JXB Advance Access originally published online on November 28, 2003
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Journal of Experimental Botany, Vol. 55, No. 394, pp. 137-143, January 1, 2004
© 2004 Oxford University Press
Plants and the Environment |
Identification of aluminium-regulated genes by cDNA-AFLP in rice (Oryza sativa L.): aluminium-regulated genes for the metabolism of cell wall components
Received 20 July 2003; Accepted 17 October 2003
The State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou 310029, PR China
* These authors contributed equally to this study. To whom correspondence should be addressed. Fax: +86 571 86971323. E-mail: docpwu{at}zju.edu.cn
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Abstract |
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Aluminium (Al) toxicity is the major factor limiting crop productivity in acid soils. To investigate the molecular mechanisms of Al toxicity and Al tolerance of rice, cDNA-amplified fragment length polymorphism (cDNA-AFLP) was used for identifying Al-regulated genes in roots of an Al-tolerant tropical upland rice, Azucena, and an Al-sensitive lowland rice, IR1552. Nineteen function-known genes were found among 34 transcript-derived fragments (TDFs) regulated by Al stress. The results indicate that Al stress could induce the biosynthesis of lignin and other cell wall components in roots. Temporal expression patterns of 14 genes were identified between the two varieties. In silico mapping was performed for all the 33 unique genes. Two genes for a function-unknown protein and for a ubiquitin-like protein, respectively, were mapped on the interval with the common QTL (quantitative trait loci) for Al tolerance in rice on chromosome 1.
Key words: Aluminium stress, cDNA-AFLP, cell wall components, Oryza sativa L.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Aluminium (Al) is the most abundant metal in the earth’s crust and is the major factor limiting crop productivity in acid soils, which comprises up to 40% of the world’s arable lands (Kochian, 1995). The abundance of Al products in the environment and the potential of Al as a plant growth inhibitor make it necessary to understand the mechanisms of Al phytotoxicity and Al tolerance of plant (Kochian, 1995).
The major symptom of Al toxicity is a rapid inhibition of root growth. Al accumulates rapidly in the apoplast, in the plasma membrane, and eventually enters the cytosol (Lazof et al., 1994). Many different mechanisms of Al toxicity have been hypothesized, including Al interactions with the root cell wall and Al interactions with symplasmic constituents such as the cytoskeleton etc. (Kochian, 1995). Alhough the mechanisms of Al toxicity have been studied by many researchers, the specific mechanism by which Al inhibits root elongation is still elusive (Matsumoto, 2000). It is still not clear whether Al affects the root symplastically or apoplastically, but the increased evidence supports the view that the apoplast plays the major role in Al perception (Horst, 1995).
Al tolerance has been speculated to be the result of either exclusion of Al from the root apex and/or the tolerance for symplasmic Al. Detoxification of Al in the rhizosphere by releasing organic acids to chelate Al has been reported in wheat and maize, while the detoxification of Al internally was also found by forming complexes with organic acids in plants (Ma et al., 2001). Rice was the most Al tolerance species among small-grain cereal crops (Foy, 1988). However, information on Al tolerance mechanisms in rice is limited. Ma et al. (2002) reported that no organic acid was induced by Al exposure, except citrate in small amounts in rice, and there was no significant effect on Al detoxification in both Al-tolerant and Al-sensitive varieties. It means that rice may have a different Al tolerance mechanism other than the release of organic acids.
Up to now, a number of Al-regulated genes has been reported from the roots of wheat (Snowden and Gardner, 1993; Richards et al., 1994; Hamel et al., 1998; Sasaki et al., 2002), Arabidopsis (Richards et al., 1998), rye (Milla et al., 2002), and sugarcane (Watt, 2003). However, most of these genes were also found to be responsive to other toxic metals, low Ca2+ levels, physical wounding (Snowden et al., 1995), oxidative stress (Watt, 2003), and pathogens (Hamel et al., 1998), and were expressed equally well in both Al-tolerant and Al-sensitive genotypes (Hamel et al., 1998). Up to now, there has been no Al-regulated gene reported in rice.
cDNA-amplified fragment length polymorphism (cDNA-AFLP) (Bachem et al., 1996) is an extremely efficient method for the isolation of differentially expressed genes, which gave reproducible results that were confirmed using RNA gel blot analysis (Bachem et al., 1996, 1998). It is a genome-wide expression analysis tool which does not require prior sequence information and therefore constitutes a useful tool for gene discovery (Ditt et al., 2001). In this study, cDNA-AFLP was used to identify differentially expressed genes from rice subjected to Al stress treatment. Thirty-four Al-regulated transcript derived fragments (TDFs) were isolated. The information from the genes may be helpful for a better understanding of the mechanisms of Al toxicity and the Al tolerance of rice and other plant species.
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Materials and methods |
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Plant material and culture experiment
According to previous work (Wu et al., 2000), an Al-tolerant upland tropical japonica (Oryza sativa L.) rice, Azucena, and an Al-sensitive indica rice, IR1552, were used in this study. Uniform seeds were rinsed with distilled water, and incubated with distilled water in the dark at 30 °C for 2 d. Germinated seeds were grown in distilled water for another 2 d at 27±2 °C. Seedlings were then transferred to plastic trays that were covered by a PVC sheet with a nylon mesh. Half-strength nutrient solution was used (Yoshida et al., 1976). The pH of the solution was adjusted daily to 4.0 with 1 mol l–1 NaOH or 1 mol l–1 HCl. Four-day-old seedlings were used for the Al-stress treatment. Seedlings were exposed to a 0.5 mmol l–1 CaCl2 solution (pH 4.0) for 2 h and then exposed to a 0.5 mmol l–1 CaCl2 solution (pH 4.0) containing 0 or 183 µmol l–1 AlCl3, with a free active Al3+ concentration of 100 µmol l–1 as determined by the Geochem-PC program (Parker et al., 1995). Roots and shoots of seedlings sampled at 0, 0.5, 2, 12, 24, and 48 h were cut, quickly frozen in liquid nitrogen, and stored at –70 °C for RNA extraction.
The experiment was conducted in a greenhouse under a diurnal photoperiod of 12 h light (158 µmol m–2 s–1). The daily maximum and minimum temperatures were 28 °C and 22 °C, respectively. The relative humidity ranged from 65% to 85%.
Root length measurements
The longest root of each seedling was measured after 60 h of growth in the control or Al stress solutions. The relative root elongation (RRE) was calculated as
RRE=(TAl–Tinitial)/(Ccontrol– Cinitial)
where T and C refer to the measured root lengths under Al-stress and control conditions, respectively.
cDNA-AFLP analysis
Total RNA was extracted from the roots, sampled at the five indicated time points, using Trizol reagent (Gibco, Germany) and poly (A)+ RNA was purified with the Oligotex mRNA Mini Kit (Qiagen, Germany). Treated RNA and control RNA of Azucena and IR1552 were prepared by pooling equal amounts of RNA at the four time points (0.5, 2, 12, and 24 h). Double-stranded cDNA was synthesized using the SMARTTM cDNA Library Construction Kit (Clontech, USA) according to the manufacturer’s instructions, purified by QIAquick PCR Purification Kit (Qiagen, Germany) and digested by the TaqI/AseI enzyme combination. AFLP reactions were performed according to the methods of Bachem et al. (1996). DNA fragments were visualized by silver staining according to the Silver SequenceTM DNA Sequencing System Technical Manual (Promega, USA).
Isolation and sequencing of TDFs
The Al-regulated TDFs were recovered by PCR under the same conditions used for the pre-amplification. Purified PCR products were ligated to the pUCm-T vector. The clones were sequenced using MegaBACETM 1000 (Amersham Pharmacia, USA).
Northern blot analysis and densitometry
Total RNA (20 µg) was separated by electrophoresis on a 1.2% formaldehyde agarose gel followed by blotting onto nylon membrane (Hybond-N+, Amersham Pharmacia, USA). Hybridization was performed as described previously (Sambrook and Russell, 2001). The hybridization signals were scanned by Typhoon 8600 scanner (Molecular Dynamics, USA) and quantified using the ImageQuant 5.0 software (Molecular Dynamics, USA). The signals obtained from the genes were weighted against those obtained from the 18s rRNA to correct for minor differences in RNA loading and normalized to that at 0 h of Azucena, which was set at 1 for each gene.
Gene function analysis
Database searches were performed using the BLAST Network Service (NCBI, National Center for Biotechnology Information) (http://www.ncbi.nlm.nih.gov/BLAST). The sequence of each TDF was searched against all sequences in the non-redundant databases using the BLASTN, BLASTX and TBLASTX algorithm, and in the EST database using the BLASTN program in turn. Sequences that; Returned with no significant homology were compared again against genomic sequence databases using the BLASTN program or Genomic BLAST pages. The retrieved genomic sequences were further annotated at the web site (http://ricegaas.dna.affrc.go.jp/) or analysed using the Genscan program (http://bioweb.pasteur.fr/seqanal/interfaces/genscan.html). The function of function-known genes (BLASTX and TBLASTX, E values less than 1e–5) (Ditt et al., 2001) was classified according to the putative function.
In silico mapping
The sequence of markers near the common QTL for Al tolerance in rice were obtained from the website (http://www.ncbi.nlm.nih.gov/). Rice bacterial artificial chromosome (BAC) clones were found, based on the sequence information or accession number of 33 TDFs and the markers, and were anchored to the Rice Genetic Map in silico (http://www.tigr.org/tdb/e2k1/osa1/sequencing.shtml).
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Results |
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Tolerance performance of the two varieties
An Al-tolerant upland japonica rice, Azucena, and an Al-sensitive lowland indica rice, IR1552, were used for the Al stress treatments using 100 µmol l–1 active Al3+ in this work. Root elongation was significantly inhibited by Al stress in the first 12 h in both varieties with RRE (relative root elongation) of 76% in Azucena and 34% in IR1552. The RRE was 89% in Azucena and 29% in IR1552 after the 48 h stress treatment.
Identification of Al-regulated genes
To analyse genes responsive to Al stress, cDNA-AFLP analysis was performed on roots of Azucena and IR1552 subjected to Al stress by a non-radioactive procedure. The differentially expressed fragments were investigated by selective amplification using 35 primer combinations. More than 2100 bands were generated and all the bands longer than 100 bp in length were compared in all four treatments: Azucena +/– Al and IR1552 +/– Al. Fragments up-regulated or down-regulated by Al in Azucena or IR1552, or in both were identified as Al-regulated TDFs. Thirty-four significantly Al-regulated TDFs ranging in length from 100 to 600 bp were cloned and sequenced, including three up-regulated TDFs in Azucena, one in IR1552, 29 in both varieties, and one down-regulated TDF in Azucena (Table 1). The clones corresponding to different TDFs were renamed as OsAR (Oryza sativa Al-regulated). OsAR7 and OsAR8 showed homology with different parts of p-coumarate 3-hydroxylase, suggesting that these two TDFs may be the same gene. Nineteen of the 33 unique genes showed significant homology with function-known genes by BLAST searches (Table 1). Ten TDFs with no significant homology with function-known protein and four TDFs with no match in the database were classified into a function-unknown gene and an unknown gene, respectively.
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Of the 19 function-known genes, seven genes were possibly involved in the metabolism of cell wall components, including lignin synthesis (OsAR4, OsAR5, OsAR6, and OsAR7), hemicellulose (OsAR9), glycoprotein (OsAR11), and other components (OsAR10). One gene is involved in oxidative stress (OsAR13). Nine genes are related to cellular metabolism (OsAR1, OsAR2 and OsAR3), retroelement (OsAR19), transcription (OsAR20), protein metabolism (OsAR14, OsAR15 and OsAR16), and the cell cycle (OsAR17). All the 17 genes were up-regulated by Al in both Azucena and IR1552 (Table 1). One TDF (OsAR18), up-regulated only in Azucena, showed homology to KN1-like protein. Another TDF (OsAR12), up-regulated in IR1552, is for the biosynthesis of taxol (Table 1).
Among the ten function-unknown genes and the four unknown genes, two genes (OsAR24 and OsAR34) and one gene (OsAR25) were up-regulated and down-regulated in Azucena, respectively, and 11 other genes were up-regulated in both Azucena and IR1552 (Table 1).
Temporal expression of some Al-regulated genes
To validate the Al-regulated genes and to analyse the temporal expression patterns, 17 genes, including seven genes for cell-wall-related functions (OsAR4 to OsAR11), one for taxol synthesis (OsAR12), one for cellular metabolism (OsAR1), two for protein metabolism (OsAR15, OsAR16), two for quinone oxidoreductase (OsAR13) and KN1-like protein (OsAR18), and four for unknown proteins (OsAR24, OsAR25, OsAR28, and OsAR29) with different expression patterns, were used for northern blotting analysis. The results were comparable to the expression patterns revealed by cDNA-AFLP except for OsAR25, which was inhibited by Al in both Azucena and IR1552, but no inhibition was revealed in IR1552 by cDNA-AFLP (Table 1; Figs 1, 2). The transcripts of three genes (OsAR1, OsAR12 and OsAR24) could not be detected in the northern blotting.
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For genes involved in cell wall metabolism (Fig. 1), three genes (OsAR9 to OsAR11) for the synthesis of hemicellulose, glycoprotein and other cell wall components, showed the same expression patterns in both Al-tolerant and Al-sensitive varieties with the highest up-regulation at 12 h (OsAR9) and 48 h (OsAR10 and OsAR11). Four genes (OsAR4 to OsAR7) for lignin synthesis showed different expression patterns in Al-tolerant and Al-sensitive varieties. OsAR6 and OsAR7 were up-regulated gradually up to 48 h in Azucena, but were up-regulated in IR1552 within 2 h then decreased. OsAR4 and OsAR5 showed a biphasic regulation in Azucena, transiently up-regulated within 2 h and decreased at 12 h and 24 h and then up-regulated again; in IR1552, they were transiently up-regulated within 0.5 h and then decreased and up-regulated again for OsAR5.
For genes involved in other metabolism pathways (Fig. 2), four (OsAR13, OsAR16, OsAR28, and OsAR29) showed similar expression patterns in Azucena and IR1552, with OsAR13 and OsAR16 up-regulated gradually after Al treatment, OsAR25 down-regulated, and OsAR29 showed a biphasic regulation which was up-regulated within 2 h and after 24 h, but decreased at 12 h. Three genes showed different temporal expression patterns in Azucena and IR1552. The gene for KN1-like protein (OsAR18) was up-regulated in Azucena, but not in IR1552. A function-unkown gene (OsAR28) was more strongly induced within 2 h in IR1552 than in Azucena and was more strongly induced at 48 h in Azucena than in IR1552. By contrast, the gene of the elongation factor EF-2 (OsAR15) was induced within 2 h in Azucena, but induced up to 48 h in IR1552.
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Discussion |
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cDNA-AFLP is an efficient method for the isolation of differentially expressed genes and this was confirmed by northern blotting analysis of 14 genes (42% of the 33 Al-regulated genes). Three of the 33 Al-regulated genes found are reported to be Al-regulated in wheat (Snowden and Gardner, 1993; Snowden et al., 1995; Cruz-Ortega et al., 1997), including phenylalanine ammonia-lyase, proteinase inhibitor and ß-1,3-glucanase. The result indicates that different crops may have similar Al-responsive mechanisms.
Al stress-induced genes for cell wall components
Nineteen function-known genes isolated here are involved in different metabolic pathways, which indicates that Al toxicity can affect different physiological and biochemical pathways. Seven of the 19 genes may function in modifying cell wall components (Table 1). Morphological and histological studies have revealed that Al stress could increase the amounts of certain cell wall components, such as polysaccharides and lignin (Eleftheriou et al., 1993; Sasaki et al., 1996).
Four genes (OsAR4, OsAR5, OsAR6, and OsAR7) encoding the enzymes catalysing different steps of lignin biosynthesis according to the lignin roadmap (Humphreys and Chapple, 2002) were up-regulated by Al stress in this work. Northern blotting analysis indicated that transcripts of these genes were accumulated to a much higher extent in roots than in shoots (data not shown). The Al-induced up-regulation of these genes was within 2 h in the Al-sensitive variety IR1552, and this was earlier than in the Al-tolerant variety Azucena. The transcripts of phenylalanine ammonia-lyase (OsAR5), a key enzyme that catalyses the first step of the phenylpropanoid pathway leading to lignin synthesis, was accumulated more in IR1552 than in Azucena (Fig. 1). Lignin is the principal structural component of plant cell walls. Various stress factors, including ion deficiency, invasion by fungal pathogens and wounding, can induce the deposition of lignin in cell walls. Research by Sasaki et al. (1996) indicated that the extent of growth inhibition is closely correlated with the extent of lignin deposition in both Al-tolerant and Al-sensitive varieties, and Al-sensitive varieties would accumulate more lignin in the roots than Al-tolerant varieties. This was in accordance with the expression of the genes.
Three genes for xylose isomerase (OsAR9), ß-1,3-glucanase (OsAR10) and UDP-N-acetylglucosamine (UDP-GlcNAc) pyrophosphorylase (OsAR11), were up-regulated by Al stress in both Al-tolerant and Al-sensitive varieties in this study. Xylose isomerase (OsAR9) catalyses the conversion of D-xylulose to D-xylose (http://www.brenda.uni-koeln.de/), which is a major constituent of hemicellulose. It coincided with the physiological phenomenon that Al can induce hemicellulose deposition in cell walls (Tabuchi and Matsumoto, 2001). ß-1,3-glucanase plays an important role in plant defence against pathongen attack. It is strongly induced when plants respond to wounding or infection by fungal, bacterial or viral pathogens (Leubner-Metzger and Meins, 1999). It was also induced by Al stress in wheat (Cruz-Ortega et al., 1997). It has been hypothesized that ß-1,3-glucanase contributes to the hydrolysis of cell wall components during seed germination (Leubner-Metzger and Meins, 1999) and suggested that it participates in the modification of cell wall components under Al stress. The UDP-N-acetylglucosamine (UDP-GlcNAc) pyrophosphorylase reversibly catalyses the synthesis of UDP-GlcNAc from UDP-GlcNAc-1-P and UTP (http://www.brenda.uni-koeln.de/). UDP-GlcNAc acts as a specific glycosyl donor for the biosynthesis of N- and O-linked glycoproteins (Piro et al., 1994), which is one of the plant cell wall components. The transcripts accumulated of the two genes, OsAR10 and OsAR11, increased with time of Al treatment, and the transcripts accumulation in the Al-sensitive variety was higher than that in Al-tolerant variety after 48 h (Fig. 1). It suggested that the up-regulation of the two genes should associate with the extent of Al toxicity.
Tabuchi and Matsumoto (2001) suggested that Al modifies the metabolism of cell wall components and thus makes the cell wall thick and rigid, which is supported by these results. Lignin, hemicellulose, glycoprotein, and other secondary metabolites deposition in the cell wall may thicken the cell wall and prevent Al from entering into the plasma membrane. However, it may also result in the arrest of root growth and cellular elongation (Le Van et al., 1994) and impose oxidative stress on the plant, which was implied by the up-regulation of the gene for quinone oxidoreductase (OsAR13), an enzyme believed to protect an organism against oxidative stress.
Temporal expression patterns of the genes result from Al toxicity
Among the 33 Al-regulated genes detected in this study, 28 genes were regulated by Al in both Al-tolerant and Al-sensitive varieties, suggesting that these genes result from Al-toxicity. Temporal expression patterns of 14 genes responsive to Al, including seven genes for cell wall metabolism, were revealed by northern blotting analysis (Figs 1, 2). Most of the blotted genes (OsAR9 to OsAR11, OsAR13, OsAR16, OsAR25, OsAR29) were regulated similarly in both Al-tolerant and Al-sensitive varieties and were induced after 12 h of Al stress, except for the gene for xylose isomerase (OsAR9) which was induced before 12 h, suggesting that they could be involved in the secondary mechanisms of Al toxicity. Different temporal expression patterns of the Al-induced genes in the Al-tolerant and Al-sensitive varieties were also found. This could be because of the different tolerance levels of the two rice varieties. On the other hand, the two rice varieties with different Al sensitivity were subjected to the same level of Al and this factor may also be contributing to the differences observed in expression patterns.
Candidate genes for Al tolerance
Thirty-three unique genes regulated by Al were isolated in this study, but no gene involved in organic acid synthesis and release was found. This result is consistent with other reports that no organic acid was released other than a small amount of citrate in rice under Al stress (Ma et al., 2002). It is reported that Al-regulated genes may have protective roles (Ezaki et al., 2000, 2001), which implies that Al-regulated genes can be tolerance genes. Up to now, several studies have reported QTL analysis for Al tolerance in rice. It will be very helpful for selecting candidate Al tolerance genes in rice from the Al-regulated genes.
All the Al-regulated genes were used for in silico mapping and 26 were mapped (data not shown). Two genes for a function-unknown protein (OsAR28) and for SUMO-1 (small ubiquitin-like modifier-1, OsAR16) were in silico mapped on the common QTL interval for Al tolerance in rice on chromosome 1 (Fig. 3). OsAR16 (112 bp) is for a ubiquitin-like protein SUMO-1 (a member of the SUMO conjugation system). The SUMO conjugation system appears to be a complex and functionally heterogeneous pathway for protein modification in plants. It may have important functions in stress protection and/or repair (Kurepa et al., 2003). However, it was expressed equally well in both Al-tolerant and Al-sensitive varieties (Fig. 2), and might be the result of Al toxicity. OsAR28 (181 bp) showed different expression patterns between Azucena and IR1552, its transcript accumulation increased gradually up to 48 h in Azucena, whereas in IR1552, it was up-regulated early (0.5 h) and then decreased gradually almost to the level of CK (0 h) (Fig. 1). It suggests that OsAR28 could be a candidate gene for Al tolerance from its different temporal expression patterns and its location on the QTL interval. To investigate the gene further for possible tolerance to Al toxicity in rice, transgenic work is being carried out.
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Acknowledgement |
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This research was funded by The National Science Foundation of China (No. 30070070).
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References |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Bahem CW, Oomen RJF, Visser RG. 1998. Transcript imaging with cDNA-AFLP: a step-by-step protocol. Plant Molecular Biology Reporter 16, 157–173.
Bachem CW, van der Hoeven RS, de Bruijn SM, Vreugdenhil D, Zabeau M, Visser RG. 1996. Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. The Plant Journal 9, 745–753.[CrossRef][Web of Science][Medline]
Cruz-Ortega R, Cushman JC, Ownby JD. 1997. cDNA clones encoding 1,3-beta-glucanase and a fimbrin-like cytoskeletal protein are induced by Al toxicity in wheat roots. Plant Physiology 114, 1453–1460.[Abstract]
Ditt RF, Nester EW, Comai L. 2001. Plant gene expression response to Agrobacterium tumefaciens. Proceedings of the National Academy of Sciences, USA 98, 10954–10959.
Eleftheriou E, Moustakas M, Fragiskos N. 1993. Aluminate-induced changes in morphology and ultrastructure of Thinopyrum roots. Journal of Experimental Botany 44, 427–436.
Ezaki B, Gardner RC, Ezaki Y, Matsumoto H. 2000. Expression of aluminium-induced genes in transgenic Arabidopsis plants can ameliorate aluminium stress and/or oxidative stress. Plant Physiology 122, 657–665.
Ezaki B, Katsuhara M, Kawamura M, Matsumoto H. 2001. Different mechanisms of four aluminium (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiology 127, 918–927.
Foy CD. 1988. Plant adaptation to acid, aluminium-toxic soils. Communications in Soil Science and Plant Analysis 19, 959–987.
Hamel F, Breton C, Houde M. 1998. Isolation and characterization of wheat aluminium-regulated genes: possible involvement of aluminium as a pathogenesis response elicitor. Planta 205, 531–538.[CrossRef][Web of Science][Medline]
Horst WJ. 1995. The role of the apoplast in aluminium toxicity and resistance of higher plants: a review. The Journal of Plant Nutrition and Soil Science 158, 419–428.
Humphreys JM, Chapple C. 2002. Rewriting the lignin roadmap. Current Opinion in Plant Biology 5, 224–229.[CrossRef][Web of Science][Medline]
Kochian LV. 1995. Cellular mechanisms of aluminium toxicity and resistance in plants. Annual Reveiw of Plant Physiology and Plant Molecular Biology 46, 237–260.
Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD. 2003. The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO-1 and -2 conjugates is increased by stress. Journal of Biological Chemistry 278, 6862–6872.
Lazof DB, Goldsmith JG, Rufty TW, Linton RW. 1994. Rapid uptake of aluminium into cells of intact soybean root tips (a microanalytical study using secondary ion mass spectrometry). Plant Physiology 106, 1107–1114.[Abstract]
Le Van H, Kuraishi S, Sakurai N. 1994. Aluminium-induced rapid root inhibition and changes in cell-wall components of squash seedlings. Plant Physiology 106, 971–976.[Abstract]
Leubner-Metzger G, Meins FJ. 1999. Functions and regulation of plant ß-1,3-glucanases (PR-2). In: Datta SK, Muthukrishnan S, eds. Pathogenesis-related proteins in plants. Boca Raton, FL: CRC Press, 49–76.
Ma JF, Ryan PR, Delhaize E. 2001. Aluminium tolerance in plants and the complexing role of organic acids. Trends in Plant Science 6, 273–278.[CrossRef][Web of Science][Medline]
Ma JF, Shen R, Zhao Z, Wissuwa M, Takeuchi Y, Ebitani T, Yano M. 2002. Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant and Cell Physiology 43, 652–659.
Matsumoto H. 2000. Cell biology of aluminium toxicity and tolerance in higher plants. International Review of Cytology 200, 1–46.[CrossRef][Web of Science][Medline]
Milla MAR, Butler E, Huete AR, Wilson CF, Anderson O, Gustafson JP. 2002. Expressed sequence tag-based gene expression analysis under aluminium stress in rye. Plant Physiology 130, 1706–1716.
Nguyen VT, Burow MD, Nguyen HT, Le BT, Le TD, Paterson AH. 2001. Molecular mapping of genes conferring aluminium tolerance in rice (Oryza sativa L.). Theoretical and Applied Genetics 102, 1002–1010.[CrossRef]
Nguyen VT, Nguyen BD, Sarkarung S, Martinez C, Paterson AH, Nguyen HT. 2002. Mapping of genes controlling aluminium tolerance in rice:comparison of different genetic backgrounds. Molecular Genetics and Genomics 267, 772–780.[CrossRef][Web of Science][Medline]
Parker D, Norvell W, Chaney R. 1995. Geochem-PC: a chemical speciation program for IBM-compatibles. In: Loeppert RH, Schwab AP, Goldberg S, eds. Chemical equilibrium and reaction models. Madison, WI: Soil Science Society of America, 253–269.
Piro G, Buffo M, Dalessandro G. 1994. Membrane-bound glucosamine acetyltransferase in coleoptile segments of Avena sativa. Physiologia Plantarum 90, 181–186.[CrossRef]
Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC. 1998. Aluminium induces oxidative stress genes in Arabidopsis thaliana. Plant Physiology 116, 409–418.
Richards KD, Snowden KC, Gardner RC. 1994. Wali6 and wali7, genes induced by aluminium in wheat (Triticum aestivum L.) roots. Plant Physiology 105, 1455–1456.[CrossRef][Web of Science][Medline]
Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory Press.
Sasaki M, Yamamoto Y, Matsumoto H. 1996. Ligin deposition induced by aluminium in wheat (Triticum aestivum) roots. Physiologia Plantarum 96, 193–198.[CrossRef]
Sasaki T, Ezaki B, Matsumoto H. 2002. A gene encoding multidrug resistance (MDR)-like protein is induced by aluminium and inhibitors of calcium flux in wheat. Plant and Cell Physiology 43, 177–185.
Snowden KC, Gardner RC. 1993. Five genes induced by aluminium in wheat (Triticum aestivum L.) roots. Plant Physiology 103, 855–861.[Abstract]
Snowden KC, Richards KD, Gardner RC. 1995. Aluminium-induced genes (induction by toxic metals, low calcium, and wounding and pattern of expression in root tips). Plant Physiology 107, 341–348.[Abstract]
Tabuchi A, Matsumoto H. 2001. Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminium-induced growth inhibition. Physiologia Plantarum 112, 353–358.[CrossRef][Medline]
Watt DA. 2003. Aluminium-responsive genes in sugarcane: identification and analysis of expression under oxidative stress. Journal of Experimental Botany 54, 1163–1174.
Wu P, Liao CY, Hu B, Yi KK, Jin WZ, Ni JJ, He C. 2000. QTLs and epistasis for aluminium tolerance in rice (Oryza sativa L) at different seedling stages. Theoretical and Applied Genetics 100, 1295–1303.[CrossRef]
Yoshida S, Forno D, Cock J, Gomez K. 1976. Laboratory manual for physiological studies of rice. Manila, Philippines: International Rice Research Institute.
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L. Gutierrez, G. Conejero, M. Castelain, S. Guenin, J.-L. Verdeil, B. Thomasset, and O. Van Wuytswinkel Identification of new gene expression regulators specifically expressed during plant seed maturation J. Exp. Bot., June 1, 2006; 57(9): 1919 - 1932. [Abstract] [Full Text] [PDF]
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N. Fusco, L. Micheletto, G. Dal Corso, L. Borgato, and A. Furini Identification of cadmium-regulated genes by cDNA-AFLP in the heavy metal accumulator Brassica juncea L. J. Exp. Bot., November 1, 2005; 56(421): 3017 - 3027. [Abstract] [Full Text] [PDF]
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