Outside of organic acid release as a form of Al tolerance or resistance, a logical but unproven mechanism of Al tolerance is root-mediated alkalinization of the rhizosphere, since Al toxicity is dependent on the pH of the growth environment. Despite the appeal of this process as an Al tolerance mechanism, there is only one report that clearly demonstrates this role in Al tolerance. An Al tolerant mutant in Arabidopsis was shown to release similar amounts of organic acids to wild-type seedlings, indicating that this mutant has a different mechanism of Al tolerance. It was then found that its mechanism of Al tolerance was correlated with an Alactivated root apical H+ influx. This H+ influx resulted in an increase in rhizosphere pH at the surface of the root tip, which was significant enough to decrease Al activity around the root tip . In addition to the various resistance mechanisms described, there has been limited evidence that modification of extra- and intracellular anionic sites can have a positive impact on Al resistance. Polyamines are small aliphatic polycationic molecules that could compete with Al ions for binding sites at the cell wall and membrane to prevent Al from entering the cell . Plant polyamines are detected in actively growing tissues and under stress conditions. They also have been connected to the control of cell division, embryogenesis, root formation, fruit development and ripening, and responses to biotic and abiotic stresses .There have been two reports that describe the relationship between Al and polyamines; one report has demonstrated the positive effects of polyamines on Al tolerance, while another has discussed the effects of Al on cellular polyamines. In saffron, 1mM polyamines were able to reduce Al toxicity. Polyamines were also able to decrease H2O2 content in the presence of Al, as well as decrease Al accumulation at the roots . In cell cultures of a woody plant Catharanthus roseus, it was observed that polyamine levels increase upon Al exposure. Spermine levels increased by two- to three-fold after 24 and 48 hours of exposure to Al, and putrescine levels slightly increased after four hours of exposure,black flower buckets but was surprisingly followed by a sharp decrease . This suggests that even non-chelating molecules can have a significant impact on Al tolerance in plants. It has been argued based on these studies that Al exclusion must be a rapid response to minimize Al uptake and subsequent Al-dependent stress.
Interestingly, much of the findings on Al exclusion mechanisms have arisen from studies that move roots from a no Al environment to one that has highly toxic levels with the research focused on the immediate responses to Al. It is hard to imagine a real world situation in which roots go from an environment with little to no Al to one that has highly inhibitory concentrations. Therefore, it is arguable whether the approach of studying immediate responses to Al is necessarily relevant to Al toxicity in soils since stoppage of root growth in such an environment is likely due to chronic long-term exposure to Al. Consequently, it is of critical importance to determine the toxic effects of Al as it accumulates within plant tissue.It has been very difficult to determine other mechanisms of Al tolerance and resistance in agriculturally relevant plants due to issues such as genome size, availability of knockout lines, generation time, and difficulty in creating transgenic lines. The use of Arabidopsis thaliana has evaded this issue by utilizing the model plant that has a smaller diploid genome, an extensive library of knockout lines, and short generation time . Additionally Arabidopsis has similar sensitivity to Al in comparison to other crop plants and shows classic signs of Al toxicity, making Arabidopsis a suitable plant model for Al toxicity for crop species . The mechanisms of Al resistance have been intensively studied on crop species using natural genetic variation within and across species, such as wheat and maize. While clearly an insightful approach that has given extensive knowledge on Al exclusion mechanisms, this work is limited based on currently existing variability with regard to growth in the presence of Al. Beyond the obvious advantages of using a model species, Arabidopsis has a similar Al toxic threshold to many agriculturally relevant crop species making it a valuable system for investigating how plants sense and respond to Al through the identification of mutants with altered growth capabilities in the presence of Al . This has been particularly true with regard to identification ofAl sensitiveArabidopsis mutants, which have reduced root growth in the presence of Al likely due to deffects in mechanisms required for Al exclusion, Al detoxification, or response to Al-dependent damage.
By screening for Al sensitive Arabidopsis mutants, eight complementation groups were identified indicating that Al toxicity is complex, which is to be expected considering the likely number of factors involved in mechanisms of Al resistance and tolerance . Most importantly, as will be discussed later, identification of these als mutants has allowed for use of a suppressor mutagenesis approach that has resulted in identification of factors that are important for Al-dependent stoppage of root growth. In order to find factors that are required for Al stress response, a genetic approach was taken to identify Arabidopsis mutants that exhibit increased Al sensitivity. Mutant lines were generated through ethyl methanesulfonate mutagenesis of Arabidopsis thaliana ecotype Col-0 wt. M2 seedlings were subsequently screened for their response to Al by identifying seedlings with normal growth in the absence of Al, but restricted growth on low levels of Al. The seedlings were grown on a two-layer gel system, with the upper layer consisting of nutrient medium with no added Al and the lower layer consisting of the same nutrient medium equilibrated with a subtoxic level of AlCl3. Any seedlings that could grow normally through the upper layer but could not penetrate the lower layer were isolated. Each of these Al sensitivemutants likely represents deffects in genes that are required for mechanisms for Al resistance or tolerance. Two of the identified mutants, als1-1 and als3-1 have been studied in depth. Both of these mutations represent a recessive loss of function mutations resulting in greater than wild type root growth inhibition in the presence of sub-threshold levels of AlCl3. The first mutant characterized was als3-1 due to its extreme sensitivity to Al at low levels. When grown on Al asl3-1 shows complete arrest of growth of the primary root and shoot meristems. The roots of als3-1 are stunted and have a swollen club shaped root apex, with root hairs at or near the root tip when grown on Al media. Also, als3-1 roots do not initiate any lateral roots, but can produce secondary roots from the base of the hypocotyl. Growth of lateral roots can reinitiate if als3-1 plants are removed from Al media, but the primary root is irreversibly inhibited by the Al treatment. This response differs from the roots of wild type plants, which are able to fully recover from the Al treatment. Following Al treatment the shoot phenotype of als3-1 shows reduced cotyledon expansion. als3-1 shoots show a delayed growth recovery in comparison to the root, which does not recover at all. Leaf expansion is blocked for several days after the Al recovery.
In addition, the first true leaves of als3-1 develop abnormally following Al treatment. They are severely stunted with very few trichomes, poor leaf expansion,french flower bucket and irregular shaped epidermal cells with a rough leaf surface. The leaves that developed after Al treatment also do not expand but became a disorganized cluster of leaf pegs that eventually expand without petiole development. Eight days after removal from Al, a second shoot apex forms that develops relatively normally except for a greater number of rosette leaves and some fused inflorescences. This shoot phenotype is found to only in als3-1 plants that were challenged with Al and has not been described for als mutants in general. Since this mutation is completely Al-dependent, it was hypothesized that als3-1 represents a factor required for Al-tolerance or resistance. This factor was found to be specific for Al tolerance since als3-1 did not show increased sensitivity to other metals such as copper, nickel, cadmium or lanthanum and does not display any other growth deffects in low pH without Al. Staining of als3-1 roots with hematoxylin and morin, two stains that bind to Al, resulted in similar intensity of staining to wild type, suggesting that als3-1 mutation does not alter the amount of Al uptake . This was later confirmed using ICP-OES . Although there was no difference in the amount of Al uptake, when wild type and als3-1 roots were stained with hematoxylin, wild type plants showed a diffuse pattern of surface bound Al extending from the root apex to the mature region of the root, while als3-1 roots displayed intense staining just proximal to the root tip . Map-based cloning of als3-1 showed that it represents a defect in a gene that encodes an ABC-like transporter homologous to bacterial ybbM, which is a metal resistance protein from Escherichia coli. Based on this similarity and the localization pattern of ALS3, which shows it predominantly at the plasma membrane of root cortical cells and cells of the vasculature, it was proposed that it redistributes Al away from the most sensitive plant tissues in order to maintain cell division . Loss of ALS3 as in the als3-1 mutant would result in inappropriate accumulation of Al in vulnerable areas such as the root tip and would consequently cause growth arrest at levels of Al that have no measurable effect on wild type. GUS staining of plants harboring the ALS3 promoter fused with GUS indicates that ALS3 expression is localized primarily to the sieve tube elements of the phloem in all plant organs, and trichoblast cell files and immature root hairs. GUS activity was also found in the epithem tissue of the hydathodes but not in the actual water pore of the hydathode. Since Northern analysis determined that ALS3 is Al inducible, GUS analysis of Al treated lines resulted in a shift of expression from the root epidermis to the root cortex.
From these results, ALS3 was hypothesized to mediate Al transport within the plant, transporting Al from sensitive tissues from the plant such as the root apical meristem in order to sequester it in less sensitive tissues or also to the hydathodes for excretion by guttation. It is hypothesized that by disrupting this partial ABC transporter, there is inappropriate accumulation of Al in the root, leading to severe symptoms of Al toxicity . Consistent with the importance of ALS3 to Al tolerance, an ALS3 homolog was identified in rice, called STAR2. Although both ALS3 and STAR2 are required for plant Al tolerance, the expression patterns and cellular localization differ. STAR2 is only expressed in roots upon Al treatment and is located in all cell types except for the epidermal cells in the mature root zone . In contrast, ALS3 is expressed at a basal level in the vasculature throughout the plant and its expression is dramatically increased in the Arabidopsis root tip following exposure to Al . Similar to ALS3, STAR2 contains several transmembrane domains that likely form a pore or channel that is involved in substrate movement. Both ALS3 and STAR2 lack an ATPase domain, making them unusual with regard to ABC transporters that often have the transmembrane domains and ATPase domain all as part of one protein. While a separate ATPase domain containing protein partner has not been found for ALS3 , rice STAR2 was shown to interact with another protein, STAR1, which contains an ATPase domain . The STAR1/STAR2 complex functions together as a bacterial-type ABC transporter that is speculated to transport UDP-glucose, although it is currently unclear as to how the transport of UDP-glucose by STAR1/2 is responsible for rice Al tolerance . Other Arabidopsis mutants that have been identified with altered responses to Al include als1 and als7. Both als1 and als7 were identified in the original screen for Arabidopsis mutants with Al hypersensitivity. als1-1 was also identified by mapped based cloning and subsequently characterized. Similarly to als3- 1, als1-1 has an extreme increase in Al sensitivity.