Effect of controlled inoculation with specific mycorrhizal fungi from the urban environment on growth and physiology of containerized shade tree species growing under different water regimes

The aim of this work was to evaluate the effects of selected mycorrhiza obtained in the urban environment on growth, leaf gas exchange, and drought tolerance of containerized plants growing in the nursery. Two-year-old uniform Acer campestre L., Tilia cordata Mill., and Quercus robur L. were inoculated with a mixture of infected roots and mycelium of selected arbuscular (maple, linden) and/or ectomycorrhiza (linden, oak) fungi and grown in well-watered or water shortage conditions. Plant biomass and leaf area were measured 1 and 2 years after inoculation. Leaf gas exchange, chlorophyll fluorescence, and water relations were measured during the first and second growing seasons after inoculation. Our data suggest that the mycelium-based inoculum used in this experiment was able to colonize the roots of the tree species growing in the nursery. Plant biomass was affected by water shortage, but not by inoculation. Leaf area was affected by water regime and, in oak and linden, by inoculation. Leaf gas exchange was affected by inoculation and water stress. Vcmax and Jmax were increased by inoculation and decreased by water shortage in all species. Fv/Fm was also generally higher in inoculated plants than in control. Changes in PSII photochemistry and photosynthesis may be related to the capacity of inoculated plants to maintain less negative leaf water potential under drought conditions. The overall data suggest that inoculated plants were better able to maintain physiological activity during water stress in comparison to non-inoculated plants.

[1]  A. Quoreshi The Use of Mycorrhizal Biotechnology in Restoration of Disturbed Ecosystem , 2008 .

[2]  B. Tisserant,et al.  In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections , 1993 .

[3]  R. Agerer Colour Atlas of Ectomycorrhizae , 1997 .

[4]  R. Strasser,et al.  Mycorrhizal impact on drought stress tolerance of rose plants probed by chlorophyll a fluorescence, proline content and visual scoring , 2005, Mycorrhiza.

[5]  J. Flexas,et al.  Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. , 2002, Annals of botany.

[6]  B. Söderström,et al.  Effects of liming on ectomycorrhizal fungi infecting Pinus sylvestris L. , 1990 .

[7]  C. Cruz,et al.  Functional aspects of root architecture and mycorrhizal inoculation with respect to nutrient uptake capacity , 2004, Mycorrhiza.

[8]  F. Ferrini,et al.  Withholding Irrigation During the Establishment Phase Affected Growth and Physiology of Norway Maple (Acer platanoides) and Linden (Tilia spp.) , 2009 .

[9]  A. Newton,et al.  Mineral nutrition and mycorrhizal infection of seedling oak and birch II. The effect of fertilizers on growth, nutrient uptake and ectomycorrhizal infection , 1991 .

[10]  M. Gryndler,et al.  The rhizosphere of mycorrhizal plants , 2002 .

[11]  A. Torrecillas,et al.  Water stress preconditioning to improve drought resistance in young apricot plants. , 2000, Plant science : an international journal of experimental plant biology.

[12]  Robert W. Pearcy,et al.  Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia , 1997 .

[13]  K. Futai,et al.  Mycorrhizae : sustainable agriculture and forestry , 2008 .

[14]  J. Barea,et al.  Mycorrhizal Technology in Agriculture , 2002, Birkhäuser Basel.

[15]  G. Fairchild,et al.  A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. , 1990, The New phytologist.

[16]  A. Saxton,et al.  Mycorrhizal influence on hydraulic and hormonal factors implicated in the control of stomatal conductance during drought , 1996 .

[17]  C. Davey,et al.  Comparative effectivity of three Fraxinus pennsylvanica Marsh, vesicular‐arbuscular mycorrhizal fungi in a high‐phosphorus nursery soil , 1988 .

[18]  D. Whitehead,et al.  Photosynthetic characteristics in canopies of Quercus rubra, Quercus prinus and Acer rubrum differ in response to soil water availability , 2002, Oecologia.

[19]  W. C. Fonteno,et al.  Transplant Growth Control through Water Deficit Stress-A Review , 1998 .

[20]  J. Alarcón,et al.  Hardening of oleander seedlings by deficit irrigation and low air humidity , 2006 .

[21]  J. Zwiazek,et al.  Ectomycorrhizas and water relations of trees: a review , 2011, Mycorrhiza.

[22]  J. Churin,et al.  Effect of Ectomycorrhizal Inoculation at Planting on Growth and Foliage Quality of Tilia Tomentosa , 1996, Arboriculture & Urban Forestry.

[23]  A. Dvořáčková,et al.  Development and activity of Glomus intraradices as affected by co-existence with Glomus claroideum in one root system , 2009, Mycorrhiza.

[24]  J. Pera,et al.  Evaluation of mycelial inocula of edible Lactarius species for the production of Pinus pinaster and P. sylvestris mycorrhizal seedlings under greenhouse conditions , 2004, Mycorrhiza.

[25]  P. C. Flanagan,et al.  Arbuscular mycorrhizal assessment of ornamental trees grown in Tennessee field soils , 2002 .

[26]  Ü. Niinemets,et al.  Drought acclimation of two deciduous tree species of different layers in a temperate forest canopy , 2003, Trees.

[27]  R. K. Dixon,et al.  Water deficits and root growth of ectomycorrhizal white oak seedlings. , 1980 .

[28]  E. Gilman Effect of Nursery Production Method, Irrigation, and Inoculation with Mycorrhizae-Forming Fungi on Establishment of Quercus Virginiana , 2001, Arboriculture & Urban Forestry.

[29]  D. Sylvia,et al.  Compatible host/mycorrhizal fungus combinations for micropropagated sea oats , 2003, Mycorrhiza.

[30]  M. Rai Handbook of Microbial Biofertilizers , 2005 .

[31]  J. Syvertsen,et al.  Moderate shade can increase net gas exchange and reduce photoinhibition in citrus leaves. , 2003, Tree physiology.

[32]  R. Augé Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis , 2001, Mycorrhiza.

[33]  S. Timonen,et al.  Mycorrhizal colonisation patterns of Tilia trees in street, nursery and forest habitats in southern Finland , 2008 .

[34]  L. Watrud,et al.  Influence of adverse soil conditions on the formation and function of Arbuscular mycorrhizas , 2002 .

[35]  D. Read,et al.  Mycorrhizas in ecosystems , 1991, Experientia.

[36]  J. Pereira,et al.  Responses to water stress in two Eucalyptus globulus clones differing in drought tolerance. , 2004, Tree physiology.

[37]  N. C. Schenck,et al.  Manual for the identification of va mycorrhizal fungi , 1990 .

[38]  D. Lemoine,et al.  Comparative studies of the water relations and the hydraulic characteristics in Fraxinus excelsior, Acer pseudoplatanus and A. opalus trees under soil water contrasted conditions , 2001 .

[39]  D. Bryla,et al.  Effects of mycorrhizal infection on drought tolerance and recovery in safflower and wheat , 1997, Plant and Soil.

[40]  S. Smith INFLOW OF PHOSPHATE INTO MYCORRHIZAL AND NON-MYCORRHIZAL PLANTS OF TRIFOLIUM SUBTERRANEUM AT DIFFERENT LEVELS OF SOIL PHOSPHATE , 1982 .

[41]  Mohammad Yunus,et al.  Probing photosynthesis : mechanisms, regulation, and adaptation , 2000 .

[42]  Mark C. Brundrett,et al.  Coevolution of roots and mycorrhizas of land plants. , 2002, The New phytologist.

[43]  R. Augé,et al.  Arbuscular mycorrhizal symbiosis and nonhydraulic signaling of soil drying in Vigna unguiculata (L.) Walp. , 1996, Mycorrhiza.

[44]  R. Strasser,et al.  A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient , 2007, Photosynthesis Research.

[45]  A. Khalafallah,et al.  Effect of Arbuscular Mycorrhizal Fungi on the Metabolic Products and Activity of Antioxidant System in Wheat Plants Subjected to Short-term Water Stress, Followed by Recovery at Different Growth Stages , 2008 .

[46]  A. Morte,et al.  Effects of nursery preconditioning through mycorrhizal inoculation and drought in Arbutus unedo L. plants , 2010, Mycorrhiza.

[47]  G. Bethlenfalvay,et al.  Plant Response to Mycorrhizal Fungi: Host, Endophyte, and Soil Effects1 , 1985 .

[48]  C. Walker Taxonomic concepts in the Endogonaceae: spore wall characteristics in species descriptions , 1983 .

[49]  A. Morte,et al.  The influence of mycorrhizal inoculation and paclobutrazol on water and nutritional status of Arbutus unedo L. , 2009 .

[50]  R. Linderman,et al.  Varied response of marigold (Tagetes spp.) genotypes to inoculation with different arbuscular mycorrhizal fungi , 2004 .

[51]  S. Bañón,et al.  Selection and nursery production of ornamental plants for landscaping and xerogardening in semi-arid environments , 2006 .

[52]  L. Guidi,et al.  Interactions of water stress and solar irradiance on the physiology and biochemistry of Ligustrum vulgare. , 2008, Tree physiology.

[53]  S. Long,et al.  Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. , 2003, Journal of experimental botany.

[54]  D. Struve,et al.  Quercus macrocarpa and Q. Prinus physiological and morphological responses to drought stress and their potential for urban forestry , 2005 .

[55]  J. M. Ruiz-Lozano,et al.  Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. , 2004, Journal of experimental botany.

[56]  T. Sharkey,et al.  Fitting photosynthetic carbon dioxide response curves for C(3) leaves. , 2007, Plant, cell & environment.

[57]  F. Davies,et al.  Colonization and growth effects of the mycorrhizal fungus Glomus intraradicies in a commercial nursery container production system. , 2000 .

[58]  Chris A. Martin,et al.  Growth of Argentine Mesquite Inoculated with Vesicular-Arbuscular Mycorrhizal Fungi , 1994, Arboriculture & Urban Forestry.

[59]  F. Ferrini,et al.  Response of English Oak (Quercus Robur L.) Trees to Biostimulants Application in the Urban Environment , 2002, Arboriculture & Urban Forestry.

[60]  J. Flexas,et al.  Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration. , 2006, The New phytologist.

[61]  F. Davies,et al.  Drought resistance of mycorrhizal pepper plants independent of leaf P concentration - response in gas exchange and water relations , 1993 .

[62]  R. Strasser,et al.  The fluorescence transient as a tool to characterize and screen photosynthetic samples , 2000 .

[63]  Manuela Giovannetti,et al.  Biodiversity in arbuscular mycorrhizal fungi , 1994 .

[64]  S. Declerck,et al.  Methods for large-scale production of AM fungi: past, present, and future , 2010, Mycorrhiza.

[65]  Marc W. van Iersel,et al.  Growth and Water Use of Petunia as Affected by Substrate Water Content and Daily Light Integral , 2010 .

[66]  R. Augé,et al.  Non-hydraulic root-to-shoot signalling in mycorrhizal and non-mycorrhizal sorghum exposed to partial soil drying or root severing , 1994 .

[67]  M. Allen,et al.  COMPARATIVE WATER RELATIONS AND PHOTOSYNTHESIS OF MYCORRHIZAL AND NON-MYCORRHIZAL BOUTELOUA GRACILIS H.B.K. LAG EX STEUD. , 1981 .

[68]  G. Berta,et al.  Arbuscular mycorrhizal induced changes to plant growth and root system morphology in Prunus cerasifera. , 1995, Tree physiology.

[69]  D. Oosterhuis,et al.  Effect of Water Deficit on Gas Exchange, Osmotic Solutes, Leaf Abscission, and Growth of Four Birch Genotypes (Betula L.) Under a Controlled Environment , 2007 .

[70]  T. Grove,et al.  Working with Mycorrhizas in Forestry and Agriculture , 1996 .

[71]  Andrew F. S. Taylor,et al.  Fungal communities in mycorrhizal roots of conifer seedlings in forest nurseries under different cultivation systems, assessed by morphotyping, direct sequencing and mycelial isolation , 2005, Mycorrhiza.

[72]  P. F. Scholander,et al.  HYDROSTATIC PRESSURE AND OSMOTIC POTENTIAL IN LEAVES OF MANGROVES AND SOME OTHER PLANTS. , 1964, Proceedings of the National Academy of Sciences of the United States of America.

[73]  J. Syvertsen,et al.  Carbon Economy of Sour Orange in Relation to Mycorrhizal Colonization and Phosphorus Status , 1993 .

[74]  R. Strasser,et al.  Dark recovery of the Chl a fluorescence transient (OJIP) after light adaptation: the qT-component of non-photochemical quenching is related to an activated photosystem I acceptor side. , 2006, Biochimica et biophysica acta.

[75]  J. Syvertsen,et al.  INFLUENCE OF VESICULAR–ARBUSCULAR MYCORRHIZA ON THE HYDRAULIC CONDUCTIVITY OF ROOTS OF TWO CITRUS ROOTSTOCKS , 1984 .

[76]  J. Klironomos,et al.  The mycorrhizal status and colonization of 26 tree species growing in urban and rural environments , 2011, Mycorrhiza.

[77]  J. Pereira,et al.  How plants cope with water stress in the field. Photosynthesis and growth. , 2002, Annals of botany.

[78]  E. Sieverding,et al.  Vesicular-Arbuscular Mycorrhiza Man-agement in Tropical Agrosystems , 1991 .

[79]  S. Gianinazzi,et al.  Cytology, Histochemistry and Immunocytochemistry as Tools for Studying Structure and Function in Endomycorrhiza , 1992 .

[80]  M. Daft,et al.  Interactions between water-stress and different mycorrhizal inocula on plant growth and mycorrhizal development in maize and sorghum , 1990, Plant and Soil.

[81]  M. Allen INFLUENCE OF VESICULAR‐ARBUSCULAR MYCORRHIZAE ON WATER MOVEMENT THROUGH BOUTELOUA GRACILIS (H.B.K.) LAG EX STEUD* , 1982 .

[82]  J. Barea,et al.  Analysing natural diversity of arbuscular mycorrhizal fungi in olive tree (Olea europaea L.) plantations and assessment of the effectiveness of native fungal isolates as inoculants for commercial cultivars of olive plantlets , 2004 .

[83]  Christina E. Wells,et al.  Arbuscular mycorrhizal inoculation affects root development of Acer and Magnolia species. , 2009 .

[84]  Chris A. Martin,et al.  Effect of Urban Expansion on Arbuscular Mycorrhizal Fungal Mediation of Landscape Tree Growth , 2001, Arboriculture & Urban Forestry.

[85]  Sally E. Smith,et al.  Effects of soil compaction on plant growth phosphorus uptake and morphological characteristics of vesicular—arbuscular mycorrhizal colonization of Trifolium subterraneum , 1997 .

[86]  F. Ferrini,et al.  Physiological responses to different irrigation regimes of shade trees grown in container , 2008 .

[87]  H. Marschner,et al.  EFFECT OF VA MYCORRHIZAL FUNGI AND RHIZOSPHERE MICROORGANISMS ON ROOT AND SHOOT MORPHOLOGY, GROWTH AND WATER RELATIONS IN MAIZE , 1990 .

[88]  K. Mulongoy,et al.  Interactions between drought stress and vesicular-arbuscular mycorrhiza on the growth of Faidherbia albida (syn. Acacia albida) and Acacia nilotica in sterile and non-sterile soils , 1992, Biology and Fertility of Soils.

[89]  P. Reddell,et al.  In vitro synthesis of ectomycorrhizas on Casuarinaceae with a range of mycorrhizal fungi. , 1991, The New phytologist.

[90]  F. Davies,et al.  Arbuscular Mycorrhizal Fungi, Organic and Inorganic Controlled-release Fertilizers: Effect on Growth and Leachate of Container-grown Bush Morning Glory (Ipomoea carnea ssp. fistulosa) Under High Production Temperatures , 2005 .

[91]  R. Augé,et al.  Osmotic Adjustment in Leaves of VA Mycorrhizal and Nonmycorrhizal Rose Plants in Response to Drought Stress. , 1986, Plant physiology.

[92]  R. Harris,et al.  MYCORRHIZAL FUNGAL INOCULATION OF ESTABLISHED STREET TREES , 2003 .

[93]  J. Pera,et al.  Influence of the fertilisation method in controlled ectomycorrhizal inoculation of two Mediterranean pines , 2007, Annals of Forest Science.

[94]  E. Roberts,et al.  Mycorrhizal fungi improve drought resistance in creeping bentgrass , 1997 .

[95]  D. Lawlor Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. , 2002, Annals of Botany.

[96]  G. Weber,et al.  The influence of chemical soil factors on the development of VA mycorrhizas of ash (Fraxinus excelsior L.) and sycamore (Acer pseudoplatanus L.) in pot experiments. , 2000 .

[97]  M. Allen,et al.  Effectiveness of Commercial Mycorrhizal Inoculants on the Growth of Liquidambar styraciflua in Plant Nursery Conditions , 2005 .

[98]  R. Agerer Exploration types of ectomycorrhizae , 2001, Mycorrhiza.

[99]  N. Requena,et al.  Assessment of natural mycorrhizal potential in a desertified semiarid ecosystem , 1996, Applied and environmental microbiology.

[100]  S. Smith,et al.  The effect of soil compaction on growth and P uptake by Trifolium subterraneum: interactions with mycorrhizal colonisation , 1996, Plant and Soil.

[101]  A. Newton Mineral nutrition and mycorrhizal infection of seedling oak and birch , 1991 .

[102]  O. Osonubi Comparative effects of vesicular-arbuscular mycorrhizal inoculation and phosphorus fertilization on growth and phosphorus uptake of maize (Zea mays L.) and sorghum (Sorghum bicolor L.) plants under drought-stressed conditions , 1994, Biology and Fertility of Soils.

[103]  N. Uphoff Biological Approaches to Sustainable Soil Systems , 2006 .

[104]  M. Abrams Adaptations and responses to drought in Quercus species of North America. , 1990, Tree physiology.

[105]  M. Sánchez-Díaz,et al.  Gas exchange is related to the hormone balance in mycorrhizal or nitrogen‐fixing alfalfa subjected to drought , 1997 .

[106]  M. Habte The Roles of Arbuscular Mycorrihizas in Plantand Soil Health , 2006 .

[107]  R. E. Koske,et al.  A modified procedure for staining roots to detect VA mycorrhizas , 1989 .

[108]  M. Allen,et al.  Effects of Mycorrhizae and Nontarget Organisms on Restoration of a Seasonal Tropical Forest in Quintana Roo, Mexico: Factors Limiting Tree Establishment , 2005 .