, 14:142 | Cite as

Metabolic fingerprinting analysis of oil palm reveals a set of differentially expressed metabolites in fatal yellowing symptomatic and non-symptomatic plants

  • Jorge Candido Rodrigues-Neto
  • Mauro Vicentini Correia
  • Augusto Lopes Souto
  • José Antônio de Aquino Ribeiro
  • Letícia Rios Vieira
  • Manoel Teixeira SouzaJr.
  • Clenilson Martins Rodrigues
  • Patrícia Verardi AbdelnurEmail author
Original Article
Part of the following topical collections:
  1. Plant metabolomics and lipidomics



Oil palm (E. guineensis), the most consumed vegetable oil in the world, is affected by fatal yellowing (FY), a condition that can lead to the plant’s death. Although studies have been performed since the 1980s, including investigations of biotic and abiotic factors, FY’s cause remains unknown and efforts in researches are still necessary.


This work aims to investigate the metabolic expression in plants affected by FY using an untargeted metabolomics approach.


Metabolic fingerprinting analysis of oil palm leaves was performed using ultra high liquid chromatography–electrospray ionization–mass spectrometry (UHPLC–ESI–MS). Chemometric analysis, using principal component analysis (PCA) and partial least square discriminant analysis (PLS-DA), was applied to data analysis. Metabolites identification was performed by high resolution mass spectrometry (HRMS), MS/MS experiments and comparison with databases and literature.


Metabolomics analysis based on MS detected more than 50 metabolites in oil palm leaf samples. PCA and PLS-DS analysis provided group segregation and classification of symptomatic and non-symptomatic FY samples, with a great external validation of the results. Nine differentially expressed metabolites were identified as glycerophosphorylcholine, arginine, asparagine, apigenin 6,8-di-C-hexose, tyramine, chlorophyllide, 1,2-dihexanoyl-sn-glycero-3-phosphoethanolamine, proline and malvidin 3-glucoside-5-(6″-malonylglucoside). Metabolic pathways and biological importance of those metabolites were assigned.


Nine metabolites were detected in a higher concentration in non-symptomatic FY plants. Seven are related to stress factors i.e. plant defense and nutrient absorption, which can be affected by the metabolic depression of these compounds. Two of those metabolites (glycerophosphorylcholine and 1,2-dihexanoyl-sn-glycero-3-phosphoethanolamine) are presented as potential biomarkers, since they have no known direct relation to plant stress.


Metabolomics Fatal yellowing Oil palm Chemometrics High resolution mass spectrometry Biomarkers 



The authors would like to thank the Brazilian Agricultural Research Corporation (EMBRAPA), the Federal Foundation for the Brazilian Research and Development (FINEP) and Coordination for the Improvement of Higher Education Personnel (CAPES) for the financial support; and Marborges Agroindustry S.A. for the E. guineensis leaves samples. The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The Grant (01.13.0315.02—DendePalm Project) for this study was awarded by the Brazilian Ministry of Science, Technology and Innovation (MCTI) via the Brazilian Innovation Agency (FINEP). The authors confirm that the funder had no influence over the study design, the content of article, or selection of this journal.

Author contributions

PVA designed and JCRN/JAAR performed the experiments. JCRN, ALS and MVC derived the models and analyzed the data. LRV and MTSJ performed the biological interpretations. PVA and JCRN wrote the manuscript in consultation with MVC, ALS, LRV, CMR and MTSJ. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Research involving human and animal participants

This article does not contain any studies with human and/or animal participants performed by any of the authors.

Supplementary material

11306_2018_1436_MOESM1_ESM.docx (547 kb)
Supplementary material 1 (DOCX 546 KB)


  1. Abdelnur, P. V., Caldana, C., & Martins, M. C. M. (2014). Metabolomics applied in bioenergy. Chemical and Biological Technologies in Agriculture, 1, 22. Scholar
  2. Acevedo, J. C., Hernandez, J. A., Valdes, C. F., & Khanal, S. K. (2015). Analysis of operating costs for producing biodiesel from palm oil at pilot-scale in Colombia. Bioresource Technology, 188, 117–123. Scholar
  3. Alcázar, R., Altabella, T., Marco, F., Bortolotti, C., Reymond, M., Koncz, C., et al. (2010). Polyamines: Molecules with regulatory functions in plant abiotic stress tolerance. Planta, 231, 1237. Scholar
  4. Balendres, M. A., Nichols, D. S., Tegg, R. S., & Wilson, C. R. (2016). Metabolomes of potato root exudates: Compounds that stimulate resting spore germination of the soil-borne pathogen Spongospora subterranea. Journal of Agricultural and Food Chemistry, 64, 7466–7474. Scholar
  5. Ballabio, D., & Consonni, V. (2013). Classification tools in chemistry. Part 1: Linear models. PLS-DA. Analytical Methods, 5, 3790–3798. Scholar
  6. Bennett, R. N., & Wallsgrove, R. M. (1994). Secondary metabolites in plant defence mechanisms. New Phytologist, 127, 617–633. Scholar
  7. Boari, A. J. (2008). Estudos realizados sobre o amarelecimento fatal do dendezeiro. 1st ed. Belém, PA: Embrapa Amazônia Oriental-Documentos (INFOTECA-E).Google Scholar
  8. Bourgis, F., et al. (2011). Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning. Proceedings of the National Academy of Sciences of the United States of America, 108, 12527–12532. Scholar
  9. Campos, C. G., et al. (2017). New protocol based on UHPLC-MS/MS for quantitation of metabolites in xylose-fermenting yeasts. Journal of the American Society for Mass Spectrometry. Scholar
  10. de Assis Costa, O. Y., Tupinambá, D. D., Bergmann, J. C., Barreto, C. C., & Quirino, B. F. (2018). Fungal diversity in oil palm leaves showing symptoms of Fatal Yellowing disease. PLoS One, 13(1), e0191884. Scholar
  11. Degtyarenko, K., et al. (2008). ChEBI: A database and ontology for chemical entities of biological interest. Nucleic Acids Research, 36, D344–D350. Scholar
  12. Di Sansebastiano, G. P., Fornaciari, S., Barozzi, F., Piro, G., & Arru, L. (2014). New insights on plant cell elongation: A role for acetylcholine. International Journal of Molecular Sciences, 15, 4565–4582. Scholar
  13. Dias, D. A., Urban, S., & Roessner, U. (2012). A historical overview of natural products in drug discovery. Metabolites, 2, 303–336. Scholar
  14. Domingos, P., Prado, A. M., Wong, A., Gehring, C., & Feijo, J. A. (2015). Nitric oxide: A multitasked signaling gas in plants. Molecular Plant Pathology, 8, 506–520. Scholar
  15. Duportet, X., Aggio, R. B. M., Carneiro, S., & Villas-Bôas, S. G. (2012). The biological interpretation of metabolomic data can be misled by the extraction method used. Metabolomics, 8, 410–421. Scholar
  16. FAOSTAT. (2018). Food and agriculture organization of the United Nations. Accessed 9 Oct 2018.
  17. Fiehn, O. (2001). Combining genomics, metabolome analysis, and biochemical modelling to understand metabolic networks. Comparative and Functional Genomics, 2, 155–168. Scholar
  18. Fiehn, O. (2002). Metabolomics—The link between genotypes and phenotypes. Plant Molecular Biology, 48, 155–171. Scholar
  19. Fraire-Velázquez, S., & Balderas-Hernández, V. E. (2013). Abiotic stress in plants and metabolic responses. Intech. Scholar
  20. Fu, Y., Liu, W., Zu, Y., Tong, M., Li, S., Yan, M., Efferth, T., & Luo, H. (2008). Enzyme assisted extraction of luteolin and apigenin from pigeonpea [Cajanuscajan (L.) Millsp.] leaves. Food Chemistry, 111, 508–512. Scholar
  21. Gaufichon, L., Reisdorf-Cren, M., Rothstein, S. J., Chardon, F., & Suzuki, A. (2010). Biological functions of asparagine synthetase in plants. Plant Science, 179, 141–153. Scholar
  22. Gaufichon, L., Rothstein, S. J., & Suzuki, A. (2016). Asparagine metabolic pathways in Arabidopsis. Plant and Cell Physiology, 57, 75–689. Scholar
  23. Giavalisco, P., et al. (2011). Elemental formula annotation of polar and lipophilic metabolites using C-13, N-15 and S-34 isotope labelling, in combination with high-resolution mass spectrometry. Plant Journal, 68, 364–376. Scholar
  24. Glauser, G., Veyrat, N., Rochat, B., Wolfender, J.-L., & Turlings, T. (2013). Ultra-high pressure liquid chromatography-mass spectrometry for plant metabolomics: A systematic comparison of high-resolution quadrupole-time-of-flight and single stage Orbitrap mass spectrometers. Journal of Chromatography A, 1292, 151–159.CrossRefGoogle Scholar
  25. Gowda, H., et al. (2014). Interactive XCMS online: Simplifying advanced metabolomic data processing and subsequent statistical analyses. Analytical Chemistry, 86, 6931–6939. Scholar
  26. Grata, E., et al. (2009). Metabolite profiling of plant extracts by ultra-high-pressure liquid chromatography at elevated temperature coupled to time-of-flight mass spectrometry. Journal of Chromatography A, 1216, 5660–5668. Scholar
  27. Gromova, M., & Roby, C. (2010). Toward Arabidopsis thaliana hydrophilic metabolome: Assessment of extraction methods and quantitative 1H NMR. Physiologia Plantarum, 140, 111–127. Scholar
  28. Gromski, P. S., Xu, Y., Correa, E., Ellis, D. I., Turner, M. L., & Goodacre, R. (2014). A comparative investigation of modern feature selection and classification approaches for the analysis of mass spectrometry data. Analytica Chimica Acta, 829, 1–8. Scholar
  29. Guillet, G., & De Luca, V. (2005). Wound-inducible biosynthesis of phytoalexin hydroxycinnamic acid amides of tyramine in tryptophan and tyrosine decarboxylase transgenic tobacco lines. Plant Physiology, 137, 692–699. Scholar
  30. Gupta, K., Dey, A., & Gupta, A. (2013). Plant polyamines in abiotic stress responses. Acta Physiol Plant, 35, 2015–2036. Scholar
  31. Hare, P. D., Cress, W. A., & Van Staden, J. (1998). Dissecting the roles of osmolyte accumulation during stress. Plant, Cell & Environment, 21, 535–553. Scholar
  32. Hu, X., Tanaka, A., & Tanaka, R. (2013). Simple extraction methods that prevent the artifactual conversion of chlorophyll to chlorophyllide during pigment isolation from leaf samples. Plant Methods, 9, 19. Scholar
  33. Hussain, S. S., Muhammad, A., Ahmad, M., & Siddique, K. H. M. (2011). Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants. Biotechnology Advances, 29, 300–311. Scholar
  34. Jorge, T. F., Rodrigues, J. A., Caldana, C., Schmidt, R., van Dongen, J. T., Thomas-Oates, J., & António, C. (2016). Mass spectrometry-based plant metabolomics: Metabolite responses to abiotic stress. Mass Spectrometry Reviews, 35, 620–649. Scholar
  35. Khan, T. A., Fariduddin, Q., & Yusuf, M. (2017). Low-temperature stress: Is phytohormones application a remedy? Environmental Science and Pollution Research, 24, 21574. Scholar
  36. Kim, H. K., Choi, Y. H., & Verpoorte, R. (2011). NMR-based plant metabolomics: Where do we stand, where do we go? Trends in Biotechnology, 29, 267–275. Scholar
  37. Kind, T., & Fiehn, O. (2010). Advances in structure elucidation of small molecules using mass spectrometry. Bioanalytical Reviews, 2, 23–60. Scholar
  38. Kovinich, N., Kayanja, G., Chanoca, A., Otegui, M. S., & Grotewold, E. (2015). Abiotic stresses induce different localizations of anthocyanins in Arabidopsis. Plant Signaling & Behavior, 10, e1027850. Scholar
  39. Krasensky, J., & Jonak, C. (2012). Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. Journal of Experimental Botany, 63, 1593–1608. Scholar
  40. Lea, P. J., Sodek, L., Parry, M. A. J., Shewry, P. R., & Halford, N. G. (2007). Asparagine in plants. Annals of Applied Biology, 150, 1–26. Scholar
  41. Lefèvre, I., Gratia, E., & Lutts, S. (2001). Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Science, 161, 943–952. Scholar
  42. Liang, X., Zhang, L., Natarajan, S. K., & Becker, D. F. (2013). Proline mechanisms of stress survival. Antioxidants & Redox Signaling, 19, 998–1011. Scholar
  43. Lotkowska, M. E., Tohge, T., Fernie, A. R., Xue, G. P., Balazadeh, S., & Mueller-Roeber, B. (2015). The Arabidopsis transcription factor MYB112 promotes anthocyanin formation during salinity and under high light stress. Plant Physiology, 169, 1862–1880. Scholar
  44. Ma, X., He, D., Ru, X., Chen, Y., Cai, Y., Bruce, I. C., et al. (2012). Apigenin, a plant-derived flavone, activates transient receptor potential vanilloid 4 cation channel. British Journal of Pharmacology, 166, 349–358. Scholar
  45. Mansour, M. (2000). Nitrogen containing compounds and adaptation of plants to salinity stress. Biologia Plantarum, 43, 491. Scholar
  46. Martinez, G., Sarria, G. A., Torres, G. A., & Varón, F. (2010). Advances in research on Phytophthora Palmivora, causal agent of bud rot of oil palm in Colombia. Palmas, 31(1), 55–63.CrossRefGoogle Scholar
  47. McEntyre, C. J., Lever, M., Chambers, S. T., MGeorge, P., Slow, S., Elmslie, J. L., et al. (2014). Variation of betaine, N,N-dimethylglycine, choline, glycerophosphorylcholine, taurine and trimethylamine-N-oxide in the plasma and urine of overweight people with type 2 diabetes over a two-year period. Annals of Clinical Biochemistry, 52, 352–360. Scholar
  48. Miean, K. H., & Mohamed, S. (2001). Flavonoid (myricetin, quercetin, kaempferol, luteolin, and apigenin) content of edible tropical plants. Journal of Agricultural and Food Chemistry, 49, 3106–3112. Scholar
  49. Murugesan, P., Aswathy, G. M., Sunil Kumar, K., Masilamani, P., Kumar, V., & Ravi, V. (2017). Oil palm (Elaeis guineensis) genetic resources for abiotic stress tolerance: A review. Indian Journal of Agricultural Sciences, 171, 12–17.Google Scholar
  50. Nagajyoti, P. C., Lee, K. D., & Sreekanth, T. V. M. (2010). Heavy metals, occurrence and toxicity for plants: A review. Environmental Chemistry Letters, 8, 199. Scholar
  51. Neuhofer, W., & Beck, F. X. (2006). Survival in hostile environments: Strategies of renal medullary cells. Physiology, 21, 171–180. Scholar
  52. Noor Lida, H. M. D., Sundram, K., Siew, W. L., Aminah, A., & Mamot, S. (2002). TAG composition and solid fat content of palm oil, sunflower oil, and palm kernel olein belends before and after chemical interesterification. Journal of the American Oil Chemists’ Society, 79, 1137–1144. Scholar
  53. Obata, T., & Fernie, A. R. (2012). The use of metabolomics to dissect plant responses to abiotic stresses. Cellular and Molecular Life Sciences, 69, 3225–3243. Scholar
  54. Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999). KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Research, 27, 29–34. Scholar
  55. Pant, B.-D., Pant, P., Erban, A., Huhman, D., Kopka, J., & Scheible, W.-R. (2015). Identification of primary and secondary metabolites with phosphorus status-dependent abundance in Arabidopsis, and of the transcription factor PHR1 as a major regulator of metabolic changes during phosphorus limitation. Plant, Cell & Environment, 38, 172–187. Scholar
  56. Pietta, P. G. (2000). Flavonoids as antioxidants. Journal of Natural Products, 63, 1035–1042. Scholar
  57. Putri, S. P., & Fukusaki, E. (2014). Mass spectrometry-based metabolomics—A practical guide. 1st edn, Boca Raton: CRC Press.CrossRefGoogle Scholar
  58. Qiao, W., & Fan, L. M. (2008). Nitric oxide signaling in plant responses to abiotic stresses. Journal of Integrative Plant Biology, 50, 1238–1246. Scholar
  59. Ramakrishna, A., & Ravishankar, G. A. (2011). Influence of abiotic stress signals on secondary metabolites in plants. Plant Signaling & Behavior, 6, 1720–1731. Scholar
  60. Rodrigues, M. D., Amblard, P., Barcelos, E., de Macedo, J. L., da Cunha, R. N., Tavares, A. M. (2007). Avaliação do estado nutricional do dendezeiro: Análise foliar (reformulada), Embrapa Amazônia Ocidental-Comunicado Técnico (INFOTECA-E).Google Scholar
  61. Rontein, D., Basset, G., & Hanson, A. D. (2002). Metabolic engineering of osmoprotectant accumulation in plants. Metabolic Engineering, 4, 49–56. Scholar
  62. Rozali, N., Yarmo, M., Idris, A., Kushairi, A., & Ramli, U. (2017). Metabolomics differentiation of oil palm (Elaeis guineensis Jacq.) spear leaf with contrasting susceptibility to Ganoderma boninense. Plant OMICS, 10, 45–52. Scholar
  63. Santos Filho, P. R., Santos, B. R., Barbosa, S., Vieira, L. R., Freitas, N. C., Dias, D. F., et al. (2014). Growth curve, biochemical profile and phytochemical analyses in calli obtained from the procambium segments of Bacupari. Brazilian Archives of Biology and Technology, 57, 326–333. Scholar
  64. Servillo, L., et al. (2017). Tyramine pathways in citrus plant defense: Glycoconjugates of tyramine and its N-methylated derivatives. Journal of Agricultural and Food Chemistry, 65, 892–899. Scholar
  65. Shi, H., & Chan, Z. (2014). Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. Journal of Integrative Plant Biology, 56, 114–121. Scholar
  66. Shulaev, V., Cortes, D., Miller, G., & Mittler, R. (2008). Metabolomics for plant stress response. Physiologia Plantarum, 132, 199–208. Scholar
  67. Sicher, R. C., & Barnaby, J. Y. (2012). Impact of carbon dioxide enrichment on the responses of maize leaf transcripts and metabolites to water stress. Physiologia Plantarum, 144, 238–253. Scholar
  68. Slocum, R. D. (2005). Genes, enzymes and regulation of arginine biosynthesis in plants. Plant Physiology and Biochemistry, 43, 729–745.CrossRefGoogle Scholar
  69. Smith, C. A., et al. (2005). METLIN—A metabolite mass spectral database. Therapeutic Drug Monitoring, 27, 747–751. Scholar
  70. Smith, L. I. (2002). A tutorial on principal components analysis (1st ed.). Ithaca: Cornell University.Google Scholar
  71. STATISTA. (2018). Statista - The portal for statistics. Accessed 9 Oct 2018.
  72. Suzuki, N., Rivero, R. M., Shulaev, V., Blumwald, E., & Mittler, R. (2014). Abiotic and biotic stress combinations. New Phytologist, 203, 32–43. Scholar
  73. Tahir, N. I., Shaari, K., Abas, F., Parveez, G. K. A., Hashim, A. T., & Ramli, U. S. (2013). Identification of oil palm (Elaeis guineensis) spear leaf metabolites using mass spectrometry and neutral loss analysis. Journal of Oil Palm Research, 25, 72–83.Google Scholar
  74. Tahir, N. I., Shaari, K., Abas, F., Parveez, G. K. A., Ishak, Z., & Ramli, U. S. (2012). Characterization of apigenin and luteolin derivatives from oil palm (Elaeis guineensis Jacq.) leaf using LC-ESI-MS/MS. Journal of Agricultural and Food Chemistry, 60, 11201–11210. Scholar
  75. Tanaka, Y., Sasaki, N., & Ohmiya, A. (2008). Biosynthesis of plant pigments: Anthocyanins, betalains and carotenoids. The Plant Journal, 54, 733–749. Scholar
  76. Tautenhahn, R., Patti, G. J., Rinehart, D., & Siuzdak, G. (2012). XCMS online: A web-based platform to process untargeted metabolomic data. Analytical Chemistry, 84, 5035–5039. Scholar
  77. Tawaraya, K., Horie, R., Saito, S., Wagatsuma, T., Saito, K., & Oikawa, A. (2014a). Metabolite profiling of root exudates of common bean under phosphorus deficiency. Metabolites, 4, 599–611. Scholar
  78. Tawaraya, K., Horie, R., Shinano, T., Wagatsuma, T., Saito, K., & Oikawa, A. (2014b). Metabolite profiling of soybean root exudates under phosphorus deficiency. Soil Science and Plant Nutrition, 60, 679–694. Scholar
  79. Tawaraya, K., et al. (2013). Metabolite profiling of shoot extracts, root extracts, and root exudates of rice plant under phosphorus deficiency. Journal of Plant Nutrition 36, 1138–1159 Scholar
  80. Tyagi, S., Raghvendra, U., Singh, T., Kalra, K., & Munjal (2010). Applications of metabolomics—A systematic study of the unique chemical fingerprints: An overview. International Journal of Pharmaceutical Sciences Review and Research, 3, 83–86.Google Scholar
  81. Urano, K., Kurihara, Y., Seki, M., & Shinozaki, K. (2010). ‘Omics’ analyses of regulatory networks in plant abiotic stress responses. Current Opinion in Plant Biology, 13, 132–138. Scholar
  82. van der Rest, B., Boisson, A. M., Gout, E., Bligny, R., & Douce, R. (2002). Glycerophosphocholine metabolism in higher plant cells. Evidence of a new glyceryl-phosphodiester phosphodiesterase. Plant Physiology, 130, 244–255. Scholar
  83. Vargas, L. H. G., et al. (2016). Metabolomics analysis of oil palm (Elaeis guineensis) leaf: Evaluation of sample preparation steps using UHPLC-MS/MS. Metabolomics. Scholar
  84. Verbruggen, N., & Hermans, C. (2008). Proline accumulation in plants: A review. Amino Acids, 35, 753. Scholar
  85. Vitavska, O., Edemir, B., & Wieczorek, H. (2016). Putative role of the H+/sucrose symporter SLC45A3 as an osmolyte transporter in the kidney. Archiv European Journal of Physiology, 468, 1353. Scholar
  86. Vuckovic, D. (2012). Current trends and challenges in sample preparation for global metabolomics using liquid chromatography-mass spectrometry. Analytical and Bioanalytical Chemistry, 403, 1523–1548. Scholar
  87. Wimalasekera, R., Tebartz, F., & Scherer, G. F. E. (2011). Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Science, 181, 593–603. Scholar
  88. Wu, H. F., et al. (2013). Recent developments in qualitative and quantitative analysis of phytochemical constituents and their metabolites using liquid chromatography-mass spectrometry. Journal of Pharmaceutical and Biomedical Analysis, 72, 267–291. Scholar
  89. Xia, J., & Wishart, D. S. (2016). Using MetaboAnalyst 3.0 for comprehensive metabolomics data analysis current protocols in bioinformatics. New York: WileyGoogle Scholar
  90. Xia, J. G., Sinelnikov, I. V., Han, B., & Wishart, D. S. (2015). MetaboAnalyst 3.0-making metabolomics more meaningful. Nucleic Acids Research, 43, W251–W257. Scholar
  91. Zhao, D., & Tao, J. (2015). Recent advances on the development and regulation of flower color in ornamental plants. Frontiers in Plant Science, 6, 261. Scholar
  92. Zhu, X. F., Wan, J. X., Sun, Y., Shi, Y. Z., Braam, J., Li, G. X., et al. (2014). Xyloglucan Endotransglucosylase-Hydrolase17 interacts with xyloglucan endotransglucosylase-hydrolase31 to confer xyloglucan endotransglucosylase action and affect aluminum sensitivity in Arabidopsis. Plant Physiology, 165, 1566–1574. Scholar

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Authors and Affiliations

  • Jorge Candido Rodrigues-Neto
    • 1
    • 2
  • Mauro Vicentini Correia
    • 1
    • 3
  • Augusto Lopes Souto
    • 1
  • José Antônio de Aquino Ribeiro
    • 1
  • Letícia Rios Vieira
    • 1
    • 4
  • Manoel Teixeira SouzaJr.
    • 1
    • 4
  • Clenilson Martins Rodrigues
    • 1
  • Patrícia Verardi Abdelnur
    • 1
    • 2
    Email author
  1. 1.Brazilian Agricultural Research CorporationEmbrapa AgroenergyBrasíliaBrazil
  2. 2.Institute of ChemistryFederal University of GoiásGoiâniaBrazil
  3. 3.Institute of ChemistryUniversity of Brasília, Campus Universitário Darcy RibeiroBrasíliaBrazil
  4. 4.Graduate Program in Plant BiotechnologyFederal University of LavrasLavrasBrazil

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