Os01g0919400

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Please cite: Man Li, Zhennan Wang (2016) Gene: "Os01g0919400" in RiceWiki, available at http://wiki.ic4r.org/index.php?title=Os01g0919400&oldid=271569 (Last update: Jul 01, 2016). [See details]

OsSPS1 is a gene encoding sucrose phosphate synthase(SPS) and is a menber of the sucrose phosphate synthase gene family in rice(OsSPSs).

Contents

Background

  • In many plants, sucrose is the main form of photoassimilate translocated from source tissue, like leaves, to sink tissues, such as expanding leaves or panicles, and the efficiency of sucrose translocation is a major factor affecting plant growth. Sucrose phosphate synthase (SPS) is known to be the rate-limiting enzyme in sucrose synthesis and to play a dominant role in sucrose metabolism. It catalyzes the conversion of fructose-6-phosphate and UDP-glucose into sucrose-6-phosphate, which is subsequently hydrolyzed to sucrose by sucrose phosphatase (SPP). It is also known that SPS activity is regulated at different levels. The enzyme itself is regulated via allosteric activation by glucose-6-phosphate and inhibition by inorganic phosphate. In addition, SPS is activated by light and osmotic stress through changes in the phosphorylation state of several serine residues in the protein. SPS gene transcriptionis also regulated by environmental factors such as light and cold stress. However, there are fewer reports on the transcriptional regulation than on the protein regulation.
  • Several studies have associated SPS activity with plant growth and productivity. For example, in maize, it has been demonstrated that SPS activity in source leaves is positively correlated with vegetative growth, forage yield, and grain yield . The introduction of maize ZmSPS into potato was shown to improve the photosynthetic rate, inhibit leaf senescence, and increase yield [7]. In rice, the QTL for plant height appears to coincide with the OsSPS1 locus. A report on ZmSPS-introduced rice plants concluded that the sucrose/starch ratio is positively correlated with SPS activity in leaf blades, although the impact of elevated SPS activity on productivity was not investigated.
  • In the present study, we investigated the tissue- and developmental stage-specific expression patterns of the rice SPS gene family using real-time RT-PCR techniques. The diurnal changes in SPS gene expression and activity in leaves were also examined. Based on the results presented here, predictions of the key transcriptional regulator of each SPS gene are discussed.

Annotated Information

Function

  • OsSPS1 is a gene encoding sucrose phosphate synthase(SPS). SPS catalyzes the conversion of fructose 6-phosphate and UDPglucose into sucrose 6-phosphate, and it is generally considered to be the rate-limiting enzyme in sucrose synthesis. OsSPS1 is one of the 5 isogenes encoding SPS in the rice genome and and plays a dominant role in sucrose synthesis among them[1].
  • The suppression of OsSPS1 shortens the plant length of rice seedlings[2], and the locus of OsSPS1 appears to coincide with the quantitative trait locus(QTL)for plant height[3].
  • Sucrose synthesis via OsSPS1 is essential in pollen germination in rice[4].
  • In rice, the expression patterns of most of the SPS gene family, except for SPS1, have not been examined previously. The mRNA of SPS1 was reported to be present in source tissues such as the mature leaf blades of young plants and scutella of germinating seeds. In the present study, we confirmed that the mRNA of SPS1 was abundant in source tissues, particularly in leaf blades. In addition to the germinating and seedling stages, we measured the mRNA in leaves at the heading stage, and showed that the source-specific expression of SPS1 was irrespective of developmental stage. Therefore, SPS1 can be regarded as a source-specific gene. In addition, the mRNA level of SPS1 was high in senescent leaves, suggesting its contribution to the retention of SPS activity during leaf senescence.
  • However, the mRNA levels of SPS2, SPS6, and SPS8 were also high in some sink tissues, such as elongating leaf, indicating that these SPS isogenes play a different role in source and/or sink tissues and are differently regulated at the level of transcription. Interestingly, the genes expressed in sink tissues (SPS2, SPS6, and SPS8) are relatively similar in amino acid sequence. Furthermore, the SPS2 and SPS6 proteins appear to be structurally different from the other SPS isoforms, and lack both the 14-3-3 binding and osmotic stress regulation sites. These two SPS genes appeared to be expressed at relatively low levels compared to the source-specific gene, SPS1. Perhaps there is a correlation between the protein function that is affected by the absence of regulatory sites and the characteristics of transcriptional regulation.

Mutation

Figure 1. SPS activity of Koshihikari and NIL-SPS1 during the transplanting, panicle formation, heading, and mid-ripening stages[5].
  • An NIL of rice (O. sativa L.) was generated in the process of developing chromosome segment substitution lines (CSSLs). The NIL-SPS1 carries a chromosome segment containing OsSPS1 of Kasalath on chromosome 1 in the genetic background of Koshihikari[5].
  • Figure 1. shows the SPS enzyme activities in the source leaf blades of Koshihikari and NIL-SPS1 at different developmental stages. The SPS activity in NIL-SPS1 was 30% and 59% higher than that in Koshihikari at the transplanting and panicle formation stages, respectively. However, at later developmental stages, the SPS activity in NIL-SPS1 leaves did not differ significantly from that of Koshihikari[5].
  • The plant height of NIL-SPS1 tended to be higher than that of Koshihikari throughout the measurement period, particularly after heading (Figure 2A). In contrast, tiller number in NIL-SPS1 tended to be lower than that in Koshihikari, but the difference was not significant(Figure 2B)[5].
Figure 2. Growth analysis of Koshihikari and NIL-SPS1. (A) Plant height of Koshihikari and NIL-SPS1. (B) Tiller number of Koshihikari and NIL-SPS1[5].


  • To clarify the yield characteristics of NIL-SPS1 in comparison with Koshihikari, data on the yield and yield components obtained in 2009, 2010, and 2012 were combined and analyzed statistically (Table 1)[5].
Table 1. Yield and yield components of Koshihikari and NIL-SPS1[5].
  • Since NIL-SPS1 exhibited a higher spikelet number per panicle in comparison with Koshihikari, we further compared the panicle architecture of Koshihikari and NIL-SPS1. Panicles were separated into primary and secondary rachis branches, and the number of each rachis branch, percentage of ripened grain, and single-grain weight were measured (Table 2)[5].
Table 2. Panicle architecture of Koshihikari and NIL-SPS1[5].
  • To investigate the ripening pattern of spikelets within a panicle, all spikelets were classified into 4 groups based on their positions and relative densities, and the weight of each spikelet was measured. Figure 3. shows the frequency of distribution of the spikelet weight in each of the 4 groups. On the primary rachis branch, the frequency of unripened grain in NIL-SPS1 was not different from that in Koshihikari. However, on the secondary rachis branch, the

frequency of unripened grain at 50–80% in NIL-SPS1 was much higher than that in Koshihikari[5].

Figure 3. Distribution of spikelet weight of the Koshihikari and NIL-SPS1[5].
  • Figure 4. shows the changes in the dry weight of the aboveground parts of Koshihikari and NIL-SPS1 from the heading stage to maturity stage[5].
Figure 4. Aboveground biomass accumulation of Koshihikari and NIL-SPS1 after heading[5].


  • A chemically inducible gene expression system was used on OsSPS1. Inducible gene suppression works with an RNAi cassette and this cassette targets OsSPS1. The inducer is β-estradiol. The seeds of the transgenic plants were sown on the MS agar plates containing 30 μM of β-estradiol and grown for a week. In two of the three independent transgenic lines that were examined, the transcript levels of OsSPS1 in the leaf blades of the β-estradiol-treated plants were significantly less than the levels in the control plants (Fig. 5A). Concomitantly, the shoot length of the β -estradiol-treated plants was shorter than that of the control plants (Fig. 5B). In another experiment, the induced seedlings were transplanted into plastic pots filled with soil and were further grown for four weeks. During this period, 100 μM of β-estradiol containing 0.02% Tween-20 was sprayed onto the terrestrial portions of the plant parts every week (three times in total). Again, the OsSPS1 mRNA levels in the leaf blades decreased significantly in two of the three transgenic lines (Fig. 6A). In the leaf blades of the induced plants, the molar ratio of sucrose to starch decreased significantly when compared to the uninduced control plants (Fig. 6B)[6].
Figure 5.  Effects of β-estradiol on the transcript levels of OsSPS1 in the leaf blades (A) and plant lengths (B) of the inducible RNAi transgenic plants[6].
Figure 6. Effect of β-estradiol on transcript levels of OsSPS1 (A) and the molar ratio of sucrose to starch (B) in the leaf blades of the inducible RNAi transgenic plants[6].

Expression Pattern

Figure 9. Diurnal patterns of the promoter activities of OsSPS1 under light/dark cycles [7].
  • Expression analysis revealed that OsSPS1 is preferentially expressed in the source tissue, particularly in leaf blades, and it plays a dominant role in sucrose synthesis in the source leaf blades among the 5 isogenes for SPS[1].
  • The promoter activities of sucrose phosphate synthase gene in rice, OsSPS1, is controlled by light and circadian clock, but not by sucrose[7]. The promoter activities of OsSPS1 is low during the dark period and increased rapidly after the onset of the light period. While the promoter activity of OsSPS1 decreased gradually during the day and remained low through out the night(Figure2A)[7].
  • The mRNA levels of SPS2 and SPS8 were highest in the early dark period, were not correlated with sugar content under light/dark conditions, and did not show a clear circadian pattern under continuous light. It is likely that their transcription is mainly regulated by light and only slightly by endogenous rhythm. However, the regulation of SPS11 is probably more complex because its mRNA levels were high in the early dark period, and a prolonged light period tended to increase it.

Knowledge Extension

  • Sucrose phosphate synthase(SPS,EC2.3.1.14)catalyzes the conversion of fructose-6-phosphate and UDP-glucose into sucrose-6-phosphate and isknown to be the major rate-limiting enzyme insucrose biosynthesis in plants.
  • plant SPS genes are clustered into four groups(groupsA,B,C, andD),based on their amino acid sequences. Rice has five SPS genes, OsSPSs, classified into four groups: OsSPS8, OsSPS1, OsSPS11, and OsSPS2 and OsSPS6 in groupsA,B,C,andD,respectively.
  • In rice, the expression patterns of most of the SPS gene family, except for SPS1, have not been examined previously. The mRNA of SPS1 was reported to be present in source tissues such as the mature leaf blades of young plants and scutella of germinating seeds. In the present study, we confirmed that the mRNA of SPS1 was abundant in source tissues, particularly in leaf blades. In addition to the germinating and seedling stages, we measured the mRNA in leaves at the heading stage, and showed that the source-specific expression of SPS1 was irrespective of developmental stage. Therefore, SPS1 can be regarded as a source-specific gene. In addition, the mRNA level of SPS1 was high in senescent leaves, suggesting its contribution to the retention of SPS activity during leaf senescence.
  • We also found that the expression pattern of SPS11 was unique. It was relatively low in all tissues harvested in the daytime, except for in germinating seeds, which were germinated and harvested in the dark. However, the mRNA levels were higher in leaf blades and sheaths at night. This probably suggests that SPS11 may function only in the dark period, which might be the reason why SPS11 was reported as a poorly represented gene in a previous study in which expressed sequence tags (ESTs) of rice SPS11 were catalogued.
  • Previous studies have indicated that light is the major factor that affects SPS activity. In many species, including rice, the activity of SPS is higher under illumination and shows diurnal changes due to the dephosphorylation of SPS proteins. In maize and Arabidopsis, the mRNA levels of SPS genes also showed diurnal changes and were highest in the light period [4,12]. Surprisingly, in this study, all 5 SPS mRNAs tended to be higher at night or in the early morning. However, the total activity, which was similar to the total amount of the SPS proteins, was almost constant over a day, and the selective activity, which preferentially measures the activated form of the enzyme, was higher in the daytime. These results suggest that in rice, the main form of regulation causing diurnal changes in SPS activity is protein modification by phosphorylation, and diurnal changes in transcription may not be physiologically significant.
  • To investigate the regulatory mechanism(s) of the diurnal changes in SPS mRNAs in leaf blades, we compared the mRNA levels and soluble sugar content under light/dark and continuous light conditions. The mRNA levels of SPS1 were higher in the dark period, and the same diurnal pattern was observed on the first day under continuous light. However, the mRNA levels were only correlated with sucrose content under light/dark conditions. Although this implies that the transcription of SPS1 is partially regulated by endogenous rhythm, the possibility of direct regulation by light cannot be rejected. Indeed, light-responsive elements, which are involved in the light-specific regulation of photosynthetic genes, have been reported in the promoter region of the rice SPS1 gene. Chávez-Bárcenas et al. reported that SPS1 expression was positively regulated by light; however, their results do not contradict our results because they did not compare plants at day and night, but compared 7-day-old plants grown under continuous dark and 16-h light/8-h dark conditions.

Labs working on this gene

  • Bio ResearchLaboratory,ToyotaMotorCorporation,Toyota,Aichi,Japan
  • LaboratoryofCropScience,GraduateSchoolofAgriculturalandLifeSciences,TheUniversityofTokyo,Bunkyo-ku,Tokyo,Japan
  • NAROAgriculturalResearchCenter,Joetsu,Niigata,Japan
  • Center forGeneResearch,NagoyaUniversity,Chikusa-ku,Nagoya,Japan
  • Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan
  • Toyama Prefectural Agricultural, Forestry & Fisheries Research Center, Toyama, Toyama 939-8153, Japan
  • NARO Agricultural Research Center, Joetsu, Niigata 943-0193, Japan
  • Graduate School of Science and Technology, Niigata University, Ikarashi, Nishi-ku, Niigata 950-2181, Japan
  • Bio Research Laboratory, Toyota Motor Corporation, 1 Toyota-cho, Toyota, Aichi 471-8572, Japana

References

  1. 1.0 1.1 Okamura, M., Aoki, N., Hirose, T., Yonekura, M., Ohto, C., Ohsugi, R., 2011. Tissue specificity and diurnal change in gene expression of the sucrose phosphate synthase gene family in rice. Plant Sci. 181, 159–166.
  2. Hirose,T.,Mizutani,R.,Mitsui,T., and Terao,T.(2012).Achemically inducible gene expression system and its application to inducible gene suppression in rice. PlantProd.Sci. 15, 73–78.
  3. Ishimaru,K.,Ono,K.,andKashiwagi,T. (2004). Identification of a new gene controlling plant height in rice using the candidate-gene approach. Planta 218, 388–395.
  4. Hirose T, Hashida Y, Aoki N, Okamura M, Yonekura M, Ohto C, Terao T, Ohsugi R. Analysis of gene-disruption mutants of a sucrose phosphate synthase gene in rice, OsSPS1, shows the importance of sucrose synthesis in pollen germination. Plant Sci. 2014 Aug;225:102-6. doi: 10.1016/j.plantsci.2014.05.018. Epub 2014 Jun 2. PubMed PMID: 25017165.
  5. 5.00 5.01 5.02 5.03 5.04 5.05 5.06 5.07 5.08 5.09 5.10 5.11 5.12 Hashida Y, Aoki N, Kawanishi H, et al. A near isogenic line of rice carrying chromosome segments containing OsSPS1 of Kasalath in the genetic background of Koshihikari produces an increased spikelet number per panicle[J]. Field Crops Research, 2013, 149: 56-62.
  6. 6.0 6.1 6.2 Hirose T, Mizutani R, Mitsui T, et al. A chemically inducible gene expression system and its application to inducible gene suppression in rice[J]. Plant Production Science, 2012, 15(2): 73-78.
  7. 7.0 7.1 7.2 Yonekura M, Aoki N, Hirose T, Onai K, Ishiura M, Okamura M, Ohsugi R, Ohto C. The promoter activities of sucrose phosphate synthase genes in rice, OsSPS1 and OsSPS11, are controlled by light and circadian clock, but not by sucrose. Front Plant Sci. 2013 Mar 1;4:31. doi: 10.3389/fpls.2013.00031. eCollection 2013. PubMed PMID: 23460029; PubMed Central PMCID: PMC3585450.

Structured Information

Gene Locus Os01g0919400
Organism Oryza sativa japonica group
Length 932 bp
Chromosome Chromosome 01
Location Chromosome 01:40105663...40106595
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Please cite: Man Li, Zhennan Wang (2016) Gene: "Os01g0919400" in RiceWiki, available at http://wiki.ic4r.org/index.php?title=Os01g0919400&oldid=271569 (Last update: Jul 01, 2016).
ContributorContribution Score*Edit Count#Summed Edit QuantityΛAveraged Edit QualityLatest Edit TimeEdit Details
Man Li9.787198370.9952016-06-06 17:48:51[show]
Zhennan Wang7.61760012016-07-01 20:57:32[show]
Contributors with score < 1 are excluded from the authorship.
ContributorContribution Score*Edit Count#Summed Edit QuantityΛAveraged Edit QualityLatest Edit TimeEdit Details
Jian Sang0.02612612016-06-30 16:03:54[show]
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