Sains Malaysiana 52(1)(2023): 57-69

http://doi.org/10.17576/jsm-2023-5201-05

 

Drought Stress Induced the Flavonoid Content in Moringa (Moringa oleifera Lam.) Leaves

(Stres Kemarau Mengaruh Kandungan Flavonoid pada Daun Moringa (Moringa oleifera Lam.))

 

RIDWAN1,2, HAMIM1,*, SUHARSONO1& NURIL HIDAYATI2

 

1Department of Biology, Faculty of Mathematics and Natural Sciences, IPB University, Bogor, Indonesia

2National Research and Innovation Agency, Indonesia

 

Received: 26 April 2022/Accepted: 27 October 2022

 

Abstract

Flavonoid is one of the most widely available bioactive compounds presence in the Moringa (Moringa oleifera Lam.) leaves. Osmotic stress is known to induce flavonoid production, however, the water level varies among plant species. This study aimed to examined the effects of water stress levels on the flavonoid content of Moringa leaves. The plants were treated withholding watering at three intervals (I): i.e.,: 1 (as control), 3 and 7 days based on the evaporated water during the treatments. The drought treatments were given within 4 different periods (D) before the plants were harvested, i.e.,: 8, 16, 24 and 32 days, and measured for the growth and biomass, proline (Pro) and chlorophyll (Chl) content, leaf water potential (WP), leaf relative water content (RWC), quercetin (Q) and kaempferol (K) content, and water use efficiency of flavonoid (WUEf). The results showed that the drought treatments induced different water statuses in the plants by decreases the leaf relative water content (RWC) and leaf water potential (WP) and increases of proline content significantly (up to 3 fold). Growth and biomass production decreased with the increase of water stress, whereas flavonoid content increased when the drought was mild and decreased again under severe drought. The highest content of flavonoids (1314.53 mg/kg leave biomass for Q and 2984.15 mg/kg leave biomass for K) and WUEf were shown when the plants were treated with 3 days drought for 16 days periods before the plants were harvested (I2D2) with no significant reduction in leaf biomass. This result suggests that the treatment of I2D2 is the best for bioactive production in Moringa.

 

Keywords: Bioactive compounds; drought; kaempferol; quercetin

 

Abstrak

Salah satu sebatian bioaktif yang paling banyak digunakan yang diperoleh daripada daun Moringa (Moringa oleifera Lam.) ialah flavonoid. Kajian ini bertujuan untuk mendorong kandungan flavonoid daun Moringa melalui rawatan tekanan air yang tidak mengurangkan jumlah pengeluaran bioaktif. Rawatan kemarau digunakan dengan menahan penyiraman dengan selang 1 (sebagai kawalan), 3 dan 7 hari. Rawatan kemarau diberikan dalam 4 tempoh (kitaran) yang berbeza sebelum tanaman dituai, iaitu: 8, 16, 24 dan 32 hari. Isi padu pengairan ditentukan berdasarkan perbezaan di antara berat pasu di bawah kapasiti ladang dan di bawah rawatan kemarau sejurus sebelum penyiraman seterusnya. Pemboleh ubah yang diperhatikan ialah pertumbuhan dan biojisim, prolin (Pro), klorofil (Chl), potensi air daun (WP), kandungan air relatif daun (RWC), kandungan kuersetin (Q) dan kaempferol (K) dan kecekapan penggunaan air flavonoid. (WUEf). Hasil kajian menunjukkan bahawa rawatan kemarau mampu menyebabkan status air yang berbeza antara rawatan yang ditunjukkan oleh penurunan kandungan air relatif daun (RWC) dan potensi air daun (WP) akibat kemarau yang lebih lama, manakala ia menyebabkan peningkatan kandungan prolin dengan ketara. Pertumbuhan dan pengeluaran biojisim menurun dengan peningkatan tekanan air, manakala kandungan flavonoid meningkat apabila kemarau sederhana dan berkurangan semula di bawah kemarau yang teruk. Kandungan flavonoid (Q dan K) dan WUEf tertinggi ditunjukkan apabila tumbuhan dirawat dengan kemarau 3 hari selama tempoh 16 hari sebelum tanaman dituai (I2D2) tanpa pengurangan ketara dalam biojisim daun. Keputusan ini menunjukkan bahawa rawatan I2D2 adalah yang terbaik untuk pengeluaran bioaktif di Moringa.

 

Kata kunci: Kaempferol; kuersetin; sebatian bioaktif; tekanan air

 

REFERENCES

Abdelkawy, K.S., Balyshev, M.E. & Elbarbry, F. 2016. A new validated HPLC method for the determination of quercetin: Application to study pharmacokinetics in rats. Biomedical Chromatography 31(3). doi: 10.1002/bmc.3819

Ahmed, U., Rao, M.J., Qi, C., Xie, Q., Noushashi, H.A., Yaseen, M., Shi, X. & Zheng, B. 2021. Expression profiling of flavonoid biosynthesis genes and secondary metabolites accumulation in populus under drought stress. Molecules 26: 5546. https://doi.org/10.3390/molecules26185546

Al-Gabbiesh, A., Kleinwächter, M. & Selmar, D. 2015. Influencing the contents of secondary metabolites in spice and medicinal plants by deliberately applying drought stress during their cultivation. Jordan Journal of Biological Sciences 8(1): 1-10.­

Ali, E., Iqbal, A., Hussain, S., Shah, J.M., Said, F., Imtiaz, M., Jalal, F. & Khan, M.A. 2019. Selection criteria to assess drought stress tolerance in wheat genotypes using physiological and biochemical parameters. Biosciences Biotechnology Research Asia 16(4): 751-762.

Azhar, N., Hussain, B., Ashraf, M.Y. & Abbasi, K.Y. 2011. Water stress-mediated changes in growth, physiology and secondary metabolites of desi ajwain (Trachyspermum ammi L.). Pakistan Journal of Botany 43: 15-19.

Bates, L.S., Waldren, R.P. & Teare, L.D. 1973. Rapid determination of free proline for water-stress studies. Plant Soil 39: 205-207.

Boumenjel, A., Papadopoulos, A. & Ammari, Y. 2021. Growth response of Moringa oleifera (Lam) to water stress and to arid bioclimatic conditions. Agroforestry Systems 95: 823-833.

Brunetti, C., Loreto, F., Ferrini, F., Gori, A., Guidi, L., Remorini, D., Centritto, M., Fini, A. & Tattini, M. 2018. Metabolic plasticity in the hygrophyte Moringa oleifera exposed to water stress. Tree Physiology 38(11): 1640-1654.

Edwinanto, L., Septiadi, E., Nurfazriah, L.R., Anastasya, K.S. & Pranata, P. 2018. Phytochemical features of Moringa oleifera leaves as anticancer. Journal of Medicine and Health 2(1): 680-688.

Furlan, A.L., Bianucci, E., Giordano, W., Castro, S. & Becker, D.F. 2020. Proline metabolic dynamics and implications in drought tolerance of peanut plants. Plant Physiology and Biochemistry 151: 566-578.

Gharibi, S., Tabatabaei, B.E.S., Saeidi, G. & Goli, S.A.H. 2016. Effect of drought stress on total phenolic, lipid peroxidation, and antioxidant activity of achillea species. Applied Biochemistry and Biotechnology 178: 796-809.

González-Romero, J., Arranz-Arranz, S., Verardo, V., García-Villanova, B. & Guerra-Hernández, E.J. 2020. Bioactive compounds and antioxidant capacity of moringa leaves grown in Spain versus 28 leaves commonly consumed in pre-packaged salads. Processes 8(10): 1297.

Hasan, M.M., Alharby, H.F., Uddin, N., Ali, M.A., Anwar, Y., Fang, X.W., Hakeem, K.R., Alzahrani, Y. & Hajar, A.S. 2020. Magnetized water confers drought stress tolerance in moringa biotype via modulation of growth, gas exchange, lipid peroxidation and antioxidant activity. Polish Journal of Environmental Studies 29(2): 1625-1636.

Hasym, A.M.O.M., Nor, N.M., Adnan, L.H.M., Ahmad, N.Z.B., Septama, A.W., Najihah, N.N., Lwin, O.M. & Simbak, N. 2021. Effects of apigenin, luteolin, and quercetin on the natural killer (NK-92) cells proliferation: A potential role as immunomodulator. Sains Malaysiana 50(3): 821-828.

Hauer, B. 2010.  Role of proline in plant response to drought and salinity. Handbook of Plant and Crop Stress. 3rd edition, Chapter 9. Boca Raton: CRC Press.

Hodaei, M., Rahimmalek, M., Arzani, A. & Talebi, M. 2018. The effect of water stress on phytochemical accumulation, bioactive compounds and expression of key genes involved in flavonoid biosynthesis in Chrysanthemum morifolium L. Industrial Crops & Products 120: 295-304.

Jabeen, M., Akram, N.A., Ashraf, M. & Aziz, A. 2019. Assessment of biochemical changes in spinach (Spinacea oleracea L.) subjected to varying water regimes. Sains Malaysiana 48(3): 533-541.

Juan, C.A., de la Lastra, J.M.P., Plou, F.J. & Pérez-Lebeña, E. 2021. The chemistry of reactive oxygen species (ROS) revisited: Outlining their role in biological macromolecules (DNA, lipids and proteins) and induced pathologies. International Journal of Molecular Sciences 22: 4642.

Kapoor, D., Bhardwaj, S., Landi, M., Sharma, A., Ramakrishnan, M. & Sharma, A. 2020. The impact of drought in plant metabolism: How to exploit tolerance mechanisms to increase crop production. Applied Sciences 10: 1-19.

Karuppanapandian, T., Moon, J.C., Kim, C., Manoharan, K. & Kim, W. 2011. Reactive oxygen species in plants: Their generation, signal transduction, and scavenging mechanisms. Australian Journal of Crop Science 5(6): 709-752.

Khaleghi, A., Naderi, R., Brunetti, C., Maserti, B.E., Salami, S.A. & Babalar, M. 2019. Morphological, physiochemical and antioxidant responses of Maclura pomifera to drought stress. Scientific Reports 9: 1920.

Kubra, G., Khan, M., Munir, F., Gul, A., Shah, T., Hussain, A., Caparrós-Ruiz, D. & Amir, R. 2021. Expression characterization of flavonoid biosynthetic pathway genes and transcription factors in peanut under water deficit conditions. Frontiers in Plant Science 12: 1-18.

Kumar, S. & Pandey, A.K. 2013. Chemistry and biological activities of flavonoids: An overview. The Scientific World Journal 2013: 162750.

Lima, V.M., de Lima Junior, J.A., Santos, H.C.A., da Silva, A.L.P., de Oleiveira, P.D., de Brito Neto, J.F. 2018. Growth of Capsicum chinense Jacq. subjected to different irrigation depths in the northeastern region of Pará, Brazil. Jaboticabal 46(1): 30-37.

Lin, M., Zhang, J. & Chen, X. 2018. Bioactive flavonoids in Moringa oleifera and their health-promoting properties. Journal of Functional Food 47: 469-479.

Malinowska, M., Donnison, I. & Robson, P. 2020. Morphological and physiological traits that explain yield response to drought stress in Miscanthus. Agronomy 10: 1194.

Mondal, S. & Rahman, S.T. 2020. Flavonoids: A vital resource in healthcare and medicine. Pharmacy & Pharmacology International Journal 8(2): 91-104.

Pakade, V., Cukrowska, E. & Chimuka, L. 2013. Metal and flavonol contents of Moringa oleifera grown in South Africa. South African Journal of Science 109(3-4): 7.

Patharkar, O.R. & Walker, J.C. 2019. Connections between abscission, dehiscence, pathogen defense, drought tolerance, and senescence. Plant Science 284: 25-29.

Ratzmann, G., Zakhrova, L., Tietjen, B. 2019. Optimal leaf water status regulation of plants in drylands. Scientific Reports 9: 3768.

Ridwan, Hamim, Suharsono, Nuril Hidayati & Indra Gunawan. 2021. Drumstick (Moringa oleifera) variation in biomass and total flavonoid content in Indonesia. Biodiversitas 22(1): 491-498.

Sade, N., Rubio-Wilhelmi, M.d.M., Umnajkitikorn, K. & Blumwald, E. 2018. Stress-induced senescence and plant tolerance to abiotic stress. Journal of Experimental Botany 69(4): 845-853.

Saito, K., Yonekura-Sakakibara, K., Nakabayashi, R., Higashi, Y., Yamazaki, M., Tohge, T. & Fernie, A.R. 2013. The flavonoid biosynthetic pathway in Arabidopsis: Structural and genetic diversity. Plant Physiology and Biochemistry 72: 21-34.

Sallam, A., Alqudah, A.M., Dawood, M.F.A., Baenziger, P.S. & Börner, A. 2019. Drought stress tolerance in Wheat and Barley: Advances in physiology, breeding and genetics research. International Journal of Molecular Sciences 20(13): 3137.

Sarker, U. & Oba, S. 2018. Drought stress enhances nutritional and bioactive compounds, phenolic acids and antioxidant capacity of Amaranthus leafy vegetable. BMC Plant Biology 18(1): 258.

Shah, S.H., Houborg, R. & McCabe, M.F. 2017. Response of chlorophyll, carotenoid and SPAD-502 measurement to salinity and nutrient stress in Wheat (Triticum aestivum L.). Agronomy 7: 61.

Shukla, A., Panchal, H., Mishra, M., Patel, P.R., Srivastava, H.S., Patel, P. & Shukla, A.K. 2014. Soil moisture estimation using gravimetric technique and FDR probe technique: a comparative analysis. American International Journal of Research in Formal, Applied & Natural Sciences 8(1): 89-92.

Sims, D.A. & Gamon, J.A. 2002. Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sensing of Environment 81: 337-354.

Thapa, S., Reddy, S.K., Fuentealba, M.P., Xue, Q., Rudd, J.C., Jessup, K.E., Devkota R.N. & Liu, S. 2018. Physiological responses to water stress and yield of winter wheat cultivars differing in drought tolerance. Journal of Agronomy and Crop Science204(4): 347-358.

Vongsak, B., Sithisarn, P., Mangmool, S., Tongpraditchote, S., Wongkrajang, Y. & Gritsanapan, W. 2013. Maximizing total phenolics, total flavonoids content and antioxidant activity of Moringa oleifera leaf extract by the appropriate extraction method. Industrial Crops and Products 44: 566-571.

Wang, T.Y., Li, Q. & Bi, K.S. 2018. Bioactive flavonoids in medicinal plants: Structure, activity and biological fate. Asian Journal of Pharmaceutical Sciences 13(1): 12-23.

Wasonowati, C., Sulistyaningsih, E., Indradewa, D. & Kurniasih, B. 2019. Morphophysiology and the yield of two types of moringa (Moringa oleifera Lamk) cultivated in two different regions in Madura. IOP Conf. Series: Earth and Environmental Science 250: 012004.

Yuan, Y., Liu, Y., Wu, C., Chen, S., Wang, Z., Yang, Z., Qin, S. & Huang, L. 2012. Water deficit affected flavonoid accumulation by regulating hormone metabolism in Scutellaria baicalensis Georgi roots. PLoS ONE 7(10): e42946.

Zhang, W., Cao, Z., Xie, Z., Lang, D., Zhou, L., Chu, Y., Zhao, Q., Zhang, X. & Zhao, Y. 2017. Effect of water stress on roots biomass and secondary metabolites in the medicinal plant Stellaria dichotoma L. var. lanceolata Bge. Scientia Horticulturae 224: 280-285.

 

*Corresponding author; email: hamim@apps.ipb.ac.id

 

 

 

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