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The Highly Charged Region of Plant β-type Phosphatidylinositol 4-kinase is Involved in Membrane Targeting and Phospholipid Binding

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Abstract

In Arabidopsis thaliana and Oryza sativa, two types of PI 4-kinase (PI4Ks) have been isolated and functionally characterized. The α-type PI4Ks (~220 kDa) contain a PH domain, which is lacking in β-type PI4Ks (~120 kDa). β-Type PI4Ks, exemplified by Arabidopsis AtPI4Kβ and rice OsPI4K2, contain a highly charged repetitive segment designated PPC (Plant PI4K Charged) region, which is an unique domain only found in plant β-type PI4Ks at present. The PPC region has a length of ~300 amino acids and harboring 11 (AtPI4Kβ) and 14 (OsPI4K2) repeats, respectively, of a 20-aa motif. Studies employing a modified yeast-based “Sequence of Membrane-Targeting Detection” system demonstrate that the PPC(OsPI4K2) region, as well as the former 8 and latter 6 repetitive motifs within the PPC region, are able to target fusion proteins to the plasma membrane. Further detection on the transiently expressed GFP fusion proteins in onion epidermal cells showed that the PPC(OsPI4K2) region alone, as well as the region containing repetitive motifs 1–8, was able to direct GFP to the plasma membrane, while the regions containing less repetitive motifs, i.e. 6, 4, 2 or single motif(s) led to predominantly intracellular localization. Agrobacterium-mediated transient expression of PPC-GFP fusion protein further confirms the membrane-targeting capacities of PPC region. In addition, the predominant plasma membrane localization of AtPI4Kβ was mediated by the PPC region. Recombinant PPC peptide, expressed in E. coli, strongly binds phosphatidic acid, PI and PI4P, but not phosphatidylcholine, PI5P, or PI(4,5)P2 in vitro, providing insights into potential mechanisms for regulating sub-cellular localization and lipid binding for the plant β-type PI4Ks.

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Abbreviations

PI:

phosphatidylinositol

PI4P:

PI 4-monophosphate

PI5P:

PI 5-monophosphate

PI(4,5)P2:

PI 4,5-bisphosphate

PI4K:

PI 4-kinase

PA:

phosphatidic acid

PAGE:

polyacrylamide gel electrophoresis

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Author notes

  1. Hui Ma

    Present address: ERRB, NICHD, Unit of Molecular Signal Transduction, Bldg 49, Rm 6C64, Bethesda, MD, 20892, USA

  2. Zhao-Qing Chu

    Present address: Temasek Life Sciences Laboratory, 1 Research Link, The National University of Singapore, 117604, Singapore

Authors and Affiliations

  1. National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Science (SiBS), Chinese Academy of Sciences; and Partner Group of Max–Planck-Institute of Molecular Plant Physiology (MPI-MP) on “Plant Molecular Physiology and Signal Transduction”, 300 Fenglin Road, Shanghai, 200032, P.R. China

    Ying Lou, Hui Ma, Wen-Hui Lin, Zhao-Qing Chu, Zhi-Hong Xu & Hong-Wei Xue

  2. Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Street 25, Haus 20, D-14476, Golm, Germany

    Bernd Mueller-Roeber

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  1. Ying Lou
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Correspondence to Hong-Wei Xue.

Additional information

The nucleotide sequences reported in this paper have been submitted to the GenBankTM/EMBL Data Bank under accession number AY536061 (highly charged region of OsPI4K2) and AJ277791 (partial cDNA of OsPI4K2).

Ying Lou and Hui Ma: These authors contributed equally

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Lou, Y., Ma, H., Lin, WH. et al. The Highly Charged Region of Plant β-type Phosphatidylinositol 4-kinase is Involved in Membrane Targeting and Phospholipid Binding. Plant Mol Biol 60, 729–746 (2006). https://doi.org/10.1007/s11103-005-5548-x

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