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Juglone promotes shooting and inhibits rooting in leaf explants of in vitro raised tomato (Solanum lycopersicum L. var. Pusa Ruby) seedlings

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Abstract

Juglone is an inhibitor of choline acetyltransferase, an enzyme that catalyzes the synthesis of acetylcholine. Previous works have shown the effect of acetylcholine on in vitro morphogenesis in tomato explants. This work on juglone is designed to indirectly test the presence of acetylcholine biosynthesis in tomato plants. Leaf explants harvested from 30-d-old tomato (Solanum lycopersicum L. variety Pusa Ruby) seedlings were cultured on juglone-fortified control media. Juglone concentrations ranging from 10−9 to 10−3 M were used to check the dose response. It was observed that juglone significantly inhibited rooting and caused transition from rhizogenesis to caulogenesis at 10−7 to 10−6 M. Supplementation of different levels of juglone to the shoot regeneration medium enhanced the shoot formation and callus amounts, exhibiting best response at 10−5 M. This study suggests that juglone regulates morphogenesis in tomato via the acetylcholine system in plants.

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Data availability

All data generated or analyzed during this study are included in this manuscript, and the raw data will be made available from the corresponding author if required.

References

  • Ahmad T, Suzuki YJ (2019) Juglone in oxidative stress and cell signaling. Antioxidants 8:91

    Article  CAS  Google Scholar 

  • Antić TC, Milenković V (2015) Effects of juglone on pea and maize seed germination, early seedling development and detoxification enzyme activities. Bot Serbica 39:87–93

    Google Scholar 

  • Bamel K, Gupta R (2018) Acetylcholine as a regulator of differentiation and development in tomato. In: Ramakrishna A, Roschina VV (eds) Neurotransmitters in plants-perspectives and applications. CRC Press, Taylor & Francis Group, pp 113–132

    Chapter  Google Scholar 

  • Bamel K, Gupta R, Gupta SC (2015) Nicotine promotes rooting in leaf explants of in vitro raised seedlings of tomato, Lycopersicon esculentum Miller var. Pusa Ruby Int Immunopharmacol 29:231–234

    Article  CAS  Google Scholar 

  • Bamel K, Gupta R, Gupta SC (2016) Acetylcholine suppresses shoot formation and callusing in leaf explants of in vitro raised seedlings of tomato, Lycopersicon esculentum Miller var. Pusa Ruby Plant Signal Behav 11(e1187355):1–7

    Google Scholar 

  • Bamel K, Gupta SC, Gupta R (2007) Acetylcholine causes rooting in leaf explants of in vitro raised tomato (Lycopersicon esculentum Miller) seedlings. Life Sci 80:2393–2396

    Article  CAS  Google Scholar 

  • Basler E, McBride R (1977) Effects of coumarin, juglone and abscisic acid on the translocation of auxin, Proc. PGR Working Group IVth Annual Meeting, Hot Springs, Arkansas, 295–300

  • Dawson JO, Seymour PE (1983) Effects of juglone concentration on in vitro growth of Frankia ArI3 and Rhizobium japonicum strain 71. J Chem Ecol 9:1175–1183

    Article  CAS  Google Scholar 

  • Ercisli S, Esitken A, Turkkal C, Orhan E (2005) The allelopathic effects of juglone and walnut leaf extracts on yield, growth, chemical and PNE compositions of strawberry cv. Fern Plant Soil Environ 51:283–287

    Article  CAS  Google Scholar 

  • Fang F, Qin Y, Qi L, Fang Q, Zhao L, Chen S, Li Q, Zhang D, Wang L (2015) Juglone exerts antitumor effect in ovarian cancer cells. Iran J Basic Med Sci 18:544–548

    Google Scholar 

  • Hejl AM, Koster KL (2004) Juglone disrupts root plasma membrane H+-ATPase activity and impairs water uptake, root respiration, and growth in soybean (Glycine max) and corn (Zea mays). J Chem Ecol 30:453–471

    Article  CAS  Google Scholar 

  • Islam AKM, Widhalm JR (2020) Agricultural uses of juglone: opportunities and challenges. Agronomy 10:1500

    Article  CAS  Google Scholar 

  • Jay-Alleuran C, Doumas P, Sotta B, Tranvan H, Miginiac E, Sandermann H (1995) Juvenility and physiology of rhizogenesis in two woody species (Sequoia sempervirens and Juglans nigra x Juglans regia), Eurosilvia: Contribution to Forest Tree Physiology. Final Workshop, Eurosilvia Research programme, Dourdan pp. 79–99

  • Jose S, Gillespie AR (1998) Allelopathy in black walnut (Juglans nigra L.) alley cropping. II. Effects of juglone on hydroponically grown corn (Zea mays L.) and soybean (Glycine max L. Merr.) growth and physiology. Plant Soil 203:199–206

    Article  CAS  Google Scholar 

  • Kanaoka R, Kushiyama A, Seno Y, Nakatsu Y, Matsunaga Y, Fukushima Y, Tsuchiya Y, Sakoda H, Fugishiro M, Yamamotoya T, Kamata H, Matsubara A, Asano T (2015) Pin1 inhibitor juglone exerts anti-oncogenic effects on LNCaP and DU145 cells despite the patterns of gene regulation by Pin1 differing between these cell lines. PLoS ONE 10(e0127467):1–14

    Google Scholar 

  • Kobayashi A, Yata S, Hino T, Kawazu K (1987) A new fungal naphthoquinone which stimulates the production of antifungal compounds in alfalfa callus. Agri Biol Chem 51:2857–2860

    CAS  Google Scholar 

  • Kocacaliskan I, Turan E, Terzi I (2008) Juglone effects on seedling growth in intact and coatless seeds of muskmelon. Afr J Biotech 7:4446–4449

    Google Scholar 

  • Li HH, Nishimura H, Hasegawa K, Mizutani J (1993) Some physiological effects and the possible mechanism of action of juglone in plants. Weed Res 38:214–222

    CAS  Google Scholar 

  • Milewska-Hendel A, Polak M, Sala K, Zieleźnik-Rusinowska P, Gawecki R, Kurczyńska E (2017) Morpho-histological analysis of tomato (Solanum lycopersicum L.) plants after treatment with juglone. Acta Agrobot 70:1701. https://doi.org/10.5586/aa.1701

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Patil V, Chikate R, Belapure A, Padhye S (1987) Naphthoquinones as specific growth regulators for Sorghum vulgare especially under semi-arid cultivation. Ind J Exp Biol 25:337–339

    CAS  Google Scholar 

  • Perry SF (1967) Inhibition of respiration by juglone in Phaseolus and Lycopersicon. Bull Torr Bot Club 94: 26–30

    Article  CAS  Google Scholar 

  • Pfitzinger PL, Fangmann L, Wang K, et al…(2020) Indirect cholinergic activation slows down pancreatic cancer growth and tumor-associated inflammation. J Exp Clin Cancer Res 39, 289. https://doi.org/10.1186/s13046-020-01796-4

  • Ponder Jr F (1987) Allelopathic interference of black walnut trees with nitrogen-fixing plants in mixed plantings. In: Waller GR (ed) Allelochemicals: role in agriculture and forestry. ACS Symposium Series pp. 195–204

  • Ranade S, David SB (1985) Quinones as plant growth regulators. Plant Growth Reg 3:3–13

    Article  CAS  Google Scholar 

  • Randall VD, Bragg JD (1986) Effects of juglone (5ʹ-hydroxy-1, 4-naphthoquinone) on the algae Anabaena flos-aquae, Nostoc commune, and Scenedesmus acuminatus. J Ark Acad Sci 40:52–55

    Google Scholar 

  • Rietveld WJ (1983) Allelopathic effects of juglone on germination and growth of several herbaceous and woody species. J Chem Ecol 9:295–308

    Article  CAS  Google Scholar 

  • Rudnicka M, Polak M, Karcz W (2014) Cellular responses to naphthoquinones: juglone as a case study. Plant Growth Regul 72:239–248

    Article  CAS  Google Scholar 

  • Segura-Aguilar J, Hakman I, Rydström J (1992) The effect of 5OH-1, 4-naphthoquinone on Norway spruce seeds during germination. Plant Physiol 100:1955–1961

    Article  CAS  Google Scholar 

  • Sharma R, Gupta R (2007) Cyperus rotundus extract inhibits acetylcholinesterase activity from animal and plants as well as inhibits germination and seedling growth in wheat and tomato. Life Sci 80:2389–2392

    Article  CAS  Google Scholar 

  • Terzi I (2008) Allelopathic effects of Juglone and decomposed walnut leaf juice on muskmelon and cucumber seed germination and seedling growth. Afr J Biotech 7:1870–1874

    Google Scholar 

  • Tezuka T, Akita I, Yoshino N, Suzuki Y (2007) Regulation of self-incompatibility by acetylcholine and cAMP in Lilium longiflorum. J Plant Physiol 164:878–885

    Article  CAS  Google Scholar 

  • Tretyn A, Kendrick RE (1991) Acetylcholine in plants: presence, metabolism and mechanism of action. Bot Rev 57:33–73

    Article  Google Scholar 

  • Van Duuren BL, Segal A, Tseng SS, Rusch GM, Loewengart G, Mate U, Roth D, Smith A, Melchionne S, Seidman I (1978) Structure and tumor-promoting activity of analogues of anthralin (1,8-dihydroxy-9-anthrone). J Med Chem 2:126–131

    Google Scholar 

  • Vogel CS, Dawson JO (1985) Effect of juglone on growth in vitro of Frankia isolates and nodulation of Alnus glutinosa in soil. Plant Soil 87:79–89

    Article  CAS  Google Scholar 

  • Williams RD, Hoagland RE (1982) The effects of naturally occurring phenolic compounds on seed germination. Weed Sci 30:206–212

    Article  CAS  Google Scholar 

  • Willis RJ (2000) Juglans spp., juglone and allelopathy. Allelopathy J 7:1–55

    Google Scholar 

  • Yunghans H, Jaffe MJ (1972) Rapid respiratory changes due to red light or acetylcholine during the early events of phytochrome-mediated photomorphogenesis. Plant Physiol 49:1–7

    Article  CAS  Google Scholar 

Download references

Funding

Financial assistance was provided by the University Grants Commission, New Delhi, to RG as a research project entitled “Acetylcholine in Plant Growth and Development” and a Junior Research Fellowship to KB by the Council of Scientific and Industrial Research, New Delhi, India.

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RG contributed to the study conception and design. The material preparation, data collection, and analysis were performed by KB. The first draft of the manuscript was written by KB and RG read and commented on the previous versions of manuscript. Both authors read and approve the final manuscript.

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Correspondence to Kiran Bamel.

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Bamel, K., Gupta, R. Juglone promotes shooting and inhibits rooting in leaf explants of in vitro raised tomato (Solanum lycopersicum L. var. Pusa Ruby) seedlings. In Vitro Cell.Dev.Biol.-Plant 58, 942–949 (2022). https://doi.org/10.1007/s11627-022-10277-6

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