Frankincense Tree Physiology and Its Responses to Wounding Stress

  • Ahmed Al-Harrasi
  • Abdul Latif Khan
  • Sajjad Asaf
  • Ahmed Al-Rawahi


Boswellia trees are often tapped using wounding or tapping for resin collection, which is an anthropogenic activity with human-derived benefits. The tree responds to these incisions by producing resin to defend itself from the attacks of fungal pathogens, herbivores and insects. Although the resin biosynthesis pathway has not yet been fully elucidated, the tree physiology of B. sacra and B. papyrifera has recently been studied. The wounding response of B. sacra in terms of biochemical modulation has been studied by assessing the endogenous phytohormones (gibberellic acid, salicylic acid, abscisic acid and jasmonic acid), essential amino acids and related gene expression. In B. papyrifera, the vapour pressure deficit and stomatal closure in response to tapping were studied through starch/sugar metabolism and leaf gas exchange. Most defence-related biochemical pathways are activated to cope with wounding stress. However, these responses may also vary depending on the tree health, climatic conditions and growth environment. Furthermore, in-depth studies are essential for understanding the growth, ecophysiology and transcriptional regulation under a variety of environmental stresses such as heat, drought and high mineral-containing soil.


Wounding Physiochemical responses Amino acid Phytohormones Stomata Sugar metabolism Biochemical pathways Gene expression 


  1. Al-Harrasi, A., Rehman, N. U., Khan, A. L., Al-Broumi, M., Al-Amri, I., Hussain, J., … Csuk, R. (2018). Chemical, molecular and structural studies of Boswellia species: β-Boswellic Aldehyde and 3-epi-11β-Dihydroxy BA as precursors in biosynthesis of boswellic acids. PLoS One, 13(6), e0198666.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bansal, S., & Germino, M. J. (2009). Temporal variation of nonstructural carbohydrates in montane conifers: Similarities and differences among developmental stages, species and environmental conditions. Tree Physiology, 29(4), 559–568.PubMedCrossRefGoogle Scholar
  3. Bilal, S., Khan, A. L., Shahzad, R., Kim, Y.-H., Imran, M., Khan, M. J., … Lee, I.-J. (2018). Mechanisms of Cr (VI) resistance by endophytic Sphingomonas sp. LK11 and its Cr (VI) phytotoxic mitigating effects in soybean (Glycine max L.). Ecotoxicology and Environmental Safety, 164, 648–658.PubMedCrossRefGoogle Scholar
  4. Bömke, C., & Tudzynski, B. (2009). Diversity, regulation, and evolution of the gibberellin biosynthetic pathway in fungi compared to plants and bacteria. Phytochemistry, 70(15–16), 1876–1893.PubMedCrossRefGoogle Scholar
  5. Bown, A. W., & Shelp, B. J. (2016). Plant GABA: not just a metabolite. Trends in Plant Science, 21(10), 811–813.PubMedCrossRefGoogle Scholar
  6. Campanello, P. I., Gatti, M. G., & Goldstein, G. (2008). Coordination between water-transport efficiency and photosynthetic capacity in canopy tree species at different growth irradiances. Tree Physiology, 28(1), 85–94.PubMedCrossRefGoogle Scholar
  7. Choi, W. G., Miller, G., Wallace, I., Harper, J., Mittler, R., & Gilroy, S. (2017). Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals. The Plant Journal, 90(4), 698–707.PubMedCrossRefGoogle Scholar
  8. Davey, M., Stals, E., Panis, B., Keulemans, J., & Swennen, R. (2005). High-throughput determination of malondialdehyde in plant tissues. Analytical Biochemistry, 347(2), 201–207.PubMedCrossRefGoogle Scholar
  9. Dekkers, B. J., & Smeekens, S. C. (2018). Sugar and abscisic acid regulation of germination and transition to seedling growth. Annual Plant Reviews, 27, 305–327.Google Scholar
  10. Eshete, A., Sterck, F. J., & Bongers, F. (2012). Frankincense production is determined by tree size and tapping frequency and intensity. Forest Ecology and Management, 274, 136–142.CrossRefGoogle Scholar
  11. Farah, A. Y. (1994). The milk of the Boswellia forests: frankincense production among the pastoral Somali: EPOS, Environmental Policy and Society, Uppsala, Sweden.Google Scholar
  12. Fariduddin, Q., Hayat, S., & Ahmad, A. (2003). Salicylic acid influences net photosynthetic rate, carboxylation efficiency, nitrate reductase activity, and seed yield in Brassica juncea. Photosynthetica, 41(2), 281–284.CrossRefGoogle Scholar
  13. Farmer, E. E., Alméras, E., & Krishnamurthy, V. (2003). Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Current Opinion in Plant Biology, 6(4), 372–378.PubMedCrossRefGoogle Scholar
  14. Guo, W., Nazim, H., Liang, Z., & Yang, D. (2016). Magnesium deficiency in plants: An urgent problem. The Crop Journal, 4(2), 83–91.CrossRefGoogle Scholar
  15. Hauser, F., Li, Z., Waadt, R., & Schroeder, J. I. (2017). SnapShot: abscisic acid signaling. Cell, 171(7), 1708–1708. e1700.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Hayat, S., Fariduddin, Q., Ali, B., & Ahmad, A. (2005). Effect of salicylic acid on growth and enzyme activities of wheat seedlings. Acta Agronomica Hungarica, 53(4), 433–437.CrossRefGoogle Scholar
  17. Hayat, S., Yadav, S., Ali, B., & Ahmad, A. (2010). Interactive effect of nitric oxide and brassinosteroids on photosynthesis and the antioxidant system of Lycopersicon esculentum. Russian Journal of Plant Physiology, 57(2), 212–221.CrossRefGoogle Scholar
  18. Hedden, P., & Sponsel, V. (2015). A century of gibberellin research. Journal of Plant Growth Regulation, 34(4), 740–760.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Hedden, P., & Thomas, S. G. (2012). Gibberellin biosynthesis and its regulation. Biochemical Journal, 444(1), 11–25.PubMedCrossRefGoogle Scholar
  20. Helander, J. D., & Cutler, S. R. (2018). Abscisic acid signaling and biosynthesis: Protein structures and molecular probes. In Plant Structural Biology: Hormonal Regulations (pp. 113–146). Springer, Cham.Google Scholar
  21. Hofstetter, R., Mahfouz, J. B., Klepzig, K. D., & Ayres, M. (2005). Effects of tree phytochemistry on the interactions among endophloedic fungi associated with the southern pine beetle. Journal of Chemical Ecology, 31(3), 539–560.PubMedCrossRefGoogle Scholar
  22. Holbrook, N. M., & Knoblauch, M. (2018). Editorial overview: Physiology and metabolism: Phloem: a supracellular highway for the transport of sugars, signals, and pathogens: Current Opinion in Plant Biology, 43, iii-vii.Google Scholar
  23. Hyodo, H. (2017). Stress/wound ethylene The plant hormone ethylene (pp. 43-63): CRC Press, Florida, USA.Google Scholar
  24. Jacobo-Velázquez, D. A., González-Agüero, M., & Cisneros-Zevallos, L. (2015). Cross-talk between signaling pathways: The link between plant secondary metabolite production and wounding stress response. Scientific Reports, 5, 8608.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Kebede, T. (2010). Current production systems of frankincense from Boswellia papyrifera tree; its implications on sustainable utilization of the resource. MSc thesis, Mekelle University, Mekelle.Google Scholar
  26. Khan, A. L., Al-Harrasi, A., Al-Rawahi, A., Al-Farsi, Z., Al-Mamari, A., Waqas, M., … Shin, J.-H. (2016). Endophytic fungi from frankincense tree improves host growth and produces extracellular enzymes and indole acetic acid. PLoS One, 11(6), e0158207.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Khan, A. L., Al-Harrasi, A., Shahzad, R., Imran, Q. M., Yun, B.-W., Kim, Y.-H., … Lee, I.-J. (2018). Regulation of endogenous phytohormones and essential metabolites in frankincense-producing Boswellia sacra under wounding stress. Acta Physiologiae Plantarum, 40(6), 113.CrossRefGoogle Scholar
  28. Khan, A. L., Hamayun, M., Kang, S.-M., Kim, Y.-H., Jung, H.-Y., Lee, J.-H., & Lee, I.-J. (2012). Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: An example of Paecilomyces formosus LHL10. BMC Microbiology, 12(1), 3.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Khan, A. L., Hussain, J., Al-Harrasi, A., Al-Rawahi, A., & Lee, I.-J. (2015). Endophytic fungi: Resource for gibberellins and crop abiotic stress resistance. Critical Reviews in Biotechnology, 35(1), 62–74.PubMedCrossRefGoogle Scholar
  30. Khan, A. L., Waqas, M., Asaf, S., Kamran, M., Shahzad, R., Bilal, S., … Yun, B.-W. (2017). Plant growth-promoting endophyte Sphingomonas sp. LK11 alleviates salinity stress in Solanum pimpinellifolium. Environmental and Experimental Botany, 133, 58–69.CrossRefGoogle Scholar
  31. Khan, A. L., Waqas, M., Hussain, J., Al-Harrasi, A., Hamayun, M., & Lee, I.-J. (2015a). Phytohormones enabled endophytic fungal symbiosis improve aluminum phytoextraction in tolerant Solanum lycopersicum: An examples of Penicillium janthinellum LK5 and comparison with exogenous GA3. Journal of Hazardous Materials, 295, 70–78.PubMedCrossRefGoogle Scholar
  32. Khan, A. L., Waqas, M., Hussain, J., Al-Harrasi, A., Hamayun, M., & Lee, I.-J. (2015b). Phytohormones enabled endophytic fungal symbiosis improve aluminum phytoextraction in tolerant Solanum lycopersicum: An examples of Penicillium janthinellum LK5 and comparison with exogenous GA 3. Journal of Hazardous Materials, 295, 70–78.PubMedCrossRefGoogle Scholar
  33. Khan, M. A., Ungar, I. A., & Showalter, A. M. (2000). Effects of sodium chloride treatments on growth and ion accumulation of the halophyte Haloxylon recurvum. Communications in Soil Science & Plant Analysis, 31(17–18), 2763–2774.CrossRefGoogle Scholar
  34. Kim, D. S., & Hwang, B. K. (2014). An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. Journal of Experimental Botany, 65(9), 2295–2306.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Kim, I. S., Koppula, S., Park, S. Y., & Choi, D. K. (2017). Analysis of epidermal growth factor receptor related gene expression changes in a cellular and animal model of Parkinson’s disease. International Journal of Molecular Sciences, 18(2). Scholar
  36. Kim, Y.-B., Kim, S.-M., Kang, M.-K., Kuzuyama, T., Lee, J. K., Park, S.-C., … Kim, S.-U. (2009). Regulation of resin acid synthesis in Pinus densiflora by differential transcription of genes encoding multiple 1-deoxy-D-xylulose 5-phosphate synthase and 1-hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase genes. Tree Physiology, 29(5), 737–749.PubMedCrossRefGoogle Scholar
  37. Kim, Y.-H., Hwang, S.-J., Waqas, M., Khan, A. L., Lee, J.-H., Lee, J.-D., … Lee, I.-J. (2015). Comparative analysis of endogenous hormones level in two soybean (Glycine max L.) lines differing in waterlogging tolerance. Frontiers in Plant Science, 6, 714.PubMedPubMedCentralGoogle Scholar
  38. Kim, Y., Seo, C.-W., Khan, A. L., Mun, B.-G., Shahzad, R., Ko, J.-W., … Lee, I.-J. (2018). Ethylene mitigates waterlogging stress by regulating glutathione biosynthesis-related transcripts in soybeans. bioRxiv, 252312.Google Scholar
  39. Klay, I., Gouia, S., Liu, M., Mila, I., Khoudi, H., Bernadac, A., … Pirrello, J. (2018). Ethylene Response Factors (ERF) are differentially regulated by different abiotic stress types in tomato plants. Plant Science, 274, 137.PubMedCrossRefGoogle Scholar
  40. Koldenkova, V. P., & Hatsugai, N. (2018). How do Plants Keep their Functional Integrity? Plant signaling & behavior, 13(8), e1464853.Google Scholar
  41. Koo, A. J. (2018). Metabolism of the plant hormone jasmonate: A sentinel for tissue damage and master regulator of stress response. Phytochemistry Reviews, 17(1), 51–80.CrossRefGoogle Scholar
  42. Kovalchuk, A., Keriö, S., Oghenekaro, A. O., Jaber, E., Raffaello, T., & Asiegbu, F. O. (2013). Antimicrobial defenses and resistance in forest trees: Challenges and perspectives in a genomic era. Annual Review of Phytopathology, 51, 221–244.PubMedCrossRefGoogle Scholar
  43. Kramer, P. (2012). Physiology of woody plants: Academic Press, New York, USA.Google Scholar
  44. Lacombe, B., & Achard, P. (2016). Long-distance transport of phytohormones through the plant vascular system. Current Opinion in Plant Biology, 34, 1–8.PubMedCrossRefGoogle Scholar
  45. Langenheim, J. H. (2003). Plant resins: Chemistry, evolution, ecology, and ethnobotany. Oregon, US: Timber Press.Google Scholar
  46. Lautner, S., & Fromm, J. (2010). Calcium-dependent physiological processes in trees. Journal of Plant Biology, 12(2), 268–274.CrossRefGoogle Scholar
  47. León, J., Rojo, E., & Sánchez-Serrano, J. J. (2001). Wound signalling in plants. Journal of Experimental Botany, 52(354), 1–9.PubMedCrossRefGoogle Scholar
  48. MacMillan, J. (2001). Occurrence of gibberellins in vascular plants, fungi, and bacteria. Journal of Plant Growth Regulation, 20(4), 387–442.PubMedCrossRefGoogle Scholar
  49. Magome, H., Nomura, T., Hanada, A., Takeda-Kamiya, N., Ohnishi, T., Shinma, Y., … Yamaguchi, S. (2013). CYP714B1 and CYP714B2 encode gibberellin 13-oxidases that reduce gibberellin activity in rice. Proceedings of the National Academy of Sciences, 110(5), 1947–1952.CrossRefGoogle Scholar
  50. McDowell, N., Pockman, W. T., Allen, C. D., Breshears, D. D., Cobb, N., Kolb, T., … Williams, D. G. (2008). Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytologist, 178(4), 719–739.PubMedCrossRefGoogle Scholar
  51. McDowell, R. E., Amsler, M. O., Li, Q., Lancaster, J. R., Jr., & Amsler, C. D. (2015). The immediate wound-induced oxidative burst of Saccharina latissima depends on light via photosynthetic electron transport. Journal of Phycology, 51(3), 431–441.PubMedCrossRefGoogle Scholar
  52. Mengistu, T., Sterck, F. J., Anten, N. P., & Bongers, F. (2012). Frankincense tapping reduced photosynthetic carbon gain in Boswellia papyrifera (Burseraceae) trees. Forest Ecology and Management, 278, 1–8.CrossRefGoogle Scholar
  53. Mengistu, T., Sterck, F. J., Fetene, M., & Bongers, F. (2013). Frankincense tapping reduces the carbohydrate storage of Boswellia trees. Tree Physiology, 33(6), 601–608.PubMedCrossRefGoogle Scholar
  54. Mihlan, M., Homann, V., Liu, T. W. D., & Tudzynski, B. (2003). AREA directly mediates nitrogen regulation of gibberellin biosynthesis in Gibberella fujikuroi, but its activity is not affected by NMR. Molecular Microbiology, 47(4), 975–991.PubMedCrossRefGoogle Scholar
  55. Oyarce, P., & Gurovich, L. (2011). Evidence for the transmission of information through electric potentials in injured avocado trees. Journal of Plant Physiology, 168(2), 103–108.PubMedCrossRefGoogle Scholar
  56. Prisic, S., Xu, M., Wilderman, P. R., & Peters, R. J. (2004). Rice contains two disparate ent-copalyl diphosphate synthases with distinct metabolic functions. Plant Physiology, 136(4), 4228–4236.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Qi, X., Li, M.-W., Xie, M., Liu, X., Ni, M., Shao, G., … Wong, F.-L. (2014). Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nature Communications, 5, 4340.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Rehman, N. U., Ali, L., Al-Harrasi, A., Mabood, F., Al-Broumi, M., Khan, A. L., … Csuk, R. (2018). Quantification of AKBA in Boswellia sacra using NIRS coupled with PLSR as an alternative method and cross-validation by HPLC. Phytochemical Analysis, 29(2), 137–143.PubMedCrossRefGoogle Scholar
  59. Rieu, I., Ruiz-Rivero, O., Fernandez-Garcia, N., Griffiths, J., Powers, S. J., Gong, F., … Thomas, S. G. (2008). The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. The Plant Journal, 53(3), 488–504.PubMedCrossRefGoogle Scholar
  60. Rijkers, T., Ogbazghi, W., Wessel, M., & Bongers, F. (2006). The effect of tapping for frankincense on sexual reproduction in Boswellia papyrifera. Journal of Applied Ecology, 43(6), 1188–1195.CrossRefGoogle Scholar
  61. Savatin, D. V., Gramegna, G., Modesti, V., & Cervone, F. (2014). Wounding in the plant tissue: The defense of a dangerous passage. Frontiers in Plant Science, 5, 470.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Scholz, S. S., Reichelt, M., Mekonnen, D. W., Ludewig, F., & Mithöfer, A. (2015). Insect herbivory-elicited GABA accumulation in plants is a wound-induced, direct, systemic, and jasmonate-independent defense response. Frontiers in Plant Science, 6, 1128.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Schulze, E.-D., & Ehleringer, J. (1984). The effect of nitrogen supply on growth and water-use efficiency of xylem-tapping mistletoes. Planta, 162(3), 268–275.PubMedCrossRefGoogle Scholar
  64. Shahzad, R., Waqas, M., Khan, A. L., Asaf, S., Khan, M. A., Kang, S.-M., … Lee, I.-J. (2016). Seed-borne endophytic Bacillus amyloliquefaciens RWL-1 produces gibberellins and regulates endogenous phytohormones of Oryza sativa. Plant Physiology and Biochemistry, 106, 236–243.PubMedCrossRefGoogle Scholar
  65. Shakirova, F. M., Sakhabutdinova, A. R., Bezrukova, M. V., Fatkhutdinova, R. A., & Fatkhutdinova, D. R. (2003). Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Science, 164(3), 317–322.CrossRefGoogle Scholar
  66. Silpi, U., Lacointe, A., Kasempsap, P., Thanysawanyangkura, S., Chantuma, P., Gohet, E., … Thaler, P. (2007). Carbohydrate reserves as a competing sink: Evidence from tapping rubber trees. Tree Physiology, 27(6), 881–889.PubMedCrossRefGoogle Scholar
  67. Silpi, U., Thaler, P., Kasemsap, P., Lacointe, A., Chantuma, A., Adam, B., … Améglio, T. (2006). Effect of tapping activity on the dynamics of radial growth of Hevea brasiliensis trees. Tree Physiology, 26(12), 1579–1587.PubMedCrossRefGoogle Scholar
  68. Suzuki, N., Bassil, E., Hamilton, J. S., Inupakutika, M. A., Zandalinas, S. I., Tripathy, D., … Kumazaki, A. (2016). ABA is required for plant acclimation to a combination of salt and heat stress. PLoS One, 11(1), e0147625.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Tadesse, W., Feleke, S., & Eshete, T. (2004). Comparative study of traditional and new tapping methods on frankincense yield of boswellia papyrifera. Ethiopian Journal of Natural Resources.Google Scholar
  70. Takahashi, N., Kitamura, H., Kawarada, A., Seta, Y., Takai, M., Tamura, S., & Sumiki, Y. (1955). Biochemical studies on “Bakanae” fungus: Part XXXIV. Isolation of gibberellins and their properties part XXXV. Relation between gibberellins, A1, A2 and gibberellic acid. Journal of the Agricultural Chemical Society of Japan, 19(4), 267–281.Google Scholar
  71. Thomas, S. G., & Hedden, P. (2018). Gibberellin metabolism and signal transduction. Annual Plant Reviews, 24, 147–184.Google Scholar
  72. Tolera, M., Sass-Klaassen, U., Eshete, A., Bongers, F., & Sterck, F. J. (2013). Frankincense tree recruitment failed over the past half century. Forest Ecology and Management, 304, 65–72.CrossRefGoogle Scholar
  73. Torres-Contreras, A. M., Senés-Guerrero, C., Pacheco, A., González-Agüero, M., Ramos-Parra, P. A., Cisneros-Zevallos, L., & Jacobo-Velázquez, D. A. (2018). Genes differentially expressed in broccoli as an early and late response to wounding stress. Postharvest Biology and Technology, 145, 172–182.CrossRefGoogle Scholar
  74. Trapp, S. C., & Croteau, R. B. (2001). Genomic organization of plant terpene synthases and molecular evolutionary implications. Genetics, 158(2), 811–832.PubMedPubMedCentralGoogle Scholar
  75. Vishwakarma, K., Upadhyay, N., Kumar, N., Yadav, G., Singh, J., Mishra, R. K., . . . Pandey, M. (2017). Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Frontiers in plant science, 8, 161–174.Google Scholar
  76. Wasternack, C., Stenzel, I., Hause, B., Hause, G., Kutter, C., Maucher, H., … Miersch, O. (2006). The wound response in tomato–role of jasmonic acid. Journal of Plant Physiology, 163(3), 297–306.PubMedCrossRefGoogle Scholar
  77. Zarate, S. I., Kempema, L. A., & Walling, L. L. (2007). Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiology, 143(2), 866–875.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Zebelo, S. A., & Maffei, M. E. (2014). Role of early signalling events in plant–insect interactions. Journal of Experimental Botany, 66(2), 435–448.PubMedCrossRefGoogle Scholar
  79. Zhou, Y., & Underhill, S. J. (2015). Breadfruit (Artocarpus altilis) gibberellin 20-oxidase genes: Sequence variants, stem elongation and abiotic stress response. Tree Genetics & Genomes, 11(4), 84.CrossRefGoogle Scholar
  80. Zhu, Y., Nomura, T., Xu, Y., Zhang, Y., Peng, Y., Mao, B., … Li, P. (2006). ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. The Plant Cell, 18(2), 442–456.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Zou, J., Liu, A., Chen, X., Zhou, X., Gao, G., Wang, W., & Zhang, X. (2009). Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. Journal of Plant Physiology, 166(8), 851–861.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Ahmed Al-Harrasi
    • 1
  • Abdul Latif Khan
    • 1
  • Sajjad Asaf
    • 1
  • Ahmed Al-Rawahi
    • 1
  1. 1.University of NizwaNizwaOman

Personalised recommendations