Skip to main content
Log in

Identification and expression analysis of the Hevea brasiliensis phosphate transporter 1 gene family

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

Twelve HbPHT1s were identified in Hevea and most of them were induced by phosphate starvation. HbPHT1;5 complemented the defective yeast mutant strain EY917 and HbPHT1;7 only partly complemented it.

Abstract

Phosphorus is an important element of the latex of rubber tree, and its content affects the quality and yield of latex. However, with the outflow of latex, a large amount of phosphorus is lost. The phosphate transporter 1 (PHT1) family proteins regulate the phosphorus acquisition and translocation in the plants, but their expression and roles in Hevea brasiliensis remain unclear. In this work, we identified twelve HbPHT1s (HbPHT1;1 to HbPHT1;12). Evolutionary analyses suggested two duplication events: HbPHT1;5/HbPHT1;6 and HbPHT1;7/HbPHT1;8. In the promoter region of some HbPHT1s, there existed P1BS, W-box, MYB, and ethylene response cis-elements. All the HbPHT1s, except for HbPHT1;4, were expressed in the roots, and most of them were also expressed in the stems and leaves. HbPHT1;7 had the highest expression level in the roots, stems, and leaves. HbPHT1;5 and HbPHT1;6 had a relatively higher expression levels than other genes in latex. HbPHT1;5, HbPHT1;7, and HbPHT1;11 were induced by ethylene treatment. Most HbPHT1s were induced under phosphate starvation conditions in the seedling leaves, and the expression of HbPHT1;9 was 20-fold higher than the control. HbPHT1;5 complemented the deficiency of the yeast mutant strain EY917 in phosphate transportation under low- and high-phosphate conditions, and HbPHT1;7 restored the deficiency when 10 mM phosphate was supplied. These results suggested that the increased expression of PHT1s may improve the phosphate uptake, transport, and utilization in Hevea. It also provides the basis to sudy the phosphorus metabolism network and mine the gene resources for the genetic breeding of Hevea.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1 
Fig. 2 
Fig. 3 
Fig. 4 
Fig. 5 
Fig. 6 
Fig. 7 

Similar content being viewed by others

Abbreviations

PHT1:

Phosphate transporter 1

P:

Phosphorus

Pi:

Phosphate

MEME:

Multiple Em for Motif Elicitation

GSDS:

Gene Structure Display Server

P1BS:

PHR1 specific binding sequence

ACC:

1-Amino cyclopropane-1-carboxylic acid

References

  • Ai PH, Sun SB, Zhao JN et al (2009) Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. Plant J 57:798–809

    CAS  PubMed  Google Scholar 

  • Baek SH, Chung IM, Yun SJ (2001) Molecular cloning and characterization of a tobacco leaf cDNA encoding a phosphaste transporter. Mol Cell 11:1–6

    CAS  Google Scholar 

  • Chang MC, Gu M, Xia YW et al (2019) OsPHT1;3 mediates uptake, translocation, and remobilization of phosphate under extremely low phosphate regimes. Plant Physiol 179:656–670

    CAS  PubMed  Google Scholar 

  • Chao JC, Yang SG, Chen YY, Tian WM (2015) Evaluation of reference genes for quantitative real-time PCR analysis of the gene expression in laticifers on the basis of latex flow in rubber tree (Hevea brasiliensis Muell. Arg.). Front Plant Sci 7:1149. https://doi.org/10.3389/fpls.2016.01149

    Article  Google Scholar 

  • Chapin LJ, Jones ML (2009) Ethylene regulates phosphorus remobilization and expression of a phosphate transporter (PhPT1) during petunia corolla senescence. J Exp Bot 60:2179–2190

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen AQ, Chen X, Wang HM et al (2014) Genome-wide investigation and expression analysis suggest diverse roles and genetic redundancy of Pht1 family genes in response to Pi deficiency in tomato. BMC Plant Biol 14:61

    PubMed  PubMed Central  Google Scholar 

  • Chen AQ, Hu J, Sun SB, Xu GH (2007) Conservation and divergence of both phosphate- and mycorrhiza-regulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytol 173:817–831

    CAS  PubMed  Google Scholar 

  • Gao L, Sun Y, Wu M et al (2018) Physiological and proteomic analyses of molybdenum- and ethylene-responsive mechanisms in rubber latex. Front Plant Sci 9:621

    PubMed  PubMed Central  Google Scholar 

  • González-Muñoz E, Avendaño-Vázquez AO, Chávez Montes RA et al (2015) The maize (Zea mays ssp. mays var. B73) genome encodes 33 members of the purple acid phosphatase family. Front Plant Sci 6:341

    PubMed  PubMed Central  Google Scholar 

  • Grün A, Buchner P, Broadley MR, Hawkesford MJ (2018) Identification and expression profiling of Pht1 phosphate transporters in wheat in controlled environments and in the field. Plant Biol (stuttg) 20:374–389

    Google Scholar 

  • Howe E, Holton K, Nair S, Schlauch D, Sinha R, Quackenbush J (2010) MeV: MultiExperiment Viewer. In: Ochs MF, Casagrande JT, Davuluri RV (eds) Biomedical Informatics for Cancer Research, 15th edn. Springer, New York, pp 267–277

    Google Scholar 

  • Jones P, Binns D, Chang HY et al (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29

    CAS  PubMed  Google Scholar 

  • Karthikeyan AS, Varadarajan DK, Mukatira UT et al (2002) Regulated expression of Arabidopsis phosphate transporters. Plant Physiol 130:221–233

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krzywinski M, Schein J, Birol I et al (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lacote R, Gabla O, Obouayeba S et al (2007) Some considerations concerning the yield potential of some clones (Hevea brasiliensis). In: International natural rubber conference. Cambodia, Siem Reap, pp 272–286

  • Lapis-Gaza HR, Jost R, Finnegan PM (2014) Arabidopsis PHOSPHATE TRANSPORTER1 genes PHT1;8 and PHT1;9 are involved in root-to-shoot translocation of orthophosphate. BMC Plant Biol 14:334

    PubMed  PubMed Central  Google Scholar 

  • Lei M, Zhu C, Liu Y et al (2011) Ethylene signaling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyaninin Arabidopsis. New Phytol 189:1084–1095

    CAS  PubMed  Google Scholar 

  • Lescot M, Déhais P, Thijs G et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequence. Nucleic Acids Res 30:325–327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin WY, Lin S, Chiou TJ (2009) Molecular regulators of phosphate homeostasis in plants. J Exp Bot 60:1427–1438

    CAS  PubMed  Google Scholar 

  • Liu BL, Zhao S, Wu XF et al (2017) Characterization of phosphate transporter genes in potato. J Biotechnol 264:17–28

    CAS  PubMed  Google Scholar 

  • Liu F, Chang XJ, Ye Y et al (2011) Comprehensive sequence and whole-life-cycle expression profile analysis of the phosphate transporter gene family in rice. Mol Plant 4:1105–1122

    CAS  PubMed  Google Scholar 

  • Liu F, Wang ZY, Ren HY et al (2010) OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. Plant J 62:508–517

    CAS  PubMed  Google Scholar 

  • Liu F, Xu YJ, Jiang HH et al (2016a) Systematic identification, evolution and expression analysis of the Zea mays PHT1 gene family reveals several new members involved in root colonization by arbuscular mycorrhizal fungi. Int J Mol Sci 17:930

    PubMed Central  Google Scholar 

  • Liu JP, Zhuang YF, Guo XL, Li YJ (2016b) Molecular mechanism of ethylene stimulation of latex yield in rubber tree (Hevea brasiliensis) revealed by de novo sequencing and transcriptome analysis. BMC Genomics 17:257

    PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Li YS, Gao Y, Tian QY et al (2011) Stimulation of root acid phosphatase by phosphorus deficiency is regulated by ethylene in Medicago falcata. Environ Epj Bot 71:114–120

    CAS  Google Scholar 

  • Li YT, Zhang J, Zhang X et al (2015) Phosphate transporter OsPht1;8 in rice plays an important role in phosphorus redistribution from source to sink organs and allocation between embryo and endosperm of seeds. Plant Sci 230:23–32

    CAS  PubMed  Google Scholar 

  • Loth-Pereda V, Orsini E, Courty PE et al (2011) Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal Populus trichocarpa. Plant Physiol 156:2141–2154

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muchhal US, Pardo JM, Raghothama KG (1996) Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci USA 93:10519–10523

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mudge SR, Rae AL, Diatloff E, Smith FW (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J 31:341–353

    CAS  PubMed  Google Scholar 

  • Nagarajan VK, Jain A, Poling MD et al (2011) Arabidopsis Pht1;5 mobilizes phosphate between source and sink organs and influences the interaction between phosphate homeostasis and ethylene signaling. Plant Physiol 156:1149–1163

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parra-Almuna L, Pontigo S, Larama G et al (2020) Expression analysis and functional characterization of two PHT1 family phosphate transporters in ryegrass. Planta 251:6

    CAS  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 99:13324–13329

    CAS  PubMed  PubMed Central  Google Scholar 

  • Preuss CP, Huang CY, Gilliham M, Tyerman SD (2010) Channel-like characteristics of the low-affinity barley phosphate transporter PHT1;6 when expressed in Xenopus Oocytes. Plant Physiol 152:1431–1441

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pudake RN, Mehta CM, Mohanta TK et al (2017) Expression of four phosphate transporter genes from finger millet Eleusine coracana L in response to mycorrhizal colonization and Pi stress. 3 Biotech 7(1):17

    PubMed  PubMed Central  Google Scholar 

  • Remy E, Cabrito TR, Batista RA et al (2012) The Pht1;9 and Pht1;8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation. New Phytol 195:356–371

    CAS  PubMed  Google Scholar 

  • Ren F, Guo QQ, Chang LL et al (2012) Brassica napus PHR1 gene encoding a MYB-Like protein functions in response to phosphate starvation. PLoS ONE 7:e44005

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rubio V, Linhares F, Solano R et al (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schünmann PH, Richardson AE, Vickers CE, Delhaize E (2004) Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol 136:4205–4214

    PubMed  PubMed Central  Google Scholar 

  • Shen JB, Yuan LX, Zhang JL et al (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642

    CAS  PubMed  Google Scholar 

  • Smith AP, Nagarajan VK, Raghothama KG (2011) Arabidopsis Pht1;5 plays an integral role in phosphate homeostasis. Plant Signal Behav 6:1676–1678

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song L, Liu D (2015) Ethylene and plant responses to phosphate deficiency. Front Plant Sci 6:1–14

    Google Scholar 

  • Sun SB, Gu M, Cao Y et al (2012) A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphate-replete rice. Plant Physiol 159:1571–1581

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun TT, Li MJ, Shao Y et al (2017) Comprehensive genomic identification and expression analysis of the phosphate transporter (PHT) gene family in apple. Front Plant Sci 8:426

    PubMed  PubMed Central  Google Scholar 

  • Tang CR, Qi JY, Li HP et al (2007) A convenient and efficient protocol for isolating high-quality RNA from latex of Hevea brasiliensis (para rubber tree). J Biochem Bioph Meth 70:749–754

    CAS  Google Scholar 

  • Tang CR, Yang M, Fang FY et al (2016) The rubber tree genome reveals new insights into rubber production and species adaptation. Nat Plants 2:16073

    CAS  PubMed  Google Scholar 

  • Tao CC, Jin X, Zhu LP et al (2018) Genome-wide investigation and expression profiling of APX gene family in Gossypium hirsutum provide new insights in redox homeostasis maintenance during different fiber development stages. Mol Genet Genom 293:685–697

    CAS  Google Scholar 

  • Teng W, Zhao YY, Zhao XQ et al (2017) Genome-wide identification, characterization, and expression analysis of PHT1 phosphate transporters in wheat. Front Plant Sci 8:543

    PubMed  PubMed Central  Google Scholar 

  • Wang W, Feng B, Xiao J et al (2014) Cassava genome from a wild ancestor to cultivated varieties. Nat Commun 5:5110

    CAS  PubMed  Google Scholar 

  • Yang WT, Baek D, Yun DJ et al (2014) Overexpression of OsMYB4P, an R2R3-type MYB transcriptional activator, increases phosphate acquisition in rice. Plant Physiol Biochem 80:259–267

    CAS  PubMed  Google Scholar 

  • Ye J, Coulouris G, Zaretskaya I et al (2012) Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ye Y, Yuan J, Chang XJ et al (2015) The phosphate transporter gene OsPht1;4 is involved in phosphate homeostasis in rice. PLoS ONE 10:e0126186

    PubMed  PubMed Central  Google Scholar 

  • Yu J, Wang J, Lin W et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38

    PubMed  PubMed Central  Google Scholar 

  • Zhang CX, Meng S, Li MJ, Zhao Z (2016) Genomic identification and expression analysis of the phosphate transporter gene family in poplar. Front Plant Sci 7:01398

    Google Scholar 

  • Zhang F, Wu XN, Zhou HM et al (2014) Overexpression of rice phosphate transporter gene OsPT6 enhances phosphate uptake and accumulation in transgenic rice plants. Plant Soil 384:259–270

    CAS  Google Scholar 

  • Zhang Q, Wang C, Tian J, Li K, Shou H (2011) Identification of rice purple acid phosphatases related to posphate starvation signalling. Plant Biol (stuttg) 13:7–15

    Google Scholar 

Download references

Acknowledgements

This research was supported by the Hainan Provincial Natural Science Foundation of China (No. 319MS088), the Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (No. 1630022017008, 1630052017007), the Hainan Provincial Science and Technology Project of China (No. ZDYF2018240).

Funding

This research was supported by the Hainan Provincial Natural Science Foundation of China (No. 319MS088), the Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (No. 1630022017008, 1630052017007), the Hainan Provincial Science and Technology Project of China (No. ZDYF2018240).

Author information

Authors and Affiliations

Authors

Contributions

Peng He and Yong Sun conceived and designed the experiments. Wenguan Wu, Bingsun Wu, and Guihua Wang prepared the materials. Yong Sun, Jiashao Wei, and Renjun Feng participated in the experiments. Dan Wang, Zheng Tong, Yong Sun, and Min Wu performed data analysis. The first draft of the manuscript was written by Yong Sun and Le Gao, all of the authors commented on previous versions of the manuscript and read and approved the final manuscript.

Corresponding authors

Correspondence to Renjun Feng or Peng He.

Ethics declarations

Conflicts of interest

The authors declare that they have no competing interests. We declare that we do not have any commercial or associative interest that represents a conflict of interest in connection with the work submitted.

Additional information

Communicated by Pierre Emmanuel Courty.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, Y., Gao, L., Wang, D. et al. Identification and expression analysis of the Hevea brasiliensis phosphate transporter 1 gene family. Trees 35, 407–419 (2021). https://doi.org/10.1007/s00468-020-02042-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-020-02042-2

Keyword

Navigation