JXB Advance Access originally published online on June 27, 2006
Journal of Experimental Botany 2006 57(11):2571-2576; doi:10.1093/jxb/erl021
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RESEARCH PAPER |
A putative acyl-CoA-binding protein is a major phloem sap protein in rice (Oryza sativa L.)
1Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan
2Department of Biological Production, Faculty of Bioresource Sciences, Akita Prefectural University, Akita-city, Akita, 010-0195, Japan
3Biotechnology Research Center, The University of Tokyo, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan
4PRESTO, JST, Honcho, Kawaguchi, Saitama, 332-0012 Japan
*Present address and to whom correspondence should be sent: Quantum Beam Science Directorate, Japan Atomic Energy Agency, 1233 Watanuki, Takasaki, Gunma 370-1207, Japan. E-mail: suzui.nobuo{at}jaea.go.jp
Received 28 December 2005; Accepted 11 April 2006
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Abstract |
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The N-terminal amino-acid sequence of a major rice phloem-sap protein, named RPP10, was determined. RPP10 is encoded by a single gene in the rice genome. Its complete amino-acid sequence, predicted from the corresponding rice full-length cDNA, showed high similarity to plant acyl-CoA-binding proteins (ACBPs). Western blot analysis using anti-ACBP antiserum revealed that putative ACBP is abundant in the phloem sap of rice plants, and is also present in sieve-tube exudates of winter squash (Cucurbita maxima), oilseed rape (Brassica napus), and coconut palm (Cocos nucifera). These findings give rise to the idea that ACBP may involve lipid metabolism and regulation in the phloem.
Key words: Acyl-CoA-binding protein, Oryza sativa, phloem, rice, sieve tube
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In vascular plants, the phloem plays an important role in long-distance translocation of assimilates and nutrients, i.e. sugars, amino acids, organic acids, and inorganic ions from source- to sink-organs. In addition to these low-molecular-weight compounds, macromolecules including proteins are present in phloem (for a review, Hayashi et al., 2000).
Sieve elements, the individual cell components of sieve tubes, are highly specialized for substance transport, and have lost most of their intracellular organelles, such as nuclei, vacuoles, Golgi bodies, and most ribosomes during the course of differentiation (Cronshaw, 1981). Enucleated mature sieve elements are thought to lack the capacity for protein synthesis (Oparka and Cruz, 2000). Therefore, proteins required for the maintenance of the physiological functions of sieve tubes are probably supplied from the neighbouring companion cells.
There is increasing evidence that phloem proteins are functionally translocated from organ to organ (Xoconostle-Cázares et al., 1999; Yoo et al., 2004; Gomez et al., 2005), and it is often the case that proteins form complexes with nucleic acids. Aoki et al. (2005) have reported that there is a destination-selective long-distance trafficking of phloem proteins. These findings provide insight into a novel function for phloem proteins as ‘long-distance information molecules’. Although various phloem proteins have been determined in recent studies, only three of them have been identified in rice plants, namely RPP13-1 a thioredoxin h (Ishiwatari et al., 1995), RPP31 a glutathione S-transferase (Fukuda et al., 2004a), and RPP23 a small heat-shock protein (Fukuda et al., 2004b).
In this study, a novel rice phloem protein, RPP10, was identified which shows high homology with an acyl-CoA-binding protein (ACBP), and it is shown that ACBP is present in sieve-tube exudates from winter squash (Cucurbita maxima), oilseed rape (Brassica napus), and coconut palm (Cocos nucifera). ACBP is a cytosolic protein that binds long-chain fatty acyl-CoA esters with high affinity (Knudsen et al., 1999) and is involved in intracellular trafficking of acyl-CoA esters (Rasmussen et al., 1994; Knudsen et al., 1994). Possible functions of ACBP in phloem are discussed.
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Materials and methods |
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Collection of phloem sap from rice plants
Rice plants (Oryza sativa L. cv. Kantou) were grown in hydroponic culture conditions in a temperature-controlled (30/25 °C, day/night) greenhouse. Phloem sap was collected from the leaf sheathes of 4–5-week-old plants through the cut ends of brown planthopper's stylets (Kawabe et al., 1980). All procedures for collecting phloem sap were carried out at 25 °C and 60% relative humidity under artificial light conditions (20 µmol photon s–1 m–1). Phloem sap samples were stored at –20 °C until analysis.
Analysis of the N-terminal amino-acid sequence of the phloem protein
Five hundred µl of rice phloem sap were centrifuged at 13 000 g for 20 min, and the supernatant fluid was concentrated by centrifugation at 13 000 g for 150 min through a 3 kDa molecular weight cutoff filter (Microcon; Millipore Co., Bedford, MA, USA). The concentrated fluids were subjected to two-dimensional polyacrylamide gel electrophoresis (2D-PAGE), as described by Nakamura et al. (1993). The separated proteins were electroblotted onto a PVDF (polyvinylidene difluoride) membrane (Immobilon; Millipore Co.), and stained with Coomassie Brilliant Blue G-250. The spot corresponding to RPP10 was cut out from the PVDF membrane and applied to a gas-phase protein sequencer (492HT; Applied Biosystems, Foster City, CA, USA).
Production of recombinant RPP10 protein
RPP10 cDNA was amplified by PCR using the rice EST clone S16207 (GenBank accession no C24929) as the template, and two primers, 5'-CGGGGTACCGACGACGACGACAAGATGGGTCTGCAGGAGGAT-3' and 5'- ATGCCATGGTTAAGAGGCTGCAGCAGC-3'. The nucleotide sequence of the amplified fragment was confirmed by sequencing analysis. The amplified fragment was digested with KpnI and NcoI, and subcloned into pET30b (Novagen Co., Darmstadt, Germany). E. coli strain BL21 DE3 (Novagene Co.) containing the resulting plasmid was cultured in LB medium at 26.5 °C, and induced with IPTG (isopropylthio-ß-D-galactoside). The E. coli cells were collected by centrifugation at 12 000 g for 10 min, resuspended in 0.5 ml of extract buffer (20 mM TRIS–HCl (pH 7.8) and 0.2 M NaCl), and lysed by sonication. Expressed His-tagged recombinant RPP10 protein was purified from the E. coli extract by a nickel column following the manufacturer's instructions (Novagen Co.) and subjected to the treatment of enterokinase (Novagen Co.) to cleave off the His-tag. The obtained recombinant RPP10 protein was used in the following western analysis.
Extraction of proteins from rice plants
Rice roots and leaves were homogenized in liquid nitrogen and mixed with extraction buffer (25 mM TRIS–HCl (pH 6.8), 5% (v/v) ß-mercaptoethanol, 5 mM p-amidinophenylmethylsulphonyl fluoride, and 25 µg ml–1 leupeptin). The homogenate was centrifuged twice at 12 000 g for 30 min and the supernatant was used for western analysis.
Collection of sieve-tube exudates from oilseed rape plants
Oilseed rape plants (Brassica napus L. cv. Nourin No. 16) were grown in the greenhouse (20/18 °C day/night) for 4 weeks under natural light conditions. Plants were grown hydroponically in 9 cm pots using a nutrient solution containing 0.5 mM NH4H2PO4, 3.0 mM KNO3, 2.0 mM Ca(NO3)2, 1.0 mM MgSO4, 0.09 mM Na2EDTA, 0.09 mM FeSO4, 22.5 µM H3BO3, 10 µM MnSO4, 0.1 µM (NH4)6Mo7O24, 0.35 µM ZnCl2, and 0.20 µM CuCl2. The pH of the solution was adjusted to 6.7 with 0.1 M NaOH. Before transfer of plants to the greenhouse, 2-week-old plants were placed in a cold room (5 °C) with a continuous light for 4 weeks in order to induce floral buds. Sieve-tube exudates were collected by cutting the buds. In order to avoid contamination from broken cells, sap samples collected for the first 5 min after cutting the buds were not used in the analysis. Collected samples were frozen at –20 °C until subsequent analysis.
Collection of sieve-tube exudates from coconut palm trees and winter squash plants
Coconut palm trees (Cocos nucifera) were grown at the Petchaburi Horticultural Experimental Station Center (in the Petchaburi district in Thailand) for six years on sandy loam soils, under natural climatic conditions. Exudate from these trees was taken from the tops of their fruit-bearing stems as described previously (Nakamura et al., 2004). Sieve-tube exudates from winter squash plants (Cucurbita maxima) obtained by cutting stems and petioles of a 6-week-old pumpkin plant, as described by Aoki et al. (2005), was provided by Dr K Aoki. These samples were stored at –20 °C prior to western blot analysis.
Western blot analysis
The protein content was determined by Coomassie staining using Protein Assay Reagent (BIO-RAD Co., Hercules, CA, USA). Proteins were separated by SDS-PAGE and transferred to PVDF membranes. ACBP was detected with rabbit antiserum raised against ACBP of Brassica napus (Brown et al., 1998), which was provided by Dr MJ Hills (John Innes Centre, UK), and goat anti-rabbit IgG (H+L) horseradish peroxidase conjugate (BIO-RAD Co.) as the secondary antibody. Immunoreactive bands were developed using the ECL detection system (Amersham Co., Bucks, UK) and quantified by densitometry using the ImageJ software (National Institute of Health, USA).
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Results |
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RPP10 is one of the most abundant rice phloem proteins
Rice phloem sap was fractionated by centrifugation into an insoluble precipitate and a soluble fraction. Proteins of the supernatant fraction were analysed by 2D-PAGE (Fig. 1). RPP10 was the most abundant protein, revealed by Coomassie staining, in this fraction. The spot corresponding to RPP10 was excised and subjected to Edman degradation sequencing and the N-terminal amino-acid sequence was determined as GLQEDFEQYAEKAKTLPEST.
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RPP10 shows high homology with ACBP
A TBLASTN search of the 20 amino-acid N-terminal sequence against the whole-genome sequence of rice (ftp://ftp.dna.affrc.go.jp/pub/RiceGAAS/20051115/) identified a single locus on chromosome 8 (GenBank accession no. BAC99898). The full-length cDNA (GenBank accession no. AK122061) transcribed from this locus has an open reading frame encoding a 91 amino acids polypeptide. The predicted molecular mass and isoelectric point is 10 kDa and 5.4, respectively, in agreement with those estimated from the spot position of RPP10 in the 2D-PAGE (Fig. 1).
Homology searches against the GenBank database showed that RPP10 shared high similarity with ACBPs. Sequence alignments (Fig. 2) indicate that RPP10 shares 49% amino-acid identity with yeast ACBP (Rose et al., 1992), and 71–86% with ACBP of Brassica napus (Hills et al., 1994), Arabidopsis thaliana (Engeseth et al., 1996), Digitalis lanata (Metzner et al., 2000), and Ricinus communis (Erber et al., 1997). The mature RPP10 isolated from sieve tubes did not have methionine at its N-terminus although the full-length rice ACBP cDNA encodes a N-terminal Met, suggesting that the methionine is removed post-translationally. This is also the case for ACBP of Arabidopsis thaliana and Brassica napus (Engeseth et al., 1996; Hills et al., 1994).
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The EST-clustering database, UniGene (http://www.ncbi.nlm.nih.gov/UniGene/) contains rice ESTs corresponding to RPP10 derived from cDNA libraries of various organs such as leaves, roots, and panicles, suggesting that RPP10 is expressed in these organs.
Distribution of RPP10 in rice plants
To determine the distribution of RPP10 in rice plant, western blot analysis was performed using antiserum against ACBP of Brassica napus, which cross-reacted with recombinant RPP10 produced in E. coli (Fig. 3). RPP10 detected in rice plants had a lower molecular mass than recombinant RPP10. RPP10 represented a larger proportion of phloem sap proteins than those of total proteins from roots and leaves.
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The intensity of immunostained RPP10 in phloem sap was estimated to represent 7.6 µg ml–1 (Fig. 4). Considering that the content of thioredoxin h, the major phloem sap protein, was 9.4 µg ml–1 in phloem sap (Fukuda et al., 2005), this result suggested that RPP10 was also one of the major proteins in rice phloem sap.
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ACBP exists in sieve tube exudates from various plants
Western blot analysis was also performed with proteins of sieve-tube exudates collected from Brassica napus, Cocos nucifera, and Cucurbita maxima (Fig. 5). Approximately 10 kDa proteins cross-reacted with antiserum against ACBP of Brassica napus was detected in all sieve-tube exudates examined. However, their molecular weights were slightly larger than the rice protein. This result, together with the result of Fig. 3, implies that ACBP in rice plants undergoes not only initial methionine removal, but other post-translational processing as well.
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Discussion |
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The sequence of RPP10 was determined from the soluble fraction of rice phloem sap, and it was demonstrated that this protein was homologous to plant ACBPs. RPP31 has previously been identified as glutathione S-transferase (Fukuda et al., 2004a) and RPP23 as a small heat-shock protein (Fukuda et al., 2004b) from the precipitated fraction of the same sample. In this study, RPP10, shown as a putative ACBP, is one of the major proteins in rice phloem sap.
ACBP is a highly conserved cytosolic lipid-binding protein that binds long-chain acyl-CoA esters with high affinity and is expressed in a wide variety of species in eukaryotes (for a review see Knudsen et al., 1999). The ability of ACBP to mediate intermembrane acyl-CoA transport in vitro (Rasmussen et al., 1994) and to create an intracellular acyl-CoA pool (Knudsen et al., 1994) indicates that ACBP is involved in intracellular trafficking of acyl-CoA esters. In plants, ACBP was firstly isolated from Brassica napus (Hills et al., 1994), and was shown to be expressed in developing embryo, flowers, cotyledons, and other tissues (Brown et al., 1998). In Arabidopsis thaliana, besides the cytosolic 10 kDa ACBP (Engeseth et al., 1996), there exists five larger ACBPs namely ACBP1 to ACBP5 (Chye, 1998; Li and Chye, 2003; Leung et al., 2004, 2005). Fatty acids in plants are synthesized de novo primarily in the plastid, and are condensed into acyl-CoA esters upon export to the cytosol, and subsequently transported into the endoplasmic reticulum (ER) for lipid biosynthesis and into mitochondria for ß-oxidation (Somerville et al., 2000). Plant ACBPs are thought to be involved in the transport of acyl-CoA esters from the plastid to the ER and mitochondria by associating acyl-CoA esters in the cytosol or in cytomembranes.
In this study, it is shown that an ACBP was present in the sieve-tube exudates from monocotyledonous (Oryza sativa, Cocos nucifera) and dicotyledonous (Cucurbita maxima, Brassica napus) plants (Fig. 5). Walz et al. (2004) also described in their recent proteomics report that sieve-tube exudates of Cucurbita maxima contained a protein with high similarity to ACBP. These findings suggest that ACBP ubiquitously functions in phloem across angiosperms.
Despite the degradation of several major organelles, mature sieve elements (SE) contain metabolically active mitochondria (Sjölund, 1997), and significant amounts of ATP have been detected in phloem sap (Ohshima et al., 1990). Although glyoxysomes have not been reported in sieve elements, acyl-CoA oxidase, which catalyses the first step in fatty acid degradation, has been detected in phloem cells (Agarwal et al., 2001). Therefore, it is reasonable to assume that acyl-CoA, which is synthesized in plastids of the neighbouring companion cells (CC), is transferred to mitochondria in the sieve element for ß-oxidation, and that ACBP mediates the SE-CC traffic via plasmodesmata in the form of acyl-CoA/ACBP complex.
On the other hand, it is interesting to note that ACBP, which mediates intracellular transport of acyl-CoA esters, exists in phloem, which is highly specialized for long-distance transport. These results raise the possibility that ACBP may mediate the translocation of acyl-CoA from the source-organ to the sink-organ which needs substrates for membrane synthesis. In addition, acyl-CoA esters are implicated in the regulation of several enzymes, including acyl-CoA synthetase, adenine nucleotide transporters, and protein kinase C in organisms other than plants (Hunt and Alexson, 2002). Fox et al. (2001) reported that long-chain acyl-CoA inhibited the uptake in vitro of glucose-6-phosphate into plastids isolated from Pisum sativum. These findings suggest that acyl-CoA esters are not only metabolic intermediates in lipid synthesis and degradation, but also regulators of lipid metabolism. This finding implies the possibility of inter-organ regulation of lipid metabolism mediated by ACBP in the sieve tubes.
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Acknowledgements |
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We thank Mr Y Okada for the gift of rice phloem sap and Dr K Aoki (RIKEN, Japan) for the gift of sieve-tube exudates of Cucurbita maxima. We also thank Dr Matthew J Hills (John Innes Centre, UK) for the gift of antiserum against ACBP of Brassica napus and the Rice Genome Research Program of Japan for rice EST clone (C24929).
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Footnotes |
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Present address: 694 Futago, Aki, Higashikunisaki, Oita 873-0356, Japan. 
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