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

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-to-shoot 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 Al3+ 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 Al3+ 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.

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An exclusion mechanism is epistatic to an internal detoxification mechanism in aluminum resistance in Arabidopsis

10.21203/rs.2.15739/v1 ◽

2019 ◽

Author(s):

Yuqi Wang ◽

Wancong Yu ◽

Yu Cao ◽

Yanfei Cai ◽

Sangbom M. Lyi ◽

...

Keyword(s):

Cell Wall ◽

Root Cell ◽

Root Tip ◽

Biochemical Pathway ◽

Biochemical Pathways ◽

Detoxification Mechanism ◽

Exclusion Mechanism ◽

Detoxification Mechanisms ◽

Arabidopsis Plant ◽

Root Cell Wall

Abstract Background: In Arabidopsis, the aluminum (Al) exclusion mechanism is mainly facilitated by ALMT1-mediated malate exudation and MATE-mediated citrate releases from the root. Recently, we have demonstrated that coordinated functioning between the ALMT1-mediated exclusion mechanism, via exudation of malate from the root tip, and a NIP1;2-facilitated internal detoxification mechanism, via removal of Al from the root cell wall and subsequent root-to-shoot Al translocation, plays critical roles in achieving overall Al resistance. However, the genetic relationship between ALMT1 and NIP1;2 in these processes remained unclear. Results: Through genetic and physiological analyses, we demonstrate that unlike ALMT1 and MATE, which function independently and additively, ALMT1 and NIP1;2 show an epistatic relationship in Al resistance in Arabidopsis. These results indicate that ALMT1 and NIP1;2 function in the same biochemical pathway, whereas ALMT1 and MATE in different biochemical pathways.Conclusion: The establishment of the epistatic relationship and the coordinated functioning between the ALMT1 and NIP1;2-mediated exclusion and internal detoxification mechanisms are pivotal for achieving overall Al resistance in the non-accumulating Arabidopsis plant. We discuss and emphasize the indispensable roles of the root cell wall for the implementation of the Al exclusion mechanism and for the establishment of the epistatic relationship between the ALMT1-mediated exclusion mechanism and the NIP1;2-facilitated internal detoxification mechanism.

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HvHOX9, a novel homeobox leucine zipper transcription factor, positively regulates aluminum tolerance in Tibetan wild barley

Journal of Experimental Botany ◽

10.1093/jxb/eraa290 ◽

2020 ◽

Vol 71 (19) ◽

pp. 6057-6073

Author(s):

Xue Feng ◽

Wenxing Liu ◽

Huaxin Dai ◽

Yue Qiu ◽

Guoping Zhang ◽

...

Keyword(s):

Cell Wall ◽

Transcription Factor ◽

Leucine Zipper ◽

Wild Barley ◽

Critical Role ◽

Root Cell ◽

Root Tip ◽

Al Tolerance ◽

Tibetan Wild Barley ◽

Root Cell Wall

Abstract Aluminum (Al) toxicity is the primary limiting factor of crop production on acid soils. Tibetan wild barley germplasm is a valuable source of potential genes for breeding barley with acid and Al tolerance. We performed microRNA and RNA sequencing using wild (XZ16, Al-tolerant; XZ61, Al-sensitive) and cultivated (Dayton, Al-tolerant) barley. A novel homeobox-leucine zipper transcription factor, HvHOX9, was identified as a target gene of miR166b and functionally characterized. HvHOX9 was up-regulated by Al stress in XZ16 (but unchanged in XZ61 and Dayton) and was significantly induced only in root tip. Phylogenetic analysis showed that HvHOX9 is most closely related to wheat TaHOX9 and orthologues of HvHOX9 are present in the closest algal relatives of Zygnematophyceae. Barley stripe mosaic virus-induced gene silencing of HvHOX9 in XZ16 led to significantly increased Al sensitivity but did not affect its sensitivity to other metals and low pH. Disruption of HvHOX9 did not change Al concentration in the root cell sap, but led to more Al accumulation in root cell wall after Al exposure. Silencing of HvHOX9 decreased H+ influx after Al exposure. Our findings suggest that miR166b/HvHOX9 play a critical role in Al tolerance by decreasing root cell wall Al binding and increasing apoplastic pH for Al detoxification in the root.

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An exclusion mechanism is epistatic to an internal detoxification mechanism in aluminum resistance in Arabidopsis

10.21203/rs.2.15739/v3 ◽

2020 ◽

Author(s):

Yuqi Wang ◽

Wancong Yu ◽

Yu Cao ◽

Yanfei Cai ◽

Sangbom M. Lyi ◽

...

Keyword(s):

Cell Wall ◽

Genetic Relationship ◽

Root Cell ◽

Root Tip ◽

Biochemical Pathway ◽

Detoxification Mechanism ◽

Exclusion Mechanism ◽

Detoxification Mechanisms ◽

Arabidopsis Plant ◽

Root Cell Wall

Abstract Background: In Arabidopsis, the aluminum (Al) exclusion mechanism is mainly facilitated by ALMT1-mediated malate exudation and MATE-mediated citrate releases from the root. Recently, we have demonstrated that coordinated functioning between the ALMT1-mediated Al exclusion mechanism, via exudation of malate from the root tip, and a NIP1;2-facilitated internal detoxification mechanism, via removal of Al from the root cell wall and subsequent root-to-shoot Al translocation, plays critical roles in achieving overall Al resistance. However, the genetic relationship between ALMT1 and NIP1;2 in these processes remained unclear. Results: Through genetic and physiological analyses, we demonstrate that unlike ALMT1 and MATE, which function independently and additively, ALMT1 and NIP1;2 show an epistatic relationship in Al resistance. These results indicate that ALMT1 and NIP1;2 function in the same biochemical pathway, whereas ALMT1 and MATE in different ones.Conclusion: The establishment of the epistatic relationship and the coordinated functioning between the ALMT1 and NIP1;2-mediated exclusion and internal detoxification mechanisms are pivotal for achieving overall Al resistance in the non-accumulating Arabidopsis plant. We discuss and emphasize the indispensable roles of the root cell wall for the implementation of the Al exclusion mechanism and for the establishment of an epistatic relationship between the ALMT1-mediated exclusion mechanism and the NIP1;2-facilitated internal detoxification mechanism.

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An exclusion mechanism is epistatic to an internal detoxification mechanism in aluminum resistance in Arabidopsis

10.21203/rs.2.15739/v2 ◽

2020 ◽

Author(s):

Yuqi Wang ◽

Wancong Yu ◽

Yu Cao ◽

Yanfei Cai ◽

Sangbom M. Lyi ◽

...

Keyword(s):

Cell Wall ◽

Genetic Relationship ◽

Root Cell ◽

Root Tip ◽

Biochemical Pathway ◽

Detoxification Mechanism ◽

Exclusion Mechanism ◽

Detoxification Mechanisms ◽

Arabidopsis Plant ◽

Root Cell Wall

Abstract Background In Arabidopsis , the aluminum (Al) exclusion mechanism is mainly facilitated by ALMT1-mediated malate exudation and MATE-mediated citrate releases from the root. Recently, we have demonstrated that coordinated functioning between the ALMT1-mediated Al exclusion mechanism, via exudation of malate from the root tip, and a NIP1;2-facilitated internal detoxification mechanism, via removal of Al from the root cell wall and subsequent root-to-shoot Al translocation, plays critical roles in achieving overall Al resistance. However, the genetic relationship between ALMT1 and NIP1;2 in these processes remained unclear. Results Through genetic and physiological analyses, we demonstrate that unlike ALMT1 and MATE , which function independently and additively, ALMT1 and NIP1;2 show an epistatic relationship in Al resistance. These results indicate that ALMT1 and NIP1;2 function in the same biochemical pathway, whereas ALMT1 and MATE in different ones. Conclusion The establishment of the epistatic relationship and the coordinated functioning between the ALMT1 and NIP1;2-mediated exclusion and internal detoxification mechanisms are pivotal for achieving overall Al resistance in the non-accumulating Arabidopsis plant. We discuss and emphasize the indispensable roles of the root cell wall for the implementation of the Al exclusion mechanism and for the establishment of an epistatic relationship between the ALMT1-mediated exclusion mechanism and the NIP1;2-facilitated internal detoxification mechanism.

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An exclusion mechanism is epistatic to an internal detoxification mechanism in aluminum resistance in Arabidopsis

10.21203/rs.2.15739/v4 ◽

2020 ◽

Author(s):

Yuqi Wang ◽

Wancong Yu ◽

Yu Cao ◽

Yanfei Cai ◽

Sangbom M. Lyi ◽

...

Keyword(s):

Cell Wall ◽

Genetic Relationship ◽

Root Cell ◽

Root Tip ◽

Biochemical Pathway ◽

Detoxification Mechanism ◽

Exclusion Mechanism ◽

Detoxification Mechanisms ◽

Arabidopsis Plant ◽

Root Cell Wall

Abstract Background: In Arabidopsis, the aluminum (Al) exclusion mechanism is mainly facilitated by ALMT1-mediated malate exudation and MATE-mediated citrate releases from the root. Recently, we have demonstrated that coordinated functioning between the ALMT1-mediated Al exclusion mechanism, via exudation of malate from the root tip, and a NIP1;2-facilitated internal detoxification mechanism, via removal of Al from the root cell wall and subsequent root-to-shoot Al translocation, plays critical roles in achieving overall Al resistance. However, the genetic relationship between ALMT1 and NIP1;2 in these processes remained unclear. Results: Through genetic and physiological analyses, we demonstrate that unlike ALMT1 and MATE, which function independently and additively, ALMT1 and NIP1;2 show an epistatic relationship in Al resistance. These results indicate that ALMT1 and NIP1;2 function in the same biochemical pathway, whereas ALMT1 and MATE in different ones.Conclusion: The establishment of the epistatic relationship and the coordinated functioning between the ALMT1 and NIP1;2-mediated exclusion and internal detoxification mechanisms are pivotal for achieving overall Al resistance in the non-accumulating Arabidopsis plant. We discuss and emphasize the indispensable roles of the root cell wall for the implementation of the Al exclusion mechanism and for the establishment of an epistatic relationship between the ALMT1-mediated exclusion mechanism and the NIP1;2-facilitated internal detoxification mechanism.

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The Aluminum Distribution and Translocation in Two Citrus Species Differing in Aluminum Tolerance

10.21203/rs.3.rs-789821/v1 ◽

2021 ◽

Author(s):

Han Zhang ◽

Xin-yu Li ◽

Mei-lan Lin ◽

Ping-ping Hu ◽

Ning-wei Lai ◽

...

Keyword(s):

Cell Wall ◽

Lateral Root ◽

Lateral Roots ◽

Al Toxicity ◽

Root Cell ◽

Cell Organelle ◽

Citrus Species ◽

Al Tolerance ◽

Al Distribution ◽

Root Cell Wall

Abstract Background: Many citrus orchards of south China suffer from soil acidification, which induced aluminum (Al) toxicity. The Al-immobilization in vivo is crucial for Al detoxification. However, the distribution and translocation of excess Al in citrus species were not well illustrated.Results: The seedlings of ‘Xuegan’ [Citrus sinensis (L.) Osbeck] and ‘Shatianyou’ [Citrus grandis (L.) Osbeck] that differed in Al tolerance were hydroponically treated with nutrient solution (Control) or supplemented by 1.0 mM Al3+ (Al toxicity) for 21 days after three months of pre-culture. The Al distribution at the tissue level of citrus species following the order: lateral roots > primary roots > leaves > stems. The fragmentation of fresh lateral roots revealed the ratio of Al distribution at the cell wall, cell organelle and cytoplasmic supernatant was about 8:2:1 of two citrus species under Al stress. Besides, the Al distribution at the lateral root cell wall components suggested the pectin is the most Al-accumulating site in citrus species. Compared to C. grandis, C. sinensis had a significantly higher Al concentration on the cell wall of lateral roots whereas remarkably lower Al levels on the leaves and stems. Furthermore, the Al translocation revealed by the absorption kinetics of the cell wall demonstrated that C. sinensis had a higher Al retention and stronger Al affinity on the root cell wall than C. grandis. According to the FTIR (Fourier transform infrared spectroscopy) analysis, the Al distribution and translocation might be affected by modifying the structure and components of the citrus lateral root cell wall. Conclusions: A higher Al-retention, mainly targeted by the pectin of the root cell wall, and a lower Al translocation efficiency from roots to shoots contributed to a higher Al tolerance of C. sinensis than C. grandis.

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