Molecular and Physiological Analysis of Al3+ and H+ Rhizotoxicities at Moderately Acidic Conditions1[W][OPEN]

Rhizotoxicities of Al3+ and H+ occur at moderately acidic soil conditions (pH [water] = 5–5.5), especially under conditions of low Ca supply. Al3+ and H+ toxicities predicted to occur at moderately acidic conditions (pH [water] = 5–5.5) in low-Ca soils were characterized by the combined approaches of computational modeling of electrostatic interactions of ions at the root plasma membrane (PM) surface and molecular/physiological analyses in Arabidopsis (Arabidopsis thaliana). Root growth inhibition in known hypersensitive mutants was correlated with computed {Al3+} at the PM surface ({Al3+}PM); inhibition was alleviated by increased Ca, which also reduced {Al3+}PM and correlated with cellular Al responses based on expression analysis of genes that are markers for Al stress. The Al-inducible Al tolerance genes ALUMINUM-ACTIVATED MALATE TRANSPORTER1 and ALUMINUM SENSITIVE3 were induced by levels of {Al3+}PM too low to inhibit root growth in tolerant genotypes, indicating that protective responses are triggered when {Al3+}PM was below levels that can initiate injury. Modeling of the H+ sensitivity of the SENSITIVE TO PROTON RHIZOTOXICITY1 knockout mutant identified a Ca alleviation mechanism of H+ rhizotoxicity, possibly involving stabilization of the cell wall. The phosphatidate phosphohydrolase1 (pah1) pah2 double mutant showed enhanced Al susceptibility under low-P conditions, where greater levels of negatively charged phospholipids in the PM occur, which increases {Al3+}PM through increased PM surface negativity compared with wild-type plants. Finally, we found that the nonalkalinizing Ca fertilizer gypsum improved the tolerance of the sensitive genotypes in moderately acidic soils. These findings fit our modeling predictions that root toxicity to Al3+ and H+ in moderately acidic soils involves interactions between both toxic ions in relation to Ca alleviation.

[1]  Cynthia D. Nezames,et al.  Mutational loss of Arabidopsis SLOW WALKER2 results in reduced endogenous spermine concomitant with increased aluminum sensitivity. , 2012, Functional plant biology : FPB.

[2]  L. Kochian,et al.  Development of a Novel Aluminum Tolerance Phenotyping Platform Used for Comparisons of Cereal Aluminum Tolerance and Investigations into Rice Aluminum Tolerance Mechanisms1[C][W][OA] , 2010, Plant Physiology.

[3]  Peng-ling Wang,et al.  The surface charge density of plant cell membranes (σ): an attempt to resolve conflicting values for intrinsic σ , 2010, Journal of experimental botany.

[4]  H. Ohta,et al.  Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation , 2009, Proceedings of the National Academy of Sciences.

[5]  Jon E. Shaff,et al.  GEOCHEM-EZ: a chemical speciation program with greater power and flexibility , 2009, Plant and Soil.

[6]  N. Sakurai,et al.  STOP1 Regulates Multiple Genes That Protect Arabidopsis from Proton and Aluminum Toxicities1[C][W][OA] , 2009, Plant Physiology.

[7]  N. Sakurai,et al.  Comparative transcriptomic characterization of aluminum, sodium chloride, cadmium and copper rhizotoxicities in Arabidopsis thaliana , 2009, BMC Plant Biology.

[8]  L. Kochian,et al.  Characterization of AtALMT1 Expression in Aluminum-Inducible Malate Release and Its Role for Rhizotoxic Stress Tolerance in Arabidopsis1[W][OA] , 2007, Plant Physiology.

[9]  N. Sakurai,et al.  Natural variation of Arabidopsis thaliana reveals that aluminum resistance and proton resistance are controlled by different genetic factors , 2007, Theoretical and Applied Genetics.

[10]  Richard M. Clark,et al.  Common Sequence Polymorphisms Shaping Genetic Diversity in Arabidopsis thaliana , 2007, Science.

[11]  Qing Liu,et al.  A Higher Plant Δ8 Sphingolipid Desaturase with a Preference for (Z)-Isomer Formation Confers Aluminum Tolerance to Yeast and Plants[C][OA] , 2007, Plant Physiology.

[12]  K. Shinozaki,et al.  Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance , 2007, Proceedings of the National Academy of Sciences.

[13]  L. Kochian,et al.  AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. Mikkelsen,et al.  Polygalacturonase-Inhibiting Protein Interacts with Pectin through a Binding Site Formed by Four Clustered Residues of Arginine and Lysine1 , 2006, Plant Physiology.

[15]  Yuriko Kobayashi,et al.  Quantitative trait loci controlling aluminium tolerance in two accessions of Arabidopsis thaliana (Landsberg erecta and Cape Verde Islands) , 2005 .

[16]  I. Rao,et al.  Methylene Blue Stainability of Root-Tip Protoplasts as an Indicator of Aluminum Tolerance in a Wide Range of Plant Species, Cultivars and Lines , 2005 .

[17]  S. Iida,et al.  Japanese morning glory dusky mutants displaying reddish-brown or purplish-gray flowers are deficient in a novel glycosylation enzyme for anthocyanin biosynthesis, UDP-glucose:anthocyanidin 3-O-glucoside-2''-O-glucosyltransferase, due to 4-bp insertions in the gene. , 2005, The Plant journal : for cell and molecular biology.

[18]  M. Geisler,et al.  ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[19]  P. Albersheim,et al.  Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. , 2004, Annual review of plant biology.

[20]  D. Parker,et al.  Relative effectiveness of calcium and magnesium in the alleviation of rhizotoxicity in wheat induced by copper, zinc, aluminum, sodium, and low pH , 2004, Plant and Soil.

[21]  T. Kinraide Toxicity factors in acidic forest soils: attempts to evaluate separately the toxic effects of excessive Al3+ and H+ and insufficient Ca2+ and Mg2+ upon root elongation , 2003 .

[22]  T. Vision,et al.  Identification and Characterization of Aluminum Tolerance Loci in Arabidopsis (Landsberg erecta × Columbia) by Quantitative Trait Locus Mapping. A Physiologically Simple But Genetically Complex Trait1 , 2003, Plant Physiology.

[23]  T. Hibino,et al.  Extraction of total RNA from leaves of Eucalyptus and other woody and herbaceous plants using sodium isoascorbate. , 2003, BioTechniques.

[24]  Yuriko Kobayashi,et al.  QTL analysis of Al tolerance in recombinant inbred lines of Arabidopsis thaliana. , 2002, Plant & cell physiology.

[25]  H. Koyama,et al.  Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: pectin-Ca interaction may play an important role in proton rhizotoxicity. , 2001, Journal of experimental botany.

[26]  B. Schnettler,et al.  Effect of liming and gypsum on soil chemistry, yield, and mineral composition of ryegrass grown in an acidic Andisol , 1999 .

[27]  T. Kinraide,et al.  Three mechanisms for the calcium alleviation of mineral toxicities , 1998, Plant physiology.

[28]  U. Yermiyahu,et al.  Sorption of Aluminum to Plasma Membrane Vesicles Isolated from Roots of Scout 66 and Atlas 66 Cultivars of Wheat , 1997, Plant physiology.

[29]  L. Kochian,et al.  Al Inhibits Both Shoot Development and Root Growth in als3, an Al-Sensitive Arabidopsis Mutant , 1997, Plant physiology.

[30]  B. van Raij,et al.  Calcium sulphate, phosphogypsum and calcium carbonate in the amelioration of acid subsoils for root growth , 1997, Plant and Soil.

[31]  T. Kinraide Reconsidering the rhizotoxicity of hydroxyl, sulphate, and fluoride complexes of aluminium , 1997 .

[32]  K. Ojima,et al.  Physiological response of root tip of alfalfa to low pH and aluminium stress in water culture , 1995, Plant and Soil.

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

[34]  M. Hirai,et al.  Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia. , 1992, Plant physiology.

[35]  D. Parker,et al.  Apparent phytotoxicity of mononuclear hydroxy-aluminum to four dicotyledonous species. , 1990 .

[36]  T. Wagatsuma,et al.  Low surface negativity of root protoplasts from aluminum-tolerant plant species , 1989 .

[37]  R. Wright,et al.  EFFECTS OF ALUMINUM AND CALCIUM ON THE GROWTH OF SUBTERRANEAN CLOVER IN APPALACHIAN SOILS , 1987 .

[38]  H. Sekimoto,et al.  Relative abundance of Delta(5)-sterols in plasma membrane lipids of root-tip cells correlates with aluminum tolerance of rice. , 2009, Physiologia plantarum.

[39]  N. Sakurai,et al.  STOP 1 Regulates Multiple Genes That Protect Arabidopsis from Proton and Aluminum Toxicities 1 [ C ] [ W ] [ OA ] , 2009 .

[40]  N. Carpita,et al.  Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. , 1993, The Plant journal : for cell and molecular biology.

[41]  F. Adams,et al.  Chemical Factors Affecting Root Growth in Subsoil Horizons of Coastal Plain Soils 1 , 1983 .