JXB Advance Access originally published online on December 1, 2008
Journal of Experimental Botany 2009 60(2):557-565; doi:10.1093/jxb/ern298
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RESEARCH PAPER |
Proton pump OsA8 is linked to phosphorus uptake and translocation in rice
1State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China
2College of Agronomy, Hainan University, Danzhou, Hainan, 571737, China
To whom correspondence should be addressed: E-mail: ghxu{at}njau.edu.cn
Received 25 July 2008; Revised 29 October 2008 Accepted 31 October 2008
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Abstract |
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The plasma membrane (PM) proton pump ATPases (H+-ATPases) are involved in almost all aspects of biology. They are plant specific and several members of this family are supposed to play a key role in nutrient acquisition. At present, only some members of this gene family in plants have been characterized. However, no nutrient uptake associated H+-ATPase gene in rice has been functionally analysed. It is reported here that OsA8, a typical PM H+-ATPases gene that was predominantly expressed in roots of rice, is down-regulated by nutrient deficiency. The Osa8 mutant had a relatively smaller size and root to shoot biomass ratio, but higher ATPase activity than its wild-type counterparts under phosphorus (P) starvation conditions. Knockout of OsA8 affected the expression of several OsA genes and the high affinity phosphate transporter, OsPT6, and resulted in a higher P concentration in the roots and a lower amount of P in the shoots. These analyses demonstrate that OsA8 not only influences the uptake of P by roots, but also the translocation of P from the roots to the shoots in rice.
Key words: Knockout mutant, plasma membrane H+-ATPase, Oryza sativa, phosphorus, Tos17 retrotransposon, phosphate transporter
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary dataReferences |
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The P-type (plasma membrane type) ATPases, which share a common enzymatic mechanism of a phosphorylation reaction-cycle intermediate (Baxter et al., 2003), are supposed to function exclusively on the plasma membrane (Palmgren and Harper, 1999; Arango et al., 2003; Sondergaard et al., 2004). Based to their function, they are classified into five distinct groups of pumps that translocate heavy metals (P1B, HMA), Ca2+ (P2A,2B, ECA, ACA), H+ (P3A, AHA), putative aminophospholipid (P4, ALA), and unknown specificity (P5), respectively (Axelsen and Palmgren, 1998, 2001).
As a primary transporter, P-type H+-ATPases (P3A) mediate ATP-dependent H+ extrusion to the extracellular space, a process that generates pH and electrical potential difference across the PM (Arango et al., 2003; Ueno et al., 2005), and this difference works as the motive force for a large set of secondary transporters, including symporter, antiporter, or uniporter, to drive their substrates against their concentration gradients (Palmgren, 2001; Requena et al., 2003; Hirano and Hirano, 2004). Therefore, the H+-ATPase acts as a transducer: converting the chemical energy released from ATP hydrolysis into chemiosmotic energy (Arango et al., 2003).
P-type H+-ATPases are found to exist in almost all the cell types of plants that are investigated, and their basic function is the coupling ATP hydrolysis and H+-pumping. In general, the cells undergoing active metabolism have much higher activity of H+-ATPase than others (Palmgren, 2001; Arango et al., 2003; Sondergaard et al., 2004). Moreover, H+-ATPase-mediated transport is involved in almost all physiological processes including mineral nutrient uptake in roots, metabolite translocation, regulation of cytoplasmic pH, and cell turgor-related functions (Oufattole et al., 2000; Arango et al., 2003; Sondergaard et al., 2004; Baxter et al., 2005). It was suggested that the wide variety of physiological functions that are linked to H+-ATPase activity needs delicate regulation (Arango et al., 2003; Baxter et al., 2005). On the other hand, these ATPases seem to be affected, albeit with different sensitivities, by diverse physiological factors such as hormones, light, phytotoxins or environmental stresses (Moore et al., 2003; Padmanaban et al., 2004).
Phosphorus (P) is a major essential nutrient and it plays a critical role in many plant metabolic processes (Raghothama, 1999). Inorganic phosphate (Pi) in soils, the primary source of P for plants, is transported across the plasma membrane to the cytosol together with 2–4 protons (Sakano, 1990). It has been shown that a root plasma membrane H+-ATPase is involved in the adaptation of soybean to Pi starvation (Shen et al., 2006). Besides P, deficiency of iron is also shown to regulate two plasma membrane H+-ATPases at the transcriptional level in cucumber (Santi et al., 2005). These reports support the hypothesis that nutrient transport is intimately linked to the activity of H+-ATPases in plants (Gevaudant et al., 2007).
According to Baxter et al. (2003), two model plants, Arabidopsis and rice, have 11 and 10 members of putative P-type H+-ATPase genes, respectively. Despite the fact that some of the P type H+-ATPase genes in plants have been shown to be associated with salt stress, plant development, and the formation of proanthocyanidins in the seed coat endothelium (Vitart et al., 2001; Baxter et al., 2005; Gevaudant et al., 2007), no such H+-ATPase gene has been linked to Pi in rice so far. With the completion of screening of T-DNA insertion lines in Arabidopsis thaliana, single gene mutants became an attractive choice to uncover the target gene's function. In rice, apart from the T-DNA insertions, the Tos17 retrotransposon has also proved to be an efficient mechanism for creating gene knockout lines because of its lower copy number and stability under normal conditions (Miyao et al., 1998; Yamazaki et al., 2001). In this study, the role of OsA8 in relation to Pi acquisition and transport in rice plants has been evaluated using the Tos17 mutant.
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Materials and methods |
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Osa8 mutant identification
The rice Osa8 mutant (line H0310) by Tos17 retrotransposon insertion and its wild type (Oryza sativa ssp. japonica cv. Hitomebore) were obtained from the National Institute of Agrobiological Sciences, Functional Genomics Laboratory (Japan). A PCR-based strategy (Miyao et al., 1998) was used to screen homogeneous insertions. The gene-specific primers of OsA8 were: 5'-TGTTCTTTTACTTTTGGTATTTCTT-3' and 5'-ACTTCTACTTTCGTACACTTCATTT-3'. The Tos17 border-specific primer was 5'-TACTGAGGCTGAACTTCGGGC-3' (tail 1). Twenty mutant seedlings were examined to confirm the insertion.
Determination of the copy number of Tos17 insertion in the Osa8 mutant
Genomic DNA was extracted from the homogeneous mutants to determine the copy numbers of Tos17 by two strategies: (i) suppression PCR as described by Miyao et al. (1998). Genomic DNA extracted from two lines of the homozygous mutants and the wild-type control was digested with HindII; the sequences of adapter used were: AD-F: 5'-CTAATACGACTCACTATAGGGCTCGAGCGGCCGCCCGGGCAGGT-3' and AD-R: p-ACCTGCCC-NH3. The sequences of adapter primer AP1: (5'-GGATCCTAATACGACTCACTATAGGGC-3'), AP2: (5'-AATAGGGCTCGAGCGGC-3') and the Tos17 border-specific primers were tail 4 (5'-CATCGGATGTCCAGTCCATTG-3') and tail 8 (5'-ATTGTTAGGTTGCAAGTTAGTTAAGA-3'), respectively. (ii) Inverse PCR (Ochman et al., 1988; Triglia et al., 1988): genomic DNA extracted from two lines of mutant and wild-type control was digested with DraI. The Tos17-specific primers were tail 4 and tail r-2 (5'-ATGGATAGGGACCAAGAATTC-3') used in PCR amplification. The PCR products were sequenced to confirm the copy number and location of the Tos17 in the genome.
Plant growth and treatment
Seeds of homozygote lines of the Osa8 mutant were sterilized for 30 min in 10% H2O2 followed by five rinses in sterile water. Seeds of uniform size were soaked in water before germination. Fifteen days later, seedlings (two-leaf stage) were transplanted into a 5.0 l plastic container (35x26x7 cm in length, width, and height, respectively) sufficient to hold 20 sponge plugs, each with two seedlings. For the first 3 d the seedlings were supplied with water and then with half-strength nutrient solution (see below) for 4 weeks before the treatments. Wild-type plants were used as a control.
The nutrient solution was prepared without or with P (0.25 mM, as a control) using NaH2PO4. NaCl was added to the Pi-deficient solution to compensate for Na. The treatments were performed in a randomized block design with four replicates. The nutrient solution was modified according to the recommendation of the International Rice Research Institute (Yoshida et al., 1976). The concentrations of macronutrients were 0.5 mM (NH4)2SO4, 0.5 mM NH4NO3, 0.5 mM K2SO4, and 1.7 mM Na2SiO3. The concentrations of the micronutrients were 0.009 mM MnCl2, 0.0185 mM H3BO3, 0.154 µM ZnSO4, 0.157 µM CuSO4, 0.52 µM (NH4)6Mo7O24, and 0.0357 mM EDTA-Fe. The solution was replaced every 3 d and the pH was adjusted daily with 1 mM NaOH to 5.6±0.3. Plants were grown in a greenhouse under 14 h light at 26-32 °C and 10 h dark at 18-22 °C.
Nutrient analysis of the plant samples
Plant samples were harvested after 4 weeks of the treatment. Roots were washed three times (1 min each) with tap water followed by two washes (1 min each) with deionized water, to remove any adhering nutrients. The shoots and roots were dried in a forced-air oven at 70 °C for about 48 h to a constant weight for determination of biomass (dry weight) and mineral analysis. The dried samples were ground to pass a 1.0 mm screen. About 0.2 g of dried powder was digested with 5 ml of 98% H2SO4 and 1 ml of 30% H2O2 at 270 °C. After cooling, the digested sample was diluted to 100 ml with deionized water. The P concentrations were determined by the molybdate blue method (absorption at 700 nm on a 722 spectrophotometer) and N concentration was measured by colorimetric continuous flow analysis (AutoAnalyser3, Bran+Luebbe, Germany) as described by Ding et al. (2006). The K concentration was determined by flame emission photometry.
Determination of ATPase activity in rice
After 4 weeks of growth in normal P solution, rice seedlings were harvested and separated into shoots (3–4 cm above the base of the haulm) and roots (1–2 cm below the root base). The isolation of plasma membrane from the root and shoot tissue and the subsequent determination of the ATPase activity were performed according to Yan et al. (2002) and Xu et al. (2008).
Analysis of expression of H+-ATPase genes and OsPht1 genes by semi-quantitative PCR
Total RNA was isolated from leaves and roots by using a Trizol reagent (Invitrogen Life Technologies, USA). First-strand cDNA was synthesized with an oligo(dT)-18 primer and reverse transcriptase. Based on the sequences of all 10 P-type H+-ATPase genes identified by Baxter et al. (2003), the OsA-specific primers were synthesized (primer sequences are listed in Supplementary Table S1 at JXB online). In addition, the sequences for examining OsPht1 genes' expression are listed in Supplementary Table 2 at JXB online.
Real-time quantitative RT-PCR analysis
The quantitative PCR was performed on a MyiQ Single Color Real-time PCR system (Bio-Rad) with SYBR Premix Ex Taq (Takara). Each reaction contained 5 µl of 1:100 (w/v) dilution of the first strand cDNA as template, in a total volume of 20 µl reaction mixture. Primer sets for OsA8 were: 5'-CGCTCGCTGTTGCCTAT-3' and 5'-GCTCTGCGTATGGTTTCA-3'; and for actin were: 5'-TTATGGTTGGGATGGGACA-3' and 5'-AGCACGGCT TGAATAGCG-3', respectively. The amount of template RNA and the cycle number, which provided a linear range of gene amplification, were determined for all the genes (Chen et al., 2007). The relative expression level of OsA8 was shown as a percentage of copies of OsA8 to that of actin.
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Results |
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OsA8 encodes a typical P-type ATPase-like protein of rice
The cDNA sequence of OsA8 (AK068699 [GenBank] ), comprising a 3376 bp nucleotide, was retrieved from the KOME database. Comparison of its cDNA and genomic DNA sequences revealed that the gene contains 21 exons and 20 introns (Fig. 1). Sequence analysis shows that the putative OsA8 gene encodes a protein consisting of 970 amino acids with 10 transmembrane domains (see Supplementary Fig. 1 at JXB online) that are commonly identified in other P-type ATPases (Wach et al., 1992). Moreover, its predicted ATP binding and phosphorylation domains (data not shown) are conserved across the P-type H+-ATPase. According to a previous classification (Axelsen and Palmgrem, 1998; Baxter et al., 2003), OsA8 belongs to the P3A (AHA) branch, a subgroup of the P-type ATPase family that is specific to plants.
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Transcripts of OsA8 accumulated predominantly in roots of rice and could be down-regulated by nutrient starvation
Expression pattern of OsA8 was investigated in rice seedlings. As shown in Fig. 2, transcripts of OsA8 accumulated more abundantly in roots than in leaves under normal growing condition. OsA8 expression was suppressed in both roots and leaves under N, P, and K deficiency (Fig. 2), indicating a much broader role of it in nutrient acquisition in rice.
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Osa8 homozygote mutants were relatively small in size and showed lower root to shoot ratio under P starvation
Osa8 knockout mutants were compared with the wild-type plants to understand the physiological role of the gene in rice. PCR amplification confirmed that 14 out of the 20 Osa8 mutant seedlings were homozygotes (data not shown). Real-time PCR results showed that OsA8 was almost undetectable in the mutant (Fig. 2). The copy number of Tos17 insertion was determined in homogyzotes by a combination of suppression PCR and reverse PCR strategies (Fig. 3). Sequencing of the PCR products confirmed a single insertion of Tos17 in the OsA8 gene. Apart from this insertion, no other copies of Tos17 in the mutant were different from wild-type plants. Morphological comparison of the mutant and wild-type rice showed that, regardless of P supply, Osa8 mutants, in general, had smaller leaves, roots, and tillers (Fig. 4). Consistent with these differences, biomass of both roots and shoots of the mutant plants was significantly smaller than that of wild-type plants (Fig. 5I, II). Notably, the biomass ratio of the root to the shoot in the mutant was significantly lower than that in the wild-type seedlings grown under P-starvation conditions (Fig. 5III), suggesting that OsA8 plays a critical role in P-regulated root growth in rice.
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20); II, shoot dry weight (mean ±sd, n Knockout of OsA8 decreased both uptake and translocation of P from root to shoot in rice
Previous work has shown that the nutrient translocation from the root to the shoot is regulated by the relative concentration of the nutrients in the root and shoot (Ewing and Bennett, 1994; Requena et al., 2003; Smith et al., 2003; Yi et al., 2005). To evaluate the possible roles of OsA8 in Pi uptake and translocation in rice, the concentration and content of P in the Osa8 mutant and the control grown under two Pi supply levels were measured. When supplied with 0.25 mM P, the concentration of total P was almost the same as in the roots but it was significantly lower in the shoots of the mutant than in the wild-type seedlings (Fig. 6I, II). Moreover, the knockout of OsA8 resulted in a decrease of total P content by 52% and 43% in shoots and roots, respectively (Fig. 6III, IV).
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Under P-starvation conditions, both the concentration and total P in the roots were much higher in the mutant than in the wild-type seedlings; whereas in the shoots, the differences between the two plants were insignificant (Fig. 6I, II). The ratio of total P content in shoots to that in roots was 7.8 in the Osa8 mutant and 17.7 in the wild-type plants under P-starvation conditions, suggesting an altered translocation of P from the root to the shoot, particularly under P-starved conditions in the mutant. However, total P content of the whole plant was almost the same between the mutant and the wild-type plants in P-starvation condition (Fig. 6V).
Knockout of OsA8 increased ATPase activitity
To evaluate the effect of the mutation, the mutant's ATPase activity in roots and shoots were measured with wild-type rice as a control. Contrary to our expectations, total ATPase activity was enhanced in the Osa8 mutant (Fig. 7) despite the fact that the expression of OsA8 was almost undetectable.
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Knockout of OsA8 gene affected expression of several OsA and OsPht1 genes
Among 10 OsA genes in rice, expression of OsA5, OsA9, and OsA10 was not detectable under our experimental conditions (Fig. 8). Expression of OsA3 and OsA7 was relatively higher in both the mutant and the wild-type seedlings (Fig. 8). Knockout of OsA8 increased the expression of OsA1 and OsA2 in the roots of Pi-starved mutants (Fig. 8). However, a lower abundance of OsA2 was noticed in leaves of the mutant. In addition, OsA6 appears to be induced only in roots of Pi-sufficient wild-type plants (Fig. 8). OsA4 seemed to express constitutively. This suggests a complex regulation of expression of the members of the OsA family in roots and leaves under Pi starvation conditions.
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It has been reported that two Pht1 genes, OsPT2 and OsPT6, were highly expressed in P-starved roots of the rice cultivar Nipponbare (Paszkowski et al., 2002; Ai et al., 2008). In this study, the expression of these two genes was compared in wild-type and mutant plants derived from the rice cultivar Hitomebore. The expression of OsPT2 was detected in roots and leaves of the mutant and the wild type (Fig. 9). Interestingly, P-starvation did not induce the expression of OsPT6 in roots of the mutant as compared with that of the wild type (Fig. 9). In addition, knockout of OsA8 did not noticeably affect the expression of other members of the Pht1 family.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSupplementary dataReferences |
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Nutrient acquisition and proton ATPase activity are intimately associated in plants. Proton ATPases are responsible for generating both electrical and chemical gradients across the plant membranes that drive many secondary transport processes. In this study, the impact of mutation in a family member of rice proton ATPase (OsA8) on Pi acquisition was evaluated. Bioinformatics analysis strongly points to OsA8 being a bona fide plant-specific H+-ATPase belonging to the P3A branch of the P-type ATPases. This gene is predominantly expressed in roots of rice and appears to play a major role in nutrient acquisition based on its response to multiple nutrient deficiencies.
To characterize the biological role of OsA8 further, a Tos17 insertion line of rice was obtained and confirmed that it is a homozygous knockout mutant (Figs 1, 3). The mutation increased ATPase activities besides enhancing P levels in roots. These changes are likely to have contributed to the observed changes in plant growth. This supports the hypothesis that OsA8 plays a significant role in nutrient acquisition and plant development.
The uptake of nutrients from the soil solution and subsequent in vivo translocation are some of the major functions of transporters. Earlier studies have demonstrated that ATPases play an important role in nutrient uptake and translocation (Oufattole et al., 2000; Sondergaard et al., 2004). It has been suggested that 2–4 protons are translocated with a Pi ion across the plamamembrane (Sakano, 1990; Ai et al., 2008), and acidification of the rhizosphere was observed due to H+ release during P deficiency (Raghothama, 1999). As a case in point, in plants such as Brassica napus and white lupin, excretion of protons to the rhizosphere increases during Pi deficiency (Yan et al., 2002). This suggested that, under P deficiency, the activity of proton ATPase is likely to increase. However, contrary to a previous report that a root plasma membrane H+-ATPase gene was up-regulated by P starvation in soybean (Shen et al., 2006), we found that OsA8 was down-regulated by P starvation in rice (Fig. 2). It appears that other members of the gene family such as OsA1 and OsA2 are induced to a higher level in the mutant (Fig. 8) to compensate for the lack of some of the functions of OsA8. It has been proposed that some proton pumps have redundant function and they may compensate for the lack of function of others (Sondergaard et al., 2004). As a support for this assumption, the mutant's ATPase activity was increased, although expression of OsA8 was almost completely absent in the mutant (Fig. 7). This result correlated with increased root reductase activity and soluble sugar concentrations of the mutant (data not shown). However, more convincing evidence for compensation for the lack of OsA8 activity is yet to be acquired. In spite of the compensation, there is still a difference in P concentration in roots of the mutant and the control. Moreover, knockout of the gene significantly increased ATPase activity in the roots (Fig. 7). By contrast, the effect was much smaller in the shoots which agrees with the fact that the gene was expressed predominantly in the roots (Fig. 2). This suggests that OsA8 plays a specific role in P translocation across the root and the shoot that cannot be compensated for by other members of the family. In addition, one member of high affinity Pi transport gene (OsPT6) was also up-regulated in the mutant (Fig. 9). This may also have contributed, in part, to the observed increase in root P content under P deficiency. An increase in the ratio of the root to the shoot is a hallmark of a plant's adaptation to P deficiency (Raghothama, 1999). Since P concentration in roots of the mutant under P starvation was 3.5-fold higher than that in the wild type (Fig. 6I, III), the decrease in root growth and root-to-shoot ratio resulting from the knockout of OsA8 (Fig. 5) might be partially attributable to the inhibition of P translocation from the root to the shoot. It is important to note that, despite presumed compensation by other members of the family, the OsA8 mutation resulted in decreased growth as indicated by lower root and shoot biomass. Given the regulation of OsA8 expression by other tested plant nutrient deficiencies, the observed plant phenotype is not all that surprising. It is likely that OsA8 plays a much broader biological role beyond that of P nutrition.
This study provides evidence for some of the biological functions of OsA8, a member of a primary transport protein in plants. The data show that regulation of OsA8 is complex and its role may not be completely compensated by other members of the family. Further, this study establishes a direct link between Pi acquisition and transport with a proton ATPase in an economically important rice crop.
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Supplementary data |
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Supplementary data can be found at JXB online.
Supplementary Fig. S1. Hydropathy plot of OsA8.
Supplementary Fig. S2. Enhanced accumulation of GmNAC1 and GmNAC3 transcripts during leaf senescence in soybean.
Supplementary Table S1. The primers used for detecting the expression of OsA and OsPht1 genes.
Supplementary Table S2. The RT-PCR conditions for expression of OsPht1 and OsA genes.
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Acknowledgements |
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This research was supported by the National Natural Science Foundation of China (30571108), China 973 program (2005CB120903), 111 project (B07030 [GenBank] ), 863 project (2006AA10Z134). We thank Weiji Xin in our laboratory for helping with the real-time PCR analysis, Professor Nava Moran from the Hebrew University of Jerusalem and Dr Feng Yan for their valuable comments.
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Footnotes |
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* These authors contributed equally to this article.
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