Skip to main content
SpringerLink
Log in

Rice and chickpea GDPDs are preferentially influenced by low phosphate and CaGDPD1 encodes an active glycerophosphodiester phosphodiesterase enzyme

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Rice and chickpea GDPD s are transcriptionally influenced by mineral deficiencies; especially, by phosphate starvation and CaGDP1 encodes an active glycerophosphodiester phosphodiesterase enzyme.

Abstract

Glycerophosphodiester phosphodiesterases (GDPDs) are enzymes involved in the degradation of glycerophosphodiesters into sn-glycerol-3-phosphate and corresponding alcohols. These phospholipid remodeling genes have been suggested to play important roles in phosphate homeostasis. However, comprehensive information about the role of GDPDs under low phosphate (P) and other nutrient deficiencies (N, K, Fe, Zn) in rice and chickpea is missing. Here, we identified 13 OsGDPDs and 6 CaGDPDs in rice and chickpea, respectively, and partly characterized their roles in multiple nutrient stresses. Expression profiling after 7 and 15 days of deficiency treatments revealed unique and overlapping differential expression patterns of OsGDPDs and CaGDPDs under different nutrient stresses. Principal component analysis on the expression patterns of OsGDPDs and CaGDPDs revealed their preferential role in P starvation. Some of the GDPDs were also induced by N, K, Fe and Zn deficiency in temporal manner in both crops suggesting their roles in multiple nutrient stresses. Biochemical characterization of highly responsive chickpea GDPD, CaGDPD1, confirmed its in vitro GDPD activity and revealed its optimal temperature, pH and cofactor requirements. Further, CaGDPD1 showed its accumulation in ER and endomembranes. We hereby propose CaGDPD1 and various OsGDPDs as low P responsive marker genes in chickpea and rice, respectively. Our data uphold role of GDPDs in multinutrient responses and suggest them as candidates for rice and chickpea improvement for tolerance to various nutrient deficiencies.

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

GDPD:

Glycerophosphodiester phosphodiesterase

GPC:

Glycerophosphocholine

GPE:

Glycerophosphoethanolamine

GPI:

Glycerophosphoinositol

GPS:

Glycerophosphoglycerol

G3P:

Glycerol-3-Phosphate

References

  • Abida H, Dolch LJ, Meï C et al (2015) Membrane glycerolipid remodeling triggered by nitrogen and phosphorus starvation in Phaeodactylum tricornutum. Plant Physiol 167:118–136

    Article  CAS  PubMed  Google Scholar 

  • Ali MD, Krishnamurty L, Saxena NP, Rupela OP, Kumar J, Johansen C (2002) Scope for genetic manipulation of mineral acquisition in chickpea. Plant Soil 245:123–134

    Article  CAS  Google Scholar 

  • Andersson MX, Larsson KE, Tjellstrom H, Liljenberg C, Sandelius AS (2005) Phosphate-limited oat: the plasma membrane and the tonoplast as major targets for phospholipid-to-glycolipid replacement and stimulation of phospholipases in the plasma membrane. J Biol Chem 280:27578–27586

    Article  CAS  PubMed  Google Scholar 

  • Baligar VC, Fageria NK, He ZL (2001) Nutrient use efficiency in plants. Commun Soil Sci Plan 32:921–950

    Article  CAS  Google Scholar 

  • Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berrada AF, Shivakumar BG, Yaduraju NT (2007) Chickpea in cropping systems. In: Yadav SS, Chen W (eds) Chickpea breeding and management. CAB International, Wallingford, pp 193–212

    Chapter  Google Scholar 

  • Calderon-Vazquez C, Ibarra-Laclette E, Caballero-Perez J, Herrera-Estrella L (2008) Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and species-specific levels. J Exp Bot 59:2479–2497

    Article  CAS  PubMed  Google Scholar 

  • Cheng L, Bucciarelli B, Liu J, Zinn K, Miller S, Patton-Vogt J, Allan D, Shen J, Vance CP (2011a) White lupin cluster root acclimation to phosphorus deficiency and root hair development involve unique glycerophosphodiester phosphodiesterases. Plant Physiol 156:1131–1148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Y, Zhou W, Peters C, Li M, Wang X, Huang J (2011b) Characterization of the Arabidopsis glycerophosphodiester phosphodiesterase (GDPD) family reveals a role of the plastid-localized AtGDPD1 in maintaining cellular phosphate homeostasis under phosphate starvation. Plant J 66:781–795

    Article  CAS  PubMed  Google Scholar 

  • Corda D, Mosca MG, Ohshima N, Grauso L, Yanaka N, Mariggiò S (2014) The emerging physiological roles of the glycerophosphodiesterase family. FEBS J 281:998–1016

    Article  CAS  PubMed  Google Scholar 

  • de Nadal E, Ammerer G, Posas F (2011) Controlling gene expression in response to stress. Nat Rev Genet 12:833–845

    PubMed  Google Scholar 

  • Denloye T, Dalal S, Klemba M (2012) Characterization of a glycerophosphodiesterase with an unusual tripartite distribution and an important role in the asexual blood stages of Plasmodium falciparum. Mol Biochem Parasitol 186:29–37

    Article  CAS  PubMed  Google Scholar 

  • Fageria NK, Baligar VC, Heinemann AB, Carvalho MCS (2014) Nitrogen uptake and use efficiency in rice. In: Rakshit A, Singh HB, Sen A (eds) Nutrient use efficiency: from basics to advances. Springer, India, pp 285–296

    Google Scholar 

  • Farn J, Strugnell R, Hoyne P, Michalski W, Tennent J (2001) Molecular characterization of a secreted enzyme with phospholipase B activity from Moraxella bovis. J Bacteriol 183:6717–6720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández-Murray JP, McMaster CR (2005) Glycerophosphocholine catabolism as a new route for choline formation for phosphatidylcholine synthesis by the kennedy pathway. J Biol Chem 280:38290–38296

    Article  PubMed  Google Scholar 

  • Fisher E, Almaguer C, Holic R, Griac P, Patton-Vogt J (2005) Glycerophosphocholine-dependent growth requires Gde1p (YPL110c) and Git1p in Saccharomyces cerevisiae. J Biol Chem 280:36110–36117

    Article  CAS  PubMed  Google Scholar 

  • Food and Agriculture Organization (2015) World fertilizer trends and outlook to 2018. Food and Agriculture Organization of the United Nations, Rome

  • Gaude N, Bréhélin C, Tischendorf G, Kessler F, Dörmann P (2007) Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters. Plant J 49:729–739

    Article  CAS  PubMed  Google Scholar 

  • Giri J, Vij S, Dansana PK, Tyagi AK (2011) Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytol 191:721–732

    Article  CAS  PubMed  Google Scholar 

  • Graham PH, Vance CP (2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crops Res 65:93–106

    Article  Google Scholar 

  • Gunes A, Cicek N, Inal A, Alpaslan M, Eraslan F, Guneri E, Guzelordu T (2006) Genotypic response of chickpea (Cicer arietinum L.) cultivars to drought stress implemented at pre-and post-anthesis stages and its relations with nutrient uptake and efficiency. Plant Soil Environ 52:368–376

    CAS  Google Scholar 

  • Hafsi C, Russo MA, Sgherri C, Izzo R, Navari-Izzo F, Abdelly C (2009) Implication of phospholipase D in response of Hordeum vulgare root to short-term potassium deprivation. J Plant Physiol 166:499–506

    Article  CAS  PubMed  Google Scholar 

  • Hammond JP, Broadley MR, White PJ (2004) Genetic responses to phosphorus deficiency. Ann Bot 94:323–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammond JP, Broadley MR, Bowen HC, Hayden R, Spracklen WP, White PJ (2009) A molecular diagnostic for phosphorus deficiency in potatoes. In: Proceedings of the International Plant Nutrition Colloquium XVI, University of California Davis. http://www.escholarship.org/uc/item/9w97m6mz. Accessed 27 May 2009

  • Hayashi S, Ishii T, Matsunaga T, Tominaga R, Kuromori T, Wada T, Shinozaki K, Hirayama T (2008) The glycerophosphoryl diester phosphodiesterase-like proteins SHV3 and its homologs play important roles in cell wall organization. Plant Cell Physiol 49:1522–1535

    Article  CAS  PubMed  Google Scholar 

  • Hong Y, Devaiah DP, Thamasandra BN, Bahn SC, Li M, Welti R, Wang X (2009) Phospholipase Dɛ and phosphatidic acid enhance Arabidopsis growth. Plant J 58:376–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jain M, Misra G, Patel RK et al (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74:715–729

    Article  CAS  PubMed  Google Scholar 

  • Jones M, Raymond M, Smirnoff N (2006) Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J 45:83–100

    Article  CAS  PubMed  Google Scholar 

  • Kakei Y, Ogo Y, Itai RN, Kobayashi T, Yamakawa T, Nakanishi H, Nishizawa NK (2013) Development of a novel prediction method of cis-elements to hypothesize collaborative functions of cis-element pairs in iron-deficient rice. Rice 6:22

    Article  PubMed  PubMed Central  Google Scholar 

  • Kates M (1972) Identification of individual lipids and lipid moieties. In: Work TS, Work E (eds) Techniques of lipidology: isolation, analysis and identification of lipids. North Holland Publishing, Amsterdam, pp 502–579

    Google Scholar 

  • Larson TJ, Ehrmann M, Boos W (1983) Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli, a new enzyme of the glp regulon. J Biol Chem 258:5428–5432

    CAS  PubMed  Google Scholar 

  • Lemieux MJ, Huang Y, Wang DN (2004) Glycerol-3-phosphate transporter of Escherichia coli: structure, function and regulation. Res Microbiol 155:623–629

    Article  CAS  PubMed  Google Scholar 

  • Li M, Hong Y, Wang X (2009) Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochim Biophys Acta 1791:927–935

    Article  CAS  PubMed  Google Scholar 

  • Li L, Liu C, Lian X (2010) Gene expression profiles in rice roots under low phosphorus stress. Plant Mol Biol 72:423–432

    Article  CAS  PubMed  Google Scholar 

  • López-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  PubMed  Google Scholar 

  • Loppes R, Radoux M (2001) Identification of short promoter regions involved in the transcriptional expression of the nitrate reductase gene in Chlamydomonas reinhardtii. Plant Mol Biol 45:215–227

    Article  CAS  PubMed  Google Scholar 

  • Ma TL, Wu WH, Wang Y (2012) Transcriptome analysis of rice root responses to potassium deficiency. BMC Plant Biol 12:161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matos A, Pham-Thi A (2009) Lipid deacylating enzymes in plants: old activities, new genes. Plant Physiol Biochem 47:491–503

    Article  CAS  PubMed  Google Scholar 

  • Mehra P, Pandey BK, Giri J (2016) Comparative morphophysiological analyses and molecular profiling reveal Pi-efficient strategies of a traditional rice genotype. Front Plant Sci 6:1184

    Article  PubMed  PubMed Central  Google Scholar 

  • Misson J, Raghothama KG, Jain A et al (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102:11934–11939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura Y (2013) Phosphate starvation and membrane lipid remodeling in seed plants. Prog Lipid Res 52:43–50

    Article  CAS  PubMed  Google Scholar 

  • Nandwa SM, Bationo A, Obanyi SN, Rao IM, Sanginga N, Vanlauwe B (2011) Inter and intra-specific variation of legumes and mechanisms to access and adapt to less available soil phosphorus and rock phosphate. In: Bationo A, Waswa B, Okeyo JM, Maina F, Kihara J, Mokwunye U (eds) Fighting poverty in sub-Saharan Africa: the multiple roles of legumes in integrated soil fertility management. Springer, Netherlands, pp 47–66

    Chapter  Google Scholar 

  • Narasimhan R, Wang G, Li M, Roth M, Welti R, Wang X (2013) Differential changes in galactolipid and phospholipid species in soybean leaves and roots under nitrogen deficiency and after nodulation. Phytochemistry 96:81–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogawa N, DeRisi J, Brown PO (2000) New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. Mol Biol Cell 11:4309–4321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohshima N, Yamashita S, Takahashi N, Kuroishi C, Shiro Y, Takio K (2008) Escherichia coli cytosolic glycerophosphodiester phosphodiesterase (UgpQ) requires Mg2+, Co2+, or Mn2+ for its enzyme activity. J Bacteriol 190:1219–1223

    Article  CAS  PubMed  Google Scholar 

  • Oono Y, Kobayashi F, Kawahara Y, Yazawa T, Handa H, Itoh T, Matsumoto T (2013) Characterisation of the wheat (Triticum aestivum L.) transcriptome by de novo assembly for the discovery of phosphate starvation-responsive genes: gene expression in Pi-stressed wheat. BMC Genom 14:77

    Article  CAS  Google Scholar 

  • Pandey BK, Mehra P, Giri J (2013) Phosphorus starvation response in plants and opportunities for crop improvement. In: Tuteja N, Gill SS (eds) Climate change and plant abiotic stress tolerance. Wiley, Weinheim, pp 991–1012

    Chapter  Google Scholar 

  • Pariasca-Tanaka J, Satoh K, Rose T, Mauleon R, Wissuwa M (2009) Stress response versus stress tolerance: a transcriptome analysis of two rice lines contrasting in tolerance to phosphorus deficiency. Rice 2:167–185

    Article  Google Scholar 

  • Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rietz S, Holk A, Scherer GF (2004) Expression of the patatin-related phospholipase A gene AtPLA IIA in Arabidopsis thaliana is up-regulated by salicylic acid, wounding, ethylene, and iron and phosphate deficiency. Planta 219:743–753

    Article  CAS  PubMed  Google Scholar 

  • Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwenke GD, Peoples MB, Turner GL, Herridge DF (1998) Doses nitrogen fixation of commercial, dryland chickpea and faba bean crops in north-west New South Wales maintain or enhance soil nitrogen. Aust J Exp Agric 38:61–70

    Article  Google Scholar 

  • Secco D, Wang C, Shou H, Schultz MD, Chiarenza S, Nussaume L, Ecker JR, Whelan J, Lister R (2015) Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife 4:e09343

    Article  PubMed Central  Google Scholar 

  • Shah AL, Islam MR, Haque MM, Ishaque M, Miah MAM (2008) Efficacy of major nutrients in rice production. Bangladesh J Agric Res 33:639–645

    Google Scholar 

  • Simockova M, Holic R, Tahotna D, Patton-Vogt J, Griac P (2008) Yeast Pgc1p (YPL206c) controls the amount of phosphatidylglycerol via a phospholipase C-type degradation mechanism. J Biol Chem 283:17107–17115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh AP, Pandey BK, Deveshwar P, Narnoliya L, Parida SK, Giri J (2015) JAZ repressors: possible involvement in nutrients deficiency response in rice and chickpea. Front Plant Sci 6:975

    PubMed  PubMed Central  Google Scholar 

  • Sitkiewicz I, Stockbauer KE, Musser JM (2007) Secreted bacterial phospholipase A2 enzymes: better living through phospholipolysis. Trends Microbiol 15:63–69

    Article  CAS  PubMed  Google Scholar 

  • Ticconi CA, Lucero RD, Sakhonwasee S, Adamson AW, Creff A, Nussaume L, Desnos T, Abel S (2009) ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci USA 106:14174–14179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urzica EI, Vieler A, Hong-Hermesdorf A, Page MD, Casero D, Gallaher SD, Kropat J, Pellegrini M, Benning C, Merchant SS (2013) Remodeling of membrane lipids in iron-starved Chlamydomonas. J Biol Chem 288:30246–30258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van der Rest B, Boisson AM, Gout E, Bligny R, Douce R (2002) Glycerophosphocholine metabolism in higher plant cells: evidence of a new glyceryl-phosphodiester phosphodiesterase. Plant Physiol 130:244–255

    Article  PubMed  PubMed Central  Google Scholar 

  • Vinod KK, Heuer S (2012) Approaches towards nitrogen-and phosphorus-efficient rice. AoB Plants. doi:10.1093/aobpla/pls028

    Google Scholar 

  • Zheng L, Huang F, Narsai R et al (2009) Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol 51:262–274

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the research Grant of DBT (Grant No. BT/PR3299/AGR/2/813/2011), Government of India. P.M. acknowledge the financial support from CSIR, India.

Author information

Authors and Affiliations

  1. National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, 110067, India

    P. Mehra & J. Giri

Authors
  1. P. Mehra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Giri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Giri.

Ethics declarations

Conflict of interest

Authors declare that they have no conflict of interest.

Additional information

Communicated by A. Dhingra.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1 Multiple sequence alignment of GDPD domains of rice OsGDPDs and E. coli GDPDs (GlpQ and UgpQ) (PDF 271 kb)

Fig. S2 Multiple sequence alignment of GDPD domains of chickpea CaGDPDs and E. coli GDPDs (GlpQ and UgpQ) (PDF 222 kb)

299_2016_1984_MOESM3_ESM.eps

Fig. S3 Exon–intron structure organization of OsGDPDs and CaGDPDs. Gene models showing positions of exons and introns in rice and chickpea GDPDs. Illustrations were prepared by Gene Structure Display Server v. 2.0 (http://gsds.cbi.pku.edu.cn/) (EPS 2133 kb)

299_2016_1984_MOESM4_ESM.pptx

Fig. S4 Expression patterns of rice and chickpea GDPDs a Expression patterns of rice GDPDs obtained from microarray experiment GSE11966 in rice Affymetrix expression data. Color scale bar represents average log expression values (http://www.ricearray.org/expression/expression.php) b Gene expression of chickpea GDPDs in different tissues obtained from CTDB (http://www.nipgr.res.in/ctdb.html) in terms of RAM (reads per million) values. Color scale indicates levels of expression in different tissues (PPTX 209 kb)

Supplementary material 5 (DOCX 14 kb)

Supplementary material 6 (DOCX 13 kb)

Supplementary material 7 (DOCX 14 kb)

Supplementary material 8 (DOCX 14 kb)

Supplementary material 9 (PDF 162 kb)

Supplementary material 10 (PDF 120 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mehra, P., Giri, J. Rice and chickpea GDPDs are preferentially influenced by low phosphate and CaGDPD1 encodes an active glycerophosphodiester phosphodiesterase enzyme. Plant Cell Rep 35, 1699–1717 (2016). https://doi.org/10.1007/s00299-016-1984-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-016-1984-0

Keywords

Search

Navigation