Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production

Illéš, Peter; Schlicht, Markus; Pavlovkin, Ján; Lichtscheidl, Irene; Baluška, Frantǐsek; Ovečka, Miroslav

doi:10.1093/jxb/erl197

Cited by 165 publications

(77 citation statements)

References 67 publications

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“…2). Interestingly, sites of NO synthesis also have been described in roots (19) where three local centers of NO production were detected: one at the root cap statocytes, another one at the QC and distal portion of the meristem, and the third, the most prominent, at the distal part of the transition zone. The different localization patterns of NO may mirror the diverse effects of NO on plant growth and development.…”

Section: Discussionmentioning

confidence: 87%

“…Sites of NO and other reactive oxygen species production in plant tissues can be identified by using the fluorescence indicator 4,5-diaminofluorescein diacetate (DAF-2DA) (17,19). DAF-2DA is a cell-permeable compound hydrolyzed inside the cells that emits fluorescence when nitrosylated by endogenous NO.…”

Section: Determination Of Endogenous No Abundance and Distribution Inmentioning

confidence: 99%

See 1 more Smart Citation

Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport

Fernández-Marcos

Sanz

Lewis

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

273

255

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Nitric oxide (NO) is considered a key regulator of plant developmental processes and defense, although the mechanism and direct targets of NO action remain largely unknown. We used phenotypic, cellular, and genetic analyses in Arabidopsis thaliana to explore the role of NO in regulating primary root growth and auxin transport. Treatment with the NO donors S-nitroso-N-acetylpenicillamine, sodium nitroprusside, and S-nitrosoglutathione reduces cell division, affecting the distribution of mitotic cells and meristem size by reducing cell size and number compared with NO depletion by 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO). Interestingly, genetic backgrounds in which the endogenous NO levels are enhanced [chlorophyll a/b binding protein underexpressed 1/NO overproducer 1 (cue1/nox1) mirror this response, together with an increased cell differentiation phenotype. Because of the importance of auxin distribution in regulating primary root growth, we analyzed auxin-dependent response after altering NO levels. Both elevated NO supply and the NO-overproducing Arabidopsis mutant cue1/nox1 exhibit reduced expression of the auxin reporter markers DR5pro:GUS/GFP. These effects were accompanied by a reduction in auxin transport in primary roots. NO application and the cue1/nox1 mutation caused decreased PIN-FORMED 1 (PIN1)-GFP fluorescence in a proteasome-independent manner. Remarkably, the cue1/nox1-mutant root phenotypes resemble those of pin1 mutants. The use of both chemical treatments and mutants with altered NO levels demonstrates that high levels of NO reduce auxin transport and response by a PIN1-dependent mechanism, and root meristem activity is reduced concomitantly.cell division and elongation | plant growth regulator | root development N itric oxide (NO) is a signaling molecule involved in a variety of physiological processes during plant growth and development and also is an important modulator of disease resistance. Extensive research has shown that NO is involved in the promotion of seed germination, photomorphogenesis, mitochondrial activity, leaf expansion, root growth, stomatal closure, fruit maturation, senescence, and iron metabolism (as reviewed in ref. 1). NO also is important for defense response, playing key roles in the activation of defense genes (e.g., pathogenesis-related protein 1), in phytoalexin production, and in modulation of programmed cell death (1-3). The mechanism for NO signal transduction, plant resistance to pathogens and cell death, cellular transport, basic metabolism, and photosynthesis frequently occurs through an NO-induced change in transcription (4).Additionally, NO is produced in plant tissues by two major pathways, one enzymatic and the other nonenzymatic (5). The enzymatic pathway of NO production is being studied thoroughly, and much information about the type and subcellular localization of the enzymes involved is available. Different enzymes have been identified that catalyze the synthesis of NO from two different substrates, nitrate and argi...

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Section: Discussionmentioning

confidence: 87%

Section: Determination Of Endogenous No Abundance and Distribution Inmentioning

confidence: 99%

Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport

Fernández-Marcos

Sanz

Lewis

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

273

255

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“…It plays crucial functions for the perception and response to a range of external factors, as for example mechanical stimuli 42 and aluminum toxicity. [46][47][48][49] This capability seems to be, at least in part, linked to the complex system of a polar auxin transport circuit. 42 Actually, since 1993 it has been evidenced that cells belonging to this zone are strongly auxin-responsive and accomplish dramatic rearrangements of the cytoskeleton, being subjected to a series of fundamental changes in their cytoarchitecture.…”

Section: The Root Transition Zonementioning

confidence: 99%

NO signaling is a key component of the root growth response to nitrate inZea maysL.

Trevisan

Manoli

Quaggiotti

2014

Plant Signaling & Behavior

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To search for nutrients and water, roots need to efficiently explore large soil volumes. To this aim they generate complex root systems, allowing them to maximize their resource allocation efficiency. 1 Despite the vital importance of roots, the difficulty in accessing intact root systems for analysis, particularly under field conditions, have slowed down the breeding programs for plant's adaptation to environmental restrictions. 2,3 The capacity of plants to take up nutrients and water is mainly determined by changes in the architecture of the root system. 1 Three major processes affect the overall architecture of the root system: the rate of cell division, the rate of cell differentiation, and the extent of expansion and elongation of cells. [4][5][6] Disturbs in any of these 3 processes can affect the whole root-system architecture and the capacity of plants to survive and develop in adverse environments (Giehl et al. 7 and references therein).The root system results from the coordinated control of both genetic endogenous programs (regulating growth and organogenesis) and the action of abiotic and biotic environmental stimuli. 8,9 The dynamic control of the overall root system architecture (RSA) throughout time finally determines root plasticity and allows plants to efficiently adapt to environmental constraints. 10 The soil-environment from which plants extract nutrients and water is extremely heterogeneous, both spatially and temporally. 11 Among the nutrients present in soil, nitrate (NO 3 − ) may vary by an order of magnitude within centimeters or over the course of a day. 12 The effects of NO 3 − on the root system are complex and depend on several factors, such as the concentration available to the plant, the endogenous nitrogen status and the sensitivity of the species. 10,13,14 A considerable part of the studies aimed to unravel the mechanisms controlling RSA growth and development in response to nitrate have been focused on lateral roots (LR), 8,13,[15][16][17][18][19][20] while the nitrate-regulation of the primary root growth is still unclear. Beside NO 3 − , auxin has been demonstrated to strongly affect and control the LR development, [21][22][23][24] and an increasing number of studies suggests an overlap between auxin and NO 3 − signaling pathways in controlling LR development. [25][26][27][28][29][30][31][32][33] NO 3 -has a Doubtful Role in Regulating the Growth of Primary RootsDespite the high amount of reports published on nitrate effects on root elongation, the lack of univocal results makes it difficult to clearly decipher this response ( Table 1). In Arabidopsis thaliana, inhibition of primary root growth has been observed when nitrate is applied homogeneously at high concentrations (50 mM) for 7 d, but not in a range between 0.1 and 10 mM. 35 On the contrary, in this same species Linkohr et al. 36 showed an inhibition of primary root elongation with the increase of nitrate concentration already beyond 0.01 mM, but in this case seedlings were IAA, indole-3-acetic acid; SNP, sodium n...

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“…The inhibition of root elongation has been widely used as a bioassay for Al toxicity (Delhaize and Ryan, 1995). The root apex is the major target site of Al toxicity ; in maize (Zea mays), the distal part of the root-apex transition zone (TZ), located between the apical meristem and the basal elongation region, is the most Al-sensitive part of the root (Sivaguru and Horst, 1998), and a similar zone is involved in both common bean (Phaseolus vulgaris) (Rangel et al, 2007) and Arabidopsis thaliana (Illés et al, 2006). The importance of the distal part of the root TZ in the response to Al toxicity has been confirmed in sorghum (Sorghum bicolor) by the demonstration that it is the site of reactive oxygen species production (Sivaguru et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

TAA1-Regulated Local Auxin Biosynthesis in the Root-Apex Transition Zone Mediates the Aluminum-Induced Inhibition of Root Growth inArabidopsis

et al. 2014

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The transition zone (TZ) of the root apex is the perception site of Al toxicity. Here, we show that exposure of Arabidopsis thaliana roots to Al induces a localized enhancement of auxin signaling in the root-apex TZ that is dependent on TAA1, which encodes a Trp aminotransferase and regulates auxin biosynthesis. TAA1 is specifically upregulated in the root-apex TZ in response to Al treatment, thus mediating local auxin biosynthesis and inhibition of root growth. The TAA1-regulated local auxin biosynthesis in the root-apex TZ in response to Al stress is dependent on ethylene, as revealed by manipulating ethylene homeostasis via the precursor of ethylene biosynthesis 1-aminocyclopropane-1-carboxylic acid, the inhibitor of ethylene biosynthesis aminoethoxyvinylglycine, or mutant analysis. In response to Al stress, ethylene signaling locally upregulates TAA1 expression and thus auxin responses in the TZ and results in auxin-regulated root growth inhibition through a number of auxin response factors (ARFs). In particular, ARF10 and ARF16 are important in the regulation of cell wall modification-related genes. Our study suggests a mechanism underlying how environmental cues affect root growth plasticity through influencing local auxin biosynthesis and signaling.

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Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production

Cited by 165 publications

References 67 publications

Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport

Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport

NO signaling is a key component of the root growth response to nitrate inZea maysL.

TAA1-Regulated Local Auxin Biosynthesis in the Root-Apex Transition Zone Mediates the Aluminum-Induced Inhibition of Root Growth inArabidopsis

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