Journal of Plant Biology

, Volume 61, Issue 6, pp 383–400 | Cite as

Transgenic Rice Overexperessing a Tomato Mitochondrial Phosphate Transporter, SlMPT3;1, Promotes Phosphate Uptake and Increases Grain Yield

  • Guo-hong Yu
  • Sheng-cai Huang
  • Rui He
  • Ying-zhang Li
  • Xian-guo ChengEmail author
Original Article


Mitochondrial phosphate transporter plays an important regulatory role in promoting the uptake and transport of phosphate in plants. In this study, the SlMPT3;1 gene, a member of mitochondrial phosphate transporter family in tomato, was isolated and transformed into the rice Oryza sativa L. ssp. japonica cultivar Kitaake. The SlMPT3;1 is localized to the mitochondrial membrane and functions in compensating the phosphate uptake in yeast MB192 mutant that is defective in phosphate transport under Pi deficiency. RT-qPCR showed that the SlMPT3;1 is expressed in all of tomato tissues, but highly accumulated in the young leaves and stems under Pi deficiency. The data demonstrated that at least two copies of the SlMPT3;1 gene are inserted into the rice genome, and the transcripts of the SlMPT3;1 mRNA are highly accumulated in the roots of the transgenic rice. The overexpression of the SlMPT3;1 gene not only promotes phosphate uptake by the roots, but also increases the translocation of phosphate from the roots to the shoots in the transgenic rice. The transgenic rice accumulated more chlorophyll and soluble sugar in the shoots than the wild type under Pi deficiency. Microassay sequencing showed that the differentially expressed genes in the transgenic rice are mainly involved in the regulations of biological process and molecular function under Pi deficiency. Further RTqPCR analyses revealed that the differentially expressed genes, which are involved in the regulations of the biological process, cell component, and molecular function, are upregulated under Pi deficiency, and exhibit similar expression trends to the relative expression folds of these partial differentially expressed genes in the transcriptomic analyses. This study suggests that the overexpression of the SlMPT3;1 gene promoted the uptake and transport of phosphate in rice, thus leading to an enhanced increase in tiller number and effective panicle of per plant, and increasing grain yield under Pi deficiency.


Mitochondrial phosphate transporter Phosphorus deficiency Phosphate uptake SlMPT3;1 gene Transgenic rice 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

12374_2018_198_MOESM1_ESM.pdf (173 kb)
Supplementary material, approximately 176 KB.


  1. Ai P, Sun S, Zhao J, Fan X, Xin W, Guo Q, Yu L, Shen Q, Wu P, Miller AJ, Xu G (2009) Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. Plant J 57:798–809CrossRefGoogle Scholar
  2. Anders S, Huber W. (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106CrossRefGoogle Scholar
  3. Chiou T, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206CrossRefGoogle Scholar
  4. Cubero B, Nakagawa Y, Jiang X, Miura K, Li F, Raghothama KG, Bressan RA, Hasegawa PM, Pardo JM (2009) The Phosphate Transporter PHT4;6 is a Determinant of Salt Tolerance that Is Localized to the Golgi Apparatus of Arabidopsis. Mol Plant 2: 535–552CrossRefGoogle Scholar
  5. Dai X, Wang Y, Yang A, Zhang WH (2012) OsMYB2P-1, an R2R3 MYB Transcription Factor, Is Involved in the Regulation of Phosphate-Starvation Responses and Root Architecture in Rice. Plant Physiol 159:169–183CrossRefGoogle Scholar
  6. Dai X, Wang Y, Zhang W (2016) OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice. J Exp Bot 67:947–960CrossRefGoogle Scholar
  7. Dakora F, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47CrossRefGoogle Scholar
  8. Devaiah BN, Nagarajan VK, Raghothama KG (2007) Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 145: 147–59CrossRefGoogle Scholar
  9. Ding W, Wang Y, Fang W, Gao S, Li X, Xiao K (2016) TaZAT8, a C2H2-ZFP type transcription factor gene in wheat, plays critical roles in mediating tolerance to Pi deprivation through regulating P acquisition, ROS homeostasis and root system establishment. Plant Physiol 158:297–311CrossRefGoogle Scholar
  10. Duncan R, Carrow R (1999) Turfgrass molecular genetic improvement for abiotic/edaphic stress resistance. Adv Agron 67:233–305CrossRefGoogle Scholar
  11. Eicks M, Maurino V, Knappe S, Flugge UI, Fischer K (2002) The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiol 128:512–522CrossRefGoogle Scholar
  12. Feng H, Li B, Zhi Y, Chen J, Li R, Xia X, Xu G, Fan X (2017) Overexpression of the nitrate transporter, OsNRT2.3b, improves rice phosphorus uptake and translocation. Plant Cell Rep 36: 1287–1296CrossRefGoogle Scholar
  13. Furihata T, Suzuki M, Sakurai H (1992) Kinetic characterization of two phosphate uptake systems with different affinities in suspension-cultured Catharanthus roseus protoplasts. Plant Cell Physiol 33:1151–1157Google Scholar
  14. Grierson P (1992) Organic acids in the rhizosphere of Banksia integrifolia Lf. Plant Soil 144:259–265CrossRefGoogle Scholar
  15. Guo C, Zhao, X, Liu X, Zhang L, Gu J, Li X, Lu W, Xiao K (2013) Function of wheat phosphate transporter gene TaPHT2;1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions. Planta 237:1163–1178CrossRefGoogle Scholar
  16. Hamburger D, Rezzonico E, MacDonald-Comber PJ, Somerville C, Poirier Y (2012) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant cell 14:889–902CrossRefGoogle Scholar
  17. Hamel P, Saint-Georges Y, de Pinto B, Lachacinski N, Altamura N, Dujardin G (2004) Redundancy in the function of mitochondrial phosphate transport in Saccharomyces cerevisiae and Arabidopsis thaliana. Mol Microbiol 51:307–317CrossRefGoogle Scholar
  18. Hawkesford MJ (2014) Reducing the reliance on nitrogen fertilizer for wheat production. J Cereal Sci 59:276–283CrossRefGoogle Scholar
  19. Irigoyen, JJ, Emerich, DW, and Sanchezdiaz, M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol. Plantarum 84:55–60CrossRefGoogle Scholar
  20. Irigoyen S, Karlsson P. M, Kuruvilla J, Spetea C, Versaw WK (2011) The Sink-Specific Plastidic Phosphate Transporter PHT4;2 Influences Starch Accumulation and Leaf Size in Arabidopsis. Plant Physiol 157:1765–1777CrossRefGoogle Scholar
  21. Jia H, Ren H, Gu M, Zhao J, Sun S, Zhang X, Chen J, Wu P, Xu G (2011) The Phosphate Transporter Gene OsPht1;8 Is Involved in Phosphate Homeostasis in Rice. Plant Physiol 156:1164–1175CrossRefGoogle Scholar
  22. Jia F, Wan X, Zhu W, Sun D, Zheng C, Liu P, Huang J (2015) Overexpression of mitochondrial phosphate transporter 3 severely hampers plant development through regulating mitochondrial function in Arabidopsis. PLoS ONE 10:e0129717CrossRefGoogle Scholar
  23. Johnson JF, Vance C P, Allan DL (1996) Phosphorus deficiency in Lupinus albus (altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase). Plant Physiol 112:31–41CrossRefGoogle Scholar
  24. Khatun K, Nath UK, Robin AHK, Park J, Lee D, Kim M, Kim C, Lim K, Nou I, Chung MY (2017) Genome-wide analysis and expression profiling of zinc finger homeodomain (ZHD) family genes reveal likely roles in organ development and stress responses in tomato. BMC Genomics 18:695CrossRefGoogle Scholar
  25. Kirk GJD, George T, Courtois B, Senadhira D (1998) Opportunities to improve phosphorus efficiency and soil fertility in rainfed lowland and upland rice ecosystems. Field Crops Res 56:73–92CrossRefGoogle Scholar
  26. Kuan J, Saier MJ (1993) The mitochondrial carrier family of transport proteins: structural, functional, and evolutionary relationships. Crit Rev Biochem Mol Biol 28:209–233CrossRefGoogle Scholar
  27. Li Z, Xu C, Li K, Yan S, Qu X, Zhang J (2012) Phosphate starvation of maize inhibits lateral root formation and alters gene expression in the lateral root primordium zone. BMC Plant Biol 12:89CrossRefGoogle Scholar
  28. Liu F, Chang XJ, Ye Y, Xie WB, Wu P, Lian XM (2011) Comprehensive sequence and whole-life-cycle expression profile analysis of the phosphate transporter gene family in rice. Mol Plant 4:1105–1122CrossRefGoogle Scholar
  29. Liu J, Fu S, Yang L, Luan M, Zhao F, Luan S, Lan W (2016) Vacuolar SPX-MFS transporters are essential for phosphate adaptation in plants. Plant Signal Behav 11:e1213474CrossRefGoogle Scholar
  30. Lorenz A, Lorenz M, Vothknecht UC, Niopek-Witz S, Neuhaus HE, Haferkamp I (2015) In vitro analyses of mitochondrial ATP/phosphate carriers from Arabidopsis thaliana revealed unexpected Ca2+-effects. BMC Plant Biol 15:238CrossRefGoogle Scholar
  31. Lota F, Wegmuller S, Buer B, Sato S, Brautigam A, Hanf B, Bucher M (2013) The cis-acting CTTC-P1BS module is indicative for gene function of LjVTI12, a Qb-SNARE protein gene that is required for arbuscule formation in Lotus japonicus. Plant J 74: 280–293CrossRefGoogle Scholar
  32. Lv Q, Zhong Y, Wang Y, Wang Z, Zhang L, Shi J, Wu Z, Liu Y, Mao C, Yi K, Wu P (2014) SPX4 Negatively Regulates Phosphate Signaling and Homeostasis through Its Interaction with PHR2 in Rice. Plant Cell 26:1586–1597CrossRefGoogle Scholar
  33. Mehra P, Pandey BK, Giri J (2015) Genome-wide DNA polymorphisms in low phosphate tolerant and sensitive rice genotypes. Sci Rep 5:13090CrossRefGoogle Scholar
  34. Mehra P, Pandey BK, Giri J (2017) Improvement in phosphate acquisition and utilization by a secretory purple acid phosphatase (OsPAP21b) in rice. Plant Biotechnol J 15:1054–1067CrossRefGoogle Scholar
  35. Mimura T (1999) Regulation of phosphate transport and homeostasis in plant cells. Int Rev Cytol 191:149–200CrossRefGoogle Scholar
  36. Miyaji T, Kuromori T, Takeuchi Y, Yamaji N, Yokosho K, Shimazawa A, Shimazawa A, Augimoto T, Omote H, Ma JF, Shinozaki K, Moriyama Y (2015) AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis. Nat Commun 6:5928CrossRefGoogle Scholar
  37. Moscatello S, Proietti S, Buonaurio R, Famiani F, Raggi V, Walker RP, Battistelli A (2017) Peach leaf curl disease shifts sugar metabolism in severely infected leaves from source to sink. Plant Physiol Biochem 112:9–18CrossRefGoogle Scholar
  38. Muchhal US, Raghothama K (1999) Transcriptional regulation of plant phosphate transporters. Proc Natl Acad Sci USA 96:5868–5872CrossRefGoogle Scholar
  39. Muchhal US, Pardo JM, Raghothama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci USA 93:10519–10523CrossRefGoogle Scholar
  40. Nagarajan VK, Jain A, Poling MD, Lewis AJ, Raghothama KG, Smith AP (2011) Arabidopsis Pht1;5 Mobilizes Phosphate between Source and Sink Organs and Influences the Interaction between Phosphate Homeostasis and Ethylene Signaling. Plant Physiol 156:1149–1163CrossRefGoogle Scholar
  41. Nakamori K, Takabatake R, Umehara Y, Kouchi H, Izui K, Hata S (2002) Cloning, functional expression, and mutational analysis of a cDNA for Lotus japonicus mitochondrial phosphate transporter. Plant Cell Physiol 43:1250–1253CrossRefGoogle Scholar
  42. Okumura S, Mitsukawa N, Shirano Y, Shibata D (1998) Phosphate Transporter Gene Family of Arabidopsis thaliana. DNA Research 5:261–269CrossRefGoogle Scholar
  43. Oropeza-Aburto A, Cruz-Ramirez A, Acevedo-Hernandez GJ, Perez-Torres CA, Caballero-Perez J, Herrera-Estrella L (2012) Functional analysis of the Arabidopsis PLDZ2 promoter reveals an evolutionarily conserved low-Pi-responsive transcriptional enhancer element. J Exp Bot 63:2189–2202CrossRefGoogle Scholar
  44. Pandey BK, Mehra P, Verma L, Bhadouria J, Giri J (2017) OsHAD1, a Haloacid Dehalogenase-Like APase, Enhances Phosphate Accumulation. Plant Physiol 174:2316–2332CrossRefGoogle Scholar
  45. Paul EV, Sandeep S (2010) Proline Metabolism and Its Implications for Plant-Environment Interaction. The Arabidopsis Book published By American Society of Plant Biologists, November 3, e0140.10.1199/tab.0140, pp. 2-23Google Scholar
  46. Pavon LR, Lundh F, Lundin B, Mishra A, Persson BL, Spetea C (2008) Arabidopsis ANTR1 is a thylakoid Na+-dependent phosphate transporter: functional characterization in Escherichia coli. J Biol Chem 283:13520–13527CrossRefGoogle Scholar
  47. Plaxton WC, Carswell MC (1999) Metabolic aspects of the phosphate starvation response in plants. In: Lerner R (ed) Plant responses to environmental stresses: from phytohormones to genome reorganization. Marcel Dekker, New York, pp. 349–372Google Scholar
  48. Poirier Y, Bucher M (2002) Phosphate transport and homeostasis in Arabidopsis. Arabidopsis Book 1: e24CrossRefGoogle Scholar
  49. Qin L, Zhao J, Tian J, Chen L, Sun Z, Guo Y, Lu X, Gu M, Xu G, Liao H (2012) The high-affinity phosphate transporter GmPT5 regulates phosphate transport to nodules and nodulation in soybean. Plant Physiol 159:1634–1643CrossRefGoogle Scholar
  50. Roth C, Menzel G, Petetot JM, Rochat-Hacker S, Poirier Y (2004) Characterization of a protein of the plastid inner envelope having homology to animal inorganic phosphate, chloride and organicanion transporters. Planta 218:406–416CrossRefGoogle Scholar
  51. Shenoy V, Kalagudi G (2005) Enhancing plant phosphorus use efficiency for sustainable cropping. Biotechnol Adv 23:501–513CrossRefGoogle Scholar
  52. Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG (2008) Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol J 6:722–732CrossRefGoogle Scholar
  53. Singh Gahoonia T, Nielsen NE (2004) Root traits as tools for creating phosphorus effi cient crop varieties. Plant Soil 260:47–57CrossRefGoogle Scholar
  54. Sperdouli I, Moustakas M (2012) Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. J Plant Physiol 169:577–585CrossRefGoogle Scholar
  55. Stefanovic A, Ribot C, Rouached H, Wang Y, Chong J, Belbahri L, Delessert S, Poirier Y (2007) Members of the PHO1 gene family show limited functional redundancy in phosphate transfer to the shoot, and are regulated by phosphate deficiency via distinct pathways. Plant J 50:982–994CrossRefGoogle Scholar
  56. Sun S, Gu M, Cao Y, Huang X, Zhang X, Ai P, Zhao J, Fan X, Xu G (2012) A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphatereplete Rice. Plant Physiol 159:1571–1581CrossRefGoogle Scholar
  57. Thibaud MC, Arrighi JF, Bayle V, Chiarenza S, Creff A, Bustos R, Paz-Ares J, Poirier Y, Nussaume L (2010) Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64:775–789CrossRefGoogle Scholar
  58. Versaw WK (2002) A Chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphatestarvation responses. Plant Cell 14:1751–1766CrossRefGoogle Scholar
  59. Wang C, Huang W, Ying Y, Li S, Secco D, Tyerman S, Whelan J, Shou H (2012) Functional characterization of the rice SPX-MFS family reveals a key role of OsSPX-MFS1 in controlling phosphate homeostasis in leaves. New Phytol 196:139–148CrossRefGoogle Scholar
  60. Wang C, Ying S, Huang H, Li K, Wu P, Shou H (2009) Involvement of OsSPX1 in phosphate homeostasis in rice. Plant J 57: 895–904CrossRefGoogle Scholar
  61. Wang C, Yue W, Ying Y, Wang S, Secco D, Liu Y, Whelan J, Tyerman SD, Shou H (2015) Rice SPX-Major Facility Superfamily3, a Vacuolar Phosphate Efflux Transporter, Is Involved in Maintaining Phosphate Homeostasis in Rice. Plant Physiol 169:2822–2831Google Scholar
  62. Wang GY, Shi JL, Ng G, Battle SL, Zhang C, Lu H (2011) Circadian clock-regulated phosphate transporter PHT4;1 plays an important role in Arabidopsis defense. Mol Plant 4:516–526CrossRefGoogle Scholar
  63. Wintermans JF, De Mots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochim Biophys Acta 109:448–453CrossRefGoogle Scholar
  64. Wissuwa M, Yano M, Ae N (1998) Mapping of QTLs for phosphorusdeficiency tolerance in rice (Oryza sativa L.). Theor Appl Genet 97:777–783CrossRefGoogle Scholar
  65. Wu P, Shou H, Xu G, Lian X (2013) Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr Opin Plant Biol 16:205–212CrossRefGoogle Scholar
  66. Xu L, Jin L, Long L, Liu L, He X, Gao W, Zhu L, Zhang X (2012) Overexpression of GbWRKY1 positively regulates the Pi starvation response by alteration of auxin sensitivity in Arabidopsis. Plant Cell Rep 31:2177–2188CrossRefGoogle Scholar
  67. Yang H, Knapp J, Koirala P, Rajagopal D, Peer WA, Silbart LK, Murphy A, Gaxiola RA (2007) Enhanced phosphorus nutrition in monocots and dicots over-expressing a phosphorus-responsive type I H+-pyrophosphatase. Plant Biotechnol J 5:735–745CrossRefGoogle Scholar
  68. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572CrossRefGoogle Scholar
  69. Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14CrossRefGoogle Scholar
  70. Zhang F, Sun Y, Pei W, Jain A, Sun R, Cao Y, Wu X, Jiang T, Zhang L, Fan X, Chen A, Shen Q, Xu GH, Sun S (2015) Involvement of OsPht1;4 in phosphate acquisition and mobilization facilitates embryo development in rice. Plant J 82:556–569CrossRefGoogle Scholar
  71. Zhu W, Miao Q, Sun D, Yang G, Wu C, Huang J, Zheng C (2012) The mitochondrial phosphate transporters modulate plant responses to salt stress via affecting ATP and gibberellin metabolism in Arabidopsis thaliana. PLoS One 7:e43530CrossRefGoogle Scholar

Copyright information

© Korean Society of Plant Biologists and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Guo-hong Yu
    • 1
    • 2
  • Sheng-cai Huang
    • 1
  • Rui He
    • 3
  • Ying-zhang Li
    • 2
  • Xian-guo Cheng
    • 1
    Email author
  1. 1.Lab of Plant Nutrition Molecular Biology, Institute of Agricultural Resources and Regional PlanningChinese Academy of Agricultural SciencesBeijingP. R. China
  2. 2.College of Biological SciencesChina Agricultural UniversityBeijingP. R. China
  3. 3.College of Land and EnvironmentShenyang Agricultural UniversityShenyangP. R. China

Personalised recommendations