Accumulation and localization of aluminium in root tips of loblolly pine seedlings and the associated ectomycorrhiza Pisolithus tinctorius

ABSTRACT Evidence from past studies suggests that loblolly pine maybe tolerant of Al. The experiments described in this manu-script were initiated to examine Al tolerance and Al accu-mulation in the pine root and the degree of Alaccumulation in fungal hyphae when pine roots were colo-nized with the ectomycorrhiza Pisolithus tinctorius. Theexperiments used lumogallion staining and confocalmicroscopy to localize Al in root and fungal structures. Theresults clearly showed that loblolly pine seedlings werehighly resistant to Al. A decrease in primary root extensioncould not be detected until Al +3 activities approached40 m mol L - 1 , and extension was suppressed only 30% at anAl +3 activity of 580 m mol L - 1 . This contrasted with theresponse of the Al-sensitive ‘check’ species soybean, whereprimary root extension was severely restricted at Al +3 activ-ities lower than 5 m mol L - 1 . Tissue Al measurements andlumogallion fluorescence of longitudinal sections of thepine root tip indicated that tolerance was associated withboth Al exclusion from the tip region and compartmental-ization of absorbed Al in peripheral cell areas outside ofthe meristem. In lateral roots colonized with ectomycor-rhizae, lumogallion fluorescence showed that large amountsof Al accumulated at the fungal mantle and in areas withthe Hartig net. At higher magnification, lumogallion indi-cated substantial Al accumulation inside hyphae. Little Alcould be detected in lateral root cells. The results show thatpine possesses multiple mechanisms that can contribute toAl tolerance in acid field soils.Key-words: Pisolithus tinctorius; confocal scanning micros-copy; lumogallion.

[1]  S. Matsumoto,et al.  Highly sensitive analytical method for aluminum movement in soybean root through lumogallion staining , 1997, Journal of Plant Research.

[2]  J. Neves,et al.  Responses of eucalypt species to aluminum: the possible involvement of low molecular weight organic acids in the Al tolerance mechanism. , 2004, Tree physiology.

[3]  L. Kochian,et al.  Mechanisms of metal resistance in plants: aluminum and heavy metals , 2002, Plant and Soil.

[4]  M. Osaki,et al.  Al uptake kinetics in roots of Melastoma malabathricum L. – an Al accumulator plant , 2001, Plant and Soil.

[5]  T. Rufty,et al.  Altered aluminum inhibition of soybean root elongation in the presence of magnesium , 2001, Plant and Soil.

[6]  B. Frey,et al.  Effects of aluminium treatment on Norway spruce roots: Aluminium binding forms, element distribution, and release of organic substances , 1999, Plant and Soil.

[7]  L. Kochian,et al.  Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.) , 1995, Planta.

[8]  E. Mutert,et al.  Global extent, development and economic impact of acid soils , 1995, Plant and Soil.

[9]  P. C. Tam,et al.  Heavy metal tolerance by ectomycorrhizal fungi and metal amelioration by Pisolithus tinctorius , 1995, Mycorrhiza.

[10]  F. Martin,et al.  Aluminium polyphosphate complexes in the mycorrhizal basidiomyceteLaccaria bicolor: A27Al-nuclear magnetic resonance study , 1994, Planta.

[11]  L. H. Weinstein,et al.  Aluminum-mycorrhizal interactions in the physiology of pitch pine seedlings , 1990, Plant and Soil.

[12]  H. Bücking,et al.  The fungal sheath of ectomycorrhizal pine roots: an apoplastic barrier for the entry of calcium, magnesium, and potassium into the root cortex? , 2002, Journal of experimental botany.

[13]  Daniel Markewitz,et al.  Understanding Soil Change—Soil Sustainability over Millennia, Centuries, and Decades , 2001 .

[14]  E. Delhaize,et al.  FUNCTION AND MECHANISM OF ORGANIC ANION EXUDATION FROM PLANT ROOTS. , 2001, Annual review of plant physiology and plant molecular biology.

[15]  T. Rufty,et al.  Magnesium is more efficient than calcium in alleviating aluminum rhizotoxicity in soybean and its ameliorative effect is not explained by the Gouy-Chapman-Stern model. , 2001, Plant & cell physiology.

[16]  T. Nakanishi,et al.  Aluminium distribution in soybean root tip for a short time Al treatment , 2001 .

[17]  W. Horst,et al.  Aluminium tolerance is achieved by exudation of citric acid from roots of soybean (Glycine max) , 2000 .

[18]  R. Finlay,et al.  Organic acids produced by mycorrhizal Pinus sylvestris exposed to elevated aluminium and heavy metal concentrations , 2000 .

[19]  D. Godbold,et al.  Metal toxicity and ectomycorrhizas , 2000 .

[20]  T. Carter,et al.  Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy. , 2000, Plant physiology.

[21]  I. Brunner,et al.  Detection and localization of aluminum and heavy metals in ectomycorrhizal Norway spruce seedlings. , 2000, Environmental pollution.

[22]  J. F. Ma,et al.  Role of organic acids in detoxification of aluminum in higher plants. , 2000, Plant & cell physiology.

[23]  V. Appanna,et al.  Oxalic acid production and aluminum tolerance in Pseudomonas fluorescens. , 1999, Journal of inorganic biochemistry.

[24]  J. Cairney,et al.  Co-evolution of Mycorrhizal Symbionts and their Hosts to Metal-contaminated Environments , 1999 .

[25]  D. Godbold,et al.  Aluminium accumulation in root cell walls coincides with inhibition of root growth but not with inhibition of magnesium uptake in Norway spruce , 1998 .

[26]  Douglas L. Godbold,et al.  Ectomycorrhizas and amelioration of metal stress in forest trees , 1998 .

[27]  Mayandi Sivaguru,et al.  The Distal Part of the Transition Zone Is the Most Aluminum-Sensitive Apical Root Zone of Maize , 1998 .

[28]  T. Samuels,et al.  Al Partitioning Patterns and Root Growth as Related to Al Sensitivity and Al Tolerance in Wheat , 1997, Plant physiology.

[29]  G. A. Schier,et al.  Response of ectomycorrhizal and nonmycorrhizal pitch pine (Pinusrigida) seedlings to nutrient supply and aluminum: growth and mineral nutrition , 1996 .

[30]  L. Kochian,et al.  Multiple Aluminum-Resistance Mechanisms in Wheat (Roles of Root Apical Phosphate and Malate Exudation) , 1996, Plant physiology.

[31]  J. Nowak,et al.  Aluminum sensitivity of loblolly pine and slash pine seedlings grown in solution culture. , 1995, Tree physiology.

[32]  G. A. Schier,et al.  Effect of aluminum on the growth, anatomy, and nutrient content of ectomycorrhizal and nonmycorrhizal eastern white pine seedlings , 1995 .

[33]  D. Parker,et al.  GEOCHEM‐PC—A Chemical Speciation Program for IBM and Compatible Personal Computers , 1995 .

[34]  S. Cabaniss,et al.  Aqueous Al(III) Speciation by High-Performance Cation Exchange Chromatography with Fluorescence Detection of the Aluminum-Lumogallion Complex , 1995 .

[35]  G. A. Schier,et al.  Damping-off disease of pine seedlings on soils treated with simulated acidic rain , 1995 .

[36]  S. Visser Ectomycorrhizal fungal succession in jack pine stands following wildfire , 1995 .

[37]  L. Kochian Cellular Mechanisms of Aluminum Toxicity and Resistance in Plants , 1995 .

[38]  T. Rufty,et al.  Rapid Uptake of Aluminum into Cells of Intact Soybean Root Tips (A Microanalytical Study Using Secondary Ion Mass Spectrometry) , 1994, Plant physiology.

[39]  Y. Piché,et al.  I. Host plant variability and heritability of ectomycorrhizal and root traits , 1994 .

[40]  B. Kropp,et al.  Genetics of ectomycorrhizal symbiosis , 1994 .

[41]  D. Godbold,et al.  The effect of Paxillus involutus Fr. on aluminum sensitivity of Norway spruce seedlings. , 1993, Tree physiology.

[42]  L. Kochian,et al.  Aluminium Toxicity in Roots: An Investigation of Spatial Sensitivity and the Role of the Root Cap , 1993 .

[43]  D. Parker,et al.  Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat. , 1992, Plant physiology.

[44]  M. Shuman Dissociation pathways and species distribution of aluminum bound to an aquatic fulvic acid , 1992 .

[45]  D. Wilkins,et al.  Localization of aluminium in the roots of Norway spruce [Picea abies (L.) Karst.] inoculated with Paxillus involutus Fr. , 1991, The New phytologist.

[46]  D. Godbold,et al.  The effect of aluminium on uptake and distribution of magnesium and calcium in roots of mycorrhizal Norway spruce seedlings , 1991 .

[47]  H. Matsumoto Biochemical mechanism of the toxicity of aluminium and the sequestration of aluminium in plant cells , 1991 .

[48]  Guichan Zhang,et al.  Kinetics of Aluminum Uptake in Triticum aestivum L: Identity of the Linear Phase of Aluminum Uptake by Excised Roots of Aluminum-Tolerant and Aluminum-Sensitive Cultivars. , 1990, Plant physiology.

[49]  F. C. Thornton,et al.  Sensitivity of Tree Seedlings to Aluminum: III. Red Spruce and Loblolly Pine , 1990 .

[50]  D. Wilkins,et al.  The effects of aluminium and Paxillus involutus Fr. on the growth of Norway spruce [Picea abies (L.) Karst.] , 1989 .

[51]  M. Schaedle,et al.  Effect of aluminum on growth of root tips of honey locust and loblolly pine , 1989 .

[52]  D. Godbold,et al.  Aluminum toxicity and forest decline. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[53]  R. J. Medve,et al.  Effects of Aluminum and Manganese on the Growth of Ectomycorrhizal Fungi , 1984, Applied and environmental microbiology.

[54]  M. Katyal,et al.  Analytical reactions of hydroxyflavones. , 1977, Talanta.

[55]  F. Bormann Factors Determining the Role of Loblolly Pine and Sweetgum in Early Old-Field Succession in the Piedmont of North Carolina , 1953 .

[56]  Catherine Keever,et al.  Causes of Succession on Old Fields of the Piedmont, North Carolina , 1950 .