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Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin.

Sun P, Tian QY, Chen J, Zhang WH - J. Exp. Bot. (2009)

Bottom Line: The Al(3+)-induced increase in DR5:GUS activity was reduced by AVG, while the Al(3+)-induced increase in EBS:GUS activity was not altered by NPA.Al(3+) and ACC increased transcripts of AUX1 and PIN2, and this effect was no longer observed in the presence of AVG and Co(2+).These findings indicate that Al(3+)-induced ethylene production is likely to act as a signal to alter auxin distribution in roots by disrupting AUX1- and PIN2-mediated auxin polar transport, leading to arrest of root elongation.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing, P.R. China.

ABSTRACT
Aluminium (Al) is phytotoxic when solubilized into Al(3+) in acidic soils. One of the earliest and distinct symptoms of Al(3+) toxicity is inhibition of root elongation. To decipher the mechanism by which Al(3+) inhibits root elongation, the role of ethylene and auxin in Al(3+)-induced inhibition of root elongation in Arabidopsis thaliana was investigated using the wild type and mutants defective in ethylene signalling (etr1-3 and ein2-1) and auxin polar transport (aux1-7 and pin2). Exposure of wild-type Arabidopsis to AlCl(3) led to a marked inhibition of root elongation, and elicited a rapid ethylene evolution and enhanced activity of the ethylene reporter EBS:GUS in root apices. Root elongation in etr1-3 and ein2-1 mutants was less inhibited by Al(3+) than that in wild-type plants. Ethylene synthesis inhibitors, Co(2+) and aminoethoxyvinylglycine (AVG), and an antagonist of ethylene perception (Ag(+)) abolished the Al(3+)-induced inhibition of root elongation. There was less inhibition of root elongation by Al(3+) in aux1-7 and pin2 mutants than in the wild type. The auxin polar transport inhibitor, naphthylphthalamic acid (NPA), substantially alleviated the Al(3+)-induced inhibition of root elongation. The Al(3+) and ethylene synthesis precursor aminocyclopropane carboxylic acid (ACC) increased auxin reporter DR5:GUS activity in roots. The Al(3+)-induced increase in DR5:GUS activity was reduced by AVG, while the Al(3+)-induced increase in EBS:GUS activity was not altered by NPA. Al(3+) and ACC increased transcripts of AUX1 and PIN2, and this effect was no longer observed in the presence of AVG and Co(2+). These findings indicate that Al(3+)-induced ethylene production is likely to act as a signal to alter auxin distribution in roots by disrupting AUX1- and PIN2-mediated auxin polar transport, leading to arrest of root elongation.

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Effect of (A) AVG, (B) Co2+, (C) AgNO3, and (D) NPA on root elongation in the absence and presence of 50 μM AlCl3 (pH 4.5). To minimize the effect of these chemical agents on Al3+ activity, seedlings were first exposed to 10 μM AVG (A), 10 μM CoCl2 (B), or 10 μM NPA (D) for 2 h followed by incubation in 50 μM AlCl3 for another 24 h. For treatment with Ag+, seedlings were first incubated in 10 μM AgNO3 and then exposed to 50 μM Al(NO3)3 for 24 h to determine the effect of Ag+ on root elongation of Arabidopsis wild-type (Col-0) (C). Root elongation was expressed relative to root elongation in the control solution (0.5 mM CaCl2, pH 4.5). Data are means ±SE of >8 roots.
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fig4: Effect of (A) AVG, (B) Co2+, (C) AgNO3, and (D) NPA on root elongation in the absence and presence of 50 μM AlCl3 (pH 4.5). To minimize the effect of these chemical agents on Al3+ activity, seedlings were first exposed to 10 μM AVG (A), 10 μM CoCl2 (B), or 10 μM NPA (D) for 2 h followed by incubation in 50 μM AlCl3 for another 24 h. For treatment with Ag+, seedlings were first incubated in 10 μM AgNO3 and then exposed to 50 μM Al(NO3)3 for 24 h to determine the effect of Ag+ on root elongation of Arabidopsis wild-type (Col-0) (C). Root elongation was expressed relative to root elongation in the control solution (0.5 mM CaCl2, pH 4.5). Data are means ±SE of >8 roots.

Mentions: The less inhibitory effect of Al3+ on root elongation in the Arabidopsis mutants insensitive to ethylene and auxin than that in wild-type plants suggests that both ethylene and auxin may be involved in Al-induced inhibition of root elongation. To verify this hypothesis, the effects of Al3+ on root elongation in the presence of antagonists of ethylene biosynthesis (AVG and Co2+) and ethylene perception (Ag+) were examined. The Al3+-induced inhibition of root elongation was markedly recovered when Arabidopsis seedlings were exposed to 10 μM AVG and CoCl2 for 12 h prior to treatment with Al3+ (Fig. 4A, B). In the absence of Al3+, AVG reduced root elongation by ∼35% (Fig. 4A), while CoCl2 had no effect on root elongation in the absence of Al3+ (Fig. 4B). A similar ameliorative effect on the inhibition of root elongation caused by Al3+ was also observed by treatment with the ethylene perception inhibitor, AgNO3 (Fig. 4C). As root elongation in aux1-7 and pin2 mutants was also less sensitive to Al3+ than in wild-type plants (Fig. 3), the effect of an antagonist of auxin polar transport, NPA, on root elongation in the absence and presence of Al3+ was studied. As shown in Fig. 4D, NPA marginally inhibited root growth in the absence of Al3+, while NPA substantially alleviated the Al-induced inhibition of root elongation.


Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin.

Sun P, Tian QY, Chen J, Zhang WH - J. Exp. Bot. (2009)

Effect of (A) AVG, (B) Co2+, (C) AgNO3, and (D) NPA on root elongation in the absence and presence of 50 μM AlCl3 (pH 4.5). To minimize the effect of these chemical agents on Al3+ activity, seedlings were first exposed to 10 μM AVG (A), 10 μM CoCl2 (B), or 10 μM NPA (D) for 2 h followed by incubation in 50 μM AlCl3 for another 24 h. For treatment with Ag+, seedlings were first incubated in 10 μM AgNO3 and then exposed to 50 μM Al(NO3)3 for 24 h to determine the effect of Ag+ on root elongation of Arabidopsis wild-type (Col-0) (C). Root elongation was expressed relative to root elongation in the control solution (0.5 mM CaCl2, pH 4.5). Data are means ±SE of >8 roots.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2803203&req=5

fig4: Effect of (A) AVG, (B) Co2+, (C) AgNO3, and (D) NPA on root elongation in the absence and presence of 50 μM AlCl3 (pH 4.5). To minimize the effect of these chemical agents on Al3+ activity, seedlings were first exposed to 10 μM AVG (A), 10 μM CoCl2 (B), or 10 μM NPA (D) for 2 h followed by incubation in 50 μM AlCl3 for another 24 h. For treatment with Ag+, seedlings were first incubated in 10 μM AgNO3 and then exposed to 50 μM Al(NO3)3 for 24 h to determine the effect of Ag+ on root elongation of Arabidopsis wild-type (Col-0) (C). Root elongation was expressed relative to root elongation in the control solution (0.5 mM CaCl2, pH 4.5). Data are means ±SE of >8 roots.
Mentions: The less inhibitory effect of Al3+ on root elongation in the Arabidopsis mutants insensitive to ethylene and auxin than that in wild-type plants suggests that both ethylene and auxin may be involved in Al-induced inhibition of root elongation. To verify this hypothesis, the effects of Al3+ on root elongation in the presence of antagonists of ethylene biosynthesis (AVG and Co2+) and ethylene perception (Ag+) were examined. The Al3+-induced inhibition of root elongation was markedly recovered when Arabidopsis seedlings were exposed to 10 μM AVG and CoCl2 for 12 h prior to treatment with Al3+ (Fig. 4A, B). In the absence of Al3+, AVG reduced root elongation by ∼35% (Fig. 4A), while CoCl2 had no effect on root elongation in the absence of Al3+ (Fig. 4B). A similar ameliorative effect on the inhibition of root elongation caused by Al3+ was also observed by treatment with the ethylene perception inhibitor, AgNO3 (Fig. 4C). As root elongation in aux1-7 and pin2 mutants was also less sensitive to Al3+ than in wild-type plants (Fig. 3), the effect of an antagonist of auxin polar transport, NPA, on root elongation in the absence and presence of Al3+ was studied. As shown in Fig. 4D, NPA marginally inhibited root growth in the absence of Al3+, while NPA substantially alleviated the Al-induced inhibition of root elongation.

Bottom Line: The Al(3+)-induced increase in DR5:GUS activity was reduced by AVG, while the Al(3+)-induced increase in EBS:GUS activity was not altered by NPA.Al(3+) and ACC increased transcripts of AUX1 and PIN2, and this effect was no longer observed in the presence of AVG and Co(2+).These findings indicate that Al(3+)-induced ethylene production is likely to act as a signal to alter auxin distribution in roots by disrupting AUX1- and PIN2-mediated auxin polar transport, leading to arrest of root elongation.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing, P.R. China.

ABSTRACT
Aluminium (Al) is phytotoxic when solubilized into Al(3+) in acidic soils. One of the earliest and distinct symptoms of Al(3+) toxicity is inhibition of root elongation. To decipher the mechanism by which Al(3+) inhibits root elongation, the role of ethylene and auxin in Al(3+)-induced inhibition of root elongation in Arabidopsis thaliana was investigated using the wild type and mutants defective in ethylene signalling (etr1-3 and ein2-1) and auxin polar transport (aux1-7 and pin2). Exposure of wild-type Arabidopsis to AlCl(3) led to a marked inhibition of root elongation, and elicited a rapid ethylene evolution and enhanced activity of the ethylene reporter EBS:GUS in root apices. Root elongation in etr1-3 and ein2-1 mutants was less inhibited by Al(3+) than that in wild-type plants. Ethylene synthesis inhibitors, Co(2+) and aminoethoxyvinylglycine (AVG), and an antagonist of ethylene perception (Ag(+)) abolished the Al(3+)-induced inhibition of root elongation. There was less inhibition of root elongation by Al(3+) in aux1-7 and pin2 mutants than in the wild type. The auxin polar transport inhibitor, naphthylphthalamic acid (NPA), substantially alleviated the Al(3+)-induced inhibition of root elongation. The Al(3+) and ethylene synthesis precursor aminocyclopropane carboxylic acid (ACC) increased auxin reporter DR5:GUS activity in roots. The Al(3+)-induced increase in DR5:GUS activity was reduced by AVG, while the Al(3+)-induced increase in EBS:GUS activity was not altered by NPA. Al(3+) and ACC increased transcripts of AUX1 and PIN2, and this effect was no longer observed in the presence of AVG and Co(2+). These findings indicate that Al(3+)-induced ethylene production is likely to act as a signal to alter auxin distribution in roots by disrupting AUX1- and PIN2-mediated auxin polar transport, leading to arrest of root elongation.

Show MeSH
Related in: MedlinePlus