Skip to main content
Springer Nature Link
Log in

Does Inoculation with Glomus mosseae Improve Salt Tolerance in Pepper Plants?

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

A pot experiment was conducted to determine the effects of Glomus mosseae inoculation on growth and some biochemical activities in roots and shoots of pepper (Capsicum annuum L. cv. Zhongjiao 105) plants subjected to four levels of NaCl [0 (control), 25 (low), 50 (medium), and 100 (high) mM] for 30 days, after 30 days of establishment under non-saline conditions. In mycorrhizal (M) plants, root colonization varied from 48 to 16 %. M plants had higher root and shoot dry weight and leaf area compared with non-mycorrhizal (NM) plants. Under salinity stress, M plants accumulated higher amounts of leaf photosynthetic pigments as well as soluble sugar, soluble protein, and total free amino acids in roots and shoots than those of NM plants. In contrast, the accumulation of proline was less intense in M plants than NM plants. Salt stress induced oxidative stress by increasing malondialdehyde (MDA) content; however, the extent of oxidative damage in M plants was less compared with NM plants due to G. mosseae-enhanced activity of superoxide dismutase (SOD) and peroxidase (POD). We concluded that inoculation with G. mosseae improved growth performance and enhanced salt tolerance of pepper plants via improving photosynthetic pigments and the accumulation of organic solutes (except proline), reducing oxidative stress, and enhancing antioxidant activities of the SOD-POD system.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

References

  • Abbaspour H, Afshari H, Abdel-Wahhab A (2012) Influence of salt stress on growth, pigments, soluble sugars and ion accumulation in three pistachio cultivars. J Medicinal Plants Res 6:2468–2473

    Article  CAS  Google Scholar 

  • Abdel Latef AA (2010) Changes of antioxidative enzymes in salinity tolerance among different wheat cultivars. Cereal Res Comm 38:43–55

    Article  Google Scholar 

  • Abdel Latef AA (2011) Ameliorative effect of calcium chloride on growth, antioxidant enzymes, protein patterns and some metabolic activities of canola (Brassica napus L.) under seawater stress. J Plant Nutr 34:1303–1320

    Article  CAS  Google Scholar 

  • Abdel Latef AA (2013) Growth and some physiological activities of pepper (Capsicum annuum L.) in response to cadmium stress and mycorrhizal symbiosis. J Agr Sci Tech 15:1437–1448

    CAS  Google Scholar 

  • Abdel Latef AA, Chaoxing H (2011a) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hort 127:228–233

    Article  CAS  Google Scholar 

  • Abdel Latef AA, Chaoxing H (2011b) Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. Acta Physiol Plant 33:1217–1225

    Article  CAS  Google Scholar 

  • Ahmad P, Hakeem KR, Kumar A, Ashraf M, Akram NA (2012) Salt-induced changes in photosynthetic activity and oxidative defense system of three cultivars of mustard (Brassica juncea L.). Afr J Biotechnol 11:2694–2703

    CAS  Google Scholar 

  • Arnon DT (1949) Copper enzymes in isolated chloroplast polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Badour SSA (1959) Analytisch–chemische Untersuchung des Kaliummangels bei Chlorella im Vergleich mit anderen Mangelzuständen. Ph.D dissertation Göttingen. [Analytical-chemical investigation of potassium deficiency in Chlorella in comparison with other deficiencies]. Ph.D dissertation, Göttingen University, Göttingen, Germany

  • Bates LS, Wladren PR, Tear DT (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beltrano J, Ruscitti M, Arango MC, Ronco M (2013) Effects of arbuscular mycorrhiza inoculation on plant growth, biological and physiological parameters and mineral nutrition in pepper grown under different salinity and p levels. J Soil Sci Plant Nutr 13:123–141

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bruns S, Hecht-Buchholz C (1990) Light and electron microscope studies on the leaves of several potato cultivars after application of salt at various developmental stages. Potato Res 33:33–41

    Article  Google Scholar 

  • Çekiç FÖ, Ünyayar S, Ortas I (2012) Effects of arbuscular mycorrhizal inoculation on biochemical parameters in Capsicum annuum grown under long term salt Stress. Turk J Bot 36:63–72

    Google Scholar 

  • Chen Z, Zhou M, Newman I, Mendham N, Zhang G, Shabala S (2007) Potassium and sodium relations in salinised barley tissues as a basis of differential salt tolerance. Funct Plant Biol 34:150–162

    Article  CAS  Google Scholar 

  • Demir S (2004) Influence of arbuscular mycorrhiza on some physiological growth parameters of pepper. Turk J Biol 28:85–90

    Google Scholar 

  • El-Amri SM, Al-Whaibi MH, Abdel-Fattah GM, Siddiqui MH (2013) Role of mycorrhizal fungi in tolerance of wheat genotypes to salt stress. Afr J Microbiol Res 7:1286–1295

    CAS  Google Scholar 

  • Evelin H, Kapoor R (2013) Arbuscular mycorrhizal symbiosis modulates antioxidant response in salt-stressed Trigonella foenum-graecum plants. Mycorrhiza. doi:10.1007/s00572-013-0529-4

    Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Annals Bot 104:1263–1280

    Article  CAS  Google Scholar 

  • Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigat ion of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22:203–217

    Article  CAS  PubMed  Google Scholar 

  • Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23:71–86

    Article  CAS  PubMed  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases. I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenreider C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327

    Article  CAS  Google Scholar 

  • Hamdia MA, Shaddad MAK (2010) Salt tolerance of crop plants. a review. J Stress Physiol Biochem 6:64–90

    Google Scholar 

  • Hameed A, Dilfuza E, Abd-Allah EF, Hashem A, Kumar A, Ahmad P (2014) Salinity stress and arbuscular mycorrhizal symbiosis in Plants. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses, vol 1. Springer Science + Business Media, New York, pp 139–159

  • Hammerschmidt R, Nuckles EM, Kuc J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrchum lagenarium. Physiol Plant Pathol 20:73–82

    Article  CAS  Google Scholar 

  • Hassanein RA, Hassanein AA, Haider AS, Hashem HA (2009) Improving salt tolerance of Zea Mays L. plants by presoaking their grains in glycine betaine. Aust J Basic Appl Sci 3:928–942

    CAS  Google Scholar 

  • He Z, He C, Zhang Z, Zou Z, Wang H (2007) Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surf B 59:128–133

    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  PubMed  Google Scholar 

  • Huang JC, Lai WA, Singh S, Hameed A, Young CC (2013) Response of mycorrhizal hybrid tomato cultivars under saline stress. J Soil Sci Plant Nutr 13:469–484

    Google Scholar 

  • Jaleel CA, Riadh K, Gopi R, Manivannan P, Inès J, AI-Juburi HJ, Zhao CX, Shao HB, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol Plant 31:427–436

    Article  Google Scholar 

  • Kang HM, Wang G, Chen K, Bai J (2012) Antioxidative system’s responses in the leaves of six Caragana species during drought stress and recovery. Acta Physiol Plant 34:2145–2154

    Article  CAS  Google Scholar 

  • Kapoor R, Evelin H, Mathur P, Giri B (2013) Arbuscular mycorrhiza: Approaches for abiotic stress tolerance in crop plants for sustainable agriculture. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Springer Science + Business Media, LLC, Dordrecht, pp 359–401. doi:10.1007/978-1-4614-5001-6_14

  • Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna AL, Cullu MA (2009) The influence of arbuscular mycorrhizal colonisation on key growth parameters and fruit yield of pepper plants grown at high salinity. Sci Hort 121:1–6

    Article  CAS  Google Scholar 

  • Kormanik PP, Bryan WC, Schultz RC (1980) Procedure and equipment for staining large number of plant roots for endomycorrhizal assay. Can J Microbiol 26:536–538

    Article  CAS  PubMed  Google Scholar 

  • Koyro HW, Ahmad P, Geissler N (2012) Abiotic stress responses in plants: an overview. In: Ahmad P, Prasad MNV (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer Science + Business Media, New York, pp 1–28

    Chapter  Google Scholar 

  • Kravić N, Marković K, Anđelković V, Hadži-Tašković V, Babić V, Vuletić M (2013) Growth, proline accumulation and peroxidase activity in maize seedlings under osmotic stress. Acta Physiol Plant 35:233–239

    Article  Google Scholar 

  • Lee YP, Takanashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14:71–77

    Article  CAS  Google Scholar 

  • Munns R (1993) Physiological process limiting plant growth in saline soils: some dogmas and hypotheses. Plant Cell Environ 16:15–24

    Article  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Oztekin GB, Tuzel Y, Tuzel IH (2013) Does mycorrhiza improve salinity tolerance in grafted plants? Sci Hort 149:55–60

    Article  CAS  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants. Ecotoxicol Environ Safety 60:324–349

    Article  CAS  PubMed  Google Scholar 

  • Parida AK, Das AB, Mittra B (2003) Effects of NaCl stress on the structure, pigment complex composition and photosynthetic activity of mangrove Bruguiera parviflora chloroplasts. Photosynthetica 41:191–200

    Article  CAS  Google Scholar 

  • Parvaiz A, Satyawati S (2008) Salt stress and phyto-biochemical responses of plants—a review. Plant Soil Environ 54:89–99

    CAS  Google Scholar 

  • Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200

    Article  CAS  Google Scholar 

  • Rasool S, Hameed A, Azooz MM, Muneeb-u-Rehman, Siddiqi TO, Ahmad P (2013) Salt stress: causes, types and responses of plants. In: P Ahmad and others (eds.) Ecophysiology and responses of plants under salt stress. Springer Science + Business Media, LLC, New York, pp 1–24. doi:10.1007/978-1-4614-4747-4_1

  • Ruiz-Lozano JM, Porcel R, Azcόn C, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot. doi:10.1093/jxb/ers126

    Google Scholar 

  • Selvakumar G, Thamizhiniyan P (2011) The effect of the arbuscular mycorrhizal (AM) fungus Glomus intraradices on the growth and yield of Chilli (Capsicum annuum L.) under salinity stress. World Appl Sci J 14:1209–1214

    Google Scholar 

  • Sheng M, Tang M, Zhang F, Huang Y (2011) Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza 21:423–430

    Article  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, San Diego

    Google Scholar 

  • Talaat NB, Shawky BT (2011) Influence of arbuscular mycorrhizae on yield, nutrients, organic solutes, and antioxidant enzymes of two wheat cultivars under salt stress. J Plant Nutr Soil Sci 174:283–291

    Article  CAS  Google Scholar 

  • Tian CY, Feng G, Li XL, Zhang FS (2004) Different effects of arbuscular mycorrhizal fungal isolates from saline or nonsaline soil on salinity tolerance of plants. Appl Soil Ecol 26:143–148

    Article  Google Scholar 

  • Turkmen O, Sensoy S, Demir S, Erdinc C (2008) Effects of two different AMF species on growth and nutrient content of pepper seedlings grown under moderate salt stress. Afr J Biotechnol 7:392–396

    CAS  Google Scholar 

  • Wang WX, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Tang M, Sulpice R, Chen H, Tian S, Ban Y (2014) Arbuscular mycorrhizal fungi alter fractal dimension characteristics of Robinia pseudoacacia L. seedlings through regulating plant growth, leaf water status, photosynthesis, and nutrient concentration under drought stress. J Plant Growth. doi:10.1007/s00344-013-9410-0

    Google Scholar 

  • Zarei M, Paymaneh Z (2013) Effect of salinity and arbuscular mycorrhizal fungi on growth and some physiological parameters of Citrus jambheri. Arch Agron Soil Sci. doi:10.1080/03650340.2013.853289

    Google Scholar 

  • Zhang ZL, Qu W (2004) Experimental guidance of plant physiology. High Education, Beijing

    Google Scholar 

  • Zhang ZA, Zhang MS (2006) Experimental guide for plant physiology. High education, Beijing

    Google Scholar 

  • Zhani K, Elouer MA, Aloui H, Hannachi C (2012) Selection of a salt tolerant Tunisian cultivar of chili pepper (Capsicum frutescens). Eurasia J Biosci 6:47–59

    Article  Google Scholar 

  • Zhifang G, Loescher WH (2003) Expression of a celery mannose 6-phosphate reductase in Arabidopsis thaliana enhances salt tolerance and induces biosynthesis of both mannitol and glucosyl-mannitol dimmer. Plant Cell Environ 26:275–283

    Article  CAS  Google Scholar 

  • ZhongQun H, HaoRu T, HuanXiu L, ChaoXing H, ZhiBin Z, HuaiSong W (2010) Arbuscular mycorrhizal alleviated ion toxicity, oxidative damage and enhanced osmotic adjustment in tomato subjected to NaCl stress. American-Eurasian J Agric Environ Sci 7:676–683

    Google Scholar 

  • Zou YN, Liang YC, Wu QS (2013) Mycorrhizal and non-mycorrhizal responses to salt stress in trifoliate orange: plant growth, root architecture and soluble sugar accumulation. Int J Agric Biol 15:565–569

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Egyptian Ministry of Higher Education and Scientific Research (ParOwn 1207) grant and the Chinese National Science and Technology (Project 2011BAD12B03). The authors would like to thank Dr. Ahmad Hassan for revision of English.

Author information

Authors and Affiliations

  1. Department of Botany, Faculty of Science, South Valley University, Qena, 83523, Egypt

    Arafat Abdel Hamed Abdel Latef

  2. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Science, Beijing, 100081, People’s Republic of China

    He Chaoxing

Authors
  1. Arafat Abdel Hamed Abdel Latef
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. He Chaoxing
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Arafat Abdel Hamed Abdel Latef.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abdel Latef, A.A.H., Chaoxing, H. Does Inoculation with Glomus mosseae Improve Salt Tolerance in Pepper Plants?. J Plant Growth Regul 33, 644–653 (2014). https://doi.org/10.1007/s00344-014-9414-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-014-9414-4

Keywords