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

Journal of Plant Growth Regulation

Volumn 33, Issue 3, 2014, Pages 612-625

  Yang, Yurong ^a   Tang, Ming ^a   Sulpice, Ronan ^b   Chen, Hui ^a   Tian, Shuai ^a   Ban, Yihui ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Arbuscular mycorrhizal fungi; Black locust; Box counting; Fractal dimension; Photosynthesis

Indexed keywords

EID: 84891513515     PISSN: 07217595     EISSN: 14358107     Source Type: Journal    
DOI: 10.1007/s00344-013-9410-0     Document Type: Article

References (77)

1. Aroca R, del Mar AM, Vernieri P, Ruiz-Lozano JM (2008) Plant responses to drought stress and exogenous ABA application are modulated differently by mycorrhization in tomato and an ABA-deficient mutant (Sitiens). Microbial Ecol 56: 704-719.
2. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11: 3-42.
3. Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84: 373-381.
4. Barrett RP, Mebrahtu T, Hanover JW (1990) Black locust: a multipurpose tree species for temperate climates. In: Janick J, Simon JE (eds) Advances in new crops. Timber Press, Portland.
5. Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173: 11-26.
6. Cartmilla DL, Alarcónb A, Volderc A, Valdez-Aguilard LA, Arnoldc MA, Cartmille AD (2012) Arbuscular mycorrhizal fungi alleviate growth of Ulmus parvifolia Jacq. at suboptimal planting depths. Sci Hortic 144: 74-80.
7. Ciesla WM (2002) Non-wood forest products from temperate broad-leaved trees. Food and Agriculture Organization of the United Nations, Rome.
8. Colla G, Rouphael Y, Cardarelli M, Tullio M, Rivera CM, Rea E (2008) Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol Fertil Soils 44: 501-509.
9. Despland E (2003) Fractal index captures the role of vegetation clumping in locust swarming. Funct Ecol 17: 315-322.
10. Dickerson J (2002) Plant fact sheet: black locust (Robinia pseudoacacia L). USDA NCRS, Washington, DC.
11. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison J, Hobbie SE, Odell GM, Weider LJ (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3: 540-550.
12. Eshel A (1998) On the fractal dimensions of a root system. Plant Cell Environ 21: 247-251.
13. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104: 1263-1280.
14. Faber BA, Zasoske RJ, Munns DN, Shackel K (1991) A method for measuring hyphal nutrition and water uptake in mycorrhizal plants. Can J Bot 69: 87-94.
15. Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givinsh TJ (ed) On the economy of form and function. Cambridge University Press, Cambridge, pp 25-55.
16. Foroutan-pour K, Dutilleul P, Smith DL (1999) Soybean canopy development as affected by population density and intercropping with corn: fractal analysis with other quantitative methods. Crop Sci 39: 1784-1791.
17. Gao JF (2000) Techniques of plant physiology. World Publishing Corporation, Xi'an.
18. Garlock RJ, Wong YS, Balan V, Dale BE (2012) AFEX pretreatment and enzymatic conversion of black locust (Robinia pseudoacacia L.) to soluble sugars. Bioenergy Res 5: 306-318.
19. Garmendia I, Goicoechea N, Aguirreolea J (2004) Antioxidant metabolism in asymptomatic leaves of verticillium-infected pepper associated with an arbuscular mycorrhizal fungus. J Phytopathol 152: 593-599.
20. Gemma JN, Koske RE, Roberts EM, Jackson N, De Antonis K (1997) Mycorrhizal fungi improve drought resistance in creeping bentgrass. J Turkish Sci 73: 15-29.
21. Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A (2013) Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 117: 106-114.
22. Gillespie AR, Pope PE (1990) Rhizosphere acidification increases phosphorus recovery of black locust: II. Model predictions and measured recovery. Soil Sci Soc Am J 54: 538-541.
23. Harborne JB (1984) Phytochemical methods. A guide to modern techniques of plant analysis. Chapman and Hall, London.
24. Hessen DO, Jensen TC, Kyle M, Elser JJ (2007) RNA responses to N- and P-limitation; reciprocal regulation of stoichiometry and growth rate in Brachionus. Funct Ecol 21: 956-962.
25. Hilborn R (2000) Chaos and non-linear dynamics, 2nd edn. Oxford University Press, Oxford.
26. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347: 1-32.
27. Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321: 153-187.
28. Jackson ML (1958) Soil chemical analysis. Prentice Hall, Inc., Englewood Cliffs.
29. Jeffries P, Gianianazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37: 1-16.
30. Jennings DH (1995) The physiology of fungal nutrition. Cambridge University Press, Cambridge.
31. Jin T, Liu G, Fu B, Ding X, Yang L (2011) Assessing adaptability of planted trees using leaf traits: a case study with Robinia pseudoacacia L. in the Loess Plateau, China. Chin Geogr Sci 21: 290-303.
32. Jones JB (1991) Kjeldahl method for nitrogen determination. Micro-Macro, Athens.
33. Jördens C, Scheller M, Breitenstein B, Selmar D, Koch M (2009) Evaluation of leaf water status by means of permittivity at terahertz frequencies. J Biol Phys 35(3): 255-264.
34. Juge C, Champagne A, Coughlan AP, Juge N, Parrott L, Piche Y (2009) Quantifying the growth of arbuscular mycorrhizal fungi: usefulness of the fractal dimension. Botany 87: 387-400.
35. Kyle M, Watts T, Schade J, Elser JJ (2003) A microfluorometric method for quantifying RNA and DNA in terrestrial insects. J Insect Sci 3(1): 1-7.
36. Li KT, Lakso AN (2004) Photosynthetic characteristics of apple spur leaves after summer pruning to improve exposure to light. Sci Hortic 5: 969-972.
37. Li J, Du Q, Sun CX (2009) An improved box-counting method for image fractal dimension estimation. Pattern Recognit 42(11): 2460-2469.
38. Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9: 331-336.
39. Lu RK (1999) Analytical methods for soils and agricultural chemistry. China Agricultural Science and Technology, Beijing.
40. Mancuso S (2002) Discrimination of grapevine (Vitis vinifera L.) leaf shape by fractal spectrum. Vitis 41(3): 137-142.
41. Mandelbrot B (1997) How long is the coast of Britain? Statistical selfsimilarity and fractional dimension. Science 156: 636-638.
42. Mathur N, Vyas A (2000) Influence of arbuscular mycorrhizae on biomass production, nutrient uptake and physiological changes in Ziziphus mauritana Lam. under water stress. J Arid Environ 45: 191-195.
43. Maya MA, Matsubara YI (2013) Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress. Mycorrhiza. doi: 10. 1007/s00572-013-0477-z.
44. Moran JF, Becana M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparicio-Tejo P (1994) Drought induces oxidative stress in pea plants. Planta 194: 346-352.
45. Nelsen CE, Safir GR (1982) Increased drought tolerance of mycorrhizal onion plants caused by improved phosphorus nutrition. Planta 154: 407-413.
46. Palmer M (1988) Fractal geometry: a tool for describing spatial patterns of plant communities. Vegetation 75: 91-102.
47. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55: 157-160.
48. Ralph ML, Hooker JE (2005) Application of a membranegel procedure to determine the effects of root exudates on the growth of the extraradical hyphae of the arbuscular mycorrhizal fungus Glomus etunicatum. Symbiosis 40(1): 41-47.
49. Rice S, Westerman B, Federici R (2004) Impacts of the exotic, nitrogen-fixing black locust (Robinia pseudoacacia) on nitrogen-cycling in a pine-oak ecosystem. Plant Ecol 174(1): 97-107.
50. Roumet C, Urcelay C, Diaz D (2006) Suites of root traits differ between annual and perennial species growing in the field. New Phytol 170: 357-368.
51. Ruiz-Lozano JM, Azon R, Gomez M (1995) Effects of arbuscular-mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Appl Environ Microbiol 61: 456-460.
52. Sarkar N, Chaudhuri BB (1994) An efficient differential box-counting approach to compute fractal dimension of image. IEEE Trans Syst Man Cybern 24(1): 115-120.
53. Schüssler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105: 1413-1421.
54. Sheng M, Tang M, Chen H, Yang B, Zhang FF, Huang YH (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18: 287-296.
55. Shlesinger M, West B (1991) Complex fractal dimension of the bronchial tree. Phys Rev Lett 67: 2106-2108.
56. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London.
57. Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104(1): 1-13.
58. Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182: 347-358.
59. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton.
60. Subramanian KS, Charest C (1997) Nutritional, growth, and reproductive responses of maize (Zea mays L.) to arbuscular mycorrhizal inoculation during and after drought stress at tasselling. Mycorrhiza 7: 25-32.
61. Tateno R, Tokuchi N, Yamanaka N, Du S, Otsuki K, Shimamura T, Xue Z, Wang S, Hou Q (2007) Comparison of litter fall production and leaf litter decomposition between an exotic black locust plantation and an indigenous oak forest near Yan'an on the Loess Plateau, China. For Ecol Manag 241: 84-90.
62. Trappe JM (1987) Phylogenetic and ecologic aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Safir GR (ed) Ecophysiology of VA mycorrhizal plants. CRC Press, Boca Raton, pp 5-25.
63. Ussiri DAN, Lal R, Jacinthe PA (2006) Soil properties and carbon sequestration of afforested pastures in reclaimed mine soils of Ohio. Soil Sci Soc Am J 70: 1797-1806.
64. van Hees PAW, Rosling A, Essen S, Godbold DL, Finlay RD (2006) Oxalate and ferricrocin exudation by the extrametrical mycelium of an ectomycorrhizal fungus in symbiosis with Pinus sylvestris. New Phytol 169: 367-378.
65. Verbovsek T (2009) BCFD-a Visual Basic program for calculation of the fractal dimension of digitized geological image data using a box-counting technique. Geol Q 53(2): 241-248.
66. Vrede T, Dobberfuhl DR, Kooijman SALM, Elser JJ (2004) Functional connections among organism C: N: P stoichiometry, macromolecular composition and growth. Ecology 85(5): 1217-1229.
67. Wright DP, Scholes JD, Read DJ (1998) Effects of mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ 21: 209-216.
68. Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163: 417-425.
69. Wu QS, He XH, Zou YN, Liu CY, Xiao J, Li Y (2012) Arbuscular mycorrhizas alter root system architecture of Citrus tangerine through regulating metabolism of endogenous polyamines. Plant Growth Regul 68: 27-35.
70. Xue S, Liu GB, Dai QH, Wei W, Hou XL (2007) Evolution of soil microbial biomass in the restoration process of artificial Robinia pseudoacacia under erosion environment. Acta Ecol Sin 27: 909-917.
71. Yüksek T (2012) The restoration effects of black locust (Robinia pseudoacacia L.) plantation on surface soil properties and carbon sequestration on lower hillslopes in the semi-humid region of Coruh Drainage Basin in Turkey. Catena 90: 18-25.
72. Zhang JL, Cao KF (2009) Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species. Funct Ecol 23(4): 658-667.
73. Zhang HH, Tang M, Chen H, Zheng CL, Niu ZC (2010) Effect of inoculation with AM fungi on lead uptake, translocation and stress alleviation of Zea mays L. seedlings planting in soil with increasing lead concentrations. Eur J Soil Biol 46: 306-311.
74. Zhang Q, Xu L, Tang J, Bai M, Chen X (2011a) Arbuscular mycorrhizal mediation of biomass-density relationship of Medicago sativa L. under two water conditions in a field experiment. Mycorrhiza 21: 269-277.
75. Zhang SQ, Li BZ, Liu YP, Zhang LS, Wang ZQ, Han MY (2011b) Fractal characteristics of two-dimensional images of 'Fuji' apple trees trained to two tree configurations after their winter pruning. Sci Hortic 130: 102-108.
76. Zhu XC, Song FB, Liu SQ, Liu TD (2011) Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant Soil 346: 189-199.
77. Zhu XC, Song FB, Liu SQ, Liu TD, Zhou X (2012) Arbuscular mycorrhizae improves photosynthesis and water status of Zea mays L. under drought stress. Plant Soil Environ 58(4): 186-191.