    Chapter  Google Scholar 

  • Jetter R, Schaffer S (2001) Chemical composition of the Prunus laurocerasus leaf surface. Dynamic changes of the epicuticular wax film during leaf development. Plant Physiol 126(4):1725–1737

    Article  CAS  Google Scholar 

  • Jetter R, Kunst L, Samuels AL (2006) Composition of plant cuticular waxes. In: Riederer M, Muller C (eds) Biology of the plant cuticle, vol 23. Annual Plant Reviews. Blackwell Publishing, Oxford, pp 145–181

    Chapter  Google Scholar 

  • Kerstiens G (1996) Cuticular water permeability and its physiological significance. J Exp Bot 47(12):1813–1832

    Article  CAS  Google Scholar 

  • Kim M-S, Shim K-B, Park S-H, Kim K-S (2009) Changes in cuticular waxes of developing leaves in sesame (Sesamum indicum L.). J Crop Sci Biotechnol 12(3):161–167

    Article  Google Scholar 

  • Kim J, Jung JH, Lee SB, Go YS, Kim HJ, Cahoon R, Suh MC (2013) Arabidopsis 3-ketoacyl-coenzyme a synthase9 is involved in the synthesis of tetracosanoic acids as precursors of cuticular waxes, suberins, sphingolipids, and phospholipids. Plant Physiol 162(2):567–580

    Article  CAS  Google Scholar 

  • Kovats ES (1965) Gas chromatographic characterization of organic substances in the retention index system. Adv Chromatogr 1:229

    CAS  Google Scholar 

  • Kunst L (2015) New insights into biosynthesis of cuticular wax. FASEB J 29:366-3

    Google Scholar 

  • Kunst L, Samuels L (2009) Plant cuticles shine: advances in wax biosynthesis and export. Curr Opin Plant Biol 12(6):721–727

    Article  CAS  Google Scholar 

  • Lahav E (1995) Banana nutrition. Bananas and plantains, World Crop Series. Springer, Dordrecht, pp 258–316

    Chapter  Google Scholar 

  • Leide J, Hildebrandt U, Reussing K, Riederer M, Vogg G (2007) The developmental pattern of tomato fruit wax accumulation and its impact on cuticular transpiration barrier properties: effects of a deficiency in a β-ketoacyl-coenzyme A synthase (LeCER6). Plant Physiol 144(3):1667–1679

    Article  CAS  Google Scholar 

  • Lescot M, Piffanelli P, Ciampi AY, Ruiz M, Blanc G, Leebens-Mack J, da Silva FR, Santos CM, D’Hont A, Garsmeur O, Vilarinhos AD (2008) Insights into the Musa genome: syntenic relationships to rice and between Musa species. BMC Genom 9(1):58

    Article  Google Scholar 

  • Masaki H (2010) Role of antioxidants in the skin: anti-aging effects. J Dermatol Sci 58(2):85–90

    Article  CAS  Google Scholar 

  • Millar AA, Clemens S, Zachgo S, Giblin EM, Taylor DC, Kunst L (1999) CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell 11(5):825–838

    Article  CAS  Google Scholar 

  • Pollefeys P, Sharrock S, Arnaud E (2004) Preliminary analysis of the literature on the distribution of wild Musa species using MGIS and DIVA-GIS. INIBAP-IPGRI, Montpellier

    Google Scholar 

  • Ravishankar KV, Sampangi-Ramaiah MH, Ajitha R, Khadke GN, Chellam V (2015) Insights into Musa balbisiana and Musa acuminata species divergence and development of genic microsatellites by transcriptomics approach. Plant Gene 4:78–82

    Article  Google Scholar 

  • Rekha A (2016) History, Origin, Domestication, and Evolution. In: Sukhada M, Ravishankar KV (eds) Banana: genomics and transgenic approaches for genetic improvement. Springer, Singapore, pp 3–11

    Chapter  Google Scholar 

  • Robinson JC, Sauco VG (2010) Bananas and plantains. CABI Publishing, Wallingford

    Book  Google Scholar 

  • Sampangi-Ramaiah MH, Ravishankar KV (2016) Current status of banana genome in the age of next generation sequencing. In: Sukhada M, Ravishankar KV (eds) Banana: genomics and transgenic approaches for genetic improvement. Springer, Singapore, pp 51–59

    Chapter  Google Scholar 

  • Sampangi-Ramaiah MH, Ravishankar KV, Seetharamaiah SK, Roy TK, Hunashikatti LR, Rekha A, Shilpa P (2016) Barrier against water loss: relationship between epicuticular wax composition, gene expression and leaf water retention capacity in banana. Funct Plant Biol 43(6):492–501

    Article  CAS  Google Scholar 

  • Sampangi-Ramaiah MH, Ravishankar KV, Rekha A, Shivashankara KS, Hunashikatti LR (2017) A contig-based computational prediction of conserved mirnas and their probable role in regulation of cuticular wax biosynthesis in banana. Plant Mol Biol Rep 35(2):203–214

    Article  CAS  Google Scholar 

  • Sampangi-Ramaiah MH, Ravishankar KV, Rekha A (2018) Long non-coding RNAs in banana: prediction, mapping and their comparative studies using Musa balbisiana and Musa acuminata transcriptome. Trees. https://doi.org/10.1007/s00468-018-1781-1

    Article  Google Scholar 

  • Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol 59:683–707. https://doi.org/10.1146/annurev.arplant.59.103006.093219

    Article  CAS  PubMed  Google Scholar 

  • Sano M, Ernesto C, Thomas RG, Klauber MR, Schafer K, Grundman M, Schneider LS (1997) A controlled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer’s disease. N Engl J Med 336(17):1216–1222

    Article  CAS  Google Scholar 

  • Sarin (2017) This is why you must eat on a banana leaf. NDTV food. https://food.ndtv.com/food-drinks/this-is-why-you-must-eat-on-a-banana-leaf-1793056. Accessed Jun 2018

  • Stammitti L, Derridj S, Garrec JP (1996) Leaf epicuticular lipids of Prunus laurocerasus: importance of extraction methods. Phytochemistry 43(1):45–48. https://doi.org/10.1016/0031-9422(96)00241-5

    Article  CAS  Google Scholar 

  • Stover RH, Simmonds NW (1987) Bananas, 3rd edn. Longman Scientific & Technical, Harlow

    Google Scholar 

  • Tuberosa R (2012) Phenotyping for drought tolerance of crops in the genomics era. Front Physiol 3:347. https://doi.org/10.3389/fphys.2012.00347

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu W, Yang YL, He WM, Rouard M, Li WM, Xu M, Ge XJ (2016) Whole genome sequencing of a banana wild relative Musa itinerans provides insights into lineage-specific diversification of the Musa genus. Sci Rep 6:31586

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the Indian Council of Agricultural Research, New Delhi for financial assistance through the ICAR Network Project on Transgenics in Crops: Functional Genomics-Fusarium wilt and drought tolerance in Banana.

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Authors and Affiliations

  1. Division of Biotechnology, ICAR-Indian Institute of Horticultural Research, Hessaraghatta Lake Post, Bengaluru, 560089, India

    Megha Hastantram Sampangi-Ramaiah & Kundapura Venkataramana Ravishankar

  2. Division of Plant Physiology and Biochemistry, ICAR-Indian Institute of Horticultural Research, Hessaraghatta Lake Post, Bengaluru, 560089, India

    Kodthalu Seetharamaiah Shivashankar, Tapas Kumar Roy & Laxman R. Hunashikatti

  3. Division of Fruit Crops, ICAR-Indian Institute of Horticultural Research, Heatssaraghta Lake Post, Bengaluru, 560089, India

    Ajitha Rekha

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  1. Megha Hastantram Sampangi-Ramaiah
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Correspondence to Kundapura Venkataramana Ravishankar.

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Sampangi-Ramaiah, M.H., Ravishankar, K.V., Shivashankar, K.S. et al. Developmental changes in the composition of leaf cuticular wax of banana influenced by wax biosynthesis gene expression: a case study in Musa acuminata and Musa balbisiana. Acta Physiol Plant 41, 141 (2019). https://doi.org/10.1007/s11738-019-2934-6

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