Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants

Josef Kohler A , José Antonio Hernández B , Fuensanta Caravaca A C and Antonio Roldán A

A Department of Soil and Water Conservation, CSIC-Centro de Edafología y Biología Aplicada del Segura, PO Box 164, Campus de Espinardo, Murcia 30100, Spain.

B Department of Plant Breeding, CSIC-Centro de Edafología y Biología Aplicada del Segura, PO Box 164, Campus de Espinardo, Murcia 30100, Spain.

C Corresponding author. Email: fcb@cebas.csic.es

Functional Plant Biology 35(2) 141-151 https://doi.org/10.1071/FP07218
Submitted: 7 September 2007  Accepted: 14 January 2008   Published: 19 March 2008

Abstract

This study examined the effect of inoculation with the plant-growth-promoting rhizobacterium (PGPR) Pseudomonas mendocina Palleroni, alone or in combination with an arbuscular mycorrhizal (AM) fungus, Glomus intraradices (Schenk & Smith) or Glomus mosseae (Nicol & Gerd.) Gerd. & Trappe, on antioxidant enzyme activities (superoxide dismutase, catalase and total peroxidase activities), phosphatase and nitrate reductase activities and solute accumulation in leaves of Lactuca sativa L. cv. Tafalla affected by three different levels of water stress. At moderate drought, bacterial inoculation and mycorrhizal inoculation with G. intraradices, alone or in combination, stimulated significantly nitrate reductase activity. At severe drought, fertilisation and P. mendocina inoculation, alone or in combination with either of the selected AM fungi, increased significantly phosphatase activity in lettuce roots and proline accumulation in leaves. Total peroxidase (POX) and catalase (CAT) activities increased in response to drought, whereas superoxide dismutase activity decreased. Inorganic fertilisation and both combined treatments of PGPR and AM fungus showed the highest values of leaf POX activity under severe drought. The highest CAT activity was recorded in the fertilised plants followed by the P. mendocina-inoculated plants grown under severe stress conditions. These results support the potential use of a PGPR as an inoculant to alleviate the oxidative damage produced under water stress.

Additional keywords: antioxidant enzymes, proline, Pseudomonas mendocina, water stress.


References


Alguacil MM, Hernández JA, Caravaca F, Portillo B, Roldán A (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforestated in a degraded semi-arid soil. Physiologia Plantarum 118, 562–570.
CrossRef | open url image1

Anderson JV, Hess JL, Chevone BI (1990) Purification, characterization and immunological properties for two isoforms of glutathione reductase from eastern white pine needles. Plant Physiology 94, 1402–1409.
PubMed |
open url image1

Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 3–42.
CrossRef | open url image1

Azcón R, Barea JM (1997) Mycorrhizal dependency of a representative plant species in mediterranean shrublands (Lavandula spica L.) as a key factor to its use for revegetation strategies in desertification-threatened areas. Applied Soil Ecology 7, 83–92.
CrossRef | open url image1

Azcón R, Ruiz-Lozano JM, Rodríguez R (2001) Differential contribution of arbuscular mycorrhizal fungi to plant nitrate uptake (15N) under increasing N supply to the soil. Canadian Journal of Botany 79, 1175–1180.
CrossRef | open url image1

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant and Soil 39, 205–207.
CrossRef | open url image1

Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.
PubMed |
open url image1

Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. The Plant Cell 7, 1099–1111.
CrossRef | PubMed | open url image1

Bremner JM , Mulvarey CS (1982) Nitrogen total. In ‘Methods of Soil Analysis. Chemical and Microbiological Properties’. (Eds AL Page, RH Miller, DR Keeny) pp. 595–622. (American Society of Agronomy: Madison)

Caravaca F, Alguacil MM, Figueroa D, Barea JM, Roldán A (2003) Re-establishment of Retama sphaerocarpa as a target species for reclamation of soil physical and biological properties in a semiarid Mediterranean land. Forest Ecology and Management 182, 49–58.
CrossRef | open url image1

Caravaca F, Alguacil MM, Hernández JA, Roldán A (2005) Involvement of antioxidant enzyme and nitrate reductase activities during water stress and recovery of mycorrhizal Myrtus communis and Phillyrea angustifolia plants. Plant Science 169, 191–197.
CrossRef | open url image1

Carpena CA, Lax A, Vahtras K (1972) Determination of exchangeable cations in calcareous soils. Soil Science 113, 194–199.
CrossRef | open url image1

del Río LA, Sevilla F, Sandalio LM, Palma JM (1991) Nutritional effect and expression of SODs: induction and gene expression; diagnostics; prospective protection against oxygen toxicity. Free Radical Research Communications 12–13, 819–827. open url image1

Douds DD, Johnson CR, Koch KE (1988) Carbon cost of the fungal symbiont relative to net leaf P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiology 86, 491–496.
PubMed |
open url image1

Downs MR, Nadelhoffer KJ, Melillo JM, Aber JD (1993) Foliar and fine root nitrate reductase activity in seedlings of four forest tree species in relation to nitrogen availability. Trees (Berlin) 7, 233–236. open url image1

Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 84, 489–499.
CrossRef | open url image1

Goicoechea N, Antolín MC, Strnad M, Sánchez-Díaz M (1996) Root cytokinins, acid phosphatase and nodule activity in drought stressed mycorrhizal or nitrogen fixing alfalfa plants. Journal of Experimental Botany 47, 683–686.
CrossRef | open url image1

Goicoechea N, Merino S, Sánchez-Díaz M (2005) Arbuscular mycorrhizal fungi can contribute to maintain antioxidant and carbon metabolism in nodules of Anthyllis cytisoides L. subjected to drought. Journal of Plant Physiology 162, 27–35.
CrossRef | PubMed | open url image1

Ho I, Trappe JM (1980) Nitrate reductase activity of nonmycorrhizal Douglas-fir rootlets and of some associated mycorrhizal fungi. Plant and Soil 54, 395–398.
CrossRef | open url image1

Irigoyen JJ, Emerich DW, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiologia Plantarum 84, 67–72.
CrossRef | open url image1

Iturbe-Ormaetxe I, Escuredo PR, Arrese-Igor C, Becana M (1998) Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiology 116, 173–181.
CrossRef | open url image1

Khalil S, Loynachan TE, Tabatabai MA (1994) Mycorrhizal dependency and nutrient uptake by improved and unimproved corn and soybean cultivars. Agronomy Journal 86, 949–958. open url image1

Kohler J, Caravaca F, Carrasco L, Roldán A (2006) Contribution of Pseudomonas mendocina and Glomus intraradices to aggregates stabilisation and promotion of biological properties in rhizosphere soil of lettuce plants under field conditions. Soil Use and Management 22, 298–304.
CrossRef | open url image1

Kramer PJ , Boyer JS (1997) ‘Water relations of plants and soils.’ (Academic Press: San Diego)

Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Science 166, 525–530.
CrossRef | open url image1

McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymatic function for erythrocuprein (hemocuprein). Journal of Biological Chemistry 244, 6049–6055.
PubMed |
open url image1

Mhadhbi H, Jebara M, Limam F, Aouani ME (2004) Rhizobial strain involvement in plant growth, nodule protein composition and antioxidant enzyme activities of chickpea–rhizobia symbioses: modulation by salt stress. Plant Physiology and Biochemistry 42, 717–722.
CrossRef | PubMed | open url image1

Mittler R, Zilinskas BA (1994) Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. The Plant Journal 5, 397–405.
CrossRef | PubMed | open url image1

Munjal N, Sawhney SK, Sawhney V (1997) Activation of nitrate reductase in extracts of water stressed wheat. Phytochemistry 45, 659–665.
CrossRef | open url image1

Munns R, Termaat A (1986) Whole-plant responses to salinity. Australian Journal of Plant Physiology 13, 143–160. open url image1

Murphy J, Riley JP (1962) A modified single solution method for determination of phosphate in natural waters. Analitica Chimica Acta 27, 31–36.
CrossRef | open url image1

Noctor G, Veljovic-Jovanovic S, Foyer CH (2000) Peroxide processing in photosynthesis: antioxidant coupling and redox signalling. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1465–1475.
CrossRef | PubMed | open url image1

Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161. open url image1

Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. Journal of Experimental Botany 55, 1743–1750.
CrossRef | PubMed | open url image1

Price AH, Atherton NM, Hendry GAF (1989) Plants drought-stress generate activated oxygen. Free Radical Research Communications 8, 61–66.
CrossRef | PubMed | open url image1

Querejeta JI, Barea JM, Allen MF, Caravaca F, Roldán A (2003) Differential response of δ13C and water use efficiency to arbuscular mycorrhizal infection in two aridland woody plant species. Oecologia 135, 510–515.
PubMed |
open url image1

Querejeta JI, Allen MF, Caravaca F, Roldán A (2006) Differential modulation of host plant δ13C and δ18O by native and exotic arbuscular mycorrhizal fungi in a semiarid environment. The New Phytologist 169, 379–387.
CrossRef | PubMed | open url image1

Querejeta JI, Allen MF, Alguacil MM, Roldán A (2007) Plant isotopic composition provides insight into mechanisms underlying growth stimulation by AM fungi in a semiarid environment. Functional Plant Biology 34, 683–691.
CrossRef | open url image1

Quiroga M, Guerrero C, Botella MA, Barceló AR, Medina MI, Alonso FJ (2000) A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiology 122, 1119–1127.
CrossRef | PubMed | open url image1

Richards LA (1941) A pressure-membrane extraction apparatus for soil solution. Soil Science 51, 377–386.
CrossRef | open url image1

Ros-Barceló A (1998) The generation of H2O2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207, 207–216.
CrossRef | open url image1

Ros-Barceló A, Gómez-Ros LV, Ferrer MA, Hernández JA (2006) The apoplastic antioxidant enzymatic system in the wood-forming tissues of trees. Trees – Structure and Function 20, 145–156. open url image1

Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress: new perspectives for molecular studies. Mycorrhiza 13, 309–317.
CrossRef | PubMed | open url image1

Ruiz-Lozano JM, Azcón R (1996) Mycorrhizal colonization and drought stress as factors affecting nitrate reductase activity in lettuce plants. Agriculture Ecosystems & Environment 60, 175–181.
CrossRef | open url image1

Ruiz-Lozano JM, Azcón R, Gómez M (1995) Effects of arbuscular-mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Applied and Environmental Microbiology 61, 456–460.
PubMed |
open url image1

Ruiz-Lozano JM, Collados C, Barea JM, Azcón R (2001) Cloning of cDNAs encoding SODs from lettuce plants which show differential regulation by arbuscular mycorrhizal fungi and by drought stress. Journal of Experimental Botany 52, 2241–2242.
PubMed |
open url image1

Saikia R, Kumar R, Arora DK, Gogoi DK, Azad P (2006) Pseudomonas aeruginosa inducing rice resistance against Rhizoctonia solani: production of salicylic acid and peroxidases. Folia Microbiologica 51, 375–380.
PubMed |
open url image1

Scandalios JG , Guan L , Polidords AN (1997) Catalases in plants: gene structure, properties, and expression. In ‘Oxidative stress and the molecular biology of antioxidant defences’. (Ed. JG Scandalios) pp. 343–406. (Cold Spring Harbor Laboratory Press: New York)

Schellenbaum L, Müller J, Boller T, Wienken A, Schüepp H (1998) Effects of drought on non-mycorrhizal and mycorrhizal maize: changes in the pools of non-structural carbohydrates, in the activities of invertase and trehalose, and in the pools of amino acids and imino acids. The New Phytologist 138, 59–66.
CrossRef | open url image1

Sieverding E (1991) ‘Vesicular-arbuscular mycorrhiza management in tropical agrosystems.’ (GTZ: Eschborn, Germany)

Sofo A, Dichio B, Xiloyannis C, Masia A (2005) Antioxidant defences in olive trees during drought stress: changes in activity of some antioxidant enzymes. Functional Plant Biology 32, 45–53.
CrossRef | open url image1

Subramanian KS, Charest C (1999) Acquisition of N by external hyphae of an arbuscular mycorrhizal fungus and its impact on physiological responses in maize under drought-stressed and well-watered conditions. Mycorrhiza 9, 69–75. open url image1

Tabatabai MA, Bremner JM (1969) Use of p-nitrophenol phosphate in assay of soil phosphatase activity. Soil Biology & Biochemistry 1, 301–307.
CrossRef | open url image1

Turkan I, Bor M, Ozdemir F, Koca H (2005) Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius Gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress. Plant Science 168, 223–231.
CrossRef | open url image1

Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant and Soil 255, 571–586.
CrossRef | open url image1

Yeomans JC, Bremner JM (1989) A rapid and precise method for routine determination of organic carbon in soil. Communications in Soil Science and Plant Analysis 19, 1467–1476. open url image1








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