Skip to main content

Advertisement

Log in

Oligomers of carrageenan regulate functional activities and artemisinin production in Artemisia annua L. exposed to arsenic stress

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Recently, a promising technique has come forward in field of radiation-agriculture in which the natural polysaccharides are modified into useful oligomers after depolymerization. Ionizing radiation technology is a simple, pioneering, eco-friendly, and single step degradation process which is used in exploiting the efficiency of the natural polysaccharides as plant growth promoters. Arsenic (As) is a noxious and toxic to growth and development of medicinal plants. Artemisinin is obtained from the leaves of Artemisia annua L., which is effective in the treatment of malaria. The present study was undertaken to find out possible role of oligomers of irradiated carrageenan (IC) on two varieties viz. ‘CIM-Arogya’ (As-tolerant) and ‘Jeevan Raksha’ (As-sensitive) of A. annua exposed to As. The treatments applied were 0 (control), 40 IC (40 mg L−1 IC), 80 IC (80 mg L−1 IC), 45 As (45 mg kg−1 soil As), 40 IC + 45 As (40 mg L−1 IC + 45 mg kg−1 soil As), and 80 IC + 45 As (80 mg L−1 IC + 45 mg kg−1 soil As). The present study was based on various parameters namely plant fresh weight (FW), dry weight (DW), leaf area index (LAI), leaf yield (LY), chlorophyll and carotenoid content, net photosynthetic rate (PN), stomatal conductance (Gs), carbonic anhydrase activity (CA), proline content (PRO), lipid peroxidation (TBARS), endogenous ROS production (H2O2 content), catalase activity (CAT), peroxidase activity (POX), superoxide dismutase activity (SOD), ascorbate peroxidase activity (APX), As content, and artemisinin content in leaves. Plant growth and other physiological and biochemical parameters including enzymatic activities, photosynthetic activity, and its related pigments were negatively affected under As stress. Leaf-applied IC overcame oxidative stress generated due to As in plants by activating antioxidant machinery. Interestingly, leaf-applied IC enhanced the production (content and yield) of artemisinin under high As stress regardless of varieties. The oligomers of IC and As were found to be responsible for the production of endogenous H2O2 which has a pivotal role in the biosynthesis of artemisinin in A. annua.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abad LV, Aurigue FB, Relleve LS, Montefalcon DRV, Lopez GEP (2016) Characterization of low molecular weight fragments from gamma irradiated к-carrageenan used as plant growth promoter. J Radiat Phys Chem 118:75–80

    Article  CAS  Google Scholar 

  • Abad L, Dean G, Magsino G, Dela Cruz R, Tecson M, Abella M, Hizon M (2017) Semi-commercial scale production of carrageenan plant growth promoter by E-beam technology. Radiat Phys Chem 143:53–58

    Article  CAS  Google Scholar 

  • Abad LV, Aurigue FB, Montefalcon BRV, Manguiat FH, Carandang FF, Mabborang SA, Hizon MGS, Abella MES (2018) Effect of radiation-modified kappa-carrageenan as plant growth promoter on peanut (Arachis hypogaea L.). Radiat Phys Chem 153:239–244

    Article  CAS  Google Scholar 

  • Abbas G, Murtaza B, Bibi I, Shahid M, Niazi N, Khan M, Hussain M (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15(1):59

    Article  PubMed Central  CAS  Google Scholar 

  • Adriano DC (2001) Trace elements in terrestrial environments. Biogeochemistry bioavailability and risks of metals, 2nd edn 867 pp. Springer, New York

    Book  Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Ram M (2010) Boron induced oxidative stress, antioxidant defense response and changes in artemisinin content in Artemisia annua L. J Agron Crop Sci 196:423–430

    Article  CAS  Google Scholar 

  • Aftab T, Khan MMA, Teixeira da Silva JA, Idrees M, Naeem M, Moinuddin (2011a) Role of salicylic acid in promoting salt stress tolerance and enhanced artemisinin production in Artemisia annua L. J Plant Growth Regul 30:425–435

    Article  CAS  Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Hashmi N, Varshney L (2011b) Enhancing the growth, photosynthetic capacity and artemisinin content in Artemisia annua L. by irradiated sodium alginate. Radiat Phys Chem 80:833–836

    Article  CAS  Google Scholar 

  • Aftab T, Khan MMA, Idrees M, Naeem M, Siddiqui TO, Varshney L (2014) Effect of irradiated sodium alginate and phosphorus on biomass and artemisin in production in Artemisia annua. Carbohydr Polym 110:396–404

    Article  CAS  PubMed  Google Scholar 

  • Ahmad B, Khan MMA, Jaleel H, Sadiq Y, Shabbir A, Uddin M (2017) Exogenously sourced γ-irradiated chitosan-mediated regulation of growth, physiology, quality attributes and yield in Mentha piperita L. Turk J Biol 41:388–401

    Article  CAS  Google Scholar 

  • Ali A, Khan MMA, Uddin M, Naeem M, Idrees M, Hashmi N, Dar TA, Varshney L (2014) Radiolytically depolymerized sodium alginate improves physiological activities, yield attributes and composition of essential oil of Eucalyptus citriodora Hook. Carbohydr Polym 112:134–144

    Article  CAS  PubMed  Google Scholar 

  • Avery MA, Chong WKM, Jennings-White C (1992) Stereo selective total synthesis of (+)-artemisinin, the antimalarial constituent of Artemisia annua L. J Am Chem Soc 114:974–979

    Article  CAS  Google Scholar 

  • Bandurska H (2001) Proline accumulated in the leaves of water deficient stress in barley plants confine cell membrane injury? II. Proline accumulation during hardening and its involvement in reducing membrane injury in leaves subjected to severe osmotic stress. Acta Physiol Plant 23:483–490

    Article  CAS  Google Scholar 

  • Bates LS, Waldeen RP, Teare ID (1973) Rapid determination of free water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beauchamp CO, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Biswas S, Koul M, Bhatnagar AK (2015) Effect of arsenic on trichome ultrastructure, essential oil yield and quality of Ocimum basilicum L. Med Plant Res 5(6):1–9

    Google Scholar 

  • Cakmak I, Horst J (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  CAS  Google Scholar 

  • Castro J, Vera J, Gonzalez A, Moenne A (2012) Oligo-carrageenans stimulate growth by enhancing photosynthesis, basal metabolism, and cell cycle in tobacco plants (var. Burley). J Plant Growth Regul 31:173–185

    Article  CAS  Google Scholar 

  • Chandlee JM, Scandalios JG (1984) Analysis of variants affecting the catalase development program in maize scutellum. Theor Appl Genet 69:71–77

    Article  CAS  PubMed  Google Scholar 

  • Chandrakar V, Naithani SC, Keshavkant S (2016) Arsenic-induced metabolic disturbances and their mitigation mechanisms in crop plants: a review. Biologia 71(4):367–377

    Article  CAS  Google Scholar 

  • Chen DH, Ye HC, Li GF (2000) Expression of a chimeric farnesyl diphosphate synthase gene in Artemisia annua L. transgenic plants via Agrobacterium tumefaciens-mediated transformation. Plant Sci 155:179–185

    Article  CAS  PubMed  Google Scholar 

  • Chun-xi L, Shu-li F, Yan SH, Li-na J, Xu-yang L, Xiao-li H (2007) Effects of arsenic on seed germination and physiological activities of wheat seedlings. J Environ Sci 19:725–732

    Article  Google Scholar 

  • Dave R, Tripathi RD, Dwivedi S, Tripathi P, Dixit G, Sharma YK, Trivedi PK, Corpas FJ, Barroso JB, Chakrabarty D (2013) Arsenate and arsenite exposure modulate antioxidants and amino acids in contrasting arsenic accumulating rice (Oryza sativa L.) genotypes. J Hazard Mater 262:1123–1131

    Article  CAS  PubMed  Google Scholar 

  • De La Rosa A, Abad L, Relleve L, Aranilla C (2002) Radiation-modified carrageenan for agricultural and health care applications. IAEA Report. In International Atomic Energy Agency (IAEA) Project Coordination Meeting on Radiation Processing of Chitin/Chitosan, Bangkok, Thailand, 18–20 March

  • Diwan H, Ahmad A, Iqbal M (2008) Genotypic variation in the phytoremediation potential of Indian mustard for chromium. Environ Manag 41:734–741

    Article  Google Scholar 

  • Dwivedi RS, Randhawa NS (1974) Evaluation of rapid test for the hidden hunger of zinc in plants. Plant Soil 40:445–451

    Article  CAS  Google Scholar 

  • Efferth T (2007) Antiplasmodial and antitumor activity of artemisinin from bench to bedside. Planta Med 73:299–309

    Article  CAS  PubMed  Google Scholar 

  • Efferth T, Dunstan H, Sauerbrey A, Miyachi H, Chitambar CR (2001) The anti-malarial artesunate is also active against cancer. Int J Oncol 18:767–773

    CAS  PubMed  Google Scholar 

  • El-Mohdy HLA (2017) Radiation-induced degradation of sodium alginate and its plant growth promotion effect. Arab J Chem 10:S431–S438

    Article  CAS  Google Scholar 

  • Flora SJ (2011) Arsenic-induced oxidative stress and its reversibility. Free Radic Biol Med 51(2):257–281

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh NC, Singh RD (2009) Groundwater arsenic contamination in India: vulnerability and scope for remedy. Technical papers included in the special session on ground water in the 5th Asian Regional Conference of INCID, December 9–11, 2009. Vigyan Bhawan, New Delhi, pp 1–23

    Google Scholar 

  • Gonzalez A, Castro J, Vera J, Moenne A (2013) Seaweed oligosaccharides stimulate plant growth by enhancing carbon and nitrogen assimilation, basal metabolism and cell division. J Plant Growth Regul 32:443–448

    Article  CAS  Google Scholar 

  • Graham IA, Besser K, Blumer S, Branigan CA, Czechowski T, Elias L (2010) The genetic map of Artemisia annua L. identifies loci affecting yield of the antimalarial drug artemisinin. Science 327:328–331

    Article  CAS  PubMed  Google Scholar 

  • Guo C, Liu CZ, Ye HC, Li GF (2004) Effect of temperature on growth and artemisinin biosynthesis in hairy root cultures of Artemisia annua. Acta Bot Boreal-Occident Sin 24:1828–1831

    CAS  Google Scholar 

  • Hashmi N, Khan MM, Moinuddin, Idrees M, Khan ZH, Ali A, Varshney L (2012) Depolymerized carrageenan ameliorates growth, physiological attributes, essential oil yield and active constituents of Foeniculum vulgare Mill. Carbohydr Polym 90:407–412

    Article  CAS  PubMed  Google Scholar 

  • Haynes RK, Chan WC, Lung CM et al (2007) The Fe2+-mediated decomposition, PfATP6 binding, and antimalarial activities of artemisone and other artemisinins: the unlikelihood of C-centered radicals as bioactive intermediates. Chem Med Chem 2:1480–1497

    Article  CAS  PubMed  Google Scholar 

  • Ikram NKB, Simonsen HT (2017) A review of biotechnological artemisinin production in plants. Front Plant Sci 8:1966. https://doi.org/10.3389/fpls.2017.01966

    Article  PubMed  PubMed Central  Google Scholar 

  • Jha AB, Dubey RS (2004) Carbohydrate metabolism in growing rice seedlings under arsenic toxicity. J Plant Physiol 161:867–872

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Ge CM, Meng QH, Cao JP, Tong J, Fan SJ (2007) Dihydroartemisinin is an inhibitor of ovarian cancer cell growth. Acta Pharmacol Sin 28:1045–1056

    Article  CAS  PubMed  Google Scholar 

  • Khan I, Ahmad A, Iqbal M (2009) Modulation of antioxidant defense system for arsenic detoxification in Indian mustard. Ecotoxicol Environ Saf 72:626–634

    Article  CAS  PubMed  Google Scholar 

  • Kumar KB, Khan PA (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine coracana cv. PR 202) leaves during senescence. Indian J Exp Bot 20:412–416

    CAS  Google Scholar 

  • Kumar A, Dwivedi S, Singh RP, Chakrabarty D, Mallick S, Trivedi PK, Adhikari B, Tripathi RD (2014) Evaluation of amino acid profile in contrasting arsenic accumulating rice genotypes under arsenic stress. Biol Plant 58:733–742

    Article  CAS  Google Scholar 

  • Kumari A, Pandey N, Rai SP (2018) Exogenous salicylic acid-mediated modulation of arsenic stress tolerance with enhanced accumulation of secondary metabolites and improved size of glandular trichomes in Artemisia annua L. Protoplasma 255:139–152

    Article  CAS  PubMed  Google Scholar 

  • Kume T, Nagasawa N, Yoshii F (2002) Utilization of carbohydrates by radiation processing. Radiat Phys Chem 63(3):625–627

    Article  CAS  Google Scholar 

  • Li HM, Kaneko Y, Keegstra K (1994) Molecular cloning of a chloroplastic protein associated with both the envelope and thylakoid membranes. Plant Mol Biol 25(4):619–632

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. In: Wrolstad RE (ed) Current protocols in food analytical chemistry. Wiley, New York, pp F4.3.1–F4.3.8

    Google Scholar 

  • Liu CZ, Guo C, Wang YC, Ouyang F (2002) Effect of light irradiation on hairy root growth and artemisinin biosynthesis of Artemisia annua L. Process Biochem 38:581–585

    Article  CAS  Google Scholar 

  • Lv Z, Zhang F, Pan Q, Fu X, Jiang W, Shen Q, Yan T, Shi P, Lu X, Sun X, Tang K (2016) Branch pathway blocking in Artemisia annua is a useful method for obtaining high yield artemisinin. Plant Cell Physiol 57:588–602

    Article  CAS  PubMed  Google Scholar 

  • Ma LJ, Li XM, Bu N, Li N (2010) An alginate-derived oligosaccharide enhanced wheat tolerance to cadmium stress. Plant Growth Regul 62:71–76

    Article  CAS  Google Scholar 

  • Maningas JAC, Castillo KMD, Grospe FS, Juliano MJ, Abad LV (2016) Effect of foliar application of radiation modified carrageenan on the yield of rice. PNRI Newsletter. Jul-Dec (2016)12:5. Available: http://www.pnri.dost.gov.ph/images/newsletters/volume12/PNRI-Newsletter-Vol-12.pdf

  • Mathers CD, Loncar D (2006) Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 3(11):e442

    Article  PubMed  PubMed Central  Google Scholar 

  • Matysik J, Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  • Mishra S, Stark HJ, Kupper H (2014) A different sequence of events than previously reported leads to arsenic-induced damage in Ceratophyllum demersum L. Metallomics 6:444–454

    Article  CAS  PubMed  Google Scholar 

  • Miteva E, Hristova D, Nenova V, Maneva S (2005) Arsenic as a factor affecting virus infection in tomato plants: changes in plant growth, peroxidase activity and chloroplast pigments. Sci Hortic 105:343–358

    Article  CAS  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  CAS  Google Scholar 

  • Naeem M, Aftab T, Khan MMA, Varshney L (2012) Depolymerised carrageenan enhances physiological activities and menthol production in Mentha arvensis L. Carbohydr Polym 87(2):1211–1218

    Article  CAS  Google Scholar 

  • Naeem M, Idrees M, Aftab T, Alam MM, Khan MMA, Uddin M, Varshney L (2015) Radiation processed carrageenan improves plant growth, physiological activities and alkaloids production in Catharanthus roseus L. Advanc Bot:50474 11 pages

  • Naeem M, Aftab T, Khan MM (2017) Strategies for enhancing artemisinin production in Artemisia annua under changing environment. In: Ghorbanpour M, Varma A (eds) Medicinal plants and environmental challenges. Springer, Cham, pp 227–246

    Chapter  Google Scholar 

  • Naeem M, Aftab T, Ansari AA, Shabbir A, Khan MMA, Uddin M (2019) Arsenic exposure modulates physiological attributes and artemisinin biosynthesis in Artemisia annua L. Int J Herbal Med 7:19–26

    Google Scholar 

  • Nagasawa N, Mitomo H, Yoshii F, Kume T (2000) Radiation induced degradation of sodium alginate. Polym Degrad Stab 69:279–285

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nakase I, Lai H, Singh NP, Sasaki T (2008) Anticancer properties of artemisinin derivatives and their targeted delivery by transferrin conjugation. Int J Pharm 354:28–33

    Article  CAS  PubMed  Google Scholar 

  • Nguyen K, Arsenault P, Weathers P (2011) Trichomes + roots + ROS = artemisinin: regulating artemisinin biosynthesis in Artemisia annua L. In Vitro Cell Dev Biol Plant 47:329–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papageorgiou GC, Murata N (1995) The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem II complex. Photosynth Res 44:243–252

    Article  CAS  PubMed  Google Scholar 

  • Paul S, Shakya K (2013) Arsenic, chromium and NaCl induced artemisinin biosynthesis in Artemisia annua L.: a valuable antimalarial plant. Ecotoxicol Environ Saf 98:59–65

    Article  CAS  PubMed  Google Scholar 

  • Pavlik M, Pavlikova D, Staszkova L, Neuberg M, Kaliszova R, Szakova J, Tlustos P (2010) The effect of arsenic contamination on amino acids metabolism in Spinacea oleracea L. Ecotoxicol Environ Saf 73:1309–1313

    Article  CAS  PubMed  Google Scholar 

  • Pu GB, Ma DM, Chen JL, Ma LQ, Wang H, Li GF, Ye HC, Liu BY (2009) Salicylic acid activates artemisinin biosynthesis in Artemisia annua L. Plant Cell Rep 28:1127–1135

    Article  CAS  PubMed  Google Scholar 

  • Qian ZH, Gong K, Zhang L, Jb L, Jing FY, Wang YY, Guan SB, Wang GF, Tang KK (2007) A simple and efficient procedure to enhance artemisinin content in Artemisia annua L. by seeding to salinity stress. Afr J Biotechnol 6:1410–1413

    CAS  Google Scholar 

  • Qureshi MI, Israr M, Abdin MZ, Iqbal M (2005) Responses of Artemisia annua L. to lead and salt-induced oxidative stress. Environ Exp Bot 53:185–193

    Article  CAS  Google Scholar 

  • Rai R, Pandey S, Rai SP (2011a) Arsenic-induced changes in morphological, physiological, and biochemical attributes and artemisinin biosynthesis in Artemisia annua, an antimalarial plant. Ecotoxicology 20:1900–1913

    Article  CAS  PubMed  Google Scholar 

  • Rai R, Meena RP, Smita SS, Shukla A, Rai SK, Pandey-Rai S (2011b) UV-B and UV-C pre-treatments induce physiological changes and artemisinin biosynthesis in Artemisia annua L.—an antimalarial plant. J Photochem Photobiol B 105:216–225

    Article  CAS  PubMed  Google Scholar 

  • Rai R, Pandey S, Shrivastava AK, Pandey Rai SP (2014) Enhanced photosynthesis and carbon metabolism favor arsenic tolerance in Artemisia annua, a medicinal plant as revealed by homology-based proteomics. Int J Proteom:163962 21 pages

  • Relleve L, Abad L, Aranilla C, Aliganga A, De La Rosa A, Yoshii F (2000) Biological activities of radiation degraded carrageenan. In Proceedings of the Symposium on Radiation Technology in Emerging Industrial Applications Beijing, People’s Republic of China, 6-10 November, pp 98–108

  • Relleve L, Nagasawa N, Luan LQ, Yagi T, Aranilla C, Abad L (2005) Degradation of carrageenan by radiation. Poly Degrad Stabil 87:403–410

    Article  CAS  Google Scholar 

  • Ro DK, Paradise EM, Ouellet M, Fisher KJ, Newman KL et al (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440:940–943

    Article  CAS  PubMed  Google Scholar 

  • Sabharwal S (2004) Radiation processing in India: current status and future programme. Radiation processing of polysaccharides, IAEA, Vienna (IAEA-TECDOC-1422)

  • Sadiq Y, Khan MMA, Shabbir A, Ahmad B, Jaleel H, Uddin M, Varshney L (2017) Structural re-arrangement of depolymerized sodium alginate enriches peltate glandular trichomes and essential oil production of spearmint. Int J Biol Macromol 10:1043–1050

    Article  CAS  Google Scholar 

  • Salachna P, Grzeszczuk M, Meller E, Soból M (2018) Oligo-alginate with low molecular mass improves growth and physiological activity of Eucomis autumnalis under salinity stress. Molecules 23:812. https://doi.org/10.3390/molecules23040812

    Article  CAS  PubMed Central  Google Scholar 

  • Shahid M, Khalid S, Abbas G, Shahid N, Nadeem M, Sabir M, Aslam M, Dumat C (2015) Heavy metal stress and crop productivity. Crop Product Glob Environ Issue:1–25. https://doi.org/10.1007/978-3-319-23162-4-1

  • Shaibur MR, Kawai S (2009) Effect of arsenic on visible symptom and arsenic concentration in hydroponic mustard spinach. Environ Exp Bot 67:65–70

    Article  CAS  Google Scholar 

  • Shaibur MR, Kitajima N, Sugawara R, Kondo T, Huq SMI, Kawai S (2008) Physiological and mineralogical properties of arsenic-induced chlorosis in barley seedlings grown hydroponically. J Plant Nutr 31(2):333–353

    Article  CAS  Google Scholar 

  • Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72:1102–1110

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui F, Tandon PK, Srivastava S (2015) Analysis of arsenic induced physiological and biochemical responses in a medicinal plant, Withania somnifera. Physiol Mol Biol Plants 21:61–69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh HP, Batish DR, Kohli RK, Arora K (2007) Arsenic-induced root growth inhibition in Phaseolus aureus Roxb. is due to oxidative stress resulting from enhanced lipid peroxidation. Plant Growth Regul 53(1):65–73

    Article  CAS  Google Scholar 

  • Singh N, Ma LQ, Vu JC, Raj A (2009) Effects of arsenic on nitrate metabolism in arsenic hyperaccumulating and non-hyperaccumulating ferns. Environ Pollut 157:2300–2305

    Article  CAS  PubMed  Google Scholar 

  • Singh M, Khan MMA, Uddin M, Naeem M, Qureshi MI (2017) Proliferating effect of radiolytically depolymerized carrageenan on physiological attributes, plant water relation parameters, essential oil production and active constituents of Cymbopogon flexuosus Steud. under drought stress. PLoS One 12(7):e0180129

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Siriwardhana N, Lee KW, Jeon YJ, Kim SH, Haw JW (2003) Antioxidant activity of Hizikia fusiformis on reactive oxygen species scavenging and lipid peroxidation inhibition. Food Sci Technol Int 9:339–346

    Article  Google Scholar 

  • Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI (2005) The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434 (7030):214-217

  • Srivastava S, D’Souza SF (2010) Effect of variable sulfur supply on arsenic tolerance and antioxidant responses in Hydrilla verticillata (L.f.) Royle. Ecotoxicol Environ Saf 73:1314–1322

    Article  CAS  PubMed  Google Scholar 

  • Srivastava S, Sharma YK (2013) Arsenic phytotoxicity in black gram (Vigna mungo L. var. PU19) and its possible amelioration by phosphate application. J Plant Physiol Pathol 1:3. https://doi.org/10.4172/2329-955X.1000107

    Article  Google Scholar 

  • Srivastava M, Ma LQ, Singh N, Singh S (2005) Antioxidant responses of hyperaccumulator and sensitive fern species to arsenic. J Exp Bot 56:1335–1342

    Article  CAS  PubMed  Google Scholar 

  • Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Trivedi PK, Tandon PK (2007) Phytochelatins and antioxidant systems respond differentially during arsenite and arsenate stress in Hydrilla verticilliata (L.f.) Royle. Environ Sci Technol 41:2930–2936

    Article  CAS  PubMed  Google Scholar 

  • Srivastava S, Srivastava AK, Singh B, Suprasanna P, D’Souza SF (2013) The effect of arsenic on pigment composition and photosynthesis in Hydrilla verticillata. Biol Plant 57:385–389

    Article  CAS  Google Scholar 

  • Stefanache CP, Bujor OC, Necula R, Danila D, Ciocârlan N, Ghendov V, Carlen C, Simonnet X (2016) Phenolic content of Artemisia annua L. from natural habitats in Republic of Moldova. J Plant Develop 23:61–69

    Google Scholar 

  • Stoeva N, Bineva T (2003) Oxidative changes and photosynthesis in oat plants grown in As contaminated soil. Bulgarian J Plant Physiol 29:87–95

    Google Scholar 

  • Stoeva N, Berova M, Vassilev A, Zlatev Z (2005) Effect of exogenous polyamine diethylenetriamine on oxidative changes and photosynthesis in As-treated maize plants (Zea mays L.). J Cent Eur Agric 6:367–374

    Google Scholar 

  • Suberu J, Song L, Slade S, Sullivan N, Barker G, Lapkin AA (2013) A rapid method for the determination of artemisinin and its biosynthetic precursors in Artemisia annua L. crude extracts. J Pharm Biomed Anal 84:269–277

    Article  CAS  PubMed  Google Scholar 

  • Suriyagoda LD, Dittert K, Lambers H (2018) Mechanism of arsenic uptake, translocation and plant resistance to accumulate arsenic in rice grains. Agric Ecosyst Environ 253:23–37

    Article  CAS  Google Scholar 

  • Swarnakar A (2016) Mitigation of toxic effects of sodium arsenate on germination, seedling growth and amylolytic enzyme of mungbean seedlings with macronutrients, micronutrients and organic acids. Int J Curr Microbiol App Sci 5(12):151–160

    Article  CAS  Google Scholar 

  • Tham LX, Nagasawa N, Matsuhashi S, SIshioka N, Kume TT (2001) Effect of radiation-degraded chitosan on plants stressed with vanadium. Radiat Phys Chem 61:171–175

    Article  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372

    Article  CAS  PubMed  Google Scholar 

  • Wallaart TE, van Uden W, Lubberink HG, Woerdenbag HJ, Pras N, Quax WJ (1999) Isolation and identification of dihydroartemisinic acid from Artemisia annua and its possible role in the biosynthesis of artemisinin. J Nat Prod 62:430–433

    Article  CAS  PubMed  Google Scholar 

  • Wallaart TE, Pras N, Beekman AC, Quax WJ (2000) Seasonal variation of artemisinin and its biosynthetic precursors in plants of Artemisia annua of different geographical origin: proof for the existence of chemotypes. Planta Med 66:57–62

    Article  CAS  PubMed  Google Scholar 

  • Wang YC, Zhang HX, Zhao B, Yaun XF (2001) Improved growth of Artemisia annua L. hairy roots and artemisinin production under red light conditions. Biotechnol Lett 23:1971–1973

    Article  CAS  Google Scholar 

  • Watson DJ (1958) The dependence of net assimilation rate on leaf-area index. Ann Bot 22:37–54

    Article  Google Scholar 

  • Weathers PJ, Arsenault PR, Covello PS, McMickle A, Teoh KH, Reed DW (2011) Artemisinin production in Artemisia annua studies in planta and results of a novel delivery method for treating malaria and other neglected diseases. Phytochem Rev 10:173–183

  • Weathers PJ, Bunk G, Mccoy MC (2005) The effect of phytohormones on growth and artemisinin production in Artemisia annua hairy roots. In Vitro Cell Dev Biol Plant 41:47–53

    Article  CAS  Google Scholar 

  • Xie DY, Zou ZR, Ye HC, Li GF, Guo ZC (2001) Selection of hairy root clones of Artemisia annua L. for artemisinin production. Israel J Plant Sci 49:129–134

    Article  CAS  Google Scholar 

  • Xu X, Zhu J, Huang D, Zhou W (1986) Total synthesis of arteannuin and deoxyarteannuin. Tetrahedron 42:819–828

    Article  CAS  Google Scholar 

  • Zhang Y, Xu G, Zhang S, Wang D, Prabha PS, Zho Z (2018) Antitumor research on artemisinin and its bioactive derivatives. Nat Prod Bioprospect 8(4):303–319

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao SS, Zeng MY (1986) Determination of Qinghaosu in Artemisia annua L. by high performance liquid chromatography. Chin J Pharma Anal 6:3–5

    Google Scholar 

  • Zong H, Liu S, Xing R, Chen X, Li P (2017) Protective effect of chitosan on photosynthesis and antioxidative defense system in edible rape (Brassica rapa L.) in the presence of cadmium. Ecotoxicol Environ Saf 138:271–278

    Article  CAS  PubMed  Google Scholar 

  • Zu YQ, Sun JJ, He YM, Wu J, Feng GQ, Li Y (2016) Effects of arsenic on growth, photosynthesis and some antioxidant parameters of Panax notoginseng growing in shaded conditions. Int J Adv Agric Res 4:78–88

    Google Scholar 

Download references

Funding

Dr. Mu. Naeem (Project No. SB/FT/LS-242/2012) gratefully acknowledges the financial support provided by the SERB (Science and Engineering Research Board), New Delhi in the form of research project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Naeem.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests to disclose.

Additional information

Handling Editor: Néstor Carrillo

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Naeem, M., Nabi, A., Aftab, T. et al. Oligomers of carrageenan regulate functional activities and artemisinin production in Artemisia annua L. exposed to arsenic stress. Protoplasma 257, 871–887 (2020). https://doi.org/10.1007/s00709-019-01475-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-019-01475-y

Keywords

Navigation