Arbuscular mycorrhiza affects nickel translocation and expression of ABC transporter and metallothionein genes in Festuca arundinaceaby Leila Shabani, Mohammad R. Sabzalian, Sodabeh Mostafavi pour



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Arbuscular mycorrhiza affects nickel translocation and expression of ABC transporter and metallothionein genes in Festuca arundinacea

Leila Shabani1 & Mohammad R. Sabzalian2 &

Sodabeh Mostafavi pour1

Received: 11 March 2015 /Accepted: 26 May 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Mycorrhizal fungi are key microorganisms for enhancing phytoremediation of soils contaminated with heavy metals. In this study, the effects of the arbuscular mycorrhizal fungus (AMF) Funneliformis mosseae (=Glomus mosseae) on physiological and molecular mechanisms involved in the nickel (Ni) tolerance of tall fescue (Festuca arundinacea=

Schedonorus arundinaceus) were investigated. Nickel addition had a pronounced negative effect on tall fescue growth and photosynthetic pigment contents, as well as on AMF colonization. Phosphorus content increased markedly in mycorrhizal plants (M) compared to non-inoculated (NM) ones.

However, no significant difference was observed in root carbohydrate content between AMF-inoculated and noninoculated plants. For both M and NM plants, Ni concentrations in shoots and roots increased according to the addition of the metal into soil, but inoculation with F. mosseae led to significantly lower Ni translocation from roots to the aboveground parts compared to non-inoculated plants. ABC transporter and metallothionein transcripts accumulated to considerably higher levels in tall fescue plants colonized by

F. mosseae than in the corresponding non-mycorrhizal plants.

These results highlight the importance of mycorrhizal colonization in alleviating Ni-induced stress by reducing Ni transport from roots to shoots of tall fescue plants.

Keywords ABC transporters . Metallothionein .

Mycorrhiza .Nickel . Tall fescue .Schedonorus arundinaceus


It is well known that transport, chelation, and sequestration processes in living organisms function in regulating concentrations of essential metal ions in different cellular compartments andminimizing the damage caused by heavymetal ions entering the cytosol (O’Halloran and Culotta 2000; Clemens 2001). Important components of heavy metal homeostasis and detoxification systems are membrane-localized heavy metal transporters (Williams et al. 2000) and chelation processes (Cobbett 2000). Membrane transport systems are likely to play a central role in the regulation of metal concentrations within different cells and organelles. The ATP binding cassette (ABC) protein superfamily is the largest membrane protein family, well known in plants. Members of this superfamily catalyze the Mg ATP-energized transport of a broad range of substrates across biological membranes. ABC transporters mediate diverse cellular transport processes such as excretion of potentially toxic compounds and conferring of heavy metal tolerance (Martinoia et al. 2002). Once metal ions enter the cell, they are bound by chelators. Metallothioneins (MTs) are the best characterized heavy metal-binding ligands in plant cells. They belong to the superfamily of thiol-containing metal-binding proteins which modulate internal levels of metal concentrations between deficient and toxic concentrations by binding to the toxic metals through closely spaced cysteinthiol groups (Cobbett 2000).

Arbuscular mycorrhizal fungi (AMF) are an important component of the rhizosphere and have beenwell documented to enhance phytoremediation of heavy metal-contaminated * Leila Shabani; 1 Department of Biology, Faculty of Sciences, Shahrekord University,

Shahrekord, Iran 2 Department of Agronomy and Plant Breeding, College of

Agriculture, Isfahan University of Technology, Isfahan 84156-83111,



DOI 10.1007/s00572-015-0647-2 soils (Gonzalez-Chavez 2000; Davies et al. 2001).

Environmental stress conditions, such as accumulation of heavy metals, typically impose severe difficulties for plant survival and growth. The AMF symbiosis can alleviate abiotic stresses through improvement of plant growth as a result of enhanced nutrient and water uptake (Davies et al. 2002;

Carpio et al. 2005) and by stimulating or modifying specific physiological mechanisms related to the adaptation to stressful environments (Porcel et al. 2003; Auge et al. 2004).

AMF can influence certain plant physiological mechanisms, such as metal avoidance or tolerance to increase plant phytoremediation capability (Perotto and Martino 2001).

There is evidence showing that plant-encoded metal transporters and chelators are expressed in mycorrhizal plants when grown under conditions of heavy metal contamination (Rivera-Becerril et al. 2005; Gohre and Paszkowski 2006;

Hildebrandt et al. 2007). On the other hand, it has been shown that nickel (Ni) can form chelated compounds, which may replace other heavy metals from physiologically important centers in plant metabolism (Cammack et al. 1988; Kramer et al. 1996). The aim of the present study was to investigate the physiological and molecular mechanisms involved in Ni tolerance of mycorrhizal tall fescue plants inoculated with

Funneliformis mosseae. Ni translocation and the expression levels of MT and ABC genes in response to four concentrations of Ni were investigated.

Material and methods

Seeds of Festuca arundinacea (recently renamed

Schedonorus arundinaceus) were harvested from plants originally collected from Kordestan Province (Iran) and maintained in the research field of Isfahan University of

Technology (Isfahan, Iran). Fescue seeds were pregerminated on moist filter paper for about 1 week until the radicles appeared. Potting soil was taken from the bed of

Zayandeh-rood River near Chelvan (45 km to Shahrekord,

Chahar Mahal-Bakhtiari Province). The soil had a loam-sand texture and the following general chemical properties: pH 8.08, ECe 0.37 dS m−1, CEC 9.7 cmol(+)kg−1, total N 0.071 %, organic C 0.28 %, and available P, K, and Ni 5.2, 162, and 13 mg kg−1, respectively. Before the experiment, the soil was air-dried, sieved through a 2-mm sieve, and then sterilized by autoclaving for 2 h at 121 °C. Nickel (as NiCl2) was added to the soil at concentrations of 0, 30, 90, and 180 mg kg−1 (Ni 0, Ni 30, Ni 90, and Ni 180).