Enhanced seed germination of three Aristolochia species using light, karrikinolide and GA3

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Research Articles | Published:

Print ISSN : 0970-4078.
Online ISSN : 2229-4473.
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Doi: 10.1007/s42535-023-00643-z
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Keywords: n Aristolochian , Gibberellin, Light, Karrikinolide, Seed germination


Abstract


Aristolochia species form a large taxon and are used as traditional medicines. There are very few reports on seed germination of Aristolochia species. In this study, the effects of light and karrikinolide (KAR1) (1–100 nM) on seed germination of three sympatric Aristolochia species (A. labiata, A. debilis and A. ringens) from South China were investigated. The shortest germination period of the three species treated with both light and KAR1 was 8, 12 and 18 d, respectively. The percentage of seed germination in light was higher than in the dark in all three species, indicating that the seeds were light-sensitive and physiologically dormant. In the dark, the seeds of A. labiata and A. ringens could not germinate while only some A. debilis seeds germinated. After treatment with KAR1, A. debilis and A. labiata seeds germinated at a low frequency in the dark. However, A. ringens seeds could not germinate, even when exposed to a high concentration of KAR1. To investigate a possible functional mechanism of KAR1, A. labiata seeds were treated with 100 µM of some plant growth regulators, indole-3-acetic acid (IAA), abscisic acid (ABA), kinetin (KIN), gibberellic acid (GA3) and KAR1 (100 nM), and placed in the dark. Although the KAR1 + GA3 combination stimulated some seed germination, the seed germination in response to KAR1 and GA3 was not as efficient as in light. KIN, ABA, and IAA did not induced any seed germination in the dark.


n              Aristolochian            , Gibberellin, Light, Karrikinolide, Seed germination


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References


Adams CA, Baskin JM, Baskin CC (2005a) Comparative morphology of seeds of four closely related species of Aristolochia subgenus Siphisia (Aristolochiaceae, Piperales). Bot J Linn Soc 148:433–436. https://doi.org/10.1111/j.1095-8339.2005.00402.x


Adams CA, Baskin JM, Baskin CC (2005b) Trait stasis versus adaptation in disjunct relict species: evolutionary changes in seed dormancy-breaking and germination requirements in a subclade of Aristolochia subgenus Siphisia (Piperales). Seed Sci Res 15:161–173. https://doi.org/10.1079/SSR2005207


Akindele AJ, Wani Z, Mahajan G, Sharma S, Aigbe FR, Naresh Satti N, Adeyemi OO, Mondhe DM (2015) Anticancer activity of Aristolochia ringens vahl. J Tradit Complement Med 5:35–41. https://doi.org/10.1016/j.jtcme.2014.05.001. Aristolochiaceae


Alves Silva da D, Borghetti F, Thompson K, Pritchard H, Grime JP (2011) Underdeveloped embryos and germination in Aristolochia galeata seeds. Plant Biol 13:104–108. https://doi.org/10.1111/j.1438-8677.2009.00302.x


Baskin CC, Baskin JM (1998) Seeds: Ecology, biogeography, and evolution of dormancy and germination. Academic Press, San Diego, USA, p 666. https://doi.org/10.2135/cropsci2000.0009br


Baskin JM, Baskin CC (2004) A classification system for seed dormancy. Seed Sci Res 14:1–16. https://doi.org/10.1079/SSR2003150


Bliss BJ, Wanke S, Barakat A (2013) Characterization of the basal angiosperm Aristolochia fimbriata: a potential experimental system for genetic studies. BMC Plant Biol 13:13. https://doi.org/10.1186/1471-2229-13-13


Che CT, Almed MS, Kang SS, Waller DP, Bengel AS, Martin A, Rajamahendran P, Bunyapraphatsara J, Lankin DC, Cordell GA, Soejarto DD, Wijesekera ROB, Fong HHS (1984) Studies on Aristolochia III: isolation and biological evaluation of constituents of Aristolochia indica roots for fertility-regulationg activity. J Nat Prod 47:331–341. https://doi.org/10.1021/np50032a017


Corner EJH (1976) The seeds of dicotyledons, vols 1 and 2. Cambridge University Press, Cambridge


Daws MI, Jennifer D, Pritchard HW, Brown NAC, Van Staden J (2007) Butenolide from plant-derived smoke enhances germination and seeding growth of arable weed species. Plant Grow Reg 51:73–82. https://doi.org/10.1021/np900630w


Daws MI, Pritchard HW, Van Staden J (2008) Butenolide from plant derived smoke functions as a strigolactone analogue: evidence from parasitic weed seed germination. South Afr J Bot 74:116–120. https://doi.org/10.1016/j.sajb.2007.09.005


Daws N, Van Staden J (2007) The potential of the smoke-derived compound 3-methyl-2H-furo [2,3-c] pyran-2-one as a priming agent for tomato seeds. Seed Sci Res 17:175–181. https://doi.org/10.1017/S0960258507785896


De Cuyper C, Struk S, Braem L, Gevaert K, De Jaeger G, Goormachtig S (2017) Strigolactones, karrikins and beyond. Plant Cell Env 40:1691–1703. https://doi.org/10.1111/pce.12996


De Lange JH, Boucher C (1990) Autecological studies on Audouinia capitata (Bruniaceae). I. Plant-derived smoke as a seed germination cue. South Afr J Bot 56:700–703. https://doi.org/10.1016/S0254-6299(16)31009-2


Drewes FE, Smith MT, Van Staden J (1995) The effect of a plant-derived smoke extract in the germination of light sensitive lettuce seed. Plant Grow Regul 16:205–209. https://doi.org/10.1007/BF00029542


Flematti GR, Ghisalberti EL, Dixon K, Trengrove RD (2004) A compound from smoke that promotes seed germination. Science 305:977. https://doi.org/10.1126/science.1099944


Flematti GR, Ghisalberti EL, Dixon KW (2005) Synthesis of the seed germination stimulant 3-methyl-2H-furo [2, 3-c] pyran-2-one. Tetr Lett 46:5719–5721. https://doi.org/10.1016/j.tetlet.2005.06.077


International Agency for Research on Cancer, Lyon (2002) Some traditional Herbal Medicines, some mycotoxins, Naphthalene and Styrene. IARC Monogram on evaluation of carcinogenic risks in humans. IARC. https://doi.org/10.1016/S0378-8741(03)00216-2


Izquierdo AM, Zapata EV, Jiménez-Ferrer JE, Muñoz CB, Aparicio AJ, Torres KB, Torres LO (2010) Scorpion antivenom effect of micropropagated Aristolochia elegans. Pharm Biol 48:891–896. https://doi.org/10.3109/13880200903311110


Jain N, Strik WA, Van Staden J (2008) Cytokinin-and auxin-like activity of a butenolide isolated from plant-derived smoke. South Afr J Bot 74:327–331. https://doi.org/10.1016/j.sajb.2007.10.008


Kubmarawa D, Ajoku GA, Enwerem NM, Okorie DA (2007) Preliminary phytochemical and antimicrobial screening of 50 medicinal plants from Nigeria. Afr J Biotechnol 6:1690–1696. https://doi.org/10.5897/AJB2007.000-2246


Kulkarni MG, Sparg SG, Light ME, Van Staden J (2006) Stimulation of rice (Oryza sativa L.) seedling vigour by smoke-water and butenolide (3-methyl-2H-furo [2, 3-c] pyran-2-one). J Agr Crop Sci 192:395–398. https://doi.org/10.1111/j.1439-037X.2006.00213.x


Lawrence MK, González F (2003) Phylogenetic relationships in Aristolochiaceae. Syst Bot 28:236–249. https://doi.org/10.1043/0363-6445-28.2.236


Long RL, Williams K, Griffiths EM, Flematti GR, Merritt DJ, Stevens JC, Turner SR, Powles SB, Dixon KW (2010) Prior hydration of Brassica tournefortii seeds reduces the stimulatory effect of karrikinolide on germination and increases seed sensitivity to abscisic acid. Ann Bot 105:1063–1070. https://doi.org/10.1093/aob/mcq061


Lopes LMX, Nascimento IR, da Silva T (2001) Phytochemistry of the Aristolochiaceae family. In: Mohan RMM (ed) Research advances in Phytochemistry, vol 2. Global Research Network, Kerala, pp 9–108


Luciano RL, Perazella MA (2015) Aristolochic acid nephropathy: epidemiology, clinical presentation, and treatment. Drug Saf 38:55–64. https://doi.org/10.1007/s40264-014-0244-x


Ma GH, Bunn E, Dixon K, Flemati G (2006) Comparative enhancement of germination and vigour in seed and somatic embryos by the smoke chemical 3-methyl-2H-furo[2,3-c] pyran-2-one in Baloskion tetraphyllum (Restionaceae). In Vitro Cell Dev Biol - Plant 42:305–308. https://doi.org/10.1079/IVP2006758


Maekawa L, Albuquerque MCF, Coelho MFB (2010) Germination of Aristolochia esperanzae O. Kuntze seeds under different temperatures and light conditions. Rev Bras Plant Med 12:23–30. https://doi.org/10.1590/S1516-05722010000100005


Mangnus ED, Zwanenburg B (1992) Tentative molecular mechanism for germination stimulation of Striga and Orobanche seeds by strigol and its synthetic analogues. J Agric Food Chem 40:1066–1070. https://doi.org/10.1021/jf00018a032


Merritt DJ, Kristiansen M, Flematti GR, Turner SR, Ghisalberti EL, Trengove RD, Dixon KW (2006) Effects of a butenolide present in smoke on light-mediated germination of australian Asteraceae. Seed Sci Res 16:29–35. https://doi.org/10.1079/SSR2005232





Nakonechnaya OV, Gorpenchenko TY, Voronkova NM, Kholina AB, Zhuravlev YN (2013) Embryo structure, seed traits, and productivity of relict vine Aristolochia contorta (Aristolochiaceae). Flora 208:293–297. https://doi.org/10.1016/j.flora.2013.03.010


Nakonechnaya OV, Nesterova SV, Voronkova NM (2018) Germination of Aristolochia seeds (Aristolochiaceae). Mosc Univ Biol Sci Bull 73:209–216. https://doi.org/10.3103/S0096392518040077


Nedelko T, Arlt VM, Phillips DH, Hollstein M (2009) TP53 mutation signature supports involvement of aristolochic acid in the aetiology of endemic nephropathy-associated tumours. Int J Cancer 124:987–990. https://doi.org/10.1002/ijc.24006


Nelson DC, Flematti GR, Riseborough JA, Ghisalberti EL, Dixon KW, Steven MS (2010) Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proc Nat Acad Sci USA 107:7095–7100. https://doi.org/10.1073/pnas.0911635107


Nelson DC, Riseborough JA, Flematti GR, Stevens J, Ghisalberti EL, Dixon K, Smith SM (2009) Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiol 149:863–873. https://doi.org/10.1104/pp.108.131516


Ng AWT, Poon SL, Huang MN, Lim JQ, Boot A, Yu W, Suzuki Y, Thangaraju S, Ng CCY, Tan P, Pang ST, Huang HY, Yu MC, Lee PH, Hsieh SY, Chang AY, Teh BT, Rozen SG (2017) Aristolochic acids and their derivatives are widely implicated in liver cancers in Taiwan and throughout Asia. Sci Transl Med 18:eaan6446. https://doi.org/10.1126/scitranslmed.aan6446


Ribeiro LC, Pedrosa M, Borghetti F (2013) Heat shock effects on seed germination of five brazilian savanna species. Plant Biol 15:152–157. https://doi.org/10.1111/j.1438-8677.2012.00604.x





Roeder M, Ferraz IK, Hölscher D (2013) Seed and germination characteristics of 20 amazonian liana species. Plants 2:1–15. https://doi.org/10.3390/plants2010001


Rücker G, Mayer R, Breitmaier E, Will G, Kirfel A, Kordy ME (1984) Oxidized aristolane sesquiterpenes from. Aristolochia debilis Phytochemistry 23:1647–1649. https://doi.org/10.1016/S0031-9422(00)83460-3


Sami A, Rehman S, Ayyoub TM, Zhou XY, Zhu ZH, Zhou K (2021) Assessment of the germination potential of Brassica oleracea seeds treated with karrikin 1 and cyanide, which modify the ethylene biosynthetic pathway. J Plant Grow Reg 40:1257–1269. https://doi.org/10.1007/s00344-020-10186-1


Sharma G, Rajanna L (2021) GC-MS phytochemical profiling of leaf extracts of Aristolochia tagala cham. A rare and important ethnomedicinal plant. NISCAIR-CSIR, India. J Indian Chem Soc 100:100807. https://doi.org/10.1016/j.jics.2022.100807


Smith SM, Li J (2014) Signalling and responses to strigolactones and karrikins. Curr Opin Plant Biol 21:23–29. https://doi.org/10.1016/j.pbi.2014.06.003


Sparg SG, Kulkarni MG, Light ME, Van Staden J (2005) Improving seedling vigour of indigenous medicinal plants with smoke. Biores Tech 96:1323–1330. https://doi.org/10.1016/j.biortech.2004.11.015


Sulyman AO, Akolade JO, Sabiu SA, Aladodo RA, Muritala HF (2016) Antidiabetic potentials of ethanolic extract of Aristolochia ringens (vahl.) Roots. J Ethnopharmacol 182:122–128. https://doi.org/10.1016/j.jep.2016.02.002


Surhone LM, Tennoe MT, Henssonow SF (2011) Aristolochia labiata. Betascript Publishing, London


Van Staden J, Jäger AK, Strydom A (1995) Interaction between a plant-derived smoke extract, light and phytohormones on the germination of light-sensitive lettuce seeds. Plant Grow Regul 17:213–218. https://doi.org/10.1007/BF00024728


Voronkova NM, Kholina AB, Koldaeva MN, Nakonechnaya OV, Nechaev VA (2018) Morpho-physiological dormancy, germination, and cryopreservation in Aristolochia contorta seeds. Plant Ecol Evol 151:77–86. https://doi.org/10.5091/plecevo.2018.1351


Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 79:607–622. https://doi.org/10.1111/tpj.12488


Wu KM, Farrelly JG, Upton R, Chen J (2007) Complexities of the herbal nomenclature system in traditional chinese medicine (tcm): lessons learned from the misuse of Aristolochia-related species and the importance of the pharmaceutical name during botanical drug product development. Phytomedicine 14:273–279. https://doi.org/10.1016/j.phymed.2006.05.009


Wu TS, Damu AG, Su CR, Kuo PC (2004) Terpenoids of Aristolochia and their biological activities. Nat Prod Rep 21:594–624. https://doi.org/10.1002/chin.200504233


Yang T, Lian Y, Wang CY (2019) Comparing and contrasting the multiple roles of butenolide plant growth regulators: strigolactones and karrikins in plant development and adaptation to abiotic stresses. Intern J Mol Sci 20:6270. https://doi.org/10.3390/ijms20246270


Yao JR, Waters MT (2020) Perception of karrikins by plants: a continuing enigma. J Exp Bot 71:1774–1781. https://doi.org/10.1093/jxb/erz548


Yu JQ, Liao ZX, Cai XQ, Lei JC, Zouc GL (2007) Composition, antimicrobial activity and cytotoxicity of essential oils from Aristolochia mollissima. Environ Toxicol Pharmacol. https://doi.org/10.1016/j.etap.2006.08.004


Zhou J, Teixeira da Silva JA, Ma GH (2014) Effects of smoke water and karrikin on seed germination of 13 species growing in China. Centr Eur J Biol 9:1108–1116. https://doi.org/10.2478/s11535-014-0338-6


Zhou J, Xie G, Yan X (2011) Encyclopedia of Traditional Chinese Medicines: Molecular Structures, pharmacological activities, natural sources and applications. Springer, Berlin, Germany, pp 1–730. https://doi.org/10.1007/978-3-642-16744-7_1

 


Acknowledgements


This work was financially supported by the Guangdong Key Areas Biosafety Project (2022B1111040003), and the National Science and Technology Support Program (2021YFC3100400, 2022YFC3103700).


Author Information


Ma Guohua
Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, The Chinese Academy of Sciences, Guangzhou, China
magh@scib.ac.cn
da Silva Jaime A. Teixeira
Miki-cho, Japan


Zhou Junfang
Graduate University of Chinese Academy of Sciences, Beijing, China