Skip to main content
Log in

Physiological and cell ultrastructure disturbances in wheat seedlings generated by Chenopodium murale hairy root exudate

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

Abstract

Chenopodium murale L. is an invasive weed species significantly interfering with wheat crop. However, the complete nature of its allelopathic influence on crops is not yet fully understood. In the present study, the focus is made on establishing the relation between plant morphophysiological changes and oxidative stress, induced by allelopathic extract. Phytotoxic medium of C. murale hairy root clone R5 reduced the germination rate (24% less than control value) of wheat cv. Nataša seeds, as well as seedling growth, diminishing shoot and root length significantly, decreased total chlorophyll content, and induced abnormal root gravitropism. The R5 treatment caused cellular structural abnormalities, reflecting on the root and leaf cell shape and organization. These abnormalities mostly included the increased number of mitochondria and reorganization of the vacuolar compartment, changes in nucleus shape, and chloroplast organization and distribution. The most significant structural changes were observed in cell wall in the form of amoeboid protrusions and folds leading to its irregular shape. These structural alterations were accompanied by an oxidative stress in tissues of treated wheat seedlings, reflected as increased level of H2O2 and other ROS molecules, an increase of radical scavenging capacity and total phenolic content. Accordingly, the retardation of wheat seedling growth by C. murale allelochemicals may represent a consequence of complex activity involving both cell structure alteration and physiological processes.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allan AC, Fluhr R (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9:1559–1572

    Article  CAS  Google Scholar 

  • Andrzejczak O, Krasuska U, Olechowicz J, Staszek P, Ciacka K, Bogatek R, Hebelstrup K, Gniazdowska A (2018) Destabilization of ROS metabolism in tomato roots as a phytotoxic effect of meta-tyrosine. Plant Physiol Biochem 123:369–377

    Article  CAS  Google Scholar 

  • Araniti F, Grana E, Krasuska U, Bogatek R, Reigosa MJ, Abenavoli MR, Sanchez-Moreiras AM (2016) Loss of gravitropisam in farnesene –treated Arabidopsis is due to microtubule malformations related to hormonal and ROS unbalance. PLoS One 4:1–26

    Google Scholar 

  • Bartwal A, Mall R, Lohani P, Guru SK, Arora S (2013) Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J Plant Growth Regul 32:216

    Article  CAS  Google Scholar 

  • Batish DR, Lavanya K, Singh HP, Kohli RK (2007a) Phenolic allelochemicals released by Chenopodium murale affect the growth, nodulation and macromolecule content in chickpea and pea. Plant Growth Regul 51:119–128

    Article  CAS  Google Scholar 

  • Batish DR, Lavanya K, Singh HP, Kohli RK (2007b) Root-mediated allelopathic interference of nettle-leaved goosefoot (Chenopodium murale) on wheat (Triticum aestivum). J Agron Crop Sci 193(1):37–44

    Article  CAS  Google Scholar 

  • Burleigh JR, Tajani M, Seck M (1988) Effects of Pyrenophora teres and weeds on yield and yield components. Phytopathology 78:295–299

    Article  Google Scholar 

  • Burgos NR, Talbert RE, Kim KS, Kuk YI (2004) Growth inhibition and root ultrastructure of cucumber seedlings exposed to allelochemicals from rye (Secale cereale). J Chem Ecol 30:671–689

    Article  CAS  Google Scholar 

  • Chanliaud E, Burrows KM, Jeronimidis G, Gidley MJ (2002) Mechanical properties of primary plant cell wall analogues. Planta 215:989–996

    Article  CAS  Google Scholar 

  • Cheng Z, Moore J, Yu L (2006) High-throughput relative DPPH radical scavenging capacity assay. J Agric Food Chem 54:7429–7436

    Article  CAS  Google Scholar 

  • Cheng F, Cheng Z (2015) Research progress on the use of plant allelopathy in agriculture and the physiological and ecological mechanisms of allelopathy. Front Plant Sci 6:1020

    PubMed  PubMed Central  Google Scholar 

  • Ding H, Cheng Z, Liu M, Hayat S, Feng H (2016) Garlic exerts allelopathic effects on pepper physiology in a hydroponic co-culture system. Biol Open 5:631–637

    Article  CAS  Google Scholar 

  • Dmitrović S, Simonović A, Mitić N, Savić J, Cingel A, Filipović B, Ninković S (2015a) Hairy root exudates of allelopathic weed Chenopodium murale L. induce oxidative stress and down-regulate core cell cycle genes in Arabidopsis and wheat seedlings. Plant Growth Regul 75:365–382

    Article  Google Scholar 

  • Dmitrović S, Mitić N, Budimir S, Janošević D, Živković S, Skorić M, Ninković S (2015b) Morphohistological and bioherbicidal evaluation of wild-type and transformed hairy roots of goosefoot. S Afr J Bot 96:53–61

    Article  Google Scholar 

  • Du ZY, Bramlage WJ (1992) Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J Agric Food Chem 40:1566–1570

    Article  CAS  Google Scholar 

  • El-Khatib AA, Hegazy AK, Galal HK (2004a) Allelopathy in the rhizosphere and amended soil of Chenopodium murale. Weed Biol Manag 41:37–45

    Google Scholar 

  • El-Khatib AA, Hegazy AK, Galal HK (2004b) Does allelopathy have a role in the ecology of Chenopodium murale? Ann Bot Fennici 41:37–45

    Google Scholar 

  • Fernandez C, Monnier Y, Santonja M, Gallet C, Weston LA, Prévosto B, Saunier A, Baldy V, Bousquet-Mélou A (2016) The impact of competition and allelopathy on the trade-off between plant defense and growth in two contrasting tree species. Front Plant Sci 7:594

    PubMed  PubMed Central  Google Scholar 

  • Ferreres F, Figueiredo R, Bettencourt S, Carqueijeiro I, Oliveira J, Gil-Izquierdo A, Pereira DM, Valentao P, Andrade PB, Duarte P, Ros Barcelo A, Sottomayor M (2011) Identification of phenolic compounds in isolated vacuoles of the medicinal plant Catharanthus roseus and their interaction with vacuolar class III peroxidase: an H2O2 affair? J Exp Bot 62:2841–2854

    Article  CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 27:442–446

    Article  Google Scholar 

  • Gniazdowska A, Bogatek R (2005) Allelopathic interactions between plants. Multisite action of allelochemicals. Acta Physiol Plant 27:395–407

    Article  CAS  Google Scholar 

  • Gniazdowska A, Krasuska U, Andrzejczak O (2015) Allelopathic compounds as oxidative stress agents: YES or NO. In: Gupta KJ, Igamberdiev AU (eds) Reactive oxygen and nitrogen species signaling and communication in plants. Springer International Publishing, Switzerland, pp 155–266

    Google Scholar 

  • Grana E, SoteloT D-TC, Araniti F, Krasuska U, Bogatek R, Reigosa MJ, Sánchez-Moreiras AM (2013) Citral induces auxin and ethylene-mediated malformations and arrests cell division in Arabidopsis thaliana roots. J Chem Ecol 39:271–282

    Article  CAS  Google Scholar 

  • Guan Y, Lin H, Ma L, Yang Y, Hu X (2014) Nitric oxide and hydrogen peroxide are important signals mediating the allelopathic response of Arabidopsis to p-hydroxybenzoic acid. Physiol Plantarum 151:275–285

    Article  Google Scholar 

  • Gzyl J, Przymusinski R, Gwóźdź EA (2009) Ultrastructure analysis of cadmium-tolerant and -sensitive cell lines of cucumber (Cucumis sativus L.). Plant Cell Tissue Org Cult 99:227–232

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Holt JS, Orcutt DR (1991) Functional relationships of growth and competitiveness in perennial weeds and cotton (Gossypium hirsutum). Weed Sci 39:575–584

    Google Scholar 

  • Hussain I, Singh NB, Singh A, Singh H (2017) Allelopathic potential of sesame plant leachate against Cyperus rotundus L. Ann Agrar Sci 15(1):141–147

    Article  Google Scholar 

  • Islam I-U, Ahmed M, Asrar M, Siddiqui MF (2014) Allelopathic effects of Chenopodium murale L. on four test species. FUUAST J Biol 4(1):39–42

    Google Scholar 

  • Julkunen-Tiitto R (1985) Phenolics constituents in the leaves of northern willows: methods for the analysis of certain phenolics. J Agric Food Chem 33:213–217

    Article  CAS  Google Scholar 

  • Junglee S, Urban L, Sallanon H, Lopez-Lauri F (2014) Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. Am J Anal Chem 5:730–736

    Article  CAS  Google Scholar 

  • Kaur H, Inderjit, Kaushik S (2005) Cellular evidence of allelopathic interference of benzoic acid to mustard (Brassica juncea L.) seedling growth. Plant Physiol Biochem 43:77–81

    Article  CAS  Google Scholar 

  • Kaur G, Singh HP, Batish DR, Kohli RK (2013) Lead (Pb)-induced biochemical and ultrastructural changes in wheat (Triticum aestivum) roots. Protoplasma 250:53–62

    Article  CAS  Google Scholar 

  • Khaliq A, Hussain S, Matloob A, Wahid A, Aslam F (2013) Aqeous swine cress (Coronopus didymus) extracts inhibit wheat germination and early seedling growth. Int J Agric Biol 15:743–748

    Google Scholar 

  • Khaliq A, Hussain S, Matloob A, Tanveer A, Aslam F (2014a) Swine cress (Cronopus didymus L. Sm.) residues inhibit rice emergence and early seedling growth. Philipp Agric Sci 96:419–425

    Google Scholar 

  • Khaliq A, Matloob A, Chauhan BS (2014b) Weed management in dry-seeded fine rice under varying row spacing in the rice-wheat system of Punjab, Pakistan. Plant Prod Sci 17:321–332

    Article  Google Scholar 

  • Krasuska U, Andrzejczak O, Staszek P, Borucki W, Gniazdowska A (2016) Toxicity of canavanine in tomato (Solanum lycopersicum L.) roots is due to alterations in RNS, ROS and auxin levels. Plant Physiol Biochem 103:84–95

    Article  CAS  Google Scholar 

  • Lara-Nuñez A, Romero-Romero T, Ventura JL, Blancas V, Anaya AL, Cruz-Ortega R (2006) Allelochemical stress causes inhibition of growth and oxidative damage in Lycopersicon esculentum Mill. Plant Cell Environ 29:2009–2016

    Article  Google Scholar 

  • Macias FA, Oliva RM, Varela RM, Torres A, Molinillo JMG (1999) Allelochemicals from sunflower leaves cv Peredovick. Phytochemistry 52:613–621

    Article  CAS  Google Scholar 

  • Mitić N, Dmitrović S, Djordjević M, Zdravković-Korać S, Nikolić R, Raspor M, Djordjević T, Maksimović V, Živković S, Krstić-Milošević D, Stanišić M, Ninković S (2012) Use of Chenopodium murale L. transgenic hairy root in vitro culture system as a new tool for allelopathic assays. J Plant Physiol 169:1203–1211

    Article  Google Scholar 

  • Mitić N, Stanišić M, Savić J, Zdravković-Korać S, Ninković S (2015) Chenopodium murale hairy root exudates inhibit growth and induce oxidative stress in collard greens (Brassica oleracea L. var. acephala). Bot Serb 39(2):187–195

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Oad FC, Siddiqui MH, Buriro UA (2007) Growth and yield losses in wheat due to different weed densities. Asian J Plant Sci 6:173–176

    Article  Google Scholar 

  • Oerke EC (2006) Crop losses to pests. J Agric Sci 144(1):31–43

    Article  Google Scholar 

  • Pawlowski Â, Kaltchuk-Santos E, Zini CA, Caramão EB, Soares GLG (2012) Essential oils of Schinus terebinthifolius and S. molle (Anacardiaceae): Mitodepressive and aneugenic inducers in onion and lettuce root meristems. S Afr J Bot 80:96–103

    Article  CAS  Google Scholar 

  • Pedrol N, González L, Reigosa MJ (2006) Allelopathy and abiotic stress. In: Reigosa MJ, Pedrol N, González L (eds) Allelopathy: A physiological process with ecological implications. Springer, Dordrecht, pp 171–209

    Chapter  Google Scholar 

  • Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53:4290–4302

    Article  CAS  Google Scholar 

  • Pudełko K, Majchrzak L, Narożna D (2014) Allelopathic effect of fibre hemp (Cannabis sativa L.) on monocot and dicot plant species. Ind Crop Prod 56:191–199

    Article  Google Scholar 

  • Rice EL (1974) Allelopathy. Academic Press, New York

    Google Scholar 

  • Ritchie R (2008) Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol. Photosynthetica 46:115–126

    Article  CAS  Google Scholar 

  • Romero-Romero T, Sánchez-Nieto S, San Juan-Badillo A, Anaya AL, Cruz-Ortega R (2005) Comparative effects of allelochemical and water stress in roots of Lycopersicon esculentum Mill. (Solanaceae). Plant Sci 168(4):1059–1066

    Article  CAS  Google Scholar 

  • Rothe G, Valet G (1990) Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2′,7′-dichlorofluorescin. J Leukoc Biol 441:440–448

    Article  Google Scholar 

  • Soltys D, Rudzińska A, Kurek W, Gniazdowska A, Sliwinska E, Bogatek R (2011) Cyanamide mode of action during inhibition of onion (Allium cepa L.) root growth involves disturbances in cell division and cytoskeleton formation. Planta 234:609–621

    Article  CAS  Google Scholar 

  • Soltys D, Rudzińska-Langwald A, Kurek W, Szajko K, Sliwinska E, Bogatek R, Gniazdowska A (2014) Phytotoxic cyanamide affects maize (Zea mays) root growth and root tip function: from structure to gene expression. J Plant Physiol 171:565–575

    Article  CAS  Google Scholar 

  • Shulaev V, Oliver DJ (2006) Metabolic and proteomic markers for oxidative stress. New tools for reactive oxygen species research. Plant Physiol 141:367–372

    Article  CAS  Google Scholar 

  • Tarpey MM, Wink DA, Grisham MB (2004) Methods for detection of reactive metabolites of oxygen and nitrogen: in vitro and in vivo considerations. Am J Physiol Regul Integr Comp Physiol 286:431–444

    Article  Google Scholar 

  • Terpinc P, Bezjak M, Abramovic H (2009) A kinetic model for evaluation of the antioxidant activity of several rosemary extracts. Food Chem 115:740–744

    Article  CAS  Google Scholar 

  • Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616

    Article  CAS  Google Scholar 

  • Weir TL, Park SW, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479

    Article  CAS  Google Scholar 

  • Yang GQ, Wan FH, Liu WX, Guo J (2008) Influence of two allelochemicals from Ageratina adenophora Sprengel on ABA, IAA and ZR contents in roots of upland rice seedlings. Allelopath J 21:253–262

    Google Scholar 

  • Yu JQ, Ye SF, Zhang MF, Hu WH (2003) Effects of root exudates, aqueous root extracts of cucumber (Cucumis sativus L.) and allelochemicals on photosynthesis and antioxidant enzymes in cucumber. Biochem Syst Ecol 31:129–139

    Article  CAS  Google Scholar 

Download references

Funding

This research was funded by the Ministry of Education, Science and Technological Development of Serbia (Projects OI173015, OI173005 and OI173055).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Slavica Ninković.

Additional information

Handling Editor: Hanns H. Kassemeyer

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mitić, N., Stanišić, M., Savić, J. et al. Physiological and cell ultrastructure disturbances in wheat seedlings generated by Chenopodium murale hairy root exudate. Protoplasma 255, 1683–1692 (2018). https://doi.org/10.1007/s00709-018-1250-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-018-1250-0

Keywords

Navigation