Morpho-histological analysis of tomato (Solanum lycopersicum L.) plants after treatment with juglone

Anna Milewska-Hendel, Małgorzata Polak, Katarzyna Sala, Paulina Zieleźnik-Rusinowska, Robert Gawecki, Ewa Kurczyńska

Abstract


Juglone is a substance that limits plant growth and has a toxic effect on plant development. In this study, we analyzed the influence of juglone at two different concentrations (10−3 M and 10−4 M), which were applied to different parts of Solanum lycopersicum L. plants (root system, stem after decapitation, and surface of a younger leaf or after autografting) for a short period of time (7 days), on the morphology and histology of stems. At a lower concentration, juglone had positive effects on plant growth, which resulted in an increase in interfascicular cambial cell divisions, faster development of a continuous cambium layer along the stem circumference, and development of fibers. Additionally, under the influence of juglone, the number of developing leaves increased and adventitious roots developed. The results are discussed based on the current literature concerning the reaction of plants to juglone and to stress conditions.

Keywords


histology; cambium; fibers; juglone; morphology; tomato

Full Text:

PDF

References


Babula P, Vaverkova V, Poborilova Z, Ballova L, Masarik M, Provaznik I. Phytotoxic action of naphthoquinone juglone demonstrated on lettuce seedling roots. Plant Physiol Biochem. 2014;84:78–86. https://doi.org/10.1016/j.plaphy.2014.08.027

Jasicka-Misiak I. Allelopatyczne właściwości metabolitów wtórnych roślin uprawnych. Wiadomości Chemiczne. 2009;63:39–62.

Hejl AM, Einhellig FA, Rasmussen JA. Effects of juglone on growth, photosynthesis, and respiration. J Chem Ecol. 1993;19:559–568. https://doi.org/10.1007/BF00994325

Rudnicka M, Polak M, Karcz W. Cellular responses to naphthoquinones: juglone as a case study. Plant Growth Regul. 2013;72:239–248. https://doi.org/10.1007/s10725-013-9855-y

Kozak A, Leszczyński B, Sempruch C, Sytykiewicz H. Allelopatyczne oddziaływanie juglonu. Kosmos. 2014;305:611–622.

Gniazdowska A, Oracz K, Bogatek R. Allelopatia – nowe interpretacje oddziaływań pomiędzy roślinami. Kosmos. 2004;263:207–217.

Khodzhibaeva SM, Filatova OF, Tyshchenko AA. New aspects of the preparation and control of juglone. Chem Nat Compd. 2000;36:281–283. https://doi.org/10.1007/BF02238336

Kocacë Aliskan I, Terzi I. Allelopathic effects of walnut leaf extracts and juglone on seed germination and seedling growth. J Hortic Sci Biotechnol. 2001;76:436–440. https://doi.org/10.1080/14620316.2001.11511390

Page D, Gouble B, Valot B, Bouchet JP, Callot C, Kretzschmar A, et al. Protective proteins are differentially expressed in tomato genotypes differing for their tolerance to low-temperature storage. Planta. 2010;232:483–500. https://doi.org/10.1007/s00425-010-1184-z

Monteiro CC, Carvalho RF, Gratão PL, Carvalho G, Tezotto T, Medici LO, et al. Biochemical responses of the ethylene-insensitive Never ripe tomato mutant subjected to cadmium and sodium stresses. Environ Exp Bot. 2011;71:306–320. https://doi.org/10.1016/j.envexpbot.2010.12.020

Fischer I, Camus-Kulandaivelu L, Allal F, Stephan W. Adaptation to drought in two wild tomato species: the evolution of the Asr gene family. New Phytol. 2011;190:1032–1044. https://doi.org/10.1111/j.1469-8137.2011.03648.x

Wang M, Jiang W, Yu H. Effects of exogenous epibrassinolide on photosynthetic characteristics in tomato (Lycopersicon esculentum Mill) seedlings under weak light stress. J Agric Food Chem. 2010;58:3642–3645. https://doi.org/10.1021/jf9033893

Jeffree CE, Yeoman MM. Development of intercellular connections between opposing cells in a graft union. New Phytol. 1983;93:491–509. https://doi.org/10.1111/j.1469-8137.1983.tb02701.x

Huber DP, Philippe RN, Godard KA, Sturrock RN, Bohlmann J. Characterization of four terpene synthase cDNAs from methyl jasmonate-induced Douglas-fir, Pseudotsuga menziesii. Phytochemistry. 2005;66:1427–1439. https://doi.org/10.1016/j.phytochem.2005.04.030

Vitha S, Baluška F, Braun M, Šamaj J, Volkmann D, Barlow PW. Comparison of cryofixation and aldehyde fixation for plant actin immunocytochemistry: aldehydes do not destroy F-actin. Histochem J. 2000;32:457–466.

Rice EL. Allelopathy – update. Bot Rev. 1979;45:15–109. https://doi.org/10.1007/BF02869951

Whittaker RH, Feeny PP. Allelochemics – chemical interactions between species. Science. 1971;171:757. https://doi.org/10.1126/science.171.3973.757

Rizvi SJH, Rizvi V. Exploitation of allelochemicals in improving crop productivity. In: Rizvi SJH, Rizvi V, editors. Allelopathy basic and applied aspects. Dordrecht: Springer Netherlands; 1992. p. 443–472. https://doi.org/10.1007/978-94-011-2376-1_25

Terzi I. Allelopathic effects of juglone and decomposed walnut leaf juice on muskmelon and cucumber seed germination and seedling growth. Afr J Biotechnol. 2008;7:1870–1874.

Terzi I. Allelopathic effects of juglone and walnut leaf and fruit hull extracts on seed germination and seedling growth in muskmelon and cucumber. Asian Journal of Chemistry. 2009;21:1840–1846.

Terzi I, Kocaçalışkan I. Alleviation of juglone stress by plant growth regulators in germination of cress seeds. Scientific Research and Essays. 2009;4:436–439.

Hejl AM, Koster KL. 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. 2004;30:453–471. https://doi.org/10.1023/B:JOEC.0000017988.20530.d5

Jose S, Gillespie AR. 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. 1998;203:199–205. https://doi.org/10.1023/A:1004353326835

Torabi Z, Rafiei F, Shabani L, Danesh Shahraki A. Physiological and molecular response of annual Medicago species to juglone. Acta Physiol Plant. 2015;37:248. https://doi.org/10.1007/s11738-015-1999-0

Terzi I, Kocaçalişkan I, Benlioğlu O, Solak K. Effects of juglone on growth of cucumber seedlings with respect to physiological and anatomical parameters. Acta Physiol Plant. 2003;25:353–356. https://doi.org/10.1007/s11738-003-0016-1

Funk DT, Case PJ, Rietveld WJ, Phares RE. Notes: effects of juglone on the growth of coniferous seedlings. Forest Science. 1979;25:452–454.

Chen SY, Chi WC, Trinh NN, Cheng KT, Chen YA, Lin TC, et al. Alleviation of allelochemical juglone-induced phytotoxicity in tobacco plants by proline. J Plant Interact. 2015;10:167–172. https://doi.org/10.1080/17429145.2015.1045946

Rietveld WJ. Allelopathic effects of juglone on germination and growth of several herbaceous and woody species. J Chem Ecol. 1983;9:295–308. https://doi.org/10.1007/BF00988047

Neave IA, Dawson JO. Juglone reduces growth, nitrogenase activity, and root respiration of actinorhizal black alder seedlings. J Chem Ecol. 1989;15:1823–1836. https://doi.org/10.1007/BF01012269

Poborilova Z, Ohlsson AB, Berglund T, Vildova A, Provaznik I, Babula P. DNA hypomethylation concomitant with the overproduction of ROS induced by naphthoquinone juglone on tobacco BY-2 suspension cells. Environ Exp Bot. 2015;113:28–39. https://doi.org/10.1016/j.envexpbot.2015.01.005

Kocaçalışkan I, Turan E, Terzi I. Juglone effects on seedling growth in intact and coatless seeds of muskmelon. Afr J Biotechnol. 2008;7:4446–4449.

Kurczyńska EU, Beltowski M, Włoch W. Morphological and anatomical changes of scots pine dwarf shoots induced by air pollutants. Environ Exp Bot. 1996;36:185–197. https://doi.org/10.1016/0098-8472(96)01005-2

Kuroda K, Shimaji K. Wound effects on cytodifferentiation in hardwood xylem. IAWA Bulletin. 1985;6:107–118. https://doi.org/10.1163/22941932-90000922

Schneuwly DM, Stoffel M, Bollschweiler M. Formation and spread of callus tissue and tangential rows of resin ducts in Larix decidua and Picea abies following rockfall impacts. Tree Physiol. 2009;29:281–289. https://doi.org/10.1093/treephys/tpn026

Doncheva S, Amenos M, Poschenrieder C, Barcelo J. Root cell patterning: a primary target for aluminium toxicity in maize. J Exp Bot. 2005;56:1213–1220. https://doi.org/10.1093/jxb/eri115

Pasternak T, Rudas V, Potters G, Jansen M. Morphogenic effects of abiotic stress: reorientation of growth in seedlings. Environ Exp Bot. 2005;53:299–314. https://doi.org/10.1016/j.envexpbot.2004.04.009

Rucińska R, Waplak S, Gwóźdź EA. Free radical formation and activity of antioxidant enzymes in lupin roots exposed to lead. Plant Physiol Biochem. 1999;37:187–194. https://doi.org/10.1016/S0981-9428(99)80033-3

Arduini I, Masoni A, Mariotti M, Ercoli L. Low cadmium application increase miscanthus growth and cadmium translocation. Environ Exp Bot. 2004;52:89–100. https://doi.org/10.1016/j.envexpbot.2004.01.001

Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA. Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci. 2007;12:98–105. https://doi.org/10.1016/j.tplants.2007.01.004




DOI: https://doi.org/10.5586/aa.1701

Journal ISSN:
  • 2300-357X (online)
  • 0065-0951 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Publisher
Polish Botanical Society