Skip to main content
SpringerLink
Log in

Physiological and biochemical parameters: new tools to screen barley root exudate allelopathic potential (Hordeum vulgare L. subsp. vulgare)

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Morphological markers/traits are often used in the detection of allelopathic stress, but optical signals including chlorophyll a fluorescence emission could be useful in developing new screening techniques. In this context, the allelopathic effect of barley (Hordeum vulgare subsp. vulgare) root exudates (three modern varieties and three landraces) were assessed on the morphological (root and shoot length, biomass accumulation), physiological (Fv/Fm and F0), and biochemical (chlorophyll and protein contents) variables of great brome (Bromus diandrus Roth., syn. Bromus rigidus Roth. subsp. gussonii Parl.). All the measured traits were affected when great brome was grown in a soil substrate in which barley plants had previously developed for 30 days before being removed. The response of receiver plants was affected by treatment with activated charcoal, dependent on barley genotype and on the nature of the growing substrate. The inhibitory effect was lower with the addition of the activated charcoal suggesting the release of putative allelochemicals from barley roots into the soil. The barley landraces were more toxic than modern varieties and their effect was more pronounced in sandy substrate than in silty clay sand substrate. In our investigation, the chlorophyll content and Fv/Fm were the most correlated variables with barley allelopathic potential. These two parameters might be considered as effective tools to quantify susceptibility to allelochemical inhibitors in higher plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

F 0 :

Initial fluorescence

F v/F m :

Maximum quantum yield of PS II photochemistry

G:

Genotype

S:

Substrate

AC:

Activated charcoal

SS:

Sandy substrate

SCSS:

Silty clay sand substrate

References

  • Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin CT, Thomashow MF (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15 a gene affects both chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci USA 93:13404–13409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baghestani A, Lemieux C, Leroux GD, Baziramakenga R (1999) Determination of allelochemicals in spring cereal cultivars of different competitiveness. Weed Sci 47:498–504

    CAS  Google Scholar 

  • Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    Article  CAS  PubMed  Google Scholar 

  • Barkosky RR, Einhellig FA, Butler JL (2000) Caffeic acid-induced changes in plant–water relationships and photosynthesis in leafy spurge (Euphorbia esula). J Chem Ecol 26:2095–2109

    Article  CAS  Google Scholar 

  • Batish DR, Kaur S, Singh HP, Kohli RK (2009) Role of root-mediated interactions in phytotoxic interference of Ageratum conyzoides with rice (Oryza sativa). Flora 204:388–395

    Article  Google Scholar 

  • Baziramakenga R, Leroux GD, Simard RR, Nadeau P (1997) Allelopathic effects of phenolic acids on nucleic acid and protein levels in soybean seedlings. Can J Bot 75:445–450

    Article  CAS  Google Scholar 

  • Ben-Hammouda M, Ghorbal H, Kremer R, Oueslati O (2001) Allelopathic effects of barley extracts on germination and seedlings growth of bread and durum wheats. Agronomie 21:65–71

    Article  Google Scholar 

  • Ben-Hammouda M, Ghorbal H, Kremer RJ, Oueslati O (2002) Autotoxicity of barley. J Plant Nutr 25:1155–1161

    Article  CAS  Google Scholar 

  • Bertholdsson NO (2004) Variation in allelopathic activity over 100 years of barley selection and breeding. Weed Res 44:78–86

    Article  Google Scholar 

  • Bertholdsson NO (2005) Early vigour and allelopathy—two useful traits for enhanced barley and wheat competitiveness against weeds. Weed Res 45:94–102

    Article  Google Scholar 

  • Bouhaouel I, Gfeller A, Fauconnier ML, Slim Amara H, du Jardin P (2015) Allelopathic and autotoxicity effects of barley (Hordeum vulgare L. ssp. vulgare) root exudates. Biocontrol 60:425–436

    Article  CAS  Google Scholar 

  • Bouhaouel I, Gfeller A, Fauconnier ML, Delory B, Slim Amara H, du Jardin P (2016) Evaluation of the allelopathic potential of water-soluble compounds of barley (Hordeum vulgare L. subsp. vulgare) and great brome (Bromus diandrus Roth.) using a modified bioassay. Biotechnol Agron Soc Environ 20:482–494

    Google Scholar 

  • Bradford MM (1976) A rapid, sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cecchi AM, Koskinen WC, Cheng HH, Haider K (2004) Sorption–desorption of phenolic acids as affected by soil properties. Biol Fertil Soils 39:235–242

    Article  CAS  Google Scholar 

  • Cheremisinoff PN, Ellerbusch F (1978) Carbon adsorption handbook. Ann Arbor Science Publishers Inc, Ann Arbor

    Google Scholar 

  • Chiapusio G, Gallet C, Dobremez JF, Pellissier F (2008) Les composés allélopathiques: des molécules phytotoxiques pour demain? In: Regnault-Roger C, Philogène BJR, Vincent C (eds) Biopesticides d’origine végétales, 2nd edn. Lavoisier, Paris, pp 51–69

    Google Scholar 

  • Christensen S (1995) Weed suppression ability of spring barley varieties. Weed Res 35:241–247

    Article  Google Scholar 

  • Colton CE, Einhellig FA (1980) Allelopathic mechanisms of velvetleaf (Abutilon theophrasti Medic., Malvaceae) on soybean. Am J Bot 67:1407–1413

    Article  Google Scholar 

  • Courtois B, Olofsdotter M (1998) Incorporating the allelopathy trait in upland rice breeding programs. In: Olofsdotter M (ed) Allelopathy in rice, proceedings of the workshop on allelopathy in rice. IRRI, Manila, pp 57–67

    Google Scholar 

  • Delory BM, Delaplace P, Fauconnier ML, du Jardin P (2016) Root-emitted volatile organic compounds: can they mediate belowground plant–plant interactions? Plant Soil 402:1–26

    Article  CAS  Google Scholar 

  • Denden M, Bettaieb T, Salhi A, Mathlouthi M (2005) Effet de la salinité sur la fluorescence chlorophyllienne, la teneur en proline et la production florale de trois espèces ornementales. Tropicultura 23:220–225

    Google Scholar 

  • Dhima K, Vasilakoglou I, Gatsis T, Eleftherohorinos I (2010) Competitive interactions of fifty barley cultivars with Avena sterilis and Asperugo procumbens. Field Crops Res 117:90–100

    Article  Google Scholar 

  • Didon UME, Hansson ML (2003) Competition between six spring barley (Hordeum vulgare ssp. vulgare L.) cultivars and two weed flora in relation to interception of photosynthetic active radiation. Biol Agric Hortic 20:257–274

    Article  Google Scholar 

  • Ding J, Sun Y, Xiao CL, Shi K, Zhou YH, Yu JQ (2007) Physiological basis of different allelopathic reactions of cucumber and figleaf gourd plants to cinnamic acid. J Exp Bot 58:3765–3773

    Article  CAS  PubMed  Google Scholar 

  • El Faleh M, Maamouri A, Deghais M, El Ahmed A (1985) Three new barley cultivars from Tunisia. Rachis 4:50–51

    Google Scholar 

  • El Felah M (2011) L’orge en Tunisie; historique, état actuel et perspectives. Annales de l’INRAT 84:7–34

    Google Scholar 

  • El Felah M, Chalbi N, El Gazzeh M (1991) Analyse de l’adaptation à l’aridité de quelques ressources génétiques locales d’orge (Hordeum vulgare L.) comparativement à des variétés améliorées. In: Aupelf-UREF (ed) L’amélioration des plantes pour l’adaptation aux milieux arides. John Libbey Eurotext, Paris, pp 197–209

  • El Gharbi MS, El Felah M (2013) Les céréales en Tunisie : plus d’un siècle de recherche variétale. Annales de l’INRAT 86:45–68

    Google Scholar 

  • Elisante F, Mokiti TT, Ndakidemi PA (2013) Allelopathic effect of seed and leaf aqueous extracts of Datura stramonium on leaf chlorophyll content, shoot and root elongation of Cenchrus ciliaris and Neonotonia wightii. Am J Plant Sci 4:2332–2339

    Article  Google Scholar 

  • El-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul 45:215–224

    Article  CAS  Google Scholar 

  • Faraloni C, Cutino I, Petruccelli R, Leva AR, Lazzeri S, Torzillo G (2011) Chlorophyll fluorescence technique as a rapid tool for in vitro screening of olive cultivars (Olea europaea L.) tolerant to drought stress. Environ Exp Bot 73:49–56

    Article  CAS  Google Scholar 

  • Farhoudi R, Lee DJ (2013) Allelopathic effects of barley extract (Hordeum vulgare) on sucrose synthase activity, lipid peroxidation and antioxidant enzymatic activities of Hordeum spontoneum and Avena ludoviciana. Proc Natl Acad Sci India B 83:447–452

    Google Scholar 

  • Gallet C, Pellissier F (2002) Interactions allélopathiques en milieu forestier. Revue Forestière Française 54:557–574

    Google Scholar 

  • Gómez-Aparicio L, Canham CD (2008) Neighbourhood analyses of the allelopathic effects of the invasive tree Ailanthus altissima in temperate forests. J Ecol 96:447–458

    Article  Google Scholar 

  • Hammami Z, Sbei H, Kadri K, Jmel Z, Sahli A, Belhaj Fraj M, Naser H, Teixeira da Silva JA, Trifa Y (2016) Evaluation of performance of different barley genotypes irrigated with saline water in South Tunisian Saharan conditions. Environ Exp Biol 14:15–21

    Article  Google Scholar 

  • Hansen PK, Kristensen K, Willas J (2008) A weed suppressive index for spring barley (Hordeum vulgare) varieties. Weed Res 48:225–236

    Article  Google Scholar 

  • Hierro JL, Callaway RM (2003) Allelopathy and exotic plant invasion. Plant Soil 256:29–39

    Article  CAS  Google Scholar 

  • Hu Z, Li H, Chen S, Yang Y (2013) Chlorophyll content and photosystem II efficiency in soybean exposed to supplemental ultraviolet-B radiation. Photosynthetica 51:151–157

    Article  CAS  Google Scholar 

  • Hussain MI, Reigosa MJ (2011) Allelochemical stress inhibits growth, leaf water relations, PSII photochemistry, non-photochemical fluorescence quenching, and heat energy dissipation in three C3 perennial species. J Exp Bot 62:4533–4545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain MI, González L, Chiapusio G, Reigosa MJ (2011) Benzoxazolin-2(3H)-one (BOA) induced changes in leaf water relations, photosynthesis and carbon isotope discrimination in Lactuca sativa. Plant Physiol Biochem 49:825–834

    Article  CAS  PubMed  Google Scholar 

  • Inderjit C, Asakawa C (2001) Nature of interference potential of hairy vetch (Vicia villosa Roth) to radish (Raphanus sativus L.): does allelopathy play any role? Crop Prot 20:261–265

    Article  Google Scholar 

  • Jaradat AA (2013) Wheat landraces: a mini review. Emir J Food Agric 25:20–29

    Article  Google Scholar 

  • Jin MX, Li DY, Mi H (2002) Effects of high temperature on chlorophyll fluorescence induction and the kinetics of far red radiation-induced relaxation of apparent F 0 in maize leaves. Photosynthetica 40:581–586

    Article  CAS  Google Scholar 

  • Kalaji HM, Guo P (2008) Chlorophyll fluorescence: a useful tool in barley plant breeding programs. In: Sánchez A, Guttierrez SJ (eds) Photochemistry research progress. Nova Science Publishers Inc, New York, pp 439–463

    Google Scholar 

  • Kalaji HM, Oukarroum A, Alexandrov V, Kouzmanova M, Brestic M, Zivcak M, Samborska IA, Cetner MD, Allakhverdiev SI, Goltsev V (2014) Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. Plant Physiol Biochem 81:16–25

    Article  CAS  PubMed  Google Scholar 

  • Kamal J (2011) Impact of allelopathy of sunflower (Helianthus annuus L.) roots extract on physiology of wheat (Triticum aestivum L.). Afr J Biotechnol 10:14465–14477

    Article  CAS  Google Scholar 

  • Koocheki A, Lalegani B, Hosseini SA (2013) Ecological consequences of allelopathy. In: Zahid AC, Farooq M, Wahid A (eds) Allelopathy current trends and future applications. Springer, Berlin, pp 23–38

    Google Scholar 

  • Krause GH, Weis E (1984) Chlorophyll fluorescence as a tool in plant physiology. II. Interpretation of fluorescence signals. Photosynth Res 5:139–157

    Article  CAS  PubMed  Google Scholar 

  • Kremer R, Ben-Hammouda M (2009) Allelopathic plants. 19. Barley (Hordeum vulgare L.). Allelopath J 24:225–242

    Google Scholar 

  • Lau JA, Puliafico KP, Kopshever JA, Steltzer H, Jarvis EP, Schwarzländer M, Strauss SY, Hufbauer RA (2008) Inference of allelopathy is complicated by effects of activated carbon on plant growth. New Phytol 178:412–423

    Article  CAS  PubMed  Google Scholar 

  • Li ZH, Wang Q, Ruan Q, Pan CD, Jiang DA (2010) Phenolics and plant allelopathy. Molecules 15:8933–8952

    Article  CAS  PubMed  Google Scholar 

  • Li JY, Guo XK, Zhang Q, Liu CH, Lin ZH, Yu ZM, Wu H, He HB (2015) A novel screening method for rice allelopathic potential: the inhibitory-circle method. Weed Res 55:441–448

    Article  CAS  Google Scholar 

  • Lindqvista H, Bornman JF (2002) Influence of time of lifting and storage on the potential photosynthetic efficiency in newly developed leaves of bare-root silver birch and common oak. Sci Hortic 94:171–179

    Article  Google Scholar 

  • Liu DL, Lovett JV (1993) Biologically active secondary metabolites of barley. II. Phytotoxicity of barley allelochemicals. J Chem Ecol 19:2231–2244

    Article  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • Mersie W, Singh M (1993) Phenolic acids affect photosynthesis and protein synthesis by isolated leaf cells of velvet. J Chem Ecol 19:1293–1301

    Article  CAS  PubMed  Google Scholar 

  • Mishra A, Mishra KB, Hoermiller II, Heyer AG, Nedbal L (2011) Chlorophyll fluorescence emission as a reporter on cold tolerance in Arabidopsis thaliana accessions. Plant Signal Behav 6:301–310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morvillo CM, de la Fuente EB, Gil A, Martínez-Ghersa MA, González-Andújar JL (2011) Competitive and allelopathic interference between soybean crop and annual wormwood (Artemisia annua L.) under field conditions. Eur J Agron 34:211–221

    Article  Google Scholar 

  • Nilsson MC (1994) Separation of allelopathy and resource competition by the boreal dwarf shrub Empetrum hermaphroditum Hagerup. Oecologia 98:1–7

    Article  PubMed  Google Scholar 

  • Ninkovic V (2003) Volatile communication between barley plants affects biomass allocation. J Exp Bot 54:1931–1939

    Article  CAS  PubMed  Google Scholar 

  • Oveisi M, Mashhadi HR, Baghestani MA, Alizadeh HM, Badri S (2008) Assessment of the allelopathic potential of 17 Iranian barley cultivars in different development stages and their variations over 60 years of selection. Weed Biol Manag 8:225–232

    Article  Google Scholar 

  • Qasem JR, Hill TA (1989) On difficulties with allelopathy methodology. Weed Res 29:345–347

    Article  Google Scholar 

  • Rice EL (1984) Allelopathy, 2nd edn. Academic Press, Orlando

    Google Scholar 

  • Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126:444–450

    Article  PubMed  Google Scholar 

  • Romero-Romero T, Anaya AL, Cruz-ortega R (2002) Screening for effects of phytochemical variability on cytoplasmic protein synthesis pattern of crop plants. J Chem Ecol 28:617–629

    Article  CAS  PubMed  Google Scholar 

  • Semchenko M, Hutchings MJ, John EA (2007) Challenging the tragedy of the commons in root competition: confounding effect of neighbour presence and substrate volume. J Ecol 95:252–260

    Article  Google Scholar 

  • Shaukat SS, Munir N, Siddiqui IA (2003) Allelopathic responses of Conyza canadensis (L.) Cronquist: a cosmopolitan weed. Asian J Plant Sci 2:1034–1039

    Article  Google Scholar 

  • Singh G, Rai VK (1982) Responses of two differentially sensitive Cicer arietinum L. cultivars to water stress: protein content and drought resistance. Biol Plant 24:7–12

    Article  Google Scholar 

  • Singh A, Singh D, Singh NB (2009) Allelochemical stress produced by aqueous leachate of Nicotiana plumbaginifolia Viv. Plant Growth Regul 58:163–171

    Article  CAS  Google Scholar 

  • Souissi T, Belhadjsalah H, Mhafdhi M, Latiri K (2000) Non chemical control of Bromus diandrus Roth. in wheat in Tunisia. In: XI international conference on weed biology, Dijon

  • Souissi T, Belhadj Salah H, Latiri K (2001) Brome in cereal crops: infestations and management. L’Investisseur Agricole 42:29–32

    Google Scholar 

  • Tharayil N, Bhowmik PC, Xing B (2006) Preferential sorption of phenolic phytotoxins to soil: implications for altering the availability of allelochemicals. J Agric Food Chem 54:3033–3040

    Article  CAS  PubMed  Google Scholar 

  • Uddin MdN, Robinson RW, Caridi D (2014) Phytotoxicity induced by Phragmites australis: an assessment of phenotypic and physiological parameters involved in germination process and growth of receptor plant. J Plant Interact 9:338–353

    Article  CAS  Google Scholar 

  • Weidenhamer JD (1996) Distinguishing resource competition and chemical interference: overcoming the methodological impasse. Agron J 88:866–875

    Article  Google Scholar 

  • Weißhuhn K, Prati D (2009) Activated carbon may have undesired side effects for testing allelopathy in invasive plants. Basic Appl Ecol 10:500–507

    Article  Google Scholar 

  • Wu H, Pratley J, Lemerle D, Haig T, An M (2001) Screening methods for the evaluation of crop allelopathic potential. Bot Rev 67:403–415

    Article  Google Scholar 

  • Wurst S, Van Beersum S (2009) The impact of soil organism composition and activated carbon on grass–legume competition. Plant Soil 314:1–9

    Article  CAS  Google Scholar 

  • Wurst S, Vender V, Rillig MC (2010) Testing for allelopathic effects in plant competition: does activated carbon disrupt plant symbioses? Plant Ecol 211:19–26

    Article  Google Scholar 

  • Yang CM, Lee CN, Chou CH (2002) Effects of three allelopathic phenolics on chlorophyll accumulation of rice (Oryza sativa) seedlings: I. Inhibition of supply-orientation. Bot Bull Acad Sin 43:299–304

    CAS  Google Scholar 

  • Yang CM, Chang IF, Lin SJ, Chou CH (2004) Effects of three allelopathic phenolics on chlorophyll accumulation of rice (Oryza sativa) seedlings: II. Stimulation of consumption-orientation. Bot Bull Acad Sin 45:119–125

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zahra J, Nazim H, Cai S, Han Y, Wu D, Zhang B, Haider SI, Zhang G (2014) The influence of salinity on cell ultrastructures and photosynthetic apparatus of barley genotypes differing in salt stress tolerance. Acta Physiol Plant 36:1261–1269

    Article  CAS  Google Scholar 

  • Zhang KM, Shen Y, Zou XQ, Fang YM, Liu Y, Ma LQ (2016) Photosynthetic electron-transfer reactions in the gamethophyte of Pteris multifidi reveal the presence of allelopathic interference from the invasive plant species Bidens pilosa. J Photochem Photobiol B Biol 158:81–88

    Article  CAS  Google Scholar 

Download references

Acknowledgements

During this work, IB was the recipient of a Ph.D. fellowship of the Erasmus Mundus Averroès Partnerships Action of the European Commission. The financial support of internal grants from Gembloux Agro-Bio Tech throughout this work is acknowledged.

Author information

Author notes

  1. Aurélie Gfeller

    Present address: Swiss Federal Research Station Agroscope Changins Wädenswil AC, 1260, Nyon, Switzerland

Authors and Affiliations

  1. Plant Biology Laboratory, Gembloux Agro-Bio Tech, University of Liège, 2 Passage de Déportés, 5030, Gembloux, Belgium

    Imen Bouhaouel, Aurélie Gfeller & Patrick du Jardin

  2. General and Organic Chemistry Laboratory, Gembloux Agro-Bio Tech, University of Liège, 2 Passage de Déportés, 5030, Gembloux, Belgium

    Marie-Laure Fauconnier

  3. Genetics and Cereal Breeding Laboratory, Department of Agronomy and Plant Biotechnology, National Agronomic Institute of Tunisia, University of Carthage, 43 Charles Nicolle Street, 1082, Tunis, Tunisia

    Imen Bouhaouel, Khaoula Boudabbous & Hajer Slim Amara

Authors
  1. Imen Bouhaouel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aurélie Gfeller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Khaoula Boudabbous
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marie-Laure Fauconnier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hajer Slim Amara
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Patrick du Jardin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Imen Bouhaouel.

Additional information

Communicated by F. Araniti.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bouhaouel, I., Gfeller, A., Boudabbous, K. et al. Physiological and biochemical parameters: new tools to screen barley root exudate allelopathic potential (Hordeum vulgare L. subsp. vulgare). Acta Physiol Plant 40, 38 (2018). https://doi.org/10.1007/s11738-018-2604-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-018-2604-0

Keywords

Search

Navigation