Effect of intercropping alfalfa on physiological and biochemical parameters of young grapevine plants cultivated on agricultural and contaminated soils

Authors

  • Sabrine JEDER Laboratory of Legumes, Centre of Biotechnology of Borj-Cedria, B.P. 901, 2050 Hammam-Lif (TN)
  • Issam NOUAIRI Laboratory of Legumes, Centre of Biotechnology of Borj-Cedria, B.P. 901, 2050 Hammam-Lif (TN)
  • Fadwa MELKI Laboratory of Legumes, Centre of Biotechnology of Borj-Cedria, B.P. 901, 2050 Hammam-Lif (TN)
  • Samir CHEBIL University of Tunis El Manar, Laboratory of Plant Molecular Physiology, Centre of Biotechnology of Borj-Cedria, B.P. 901, 2050 Hammam-Lif (TN)
  • Faten LOUATI Laboratory of Legumes, Centre of Biotechnology of Borj-Cedria, B.P. 901, 2050 Hammam-Lif (TN)
  • Haythem MHADHBI Laboratory of Legumes, Centre of Biotechnology of Borj-Cedria, B.P. 901, 2050 Hammam-Lif (TN)
  • Kais ZRIBI Laboratory of Legumes, Centre of Biotechnology of Borj-Cedria, B.P. 901, 2050 Hammam-Lif (TN)

DOI:

https://doi.org/10.15835/nbha49112017

Keywords:

antioxidant enzyme; grapevine; growth; heavy metals; intercropping; Medicago sativa

Abstract

Our research aimed to reveal the capacity of intercropping with Medicago sativa-rhizobia in the amelioration of grapevine growth in agricultural and a Cd/Pb contaminated soils. A local variety of grapevine was cultivated in monocropping and in intercropping with Medicago sativa inoculated or not with its associated rhizobia. Intercropping with alfalfa induced a significant increase in shoot and root biomass of grapevine in the agricultural soil. However, in the contaminated soil, a slight increase in root biomass was observed. Concerning photosynthesis apparatus, we showed that the presence of Cd and Pb in the soil induced a significant decrease in both CO2 assimilation rate and stomatal conductance. Interestingly, intercropping with alfalfa only and with rhizobia alleviate this effect. Similar results are obtained for chlorophyll and carotenoid content. This was associated with a significant decrease in the malondialdehyde level in leaves and roots of grapevine cultivated in intercropping with alfalfa with and without inoculation in the two soils as compared the monoculture treatment. Comparison between treatments revealed also that intercropping with alfalfa induced a decrease in the activities of some enzymes implicated in the defence to the oxidative stress such as catalase and superoxide dismutase. Regarding soluble protein content, it is needed to signal the improvement of this parameter with the intercropping system in the contaminated soil when compared to the monocropping treatment. This work highlights the importance of the use of legumes in intercropping with grapevine as intercrop plant non-competitive for soil nutrient and proving N supply for associated plants.          

References

Abdelkrim S, Jebara S, Saadani O, Jebara M (2018). Potentialities of efficient and resistant plant growth promoting rhizobacteria in Pb uptake and defensive system stimulation of Lathyrus sativus under lead stress. Plant Biology 5:857. https://doi.org/10.1111/plb.12863

Acemi A, Duman YA, Karakuş YY, Özen F (2020). Effects of zinc and molybdenum on European Bluestar (Amsonia orientalis): An in vitro study. The EuroBiotech Journal 4(1):32-41. https://doi.org/10.2478/ebtj-2020-0005

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105:121. https://doi.org/10.1016/S0076-6879(84)05016-3

Aisha SA, Thoraua G, Abo El-Wafa SA, El-Kenawy MA (2017). Effect of intercropping of peas and clover corps on growth, productivity and soil characteristics of flame seedless and Thompson seedless grapevine cultivars. Egyptian Journal of Horticulture 44(2):183-197. https://doi.org/10.21608/EJOH.2017.1825.1022

Angelova, VR, Ivanov, AS, Braikov DM (1999). Heavy metals (Pb, Cu, Zn, and Cd) in the system soil-grapevine-grape. Journal of the Science of Food and Agriculture 79:713-721. https://doi.org/10.1002/(SICI)10970010(199912)79:15<2122:AID-JSFA536>3.0.CO;2-4

Beauchamp C, Fridovich I (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44:276. https://doi.org/10.1016/0003-2697(71)90370-8

Black C, Ong C (2000). Utilization of light and water in tropical agriculture. Agricultural and Forest Meteorology 104:25-47. https://doi.org/10.1016/S0168-1923(00)00145-3

Bouagga A, Chaabane H, Toumi K, Mougou Hamdane A, Nasraoui B, Joly L (2019). Pesticide residues in Tunisian table grapes and associated risk for consumer’s health. Food Additives & Contaminants: Part B 12:135-144. https://doi.org/10.1080/19393210.2019.1571532

Bouazizi H, Jouili H, Geitmann A, El Ferjani E (2010). Copper toxicity in expanding leaves of Phaseolus vulgaris L.: antioxidant enzyme response and nutrient element uptake. Ecotoxicology and Environmental Safety 73:1304-1308. https://doi.org/10.1016/j.ecoenv.2010.05.014

Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248. https://doi.org/10.1016/0003-2697(76)90527-3

Brooker RW, Bennett AE, Cong WF, Daniell TJ, George TS, Hallett PD, … Schob C (2015). Improving intercropping: A synthesis of research in agronomy, plant physiology and ecology. New Phytologist 206:107-117. https://doi.org/10.1111/nph.13132

Brunetto G, de Melo GWB, Terzano R (2016). Copper accumulation in vineyard soils: rhizosphere processes and agronomic practices to limit its toxicity. Chemosphere 162:293-307. https://doi.org/10.1016/j.chemosphere.2016.07.104

Clemens S, Ma JF (2016). Toxic heavy metal and metalloid accumulation in crop plants and foods. Annual Review of Plant Biology 67:489-512. https://doi.org/10.1146/annurev-arplant-043015-112301

Colugnati G, Cattarossi G, Crespan G (2004). Gestione del terreno in viticoltura. Vigne Vini 11:53-83.

Contreras F, Díaz J, Rombolà AD, Mora ML (2019). Prospecting intercropping between subterranean clover and grapevine as potential strategy for improving grapevine performance. Current Plant Biology 19:100-110. https://doi.org/10.1016/j.cpb.2019.100110

Contreras-Govea FE, Muck RE, Armstrong KL, Albrecht KA (2009). Fermentability of corn–lablab bean mixtures from different planting densities. Animal Feed Science and Technology 149:298-306. https://doi.org/10.1016/j.anifeedsci.2008.05.009

Crews TE, Peoples MB (2004). Legume versus fertilizer sources of nitrogen: ecological tradeoffs and human needs. Agriculture, Ecosystems & Environment 102:279-297. https://doi.org/10.1016/j.agee.2003.09.018

Darkwa K, Ambachew D, Mohammed H, Asfaw A, Blair MW (2016). Evaluation of common bean (Phaseolus vulgaris L.) genotypes for drought stress adaptation in Ethiopia. Crop Journal 4(5):367-376. https://doi.org/10.1016/j.cj.2016.06.007

De Conti L, Ceretta CA, Melo GWB, Tiecher TL, Silva LOS, Garlet LP, … Brunetto G (2019). Intercropping of young grapevines with native grasses for phytoremediation of Cu-contaminated soils. Chemosphere 216:147-156. https://doi.org/10.1016/j.chemosphere.2018.10.134

Defez R, Andreozzi A, Bianco C (2017). The overproduction of indole-3-acetic-acid (IAA) in endophytes up-regulates nitrogen fixation in both bacterial cultures and inoculated rice plants. Microbial Ecology 74:441-452. https://doi.org/10.1007/s00248-017-0948-4

Erakhrumen AA (2007). Phytoremediation: an environmentally sound technology for pollution prevention, control and remediation in developing countries. Educational Research Review 2(7):151-156. http://academicjournals.org/ERR2

Farghali KA, Quronfulah ASA (2016). Impact of lead on water soluble metabolites in some cultivars of Triticum aestivum L. grown under osmotic water potential. International Journal of Ecotoxicology and Ecobiology 1(2):20-27. https://doi.org/10.11648/j.ijee.20160102.11

García-Ruiz JM (2010). The effects of land uses on soil erosion in Spain: A review. Catena 81(1):1-11. https://doi.org/10.1016/j.catena.2010.01.001

Gorcena Y, Gordon AJ, Escuredo PR, Minchin FR, Witty JF, Moran JF, Becana M (1997). N2 fixation, carbon metabolism, and oxidative damage in nodules of dark-stressed common bean plants. Plant Physiology 113:1193. https://www.jstor.org/stable/4277641

Guerra B, Steenwerth K (2012). Influence of floor management technique on grapevine growth, disease pressure, and juice and wine composition: a review. American Journal of Enology and Viticulture 63:149-164. https://doi.org/10.5344/ajev.2011.10001

Hauggaard-Nielsen H, Jensen ES (2005). Facilitative Root Interactions in Intercrops. Plant and Soil 274:237-250. https://doi.org/10.1007/s11104-004-1305-1

Hinsinger P, Bengough AG, Vetterlein D (2009). Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant and Soil 321:117-152. https://doi.org/10.1007/s11104-008-9885-9

Kennelly MM, Gadoury DM, Wilcox W, Magarey PA, Seem RC (2005). Seasonal development of ontogenic resistance to downy mildew in grape berries and rachises. Phytopathology 95:1445-1452. https://doi.org/10.1094/PHYTO-95-1445

Li L, Tilman D, Lambers H, Zhang FS (2014). Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytologist 203:63-69. https://doi.org/10.1111/nph.12778

Li L, Zhang L-Z, Zhang F-Z (2013). Crop mixtures and the mechanisms of overyielding. In: Levin SA (Ed.) Encyclopedia of biodiversity, 2nd edn, vol, 2. Waltham, MA, USA: Academic Press pp 382-395. https://doi.org/10.1016/B978-0-12-384719-5.00363-4

Li YF, Ran W, Zhang R, Sun S, Xu G (2009). Facilitated legume nodulation, phosphate uptake and nitrogen transfer by arbuscular inoculation in an upland rice and mungbean intercropping system. Plant and Soil 315:285-296. https://doi.org/10.1007/s11104-008-9751-9

Lichtenthaler H, Wellburn A (1983). Determinations of total carotenoids and chlorophylls b of leaf extracts in different solvents. Biochemical Society Transactions 11:591. https://doi.org/10.1042/bst0110591

Liu H, Xu F, Xie Y, Wang C, Zhang AL, Xu H (2018). Effect of modified coconut shell biochar on availability of heavy metals and biochemical characteristics of soil in multiple heavy metals contaminated soil. Science of The Total Environment 645: 702. https://doi.org/10.1016/j.scitotenv.2018.07.115

MacAdam KB, Steinbach A, Wieman C (1992). A narrow‐band tunable diode laser system with grating feedback, and a saturated absorption spectrometer for Cs and Rb. American Journal of Physics 60:1098. https://doi.org/10.1119/1.16955

Medrano H, Tomás M, Martorell S et al (2015). Improving water use efficiency of vineyards in semi-arid regions-a review. Agronomy for Sustainable Development 35:499-517. https://doi.org/10.1007/s13593-014-0280-z

Mercenaro L, Nieddu G, Pulina P, Porqueddu C (2014). Sustainable management of an intercropped Mediterranean vineyard. Agriculture, Ecosystems & Environment 192:95-104. https://doi.org/10.1016/j.agee.2014.04.005

Monteiro A, Lopes CM (2007). Influence of cover crop on water use and performance of vineyard in Mediterranean Portugal. Agriculture, Ecosystems & Environment 121:336-342. https://doi.org/10.1016/j.agee.2006.11.016

Moura DJ, Péres VF, Jacques RA, Saffi J (2012). Heavy metal toxicity: oxidative stress and DNA repair. In: Metal Toxicity in Plants: Perception, Signaling and Remediation (Eds) Gupta DK, Sandalio LM (Granada: Springer-Verlag), pp 187-205. https://doi.org/10.1007/978-3-642-22081-4_9

Nagwa RA, Ahmed FF Al-Hussein SA (2014). Physiological studies on intercropping of some legumes on Sewy Date Palms. World Rural Observations 6(4):81-88. http://www.sciencepub.net/rural

Nouairi I, Mrabet M, Rabhi M, Mhadhbi H, Zribi K (2015). Cu-tolerant Sinorhizobium meliloti strain is beneficial for growth, Cu accumulation, and mineral uptake of alfalfa plants grown in Cu excess. Archives of Agronomy and Soil Science 61:1707-1718. https://doi.org/10.1080/03650340.2015.1036043

Pajuelo E, Carrasco JA, Romero LC, Chamber MA, Gotor C (2007). Evaluation of the metal phytoextraction potential of crop legumes. Regulation of the expression of O-acetylserine (thiol) lyase under metal stress. Plant Biology 9: 672-681. https://doi.org/10.1055/s-2007-965439

Paunov M, Koleva L, Vassilev A, Vangronsveld J, Goltsev V (2018). Effects of different metals on photosynthesis: cadmium and zinc affect chlorophyll fluorescence in durum wheat. International Journal of Molecular Science 19:787. https://doi.org/10.3390/ijms19030787

Pokhrel S, Pokhrel S (2013). Legumes crop rotation can improve food and nutrition security in Nepal. Agronomy journal 3:123-127. https://doi.org/10.3126/ajn.v3i0.9014

Rahman MM, Islam AM, Azirun SM, Boyce AN (2014). Tropical legume crop rotation and nitrogen fertilizer effects on agronomic and nitrogen efficiency of rice. The Scientific World Journal https://doi.org/10.1155/2014/490841

Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012). Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnology Advances 30:1562-1574. https://doi.org/10.1016/j.biotechadv.2012.04.011

Raklami A, Oufdou K, Tahiri A-I, Mateos-Naranjo E, Navarro-Torre S, Rodríguez-Llorente ID, … Pajuelo E (2019). Safe Cultivation of Medicago sativa in metal-polluted soils from semi-arid regions assisted by heat- and metallo-resistant PGPR. Microorganisms 7:212. https://doi.org/10.3390/microorganisms7070212

Rusinowski S, Szada-Borzyszkowska A, Zieleznik-Rusinowska P, Małkowski E, Krzyzak J, Wozniak G (2019). How autochthonous microorganisms influence physiological status of Zea mays L. cultivated on heavy metal contaminated soils? Environmental Science and Pollution Research 26:4746-4763. https://doi.org/10.1007/s11356-018-3923-9

Salomé C, Coll P, Lardo E, Metay A, Villenave C, Marsden C, … Le Cadre E (2016). The soil quality concept as a framework to assess management practices in vulnerable agroecosystems: A case study in Mediterranean vineyards. Ecological Indicators 61:456-465. https://doi.org/10.1016/j.ecolind.2015.09.047

Sandalio LM, Rodriguez-Serrano M, del Rio LA, Romero-Puertas MC (2009). Reactive oxygen species and signaling in cadmium toxicity. In: Reactive Oxygen Species in Plant Signaling (Eds) del Rio LA, Puppo A (Berlin; Heidelberg: Springer-Verlag), pp 175-189. doi: 10.1007/978-3-642-00390-5_11

Shao Z, Wang X, Gao Q, Zhang H, Yu H, Wang Y, … Gao Y (2020). Root contact between maize and alfalfa facilitates nitrogen transfer and uptake using techniques of foliar 15n-labeling. Agronomy 10:360. https://doi.org/10.3390/agronomy10030360

Shoeib MM (2012). Effect of intercropping on fruiting and growth of Flame seedless grapevines. Journal of Plant Production 3(1):33-50. https://doi.org/10.21608/JPP.2012.84026

Sillon JF, Ozier-Lafontaine H, Brisson N (2000). Modelling daily root interactions for water in a tropical shrub and grass alley cropping system. Agroforestry Systems 49:131-152. https://doi.org/10.1023/A:1006378708890

Sitko K, Rusinowski S, Kalaji HM, Szopinski M, Małkowski E (2017). Photosynthetic efficiency as bioindicator of environmental pressure in A. halleri. Plant Physiology 175:290-302. https://doi.org/10.1104/pp.17.00212

Stagnari F, Maggio A, Galieni A, Pisante M (2017). Multiple benefits of legumes for agriculture sustainability: an overview. Chemical and Biological Technologies in Agriculture 4:1-13. DOI 10.1186/s40538-016-0085-1

Sun B, Gao Y, Yang H (2019). Performance of alfalfa rather than maize stimulates system phosphorus uptake and overyielding of maize/alfalfa intercropping via changes in soil water balance and root morphology and distribution in a light chernozemic soil. Plant and Soil 439:145-161. https://doi.org/10.1007/s11104-018-3888-y

Sun B, Peng Y, Yang H, Li Z, Gao Y, Wang C (2014). Alfalfa (Medicago sativa L.)/maize (Zea mays L.) intercropping provides a feasible way to improve yield and economic incomes in farming and pastoral areas of Northeast China. Plos OneE 9(10):e110556. https://doi.org/10.1371/journal.pone.0110556

Szopinski M, Sitko K, Gieron Z, Rusinowski S, Corso M, Hermans C, … Małkowski E (2019). Toxic effects of Cd and Zn on the photosynthetic apparatus of the Arabidopsis halleri and Arabidopsis arenosa pseudo-metallophytes. Frontiers in Plant Science 10:748. https://doi.org/10.3389/fpls.2019.00748

Vandermeer J (1989). The ecology of intercropping. Cambridge University Press, Cambridge, pp 237. https://doi.org/10.1017/CBO978051162352

Vassilev A, Nikolova A, Koleva L, Lidon F (2011). Effects of excess Zn on growth and photosynthetic performance of young bean plants. Journal of Phytology 3:58-62. www.scholarjournals.org

Verbruggen N, Hanikenne M, Clemens S (2013). A more complete picture of metal hyperaccumulation through next-generation sequencing technologies. Frontiers in Plant Science 4:00388. https://doi.org/10.3389/fpls.2013.00388

Vincent JM (1970). A manual for the practical study of the root-nodule bacteria. https://doi.org/10.1002/jobm.19720120524

White PJ, George TS, Gregory PJ, Bengough AG, Hallett PD, McKenzie BM (2013b). Matching roots to their environment. Annals of Botany 112:207-222. https://doi.org/10.1093/aob/mct123

Xiao Y, Li L, Zhang F (2004). Effect of root contact on interspecific competition and N transfer between wheat and fababean using direct and indirect 15N techniques. Plant and Soil 262:45-54. https://doi.org/10.1038/s41598-020-61234-5

Xue Z-C, Gao H-Y, Zhang L-T (2013). Effects of cadmium on growth, photosynthetic rate, and chlorophyll content in leaves of soybean seedlings. Biologia Plantarum 57(3):587-590. https://doi.org/10.1007/s10535-013-0318-0

Yadav KK, Gupta N, Kumar A, Reece LM, Singh N, Rezania S, Khan SA (2018). Mechanistic understanding and holistic approach of phytoremediation: A review on application and future prospects. Ecological Engineering 120:274. https://doi.org/10.1016/j.ecoleng.2018.05.039

Zhang KH, Ding H, Zhou ZX, HE YN (2016). Effects of wheat/alfalfa intercropping on soil nutrients. Scholars Journal of Agriculture and Veterinary Sciences 3(5):346-350. https://doi.org/10.21276/sjavs.2016.3.5.2

Zhao M, Jones CM, Meijer J, Lundquist PO, Fransson P, Carlsson G, Hallin S (2017). Intercropping affects genetic potential for inorganic nitrogen cycling by root-associated microorganisms in Medicago sativa and Dactylis glomerata. Applied Soil Ecology 119:260. https://doi.org/10.1016/j.apsoil.2017.06.040

Zhen-Hua C, Wen-Lu B, Xin-Yi H, Yan X, Peng-Min LM, Andrew W, Qiao-Chun W (2016). Responses of in vitro-grown plantlets (Vitis vinifera) to grapevine leafroll-associated Virus-3 and PEG-induced drought stress. Frontiers in Physiology 7:203. https://doi.org/10.3389/fphys.2016.00203

Zribi K, Nouairi I, Slama I, Talbi-Zribi O, Mhadhbi H (2015). Medicago sativa-Sinorhizobium meliloti symbiosis promotes the bioaccumulation of Zinc in nodulated roots. International Journal of Phytoremediat1on 7:49-55. https://doi.org/10.1080/15226514.2013.828017

Downloads

Published

2021-02-15

How to Cite

JEDER, S. ., NOUAIRI, I., MELKI, F., CHEBIL, S. ., LOUATI, F., MHADHBI, H., & ZRIBI, K. (2021). Effect of intercropping alfalfa on physiological and biochemical parameters of young grapevine plants cultivated on agricultural and contaminated soils. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(1), 12017. https://doi.org/10.15835/nbha49112017

Issue

Section

Research Articles
CITATION
DOI: 10.15835/nbha49112017