Aluminum Targets Elongating Cells by Reducing Cell Wall Extensibility in Wheat Roots

Feng, Jian; Shen, Renfang; Nagao, Satoko; Tanimoto, Eiichi

doi:10.1093/pcp/pch060

Cited by 208 publications

(163 citation statements)

References 24 publications

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“…It has been suggested that the swollen and distorted root tip cells under Al stress are due, at least in part, to disruption of the cell wall structure, integrity, and function (SI Appendix, Fig. S6) (32)(33)(34). Therefore, limiting the accumulation of toxic Al 3+ in the root tip cell wall could help mitigate Al toxicity in plants.…”

Section: Discussionmentioning

confidence: 99%

NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance inArabidopsis

Wang

et al. 2017

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

133

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Members of the aquaporin (AQP) family have been suggested to transport aluminum (Al) in plants; however, the Al form transported by AQPs and the roles of AQPs in Al tolerance remain elusive. Here we report that NIP1;2, a plasma membrane-localized member of the Arabidopsis nodulin 26-like intrinsic protein (NIP) subfamily of the AQP family, facilitates Al-malate transport from the root cell wall into the root symplasm, with subsequent Al xylem loading and root-toshoot translocation, which are critical steps in an internal Al tolerance mechanism in Arabidopsis. We found that NIP1;2 transcripts are expressed mainly in the root tips, and that this expression is enhanced by Al but not by other metal stresses. Mutations in NIP1;2 lead to hyperaccumulation of toxic Al 3+ in the root cell wall, inhibition of root-to-shoot Al translocation, and a significant reduction in Al tolerance. NIP1;2 facilitates the transport of Al-malate, but not Al 3+ ions, in both yeast and Arabidopsis. We demonstrate that the formation of the Al-malate complex in the root tip apoplast is a prerequisite for NIP1;2-mediated Al removal from the root cell wall, and that this requires a functional root malate exudation system mediated by the Al-activated malate transporter, ALMT1. Taken together, these findings reveal a critical linkage between the previously identified Al exclusion mechanism based on root malate release and an internal Al tolerance mechanism identified here through the coordinated function of NIP1;2 and ALMT1, which is required for Al removal from the root cell wall, root-to-shoot Al translocation, and overall Al tolerance in Arabidopsis.aquaporin | nodulin 26-like protein | aluminum tolerance | organic acid exudation | malate

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Section: Discussionmentioning

confidence: 99%

NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance inArabidopsis

Wang

et al. 2017

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

133

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“…The cell wall is a major target for Al accumulation and Al toxicity in higher plants (23,24). The root, and more specifically, the root tip, is the primary site of Al toxicity, and the majority (∼90%) of the root Al resides in the cell wall (16,17).…”

Section: Discussionmentioning

confidence: 99%

Natural variation underlies alterations in Nramp aluminum transporter ( NRAT1 ) expression and function that play a key role in rice aluminum tolerance

Liu

Dong

et al. 2014

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

148

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Aluminum (Al) toxicity is a major constraint for crop production on acid soils which compose ∼40% of arable land in the tropics and subtropics. Rice is the most Al-tolerant cereal crop and offers a good model for identifying Al tolerance genes and mechanisms. Here we investigated natural variation in the rice Nramp aluminum transporter (NRAT1) gene encoding a root plasma membrane Al uptake transporter previously hypothesized to underlie a unique Al tolerance mechanism. DNA sequence variation in the NRAT1 coding and regulatory regions was associated with changes in NRAT1 expression and NRAT1 Al transport properties. These sequence changes resulted in significant differences in Al tolerance that were found to be associated with changes in the Al content of root cell wall and cell sap in 24 representative rice lines from a rice association panel. Expression of the tolerant OsNRAT1 allele in yeast resulted in higher Al uptake than did the sensitive allele and conferred greater Al tolerance when expressed in transgenic Arabidopsis. These findings indicate that NRAT1 plays an important role in rice Al tolerance by reducing the level of toxic Al in the root cell wall and transporting Al into the root cell, where it is ultimately sequestered in the vacuole. Given its ability to enhance Al tolerance in rice and Arabidopsis, this work suggests that the NRAT1 gene or its orthologs may be useful tools for enhancing Al tolerance in a wide range of plant species.aluminum transport | cell wall aluminum

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“…For example, Horst (1995) reported that aluminum bound to cell wall components increases wall rigidity, affects cell wall loosening, and thus ultimately inhibits root elongation. Ma et al (2004) demonstrated that aluminum decreases cell wall viscosity and elasticity, thus reducing cell wall extensibility, and, as a consequence, cell elongation is inhibited. Therefore, higher aluminum sensitivity is correlated with more aluminum accumulation in the cell wall, as demonstrated in maize (Zea mays) suspension cells (Schmohl and Horst, 2000) and intact root apices (Eticha et al, 2005a), rice , triticale (Liu et al, 2008), and rice bean (Vigna umbellata; Zhou et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

“…The cell wall is very complex in structure and composition. The binding of aluminum changes cell wall structure, makes the wall more rigid, and reduces mechanical extensibility and cell expansion (Tabuchi and Matsumoto, 2001;Ma et al, 2004). An aluminum-sensitive rice cultivar accumulates higher aluminum in the cell wall than an aluminum-resistant cultivar .…”

mentioning

confidence: 99%

Coordination between Apoplastic and Symplastic Detoxification Confers Plant Aluminum Resistance

et al. 2013

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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.

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Aluminum Targets Elongating Cells by Reducing Cell Wall Extensibility in Wheat Roots

Cited by 208 publications

References 24 publications

NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance inArabidopsis

NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance inArabidopsis

Natural variation underlies alterations in Nramp aluminum transporter ( NRAT1 ) expression and function that play a key role in rice aluminum tolerance

Coordination between Apoplastic and Symplastic Detoxification Confers Plant Aluminum Resistance

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