Abstract
Artemisia aucheri belongs to the Asteraceae family, which is known for its medicinal and aromatic properties. The present study was conducted to elucidate the influence of salicylic acid (SA) pretreatment on proline and glycine betaine (GB) metabolism as well as artemisinin biosynthesis in A. aucheri under in vitro osmotic stress (˗0.6 MPa) induced by polyethylene glycol (PEG). The expression of ∆1-pyrroline-5-carboxylate synthetase (P5CS) and betaine aldehyde dehydrogenase (BADH) genes and related enzymes were enhanced under osmotic stress. SA pretreatment improved accumulation of proline and GB and increased the expression of BADH and P5CS enzyme activity under osmotic stress. However, proline dehydrogenase (PDH) gene expression and PDH activity were not affected by osmotic stress and SA pretreatments. In addition, SA in combination with or without PEG induced expression of the key genes involved in artemisinin biosynthesis and increased artemisinin content. These findings indicated that, higher accumulation of proline and GB under osmotic stress by SA is possibly due to increasing of osmoprotectants biosynthesis. This study suggested that A. aucheri is one of the potential species for artemisinin biosynthesis under environmental stress and exogenous SA.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ADS:
-
Amorpha-4,11-diene synthase
- BADH:
-
Betaine aldehyde dehydrogenase
- CMO:
-
Choline monooxygenase
- CYP71AV1:
-
Cytochrome P450 monooxygenase
- GB:
-
Glycine betaine
- MS:
-
Murashige and Skoog
- PAL:
-
Phenylalanine ammonia lyase
- P5C:
-
∆1-pyrroline-5-carboxylate
- P5CDH:
-
Proline 5-carboxylate dehydrogenase
- P5CS:
-
∆1-pyrroline-5-carboxylate synthetase
- PDH:
-
Proline dehydrogenase
- PEG:
-
Polyethylene glycol
- ROS:
-
Reaction oxygen species
- SA:
-
Salicylic acid
References
Abbaspour J, Ehsanpour A (2016a) The impact of salicylic acid on some physiological responses of Artemisia aucheri Boiss. Under in vitro drought stress. Acta Agric Slov 107:287–298. https://doi.org/10.14720/aas.2016.107.2.03
Abbaspour J, Ehsanpour AA (2016b) Physiological targets of salicylic acid on Artemisia aucheri Boiss as a medicinal and aromatic plant grown under in vitro drought stress. Bot Stud 57:39. https://doi.org/10.1186/s40529-016-0154-6
Aftab T, Khan MMA, da Silva JAT, Idrees M, Naeem M (2011) Role of salicylic acid in promoting salt stress tolerance and enhanced artemisinin production in Artemisia annua L. J Plant Growth Regul 30:425–435. https://doi.org/10.1007/s00344-011-9205-0
Aftab T, Masroor M, Khan A, Idrees M, Naeem M (2010) Salicylic acid acts as potent enhancer of growth, photosynthesis and artemisinin production in Artemisia annua L. J Crop Sci Biotechnol 13:183–188. https://doi.org/10.1007/s12892-010-0040-3
Anjum SA et al. (2017) Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00069
Bandurska H, Cieślak M (2013) The interactive effect of water deficit and UV-B radiation on salicylic acid accumulation in barley roots and leaves. Environ Exp Bot 94:9–18. https://doi.org/10.1016/j.envexpbot.2012.03.001
Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Bian S, Jiang Y (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Sci Hortic 120:264–270. https://doi.org/10.1016/j.scienta.2008.10.014
Cecchini NM, Monteoliva MI, Alvarez ME (2011) Proline dehydrogenase contributes to pathogen defense in Arabidopsis. Plant Physiol 155:1947–1959. https://doi.org/10.1104/pp.110.167163
Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257. https://doi.org/10.1016/s1369-5266(02)00255-8
Covello PS, Teoh KH, Polichuk DR, Reed DW, Nowak G (2007) Functional genomics and the biosynthesis of artemisinin. Phytochemistry 68:1864–1871. https://doi.org/10.1016/j.phytochem.2007.02.016
ElSohly HN, Croom E, ElSohly M (1987) Analysis of the antimalarial sesquiterpene artemisinin in Artemisia annua by high-performance liquid chromatography (HPLC) with postcolumn derivatization and ultraviolet detection. Pharm Res 4:258–260. https://doi.org/10.1023/A:1016472531527
Fan W, Zhang M, Zhang H, Zhang P (2012) Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. PLoS One 7:e37344. https://doi.org/10.1371/journal.pone.0037344
Filippou P, Bouchagier P, Skotti E, Fotopoulos V (2014) Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environ Exp Bot 97:1–10. https://doi.org/10.1016/j.envexpbot.2013.09.010
Fitzgerald TL, Waters DL, Henry RJ (2009) Betaine aldehyde dehydrogenase in plants. Plant Biol 11:119–130
Gao XP, Wang XF, Lu YF, Zhang LY, Shen YY, Liang Z, Zhang DP (2004) Jasmonic acid is involved in the water-stress-induced betaine accumulation in pear leaves. Plant Cell Environ 27:497–507. https://doi.org/10.1111/j.1438-8677.2008.00161.x
Girma FS, Krieg DR (1992) Osmotic adjustment in sorghum I. mechanisms of diurnal osmotic potential changes. Plant Physiol 99:577–582. https://doi.org/10.1104/pp.99.2.577
Grieve C, Grattan S (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307. https://doi.org/10.1007/BF02374789
Guo C, Liu C, Ye H, Li G (2004) Effect of temperature on growth and artemisinin biosynthesis in hairy root cultures of Artemisia annua. Acta Bot Boreali-Occidential Sinica 24(10):1828–1831
Guo X-X, Yang X-Q, Yang R-Y, Zeng Q-P (2010) Salicylic acid and methyl jasmonate but not rose Bengal enhance artemisinin production through invoking burst of endogenous singlet oxygen. Plant Sci 178:390–397. https://doi.org/10.1016/j.plantsci.2010.01.014
Gupta S et al (2013) Molecular analysis of drought tolerance in tea by cDNA-AFLP based transcript profiling. Mol Biotechnol 53:237–248. https://doi.org/10.1007/s12033-012-9517-8
Hasanuzzaman M, Nahar K, Gill SS, Fujita M (2013) Drought stress responses in plants, oxidative stress, and antioxidant defense. In: Tuteja N, Gill SS (eds) Climate change and plant abiotic stress tolerance, 1rd edn. Wiley, New York, pp 209–250. https://doi.org/10.1002/9783527675265.ch09
Hayzer D, Leisinger T (1980) The gene-enzyme relationships of proline biosynthesis in Escherichia coli. Microbiology 118:287–293. https://doi.org/10.1099/00221287-118-2-287
He C, Zhang W, Gao Q, Yang A, Hu X, Zhang J (2011) Enhancement of drought resistance and biomass by increasing the amount of glycine betaine in wheat seedlings. Euphytica 177:151–167. https://doi.org/10.1007/s10681-010-0263-3
Hosseini R, Yazdani N, Garoosi G (2011) The presence of amorpha-4, 11-diene synthase, a key enzyme in artemisinin production in ten Artemisia species. DARU 19:332
Kang G et al (2013) Exogenous salicylic acid enhances wheat drought tolerance by influence on the expression of genes related to ascorbate-glutathione cycle. Biol Plant 57:718–724. https://doi.org/10.1007/s10535-013-0335-z
Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74. https://doi.org/10.1016/j.plaphy.2014.03.026
Khan MIR, Iqbal N, Masood A, Per TS, Khan NA (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8:e26374. https://doi.org/10.4161/psb.26374
Li D-M, Zhang J, Sun W-J, Li Q, Dai A-H, Bai J-G (2011) 5-Aminolevulinic acid pretreatment mitigates drought stress of cucumber leaves through altering antioxidant enzyme activity. Sci Hortic 130:820–828. https://doi.org/10.1016/j.scienta.2011.09.010
Liu J-M et al (1979) Structure and reaction of arteannuin. Acta Chim Sin 37:129–143
Liu S-C, Yao M-Z, Ma C-L, Jin J-Q, Ma J-Q, Li C-F, Chen L (2015) Physiological changes and differential gene expression of tea plant under dehydration and rehydration conditions. Sci Hortic 184:129–141. https://doi.org/10.1016/j.scienta.2014.12.036
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Mannan A, Ahmed I, Arshad W, Asim MF, Qureshi RA, Hussain I, Mirza B (2010) Survey of artemisinin production by diverse Artemisia species in northern. Pakistan Malar J 9:310. https://doi.org/10.1186/1475-2875-9-310
Marchese JA, Ferreira JF, Rehder VL, Rodrigues O (2010) Water deficit effect on the accumulation of biomass and artemisinin in annual wormwood (Artemisia annua L., Asteraceae). Braz J Plant Physiol 22(1):1–9. https://doi.org/10.1590/S1677-04202010000100001
Misra N, Saxena P (2009) Effect of salicylic acid on proline metabolism in lentil grown under salinity stress. Plant Sci 177:181–189. https://doi.org/10.1016/j.plantsci.2009.05.007
Mitsuya S, Tsuchiya A, Kono-Ozaki K, Fujiwara T, Takabe T, Takabe T (2015) Functional and expression analyses of two kinds of betaine aldehyde dehydrogenases in a glycinebetaine-hyperaccumulating graminaceous halophyte, Leymus chinensis. Springerplus 4:202. https://doi.org/10.1186/s40064-015-0997-4
Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5. https://doi.org/10.3389/fpls.2014.00004
Mojarrab M, Shiravand A, Delazar A, Heshmati Afshar F (2014) Evaluation of in vitro antimalarial activity of different extracts of Artemisia aucheri Boiss and A armeniaca Lam and fractions of the most potent extracts. Scientific World J:2014. https://doi.org/10.1155/2014/825370
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Mutlu S, Karadağoğlu Ö, Atici Ö, Nalbantoğlu B (2013) Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast. Biol Plant 57:507–513. https://doi.org/10.1007/s10535-013-0322-4
Nazar R, Umar S, Khan N, Sareer O (2015) Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. S Afr J Bot 98:84–94. https://doi.org/10.1016/j.sajb.2015.02.005
Ogawa D, Nakajima N, Tamaoki M, Aono M, Kubo A, Kamada H, Saji H (2007) The isochorismate pathway is negatively regulated by salicylic acid signaling in O3-exposed Arabidopsis. Planta 226:1277–1285. https://doi.org/10.1007/s00425-007-0556-5
Per TS, Khan NA, Reddy PS, Masood A, Hasanuzzaman M, Khan MIR, Anjum NA (2017) Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: Phytohormones, mineral nutrients and transgenics. Plant Physiol Biochem 115:126–140. https://doi.org/10.1016/j.plaphy.2017.03.018
Podlech D (1986) Artemisia L. In: Rechinger KH (ed) Flora Iranica, vol 158. Akademische Druck- und Verlagsanstalt, Graz, pp 159–223
Pu G-B et al (2009) Salicylic acid activates artemisinin biosynthesis in Artemisia annua L. Plant Cell Rep 28:1127–1135. https://doi.org/10.1007/s00299-009-0713-3
Qureshi MI, Abdin MZ, Ahmad J, Iqbal M (2013) Effect of long-term salinity on cellular antioxidants, compatible solute and fatty acid profile of sweet Annie (Artemisia annua L.). Phytochemistry 95:215–223. https://doi.org/10.1016/j.phytochem.2013.06.026
Rajaeian S, Ehsanpour A, Javadi M, Shojaee B (2017) Ethanolamine induced modification in glycine betaine and proline metabolism in Nicotiana rustica under salt stress. Biol Plant 61:797–800. https://doi.org/10.1007/s10535-017-0704-0
Ramel F, Sulmon C, Bogard M, Couée I, Gouesbet G (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol 9:28. https://doi.org/10.1186/1471-2229-9-28
Ranjbar M, Naghavi MR, Alizadeh H, Soltanloo H (2015) Expression of artemisinin biosynthesis genes in eight Artemisia species at three developmental stages. Ind Crop Prod 76:836–843. https://doi.org/10.1016/j.indcrop.2015.07.077
Rena AB, Splittstoesser WE (1975) Proline dehydrogenase and pyrroline-5-carboxylate reductase from pumpkin cotyledons. Phytochemistry 14:657–661. https://doi.org/10.1016/0031-9422(75)83010-X
Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338. https://doi.org/10.1093/jxb/err031
Senthil-Kumar M, Mysore S (2012) Ornithine-delta-aminotransferase and proline dehydrogenase genes play a role in non-host disease resistance by regulating pyrroline-5-carboxylate metabolism-induced hypersensitive response. Plant Cell Environ 35:1329–1343. https://doi.org/10.1111/j.1365-3040.2012.02492.x
Sharafi A, Sohi HH, Mirzaee H, Azadi P (2014) In vitro regeneration and agrobacterium mediated genetic transformation of Artemisia aucheri Boiss. Physiol Mol Biol Plants 20:487–494. https://doi.org/10.1007/s12298-014-0248-0
Shen C, Hu Y, Du X, Li T, Tang H, Wu J (2014) Salicylic acid induces physiological and biochemical changes in Torreya grandis cv. Merrillii seedlings under drought stress Trees 28:961–970. https://doi.org/10.1007/s00468-014-1009-y
Soni P, Abdin MZ (2017) Water deficit-induced oxidative stress affects artemisinin content and expression of proline metabolic genes in Artemisia annua L. FEBS open bio 7:367–381. https://doi.org/10.1002/2211-5463.12184
Špoljarević M, Agić D, Lisjak M, Gumze A, Wilson ID, Hancock JT, Teklić T (2011) The relationship of proline content and metabolism on the productivity of maize plants. Plant Signal Behav 6:251–257. https://doi.org/10.4161/psb.6.2.14336
Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97. https://doi.org/10.1016/j.tplants.2009.11.009
Toiu A, Vlase L, Oniga I, Tamas M (2008) HPLC analysis of salicylic acid derivatives from Viola species. Chem Nat Compd 44:357–358. https://doi.org/10.1007/s10600-008-9060-9
Wang F et al (2016) Cloning and characterization of a novel betaine aldehyde dehydrogenase gene from Suaeda corniculata. Genet Mol Res 15(2). https://doi.org/10.4238/gmr.15027848
Wani S, Brajendra Singh N, Haribhushan A, Iqbal Mir J (2013) Compatible solute engineering in plants for abiotic stress tolerance-role of glycine betaine. Curr Genomics 14:157–165. https://doi.org/10.2174/1389202911314030001
Weretilnyk EA, Hanson AD (1989) Betaine aldehyde dehydrogenase from spinach leaves: purification, in vitro translation of the mRNA, and regulation by salinity. Arch Biochem Biophys 271:56–63. https://doi.org/10.1016/0003-9861(89)90255-5
Yadav RK, Sangwan RS, Sabir F, Srivastava AK, Sangwan NS (2014) Effect of prolonged water stress on specialized secondary metabolites, peltate glandular trichomes, and pathway gene expression in Artemisia annua L. Plant Physiol Biochem 74:70–83. https://doi.org/10.1016/j.plaphy.2013.10.023
Yin H, Kjaer A, Fretté XC, Du Y, Christensen LP, Jensen M, Grevsen K (2012) Chitosan oligosaccharide and salicylic acid up-regulate gene expression differently in relation to the biosynthesis of artemisinin in Artemisia annua L process. Biochem 47:1559–1562. https://doi.org/10.1016/j.procbio.2011.12.020
Zhang C-s LQ, Verma DPS (1995) Removal of feedback inhibition of Δ1-pyrroline-5-carboxylate synthetase, a bifunctional enzyme catalyzing the first two steps of proline biosynthesis in plants. J Biol Chem 270:20491–20496. https://doi.org/10.1074/jbc.270.35.20491
Zheng Y, Li W, Sun W (2015) Effects of acclimation and pretreatment with abscisic acid or salicylic acid on tolerance of Trigonobalanus doichangensis to extreme temperatures. Biol Plant 59:382–388. https://doi.org/10.1007/s10535-015-0488-z
Acknowledgments
Authors are grateful to the University of Isfahan and Plant Antioxidants Center of Excellence (PACE) for their support. The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Jalil Abbaspour, Ali Akbar Ehsanpour. The first draft of the manuscript was written by Jalil Abbaspour and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declared no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Abbaspour, J., Ehsanpour, A.A. Sequential expression of key genes in proline, glycine betaine and artemisinin biosynthesis of Artemisia aucheri Boiss using salicylic acid under in vitro osmotic stress. Biologia 75, 1251–1263 (2020). https://doi.org/10.2478/s11756-020-00507-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-020-00507-w