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Lack of the Golgi phosphate transporter PHT4;6 causes strong developmental defects, constitutively activated disease resistance mechanisms and altered intracellular phosphate compartmentation in Arabidopsis


Hassler, Sebastian; Lemke, Lilia; Jung, Benjamin; Möhlmann, Torsten; Krüger, Falco; Schumacher, Karin; Espen, Luca; Martinoia, Enrico; Neuhaus, H Ekkehard (2012). Lack of the Golgi phosphate transporter PHT4;6 causes strong developmental defects, constitutively activated disease resistance mechanisms and altered intracellular phosphate compartmentation in Arabidopsis. The Plant Journal, 72(5):732-744.

Abstract

The Golgi-located phosphate exporter PHT4;6 has been described as involved in salt tolerance but further analysis on the physiological impact of PHT4;6 remained elusive. Here we show that PHT4;6-GFP is targeted to the trans-Golgi compartment and that loss of function of this carrier protein has a dramatic impact on plant growth and development. Knockout mutants of pht4;6 exhibit a dwarf phenotype that is complemented by the homologous gene from rice (Oryza sativa). Interestingly, pht4;6 mutants show altered characteristics of several Golgi-related functions, such as an altered abundance of certain N-glycosylated proteins, altered composition of cell-wall hemicelluose, and higher sensitivity to the Golgi α-mannosidase and the retrograde transport inhibitors kifunensine and brefeldin A, respectively. Moreover, pht4;6 mutants exhibit a 'mimic disease' phenotype accompanied by constitutively activated pathogen defense mechanisms and increased resistance against the virulent Pseudomonas syringae strain DC3000. Surprisingly, pht4;6 mutants also exhibit phosphate starvation symptoms, as revealed at the morphological and molecular level, although total Pi levels in wild-type and pht4;6 plants are similar. This suggested that subcellular Pi compartmentation was impaired. By use of nuclear magnetic resonance (NMR), increased Pi concentration was detected in acidic compartments of pht4;6 mutants. We propose that impaired Pi efflux from the trans-Golgi lumen results in accumulation of inorganic phosphate in other internal compartments, leading to low cytoplasmic phosphate levels with detrimental effects on plant performance.

Abstract

The Golgi-located phosphate exporter PHT4;6 has been described as involved in salt tolerance but further analysis on the physiological impact of PHT4;6 remained elusive. Here we show that PHT4;6-GFP is targeted to the trans-Golgi compartment and that loss of function of this carrier protein has a dramatic impact on plant growth and development. Knockout mutants of pht4;6 exhibit a dwarf phenotype that is complemented by the homologous gene from rice (Oryza sativa). Interestingly, pht4;6 mutants show altered characteristics of several Golgi-related functions, such as an altered abundance of certain N-glycosylated proteins, altered composition of cell-wall hemicelluose, and higher sensitivity to the Golgi α-mannosidase and the retrograde transport inhibitors kifunensine and brefeldin A, respectively. Moreover, pht4;6 mutants exhibit a 'mimic disease' phenotype accompanied by constitutively activated pathogen defense mechanisms and increased resistance against the virulent Pseudomonas syringae strain DC3000. Surprisingly, pht4;6 mutants also exhibit phosphate starvation symptoms, as revealed at the morphological and molecular level, although total Pi levels in wild-type and pht4;6 plants are similar. This suggested that subcellular Pi compartmentation was impaired. By use of nuclear magnetic resonance (NMR), increased Pi concentration was detected in acidic compartments of pht4;6 mutants. We propose that impaired Pi efflux from the trans-Golgi lumen results in accumulation of inorganic phosphate in other internal compartments, leading to low cytoplasmic phosphate levels with detrimental effects on plant performance.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Plant and Microbial Biology
Dewey Decimal Classification:580 Plants (Botany)
Language:English
Date:2012
Deposited On:25 Feb 2013 08:01
Last Modified:05 Apr 2016 16:32
Publisher:Wiley-Blackwell
ISSN:0960-7412
Publisher DOI:https://doi.org/10.1111/j.1365-313X.2012.05106.x
PubMed ID:22788523

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