Internal Detoxification Mechanism of Al in Hydrangea (Identification of Al Form in the Leaves)

Feng, Jian; Hiradate, Syuntaro; Nomoto, Kyosuke; Iwashita, Takasi; Matsumoto, Hideaki

doi:10.1104/pp.113.4.1033

Cited by 274 publications

(199 citation statements)

References 13 publications

Supporting

Mentioning

190

Contrasting

Unclassified

Order By: Relevance

“…The organic acid content of root tips was also investigated in response to Al exposure, as internal levels of Al-chelating organic acids have also been implicated in an internal Al tolerance mechanism in buckwheat (Fagopyrum esculentum) and hydrangea (Hydrangea macrophylla; Ma et al, 1997aMa et al, , 1997b. As shown in Figure 2B, exposure to increasing levels of Al elicited a strong (over 3-fold) increase in root tip citrate content.…”

Section: Resultsmentioning

confidence: 99%

The Physiology and Biophysics of an Aluminum Tolerance Mechanism Based on Root Citrate Exudation in Maize

Piñeros

Magalhães

Alves³

et al. 2002

Plant Physiology

189

164

View full text Add to dashboard Cite

Al-induced release of Al-chelating ligands (primarily organic acids) into the rhizosphere from the root apex has been identified as a major Al tolerance mechanism in a number of plant species. In the present study, we conducted physiological investigations to study the spatial and temporal characteristics of Al-activated root organic acid exudation, as well as changes in root organic acid content and Al accumulation, in an Al-tolerant maize (Zea mays) single cross (SLP 181/71 ϫ Cateto Colombia 96/71). These investigations were integrated with biophysical studies using the patch-clamp technique to examine Al-activated anion channel activity in protoplasts isolated from different regions of the maize root. Exposure to Al nearly instantaneously activated a concentration-dependent citrate release, which saturated at rates close to 0.5 nmol citrate h Ϫ1 root Ϫ1 , with the half-maximal rates of citrate release occurring at about 20 m Al 3ϩ activity. Comparison of citrate exudation rates between decapped and capped roots indicated the root cap does not play a major role in perceiving the Al signal or in the exudation process. Spatial analysis indicated that the predominant citrate exudation is not confined to the root apex, but could be found as far as 5 cm beyond the root cap, involving cortex and stelar cells. Patch clamp recordings obtained in whole-cell and outside-out patches confirmed the presence of an Al-inducible plasma membrane anion channel in protoplasts isolated from stelar or cortical tissues. The unitary conductance of this channel was 23 to 55 pS. Our results suggest that this transporter mediates the Al-induced citrate release observed in the intact tissue. In addition to the rapid Al activation of citrate release, a slower, Al-inducible increase in root citrate content was also observed. These findings led us to speculate that in addition to the Al exclusion mechanism based on root citrate exudation, a second internal Al tolerance mechanism may be operating based on Al-inducible changes in organic acid synthesis and compartmentation. We discuss our findings in terms of recent genetic studies of Al tolerance in maize, which suggest that Al tolerance in maize is a complex trait.Al limits crop production on the acid soils that comprise up to 50% of the world's potentially arable lands (von Uexkull and Mutert, 1995). When the soil pH drops below 5, the rhizotoxic Al species, Al 3ϩ , is solubilized into the soil solutions to levels that inhibit root growth and function. However, some plants have evolved Al tolerance mechanisms that enable them to grow in Al-toxic, acid soil environments (for review, see Kochian, 1995;Ma et al., 2001). Earlier work in this field showed that Al tolerance in wheat (Triticum aestivum) was associated with a reduced accumulation of Al in the root apex, but not the mature root (see, for example, Rincon and Gonzales, 1992;Tice et al., 1992; Delhaize et al., 1993a). Delhaize et al. (1993aDelhaize et al. ( , 1993b subsequently provided compelling evidence for the existence of an A...

show abstract

Section: Resultsmentioning

confidence: 99%

The Physiology and Biophysics of an Aluminum Tolerance Mechanism Based on Root Citrate Exudation in Maize

Piñeros

Magalhães

Alves³

et al. 2002

Plant Physiology

189

164

View full text Add to dashboard Cite

show abstract

“…Ma et al (1997aMa et al ( , 1997c identified forms of aluminumorganic acids compounds in the cell sap of hydrangea (Hydrangea macrophylla) and buckwheat leaves and proposed that these compounds might be sequestered in vacuoles. Later, Shen et al (2002) demonstrated that most aluminum and oxalate in the protoplasts of buckwheat leaves is present in the vacuoles.…”

Section: Discussionmentioning

confidence: 99%

“…The well-documented exclusion mechanism is to prevent aluminum from entering root cells by secretion of organic acid anions by the root apex, resulting in the formation of stable nonphytotoxic chelates with aluminum (Kochian, 1995;Ryan et al, 2001;Ma and Furukawa, 2003). The internal detoxification of aluminum is primarily based on the storage of aluminum in the vacuole as aluminum-oxalate (Ma et al, 1997a;Shen et al, 2002) or aluminum-citrate (Ma et al, 1997b) complexes, thus changing the distribution of aluminum within cells (Ma, 2000;Ma and Hiradate, 2000). Recently, some transporters involved in the aluminum distribution within cells have been identified.…”

mentioning

confidence: 99%

Coordination between Apoplastic and Symplastic Detoxification Confers Plant Aluminum Resistance

et al. 2013

View full text Add to dashboard Cite

Whether aluminum toxicity is an apoplastic or symplastic phenomenon is still a matter of debate. Here, we found that three auxin overproducing mutants, yucca, the recessive mutant superroot2, and superroot1 had increased aluminum sensitivity, while a transfer DNA insertion mutant, xyloglucan endotransglucosylase/hydrolases15 (xth15), showed enhanced aluminum resistance, accompanied by low endogenous indole-3-acetic acid levels, implying that auxin may be involved in plant responses to aluminum stress. We used yucca and xth15 mutants for further study. The two mutants accumulated similar total aluminum in roots and had significantly reduced cell wall aluminum and increased symplastic aluminum content relative to the wild-type ecotype Columbia, indicating that altered aluminum levels in the symplast or cell wall cannot fully explain the differential aluminum resistance of these two mutants. The expression of Al sensitive1 (ALS1), a gene that functions in aluminum redistribution between the cytoplasm and vacuole and contributes to symplastic aluminum detoxification, was less abundant in yucca and more abundant in xth15 than the wild type, consistent with possible ALS1 function conferring altered aluminum sensitivity in the two mutants. Consistent with the idea that xth15 can tolerate more symplastic aluminum because of possible ALS1 targeting to the vacuole, morin staining of yucca root tip sections showed more aluminum accumulation in the cytosol than in the wild type, and xth15 showed reduced morin staining of cytosolic aluminum, even though yucca and xth15 had similar overall symplastic aluminum content. Exogenous application of an active auxin analog, naphthylacetic acid, to the wild type mimicked the aluminum sensitivity and distribution phenotypes of yucca, verifying that auxin may regulate aluminum distribution in cells.Together, these data demonstrate that auxin negatively regulates aluminum tolerance through altering ALS1 expression and aluminum distribution within plant cells, and plants must coordinate exclusion and internal detoxification to reduce aluminum toxicity effectively.

show abstract

“…Since growth was decreased only by about 5% at that time, it would appear that low amounts of Al can be tolerated at the nucleus with minimal disruptions in function. It is conceivable that internal detoxification processes, perhaps the formation of non-toxic Al complexes (Ma et al, 1997;Watanabe et al, 1998) at the nuclear membrane surface, were helping to depress inhibitory effects.…”

Section: Discussionmentioning

confidence: 99%

Aluminum Accumulation at Nuclei of Cells in the Root Tip. Fluorescence Detection Using Lumogallion and Confocal Laser Scanning Microscopy

Silva¹,

Smyth²,

Moxley³

et al. 2000

Plant Physiology

146

View full text Add to dashboard Cite

The mechanistic basis for Al toxicity effects on root growth is still a matter of speculation, but it almost certainly involves decreased cell division at the root apex. In this series of experiments, we attempt to determine whether Al enters meristematic cells and binds to nuclei when roots are exposed to a low Al 3ϩ activity in solution. The methodology involved the use of the Al-sensitive stain lumogallion (3-[2,4 dihydroxyphenylazo]-2-hydroxy-5-chlorobenzene sulfonic acid), the DNA stain 4Ј,6-diamino-phenylindole, and confocal laser scanning microscopy. Soybean (Glycine max L. Merr.) cv Young (Al-sensitive) and PI 416937 (Al-tolerant) genotypes were exposed to 1.45 m Al 3ϩ for periods ranging from 30 min to 72 h, and then washed with 10 mm citrate to remove apoplastic Al. Fluorescence images show that within 30 min Al entered cells of the sensitive genotype and accumulated at nuclei in the meristematic region of the root tip. Substantial Al also was present at the cell periphery. The images indicated that the Al-tolerant genotype accumulated lower amounts of Al in meristematic and differentiating cells of the root tip and their cell walls. Collectively, the results support an important role for exclusion in Al tolerance.

show abstract

Internal Detoxification Mechanism of Al in Hydrangea (Identification of Al Form in the Leaves)

Cited by 274 publications

References 13 publications

The Physiology and Biophysics of an Aluminum Tolerance Mechanism Based on Root Citrate Exudation in Maize

The Physiology and Biophysics of an Aluminum Tolerance Mechanism Based on Root Citrate Exudation in Maize

Coordination between Apoplastic and Symplastic Detoxification Confers Plant Aluminum Resistance

Aluminum Accumulation at Nuclei of Cells in the Root Tip. Fluorescence Detection Using Lumogallion and Confocal Laser Scanning Microscopy

Contact Info

Product

Resources

About