Effect of aluminium on plant growth and metabolism

1 Vol. 48 No. 3/2001. 673 686. QUARTERLY. This paper is dedicated to the memory of Professor Jacek Augustyniak Review Effect of aluminium on plant growth and metabolism Teresa Mossor-Pietraszewska . Department of Biochemistry, Institute of Molecular Biology and Biotechnology, Adam Mickiewicz University of Pozna , Pozna , Poland Received: 22 January, 2001; revised: 11 July, 2001; accepted: 4 September, 2001. Key words: aluminium , oxidative stress, phytotoxicity, plant response, signal transduction pathway aluminium toxicity is one of the major factors that limit plant growth and develop- ment in many acid soils. Root cells plasma membrane, particularly of the root apex, 3+. seems to be a major target of Al toxicity. However, strong interaction of Al , the main Al toxic form, with oxygen donor ligands (proteins, nucleic acids, polysaccharides) re- sults in the inhibition of cell division, cell extension, and transport.

2 Although the iden- tification of Al tolerance genes is under way, the mechanism of their expression re- mains obscure. Soil chemical factors that limit root growth in acid soils due to Al solubility at low pH have in acid soils, diminish crop production, in- reduced root systems and exhibit a variety of clude Al, Mn and various cations, and also de- nutrient-deficiency symptoms, with a conse- ficiency or unavailability of Ca, Mg, P, Mo, quent decrease in yield. In many countries and Si. These effects are further complicated with naturally acid soils, which constitute by interactions of Al with other ions in differ- about 40% of world arable soil (LeNoble et al., ent plant genotypes and under stress condi- 1996), Al toxicity is a major agricultural prob- tions (Foy, 1992). lem, and is intensively studied in plant sys- Cytotoxicity of Al has been well documented tems.

3 In plants (Delhaize & Ryan, 1995; Horst et al., The effects of aluminium on plant growth , 1999; Kollmeier et al., 2000; Marienfeld et al., crop yield, uptake and nutrients distribution 2000). It is generally known that plants grown in vegetative and reproductive parts are still Address correspondence to: Teresa Mossor-Pietraszewska, Department of Biochemistry, Institute of Molecular Biology and Biotechnology, Adam Mickiewicz University of Pozna , A. Fredry 10, 61-701. Pozna , Poland; tel. (48 61) 829 4534, e-mail: 674 T. Mossor-Pietraszewska 2001. not fully understood. This review discusses re- fied as hyperaccumulators of various toxic cent information on aluminium toxicity with metals (Baker et al., 2000). an emphasis on plant response to Al stress. VISUAL AND CELLULAR SYMPTOMS. CHEMICAL NATURE OF aluminium OF aluminium TOXICITY.

4 AND ITS OCCURENCE IN plants . Inhibition of root and shoot growth is a visi- Al is present in water, soil and air but most ble symptom of Al toxicity. The earliest symp- of it is incorporated into aluminosilicate soil toms concern roots. Shoots in contrast to the minerals and only very small quantities (at situation observed for Mn toxicity are less af- submicromolar levels) appear in soluble fected (Chang et al., 1999). Root stunting is a forms capable of influencing biological sys- consequence of Al-induced inhibition of root tems (May & Nordstrom, 1991). Different elongation. Roots are usually stubby and brit- forms of aluminium occur in soil solution: tle and root tips and lateral roots become Al(OH)2+ and Al(OH)2+ at pH 4 5, Al3+ at pH thick and may turn brown (Mossor-Pietra- 7, and Al(OH)4 at pH 7 8. Other com- szewska et al.)

5 , 1997). Such roots are ineffi- plex ions AlO4Al12(OH)24(H2O)127+ (Al13) cient in absorbing both nutrients and water. and Al3+ are almost certainly toxic, but no Young seedlings are more susceptible than rhizotoxicity has been detected for AlSO4+ older plants . Al apparently does not interfere and Al(SO4)2 or Al-F ( AlF2+ and AlF2+). with seed germination, but does impair the The status of Al(OH)2+ and Al(OH)2+ is uncer- growth of new roots and seedling establish- tain although experimental results have ap- ment (Nosko et al., 1988). peared indicating Al-OH toxicity (Kinraide, The common responses of shoots to Al in- 1997). The following Al species are toxic for clude: cellular and ultrastructural changes in wheat roots in the following increasing order: leaves, increased rates of diffusion resistance, AlF2+ < AlF2+ < Al3+ < Al13.

6 According to reduction of stomatal aperture, decreased Kochian's (1995) opinion toxicity has been photosynthetic activity leading to chlorosis convincingly demonstrated only for Al13 and and necrosis of leaves, total decrease in leaf Al3+. number and size, and a decrease in shoot bio- Intensification of the process of Al com- mass (Thornton et al., 1986). pounds solubilization is connected with the Blancaflor et al. (1998) have studied Al-in- degree of soil acidification caused by the duced effects on microtubules and actin washing out of alkaline metals ions (Na+, K+, microfilaments in elongating cells of maize Ca2+, Mg2+) from the soil and a decrease in root apices, and related the Al-induced growth the pH of soil solutions. inhibition to stabilization of microtubules in Al ions translocate very slowly to the upper the central elongation zone.

7 With respect to parts of plants (Ma et al., 1997a). Most plants growth determinants (auxin, gibberelic acid contain no more than mg Al g 1 dry mass. and ethylene), Al apparently interacts directly However, some plants , known as Al accumula- and/or indirectly with the factors that influ- tors, may contain over 10 times more Al with- ence organization of the cytoskeleton, such as out any injury. Tea plants are typical Al accu- cytosolic levels of Ca2+ (Jones et al., 1998), mulators: the Al content in these plants can Mg2+ and calmodulin (Grabski et al., 1998), reach as high as 30 mg g 1 dry mass in old cell-surface electrical potential (Takabatake &. leaves (Matsumoto et al., 1976). Approxi- Shimmen, 1997), callose formation (Horst et mately 400 species of terrestrial plants , be- al., 1997), and lipid composition of the plasma longing to 45 families, have so far been identi- membrane (Zhang et al.)

8 , 1997). Vol. 48 Effect of Al on plant growth and metabolism 675. Recently, Yamamoto et al. (2001) have Al stress (Ligterink & Hirt, 2001; Osawa &. shown that peroxidation of lipids is a rela- Matsumoto, 2001). Osawa & Matsumoto tively early event following Al exposure and (2001) demonstrated using various inhibitors appears to partly influence the Al-induced pro- of protein phosphorylation/dephosphory- duction of callose, but not the Al-induced inhi- lation that the inhibition of Al-responsive bition of root elongation. By comparison, the malate efflux in wheat is associated with pro- loss of plasma membrane integrity is a rela- tein phosphorylation, possibly related to an tively late event and seems to be a conse- organic anion-specific channel or its upstream quence of the cracks in the root formed by the signalling by a K-252a (a broad range inhibi- inhibition of root elongation.

9 Tor of protein kinases)-sensitive protein kinase. Using in-gel kinase assay with myelin basic protein (MBP) as an artificial substrate, SIGNAL TRANSDUCTION PATHWAY these authors observed activation of a 48-kDa protein kinase in the root apex treated with Stress recognition activates signal trans- 200 mM Al. The activity of this kinase was ele- duction pathways that transmit information vated from to 5 min after the addition of within individual cells and throughout the Al, and it diminished after 5 min. This sug- plant . These pathways lead to the expression gested that transient activation of the 48-kDa of genes and resultant modification of molecu- protein kinase might be involved in the early lar and cellular processes. In plants , there is physiological response to Al. The activity of little research on Al signalling mediated by the 48-kDa kinase was approximately 10-fold second messengers.

10 Higher after the treatment with Al than with- Experimental data suggest the existence of a out Al, and the Al-induced activation was lost cascade pathway under Al stress. An increase within 5 min. Al transiently activates this pro- in cytoplasmic Ca2+ level in wheat root apexes tein kinase quickly enough to precede the ini- may be related to the expression of Al toxicity tiation of malate efflux. This protein kinase (Zhang & Rengel, 1999). Osawa & Matsumoto phosphorylated MBP, indicating that this (2001) suggested that protein phosphoryla- kinase may be categorized in the MAP kinase tion is required for the signal transduction in group. Al-activated malate efflux and that malate In yeast, expression of a MAP kinase gene could pass through organic anion-specific complemented Al tolerance in an Al-sensitive channels. Because of its rapidness and speci- mutant, indicating that MAP kinase may be ficity to Al, Al-induced malate efflux is a useful associated with the expression of physiologi- system for studying how the Al signal is trans- cal responses involved in Al-resistance mitted into the cell that expresses physiologi- (Schott & Gardner, 1997).