Abstract
Iron chlorosis in the calcareous soils is one most important stress factors worldwide that limits photosynthesis and decreases fruit yield and quality. Certain soil rhizobacteria produce organic compounds such as plant acids and they may reduce the soil rhizosphere pH and affect ferric chelate reductase (FC-R) activity in root. However, there is no knowledge regarding changes in organic acids content and FC-R activities of leaf due to rhizobacterial root inoculation. Therefore, the efficiency of six plant growth promoting rhizobacteria (PGPR) were tested on apple cv. Braeburn on M9 and MM106 rootstocks. The results of the experiment showed leaf organic acid contents, iron quantity of soil, root and leaf and root and leaf FC-R activity were significantly affected via rhizobacteria applications in apple plants. In MM106 and M9, there was a remarkable increase in Fe in M3 inoculated soil by 95 and 89%, respectively, compared to control. Average increases in citric, malic, malonic, butyric and lactic acid in the leaf were obtained from rhizobacterial root inoculations of 25.1, 21.8, 29.6, 18.0 and 18.2% in Braeburn/MM106, respectively. In Braeburn/M9, MFDCa1 application increased all organic acid concentrations compared to the control. MFDCa2 treatment caused the maximum leaf FC-R activity in Braeburn on M9 and MM106 (60.9 and 50.3 nmol Fe+2 g−1 FW h−1, respectively) while the least values were determined in the control (33.5 and 29.9 nmol Fe+2 g−1 FW h−1, respectively). This study showed the bacterial strains tested in our study may be used as a biofertilizer instead of Fe fertilizers.
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References
Bienfait H, Bino R, Bliek AV, Duivenvoorden J, Fontaine J (1983) Characterization of ferric reducing activity in roots of Fe-deficient Phaseolus vulgaris. Physiol Plant 59:196–202
Del Campillo M, Torrent J (1992) A rapid acid-oxalate extraction procedure for the determination of active Fe-oxide forms in calcareous soils. Z Pflanzenernahr Bodenk 155:437–437
Fernandez-Lopez J, Lopez-Roca J, Almela L (1993) Mineral composition of iron chlorotic Citrus limon L leaves. J Plant Nutr 16:1395–1407
Garcia-Lopez AM, Delgado A (2016) Effect of Bacillus subtilis on phosphorus uptake by cucumber as affected by iron oxides and the solubility of the phosphorus source. Agric Food Sci 25:216–224
Gerke J (1992) Phosphate, aluminium and iron in the soil solution of three different soils in relation to varying concentrations of citric acid. Zeits Pflan Boden 155:339–343
Glick B (1995) The enhancement of plant growth by free-living bacteria Canadian. J Microbiol 41:109–117
González-Vallejo EB, Morales F, Cistué L, Abadıa A, Abadıa J (2000) Iron deficiency decreases the Fe (III)- chelate reducing activity of leaf protoplasts. Plant Physiol 122:337–344
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Cal Agric Exp Sta 347
Ipek M, Pirlak L, Esitken A, Figen Dönmez M, Turan M, Sahin F (2014) Plant Growth-Promoting Rhizobacteria (PGPR) increase yield, growth and nutrition of strawberry under high-calcareous soil conditions. J Plant Nutr 37:990–1001
İpek M, Aras S, Arıkan Ş, Eşitken A, Pırlak L, Dönmez MF, Turan M (2017) Root plant growth promoting rhizobacteria inoculations increase ferric chelate reductase (FC-R) activity and Fe nutrition in pear under calcareous soil conditions. Sci Hortic 219:144–151
Jones D, Darah P, Kochian L (1996) Critical evaluation of organic acid mediated iron dissolution in the rhizosphere and its potential role in root iron uptake. Plant Soil 180:57–66
Karakurt H, Aslantas R (2010) Effects of some plant growth promoting rhizobacteria [PGPR] strains on plant growth and leaf nutrient content of apple. J Fruit Ornam Plant Res 1:101–110
Karlidag H, Esitken A, Turan M, Sahin F (2007) Effects of root inoculation of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient element contents of leaves of apple. Sci Hortic 114:16–20
Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152
Kosegarten HU, Hoffmann B, Mengel K (1999) Apoplastic pH and Fe3+ reduction in intact sunflower leaves. Plant Physiol 121:1069–1079
Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428
Marschner H (2011) Marschner’s mineral nutrition of higher plants. Academic press, CA, USA
Mengel K (1994) Iron availability in plant tissues-iron chlorosis on calcareous soils. Plant soil 165:275–283
Mengel K, Geurtzen G (1988) Relationship between iron chlorosis and alkalinity in Zea mays. Physiol Plant 72:460–465
Mengel K, Kirkby EA (2001) Principles of plant nutrition Springer Kluwer Academic Publishers, Dordrecht, Netherlands . https://doi.org/10.1007/978-94-010-1009-2
Mertens D (2005a) AOAC official method 922.02 plants preparation of laboratory sample official methods of analysis, 18th edn Horwitz W, Latimer GW (eds)., pp 1–2
Mertens D (2005b) AOAC official method 975.03 metal in plants and pet foods official methods of analysis, 18th edn Horwitz W, Latimer GW (eds)., pp 3–4
Miller G, Pushnik J, Welkie G, as FeCl I, Sites R (1984) Iron chlorosis, a world wide problem, relation of chlorophyll biosynthesis to iron. J Plant Nutr 7:1–22
Nikolic M, Römheld V (1999) Mechanism of Fe uptake by the leaf symplast: Is Fe inactivation in leaf a cause of Fe deficiency chlorosis? Plant Soil 215:229–237
Orhan E, Esitken A, Ercisli S, Turan M, Sahin F (2006) Effects of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient contents in organically growing raspberry. Sci Hortic 111:38–43
Pii Y, Penn A, Terzano R, Crecchio C, Mimmo T, Cesco S (2015) Plant-microorganism-soil interactions influence the Fe availability in the rhizosphere of cucumber plants Plant. Physiol Biochem 87:45–52
Pii Y, Marastoni L, Springeth C, Fontanella MC, Beone GM, Cesco S, Mimmo T (2016) Modulation of Fe acquisition process by Azospirillum brasilense in cucumber plants. Environ Exper Bot 130:216–225
Plänker R (1991) Die bedeutung des apoplasten-pH-wertes fuer die eisenchlorose. Untersuchungen an Helianthus annuus L, Ph.D. Thesis, Fac. Biol. Justus Leibing Univ., Giessen
Sandhya V, Ali SZ, Grover M, Reddy G, Venkateswarlu B (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul 62:21–30
Scagliola M, Pii Y, Mimmo T, Cesco S, Ricciuti P, Crecchio C (2016) Characterization of plant growth promoting traits of bacterial isolates from the rhizosphere of barley (Hordeum vulgare L.) and tomato (Solanum lycopersicon L.) grown under Fe sufficiency and deficiency Plant. Physiol Biochem 107:187–196
Sharma A, Johri B, Sharma A, Glick B (2003) Plant growth-promoting bacterium Pseudomonas sp. strain GRP 3 influences iron acquisition in mung bean (Vigna radiata L. Wilzeck. Soil Biol Biochem 35:887–894
Tagliavini M, Scudellari D, Marangoni B, Toselli M (1995) Acid-spray regreening of kiwifruit leaves affected by lime-induced iron chlorosis. Iron nutrition in soils and plants. Springer, Heidelberg, pp 191–195
Takkar P, Kaur N (1984) HCl method for Fe2+ estimation to resolve iron chlorosis in plants. J Plant Nutr 7:81–90
Toselli M, Marangoni B, Tagliavini M (2000) Iron content in vegetative and reproductive organs of nectarine trees in calcareous soils during the development of chlorosis European. J Agron 13:279–286
Wallace A, Abou-Zamzam A (1986) Uptake of labeled 14C bicarbonate by some monocot and dicot plants from nutrient solution. J Plant Nutr 9:887–892
Waters BM, Blevins DG, Eide DJ (2002) Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition. Plant Physiol 129:85–94
Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–577
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This study was supported by TUBITAK (TOVAG 111O704), The Scientific and Technological Research Council of Turkey.
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Communicated by M. J. Reigosa.
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Aras, S., Arıkan, Ş., İpek, M. et al. Plant growth promoting rhizobacteria enhanced leaf organic acids, FC-R activity and Fe nutrition of apple under lime soil conditions. Acta Physiol Plant 40, 120 (2018). https://doi.org/10.1007/s11738-018-2693-9
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DOI: https://doi.org/10.1007/s11738-018-2693-9