Skip to main content

Advertisement

SpringerLink
Log in

Phosphate supply influenced the growth, yield and expression of PHT1 family phosphate transporters in seven millets

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

Abstract

Main conclusion

Phosphate starvation altered the root morphology and phosphate uptake with the induction of PHT1 family transporter genes in root and shoot tissues of seven millets.

Abstract

Millets are nutrient-rich cereals majorly cultivated in Asia and Africa. Foxtail millet (FoxM), pearl millet (PeaM), finger millet (FinM), kodo millet (KodM), little millet (LitM), proso millet (ProM), and barnyard millet (BarM) were examined for the influence of external phosphorous (P) supply on phenotypic traits, P uptake, yield, and PHosphate Transporter1 (PHT1) family gene expression. Millet seedlings grown under low Pi condition (LPC) produced significantly lower mean values for all traits except for lateral root length (LRL) and lateral root number (LRN) which were increased under LPC. Under LPC, seed weight (SW) also reduced by > 75% and had significantly lower levels of total P (TP) and Pi contents in leaf and root tissues. Expression dynamics of 12 PHT1 family (PHT1;1–1;12) transporters genes were analyzed in 7 millets. PHT1;2 has been found to be a constitutive transporter gene in all millets. Under LPC, root tissues showed the overexpression of PHT1;2, 1;3, 1;4 and 1;9 in FoxM, PHT1;1, 1;2, 1;3, 1;4, 1;8 and 1;10 in PeaM, PHT1;2 and 1;3 in FinM and ProM and PHT1;3, 1;6 and 1;11 in BarM. In leaf, LPC induced the expression of PHT1;3, 1;4 and 1;6 in FoxM, PHT1;2, 1;3, 1;4 and 1;8 in PeaM, PHT1;2, 1;3 and 1;4 in FinM and KodM, PHT1;2 in LitM and PHT1;4 in ProM and BarnM. This comprehensive study on the influence of P in phenotype, physiology, and molecular responses may help to improve the P uptake and its use efficiency of millets in future.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

BarM:

Barnyard millet

FinM:

Finger millet

FoxM:

Foxtail millet

HPC/LPC:

High/low Pi condition

KodM:

Kodo millet

LitM:

Little millet

LRL/LRN:

Lateral root length/number

PeaM:

Pearl millet

PHT1:

Phosphate transporter 1

PRL:

Primary root length

ProM:

Proso millet

RDW/SDW:

Root/shoot dry weight

SW:

Seed weight (yield)

TP:

Total phosphorus

References

  • Ai P, Sun S, Zhao J, Fan X, Xin W, Guo Q, Yu L, Shen Q, Wu P, Miller AJ (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 

  • Ames BN (1966) Assay of inorganic phosphate, tlotal phosphate and phosphatases. Methods Enzymol 8:115–118

    CAS  Google Scholar 

  • Amtmann A, Hammond JP, Armengaud P, White PJ (2005) Nutrient sensing and signalling in plants: potassium and phosphorus. Adv Bot Res 43:209–257

    Google Scholar 

  • Baker A, Ceasar SA, Palmer AJ, Paterson JB, Qi W, Muench SP, Baldwin SA (2015) Replace, reuse, recycle: improving the sustainable use of phosphorus by plants. J Exp Bot 66:3523–3540

    CAS  PubMed  Google Scholar 

  • Basirat M, Malboobi MA, Mousavi A, Asgharzadeh A, Samavat S (2011) Effects of phosphorous supply on growth, phosphate distribution and expression of transporter genes in tomato plants. Aust J Crop Sci 5:537–543

    CAS  Google Scholar 

  • Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, Estep M, Feng L, Vaughn JN, Grimwood J (2012) Reference genome sequence of the model plant Setaria. Nat Biotechnol 30:555–561

    CAS  PubMed  Google Scholar 

  • Cakmak I, Hengeler C, Marschner H (1994) Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. J Exp Bot 45:1245–1250

    CAS  Google Scholar 

  • Ceasar SA (2018) Genome-wide identification and in silco analysis of PHT1 family genes and proteins in Setaria viridis: a best model to study the nutrient transport in millets. Plant Genome 12:1–9

    Google Scholar 

  • Ceasar SA, Ignacimuthu S (2009) Genetic engineering of millets: current status and future prospects. Biotechnol Lett 31:779–788

    CAS  PubMed  Google Scholar 

  • Ceasar SA, Hodge A, Baker A, Baldwin SA (2014) Phosphate concentration and arbuscular mycorrhizal colonisation influence the growth, yield and expression of twelve PHT1 family phosphate transporters in foxtail millet (Setaria italica). PLoS One 9:e108459

    PubMed  PubMed Central  Google Scholar 

  • Ceasar SA, Baker A, Muench SP, Ignacimuthu S, Baldwin SA (2016) The conservation of phosphate-binding residues among PHT1 transporters suggests that distinct transport affinities are unlikely to result from differences in the phosphate-binding site. Biochem Soc Trans 44:1541–1548

    CAS  PubMed  Google Scholar 

  • Ceasar SA, Baker A, Ignacimuthu S (2017) Functional characterization of the PHT1 family transporters of foxtail millet with development of a novel Agrobacterium-mediated transformation procedure. Sci Rep 7:e14064

    Google Scholar 

  • Ceasar S, Maharajan T, Ajeesh Krishna T, Ramakrishnan M, Victor Roch G, Satish L, Ignacimuthu S (2018) Finger illet [Eleusine coracana (L.) Gaertn.] improvement: current status and future interventions of whole genome sequence. Front Plant Sci 9:e1054

    Google Scholar 

  • Chen A, Chen X, Wang H, Liao D, Gu M, Qu H, Sun S, Xu G (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:e61

    Google Scholar 

  • Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CI (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–421

    CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz LM, Ricaurte J, Cajiao C, Galeano CH, Rao I, Beebe S, Raatz B (2017) Phenotypic evaluation and QTL analysis of yield and symbiotic nitrogen fixation in a common bean population grown with two levels of phosphorus supply. Mol Breed 37:76–92

    Google Scholar 

  • Edgerton MD (2009) Increasing crop productivity to meet global needs for feed, food, and fuel. Plant Physiol 149:7–13

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ganie AH, Ahmad A, Pandey R, Aref IM, Yousuf PY, Ahmad S, Iqbal M (2015) Metabolite profiling of low-P tolerant and low-P sensitive maize genotypes under phosphorus starvation and restoration conditions. PLoS One 10:e0129520

    PubMed  PubMed Central  Google Scholar 

  • Gemenet DC, Hash CT, Sanogo MD, Sy O, Zangre RG, Leiser WL, Haussmann BI (2015) Phosphorus uptake and utilization efficiency in West African pearl millet inbred lines. Field Crops Res 171:54–66

    Google Scholar 

  • Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698

    CAS  PubMed  Google Scholar 

  • Hatakeyama M, Aluri S, Balachadran MT, Sivarajan SR, Patrignani A, Grüter S, Poveda L, Shimizu-Inatsugi R, Baeten J, Francoijs KJ (2017) Multiple hybrid de novo genome assembly of finger millet, an orphan allotetraploid crop. DNA Res 25:39–47

    PubMed Central  Google Scholar 

  • Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11:610–617

    CAS  PubMed  Google Scholar 

  • Hittalmani S, Mahesh H, Shirke MD, Biradar H, Uday G, Aruna Y, Lohithaswa H, Mohanrao A (2017) Genome and transcriptome sequence of finger millet (Eleusine coracana (L.) Gaertn.) provides insights into drought tolerance and nutraceutical properties. BMC Genom 18:e465

    Google Scholar 

  • Hur YJ, Lee HG, Jeon EJ, Lee YY, Nam MH, Yi G, Eun MY, Nam J, Lee JH, Kim DH (2007) A phosphate starvation-induced acid phosphatase from Oryza sativa: phosphate regulation and transgenic expression. Biotechnol Lett 29:829–835

    CAS  PubMed  Google Scholar 

  • Jeong K, Julia CC, Waters DL, Pantoja O, Wissuwa M, Heuer S, Liu L, Rose TJ (2017) Remobilisation of phosphorus fractions in rice flag leaves during grain filling: implications for photosynthesis and grain yields. PLoS One 12:e0187521

    PubMed  PubMed Central  Google Scholar 

  • Jia H, Ren H, Gu M, Zhao J, Sun S, Chen J, Wu P, Xu G (2011) Phosphate transporter gene, OsPHT1; 8, is involved in phosphate homeostasis in rice. Plant Physiol 156:1164–1175

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones JB Jr (1998) Phosphorus toxicity in tomato plants: when and how does it occur? Commun Soil Sci Plant Anal 29:1779–1784

    CAS  Google Scholar 

  • Julia CC, Rose TJ, Pariasca-Tanaka J, Jeong K, Masuda T, Wissuwa M (2018) Phosphorus uptake commences at the earliest stages of seedling development in rice (Oryza sativa L.). J Exp Bot 69:5233–5240

    CAS  PubMed  Google Scholar 

  • Kumar A, Metwal M, Kaur S, Gupta AK, Puranik S, Singh S, Singh M, Gupta S, Babu B, Sood S (2016) Nutraceutical value of finger millet [Eleusine coracana (L.) Gaertn.], and their improvement using omics approaches. Front Plant Sci 7:e934

    Google Scholar 

  • Kumar A, Tomer V, Kaur A, Kumar V, Gupta K (2018) Millets: a solution to agrarian and nutritional challenges. Agric Food Secur 7:31–46

    Google Scholar 

  • Lazaro L, Abbate P, Cogliatti D, Andrade F (2010) Relationship between yield, growth and spike weight in wheat under phosphorus deficiency and shading. J Agric Sci 148:83–93

    CAS  Google Scholar 

  • Leiser WL, Rattunde HFW, Weltzien E, Haussmann BI (2014) Phosphorus uptake and use efficiency of diverse West and Central African sorghum genotypes under field conditions in Mali. Plant Soil 377:383–394

    CAS  Google Scholar 

  • Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain JL, Laloi M, Coutos-Thévenot P, Maurousset L (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:e272

    Google Scholar 

  • Li K, Xu C, Zhang K, Yang A, Zhang J (2007) Proteomic analysis of roots growth and metabolic changes under phosphorus deficit in maize (Zea mays L.) plants. Proteomics 7:1501–1512

    CAS  PubMed  Google Scholar 

  • Liu K, Ma B, Luan L, Li C (2011) Nitrogen, phosphorus, and potassium nutrient effects on grain filling and yield of high-yielding summer corn. J Plant Nutr 34:1516–1531

    CAS  Google Scholar 

  • Liu F, Xu Y, Jiang H, Jiang C, Du Y, Gong C, Wang W, Zhu S, Han G, Cheng B (2016) 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 17:930–948

    PubMed Central  Google Scholar 

  • López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256

    PubMed  PubMed Central  Google Scholar 

  • Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512

    Google Scholar 

  • Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131:1381–1390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahamood J, Abayomi Y, Aduloju M (2009) Comparative growth and grain yield responses of soybean genotypes to phosphorous fertilizer application. Afr J Biotechnol 8:1030–1036

    CAS  Google Scholar 

  • Maharajan T, Ceasar SA, Ajeesh krishna TP, Ramakrishnan M, Duraipandiyan V, Naif Abdulla AD, Ignacimuthu S (2018) Utilization of molecular markers for improving the phosphorus efficiency in crop plants. Plant Breed 137:10–26

    CAS  Google Scholar 

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

    CAS  PubMed  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 

  • Nadeem M, Mollier A, Morel C, Vives A, Prud’homme L, Pellerin S (2011) Relative contribution of seed phosphorus reserves and exogenous phosphorus uptake to maize (Zea mays L.) nutrition during early growth stages. Plant Soil 346:231–244

    CAS  Google Scholar 

  • 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 156:1149–1163

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nussaume L, Kanno S, Javot H, Marin E, Nakanishi TM, Thibaud MC (2011) Phosphate import in plants: focus on the PHT1 transporters. Front Plant Sci 2:e83

    Google Scholar 

  • Pandey R, Dubey KK, Ahmad A, Nilofar R, Verma R, Jain V, Zinta G, Kumar V (2015) Elevated CO2 improves growth and phosphorus utilization efficiency in cereal species under sub-optimal phosphorus supply. J Plant Nut 38:1196–1217

    CAS  Google Scholar 

  • Pariasca-Tanaka J, Vandamme E, Mori A, Segda Z, Saito K, Rose TJ, Wissuwa M (2015) Does reducing seed-P concentrations affect seedling vigor and grain yield of rice? Plant Soil 392:253–266

    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  Google Scholar 

  • Plenet D, Etchebest S, Mollier A, Pellerin S (2000) Growth analysis of maize field crops under phosphorus deficiency. Plant Soil 223:119–132

    Google Scholar 

  • Pudake RN, Mehta CM, Mohanta TK, Sharma S, Varma A, Sharma AK (2017) Expression of four phosphate transporter genes from finger millet (Eleusine coracana L.) in response to mycorrhizal colonization and Pi stress. 3 Biotech 7:17–30

    PubMed  PubMed Central  Google Scholar 

  • Puranik S, Kam J, Sahu PP, Yadav R, Srivastava RK, Ojulong H, Yadav R (2017) Harnessing finger millet to combat calcium deficiency in humans: challenges and prospects. Front Plant Sci 8:e1311

    Google Scholar 

  • Qin L, Guo Y, Chen L, Liang R, Gu M, Xu G, Zhao J, Walk T, Liao H (2012) Functional characterization of 14 PHT1 family genes in yeast and their expressions in response to nutrient starvation in soybean. PLoS One 7:e47726

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ramakrishnan M, Ceasar SA, Vinod K, Duraipandiyan V, Krishna TA, Upadhyaya HD, Al-Dhabi N, Ignacimuthu S (2017) Identification of putative QTLs for seedling stage phosphorus starvation response in finger millet (Eleusine coracana L. Gaertn.) by association mapping and cross species synteny analysis. PLoS One 12:e0183261

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ramegowda Y, Venkategowda R, Jagadish P, Govind G, Hanumanthareddy RR, Makarla U, Guligowda SA (2013) Expression of a rice Zn transporter, OsZIP1, increases Zn concentration in tobacco and finger millet transgenic plants. Plant Biotechnol Rep 7:309–319

    Google Scholar 

  • Ren P, Ma X, Li B, Meng Y, Lai Y, Si E, Wang J, Yao L, Yang K, Shang X (2016) Identification and selection of low-phosphate-tolerant germplasm in barley (Hordeum vulgare L.). Soil Sci Plant Nutr 62:471–480

    CAS  Google Scholar 

  • Ren Y, Qian Y, Xu Y, Zou C, Liu D, Zhao X, Zhang A, Tong Y (2017) Characterization of QTLs for root traits of wheat grown under different nitrogen and phosphorus supply levels. Front Plant Sci 8:e2096

    Google Scholar 

  • Saha D, Gowda MC, Arya L, Verma M, Bansal KC (2016) Genetic and genomic resources of small millets. Crit Rev Plant Sci 35:56–79

    CAS  Google Scholar 

  • Saleh AS, Zhang Q, Chen J, Shen Q (2013) Millet grains: nutritional quality, processing, and potential health benefits. Compr Rev Food Sci Food Saf 12:281–295

    CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to IMAGEJ: 25 years of image analysis. Nat Methods 9:671–675

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shivran A (2016) Biofortification for nutrient-rich millets. In: Singh U, Praharaj CS, Singh SS, Singh NP (eds) Biofortification of food crops. Springer, New Delhi, pp 409–420

    Google Scholar 

  • Teng W, Zhao YY, Zhao XQ, He X, Ma WY, Deng Y, Chen XP, Tong YP (2017) Genome-wide identification, characterization, and expression analysis of PHT1 phosphate transporters in wheat. Front Plant Sci 8:543

    PubMed  PubMed Central  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    CAS  Google Scholar 

  • Varshney RK, Shi C, Thudi M, Mariac C, Wallace J, Qi P, Zhang H, Zhao Y, Wang X, Rathore A (2017) Pearl millet genome sequence provides a resource to improve agronomic traits in arid environments. Nat Biotechnol 35:969–985

    CAS  PubMed  Google Scholar 

  • Walder F, Brulé D, Koegel S, Wiemken A, Boller T, Courty PE (2015) Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the PHT1 family in sorghum and flax. New Phytol 205:1632–1645

    CAS  PubMed  Google Scholar 

  • White P, Brown P (2010) Plant nutrition for sustainable development and global health. Ann Bot 105:1073–1080

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wissuwa M, Gamat G, Ismail AM (2005) Is root growth under phosphorus deficiency affected by source or sink limitations? J Exp Bot 56:1943–1950

    CAS  PubMed  Google Scholar 

  • Zhang G, Liu X, Quan Z, Cheng S, Xu X, Pan S, Xie M, Zeng P, Yue Z, Wang W (2012) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol 30:549–556

    CAS  PubMed  Google Scholar 

  • Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12:1047–1064

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Lynch JP (2004) The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Funct Plant Biol 31:949–958

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the International Crops Research Institute for the Semi-Arid Tropics, Hyderabad, India and Tamil Nadu Agricultural University, Coimbatore, India for providing millet seeds. Prof Alison Baker, Centre for Plant Sciences, University of Leeds, UK for supplying foxtail millet PHT1 gene-specific primers.

Funding

This work was funded by Loyola College-Times of India Grant (No: 7LCTOI14ERI001) and European Union through a Marie Curie International Incoming Fellowship to SAC (Fellowship Number: FP7-People-2-11-IIF-Prposal-921672-Acronym IMPACT). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Division of Plant Biotechnology, Entomology Research Institute, Loyola College, Chennai, 600034, India

    Theivanayagam Maharajan, Stanislaus Antony Ceasar, Thumadath Palayullaparambil Ajeesh Krishna & Savarimuthu Ignacimuthu

  2. Functional Genomics and Plant Molecular Imaging Lab, University of Liege, 4000, Liege, Belgium

    Stanislaus Antony Ceasar

Authors
  1. Theivanayagam Maharajan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stanislaus Antony Ceasar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thumadath Palayullaparambil Ajeesh Krishna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Savarimuthu Ignacimuthu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stanislaus Antony Ceasar.

Ethics declarations

Conflicts of interest

The authors declare that they have no competing interests.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 503 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maharajan, T., Ceasar, S.A., Krishna, T.P.A. et al. Phosphate supply influenced the growth, yield and expression of PHT1 family phosphate transporters in seven millets. Planta 250, 1433–1448 (2019). https://doi.org/10.1007/s00425-019-03237-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-019-03237-9

Keywords

Search

Navigation