Skip to main content

Advertisement

SpringerLink
Log in

Genome-wide expression analysis of rice aquaporin genes and development of a functional gene network mediated by aquaporin expression in roots

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

Abstract

The world population continually faces challenges of water scarcity for agriculture. A common strategy called water-balance control has evolved to adapt plant growth to these challenges. Aquaporins are a family of integral membrane proteins that play a central role in water-balance control. In this study, we identified 34 members of the rice aquaporin gene family, adding a novel member to the previous list. A combination of phylogenetic tree and anatomical meta-expression profiling data consisting of 983 Affymetrix arrays and 209 Agilent 44 K arrays was used to identify tissue-preferred aquaporin genes and evaluate functional redundancy among aquaporin family members. Eight aquaporins showed root-preferred expression in the vegetative growth stage, while 4 showed leaf/shoot-preferred expression. Integrating stress-induced expression patterns into phylogenetic tree and semi-quantitative reverse transcriptase polymerase chain reaction (RT-PCR) analyses revealed that 3 rice aquaporin genes were markedly downregulated and 4 were upregulated by water deficiency in the root, suggesting that these candidate genes are key regulators of water uptake from the soil. Finally, we constructed a functional network of genes mediated by water stress and refined the network by confirming the differential expression using RT-PCR and real-time PCR. Our data will be useful to elucidate the molecular mechanism of water-balance control in rice root.

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

Similar content being viewed by others

Abbreviations

AQP:

Aquaporin

D:

Day(s)

IDs:

Identifiers

H:

Hour(s)

Lsi:

Low silicon rice

MEGA:

Molecular evolutionary genetics analysis

Min:

Minute(s)

NIPs:

Nodulin 26-like intrinsic proteins

NPA:

Asparagine–proline–alanine region

PIPs:

Plasma membrane intrinsic proteins

qRT-PCR:

Semi-quantitative reverse transcription polymerase chain reaction

RGAP:

Rice genome annotation project database

RWC:

Rice water channel

SAM:

Shoot apical meristem

S:

Second(s)

SIPs:

Small basic intrinsic proteins

TIPs:

Tonoplast intrinsic proteins

XIPs:

Uncategorized X intrinsic proteins

References

  • Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59:469–484

    Article  PubMed  CAS  Google Scholar 

  • Boursiac Y, Prak S, Boudet J, Postaire O, Luu DT, Tournaire-Roux C, Santoni V, Maurel C (2008) The response of Arabidopsis root water transport to a challenging environment implicates reactive oxygen species- and phosphorylation-dependent internalization of aquaporins. Plant Signal Behav 3:1096–1098

    Article  PubMed  Google Scholar 

  • Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125:1206–1215

    Article  PubMed  CAS  Google Scholar 

  • Denker BM, Smith BL, Kuhajda FP, Agre P (1988) Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J Biol Chem 263:15634–15642

    PubMed  CAS  Google Scholar 

  • Eynard A, Lal R, Wiebe K (2005) Crop response in salt-affected soils. J Sustain Agric 27:5–50

    Article  Google Scholar 

  • Finkel T (2011) Signal transduction by reactive oxygen species. J Cell Biol 194:7–15

    Article  PubMed  CAS  Google Scholar 

  • Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu M, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16:277–286

    Article  PubMed  CAS  Google Scholar 

  • Hayano-Kanashiro C, Calderon-Vazquez C, Ibarra-Laclette E, Herrera-Estrella L, Simpson J (2009) Analysis of gene expression and physiological responses in three Mexican maize landraces under drought stress and recovery irrigation. PLoS ONE 4:e7531

    Article  PubMed  Google Scholar 

  • Heckwolf M, Pater D, Hanson DT, Kaldenhoff R (2011) The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO2 transport facilitator. Plant J 67:795–804

    Article  PubMed  CAS  Google Scholar 

  • Ishibashi K, Kondo S, Hara S, Morishita Y (2011) The evolutionary aspects of aquaporin family. Am J Physiol Regul Integr Comp Physiol 300:R566–R576

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa F, Suga S, Uemura T, Sato MH, Maeshima M (2005) Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana. FEBS Lett 579:5814–5820

    Article  PubMed  CAS  Google Scholar 

  • Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54:713–725

    Article  PubMed  CAS  Google Scholar 

  • Jang JY, Lee SH, Rhee JY, Chung GC, Ahn SJ, Kang H (2007) Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Mol Biol 64:621–632

    Article  PubMed  CAS  Google Scholar 

  • Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Guclu J, Vinh J, Heyes J, Franck KI, Schaffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509–522

    Article  PubMed  CAS  Google Scholar 

  • Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197

    Article  PubMed  CAS  Google Scholar 

  • Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126:1358–1369

    Article  PubMed  CAS  Google Scholar 

  • Johnson BD, Schumacher RJ, Ross ED, Toft DO (1998) Hop modulates Hsp70/Hsp90 interactions in protein folding. J Biol Chem 273:3679–3686

    Article  PubMed  CAS  Google Scholar 

  • Jolivet P, Roux E, D’Andrea S, Davanture M, Negroni L, Zivy M, Chardot T (2004) Protein composition of oil bodies in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 42:501–509

    Article  PubMed  CAS  Google Scholar 

  • Josine TL, Ji J, Wang G, Guan CF (2011) Advances in genetic engineering for plants abiotic stress control. Afr J Biotechnol 10:5402–5413

    Google Scholar 

  • Jung KH, Lee J, Dardick C, Seo YS, Cao P, Canlas P, Phetsom J, Xu X, Ouyang S, An K, Cho YJ, Lee GC, Lee Y, An G, Ronald PC (2008) Identification and functional analysis of light-responsive unique genes and gene family members in rice. PLoS Genet 4:e1000164

    Article  PubMed  Google Scholar 

  • Kaldenhoff R, Fischer M (2006) Aquaporins in plants. Acta Physiol (Oxf) 187:169–176

    Article  CAS  Google Scholar 

  • Kamiya T, Tanaka M, Mitani N, Ma JF, Maeshima M, Fujiwara T (2009) NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 284:2114–2120

    Article  PubMed  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lee I, Seo YS, Coltrane D, Hwang S, Oh T, Marcotte EM, Ronald PC (2011) Genetic dissection of the biotic stress response using a genome-scale gene network for rice. Proc Natl Acad Sci USA 108:18548–18553

    Article  PubMed  CAS  Google Scholar 

  • Li GW, Peng YH, Yu X, Zhang MH, Cai WM, Sun WN, Su WA (2008a) Transport functions and expression analysis of vacuolar membrane aquaporins in response to various stresses in rice. J Plant Physiol 165:1879–1888

    Article  PubMed  CAS  Google Scholar 

  • Li GW, Zhang MH, Cai WM, Sun WN, Su WA (2008b) Characterization of OsPIP2;7, a water channel protein in rice. Plant Cell Physiol 49:1851–1858

    Article  PubMed  CAS  Google Scholar 

  • Lian HL, Yu X, Ye Q, Ding X, Kitagawa Y, Kwak SS, Su WA, Tang ZC (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45:481–489

    Article  PubMed  CAS  Google Scholar 

  • Lian HL, Yu X, Lane D, Sun WN, Tang ZC, Su WA (2006) Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res 16:651–660

    Article  PubMed  CAS  Google Scholar 

  • Liang G, He H, Li Y, Yu D (2012) A new strategy for construction of artificial miRNA vectors in Arabidopsis. Planta 235:1421–1429

    Article  PubMed  CAS  Google Scholar 

  • Liu C, Fukumoto T, Matsumoto T, Gena P, Frascaria D, Kaneko T, Katsuhara M, Zhong S, Sun X, Zhu Y, Iwasaki I, Ding X, Calamita G, Kitagawa Y (2013) Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination. Plant Physiol Biochem 63:151–158

    Article  PubMed  CAS  Google Scholar 

  • Lu HA, Sun TX, Matsuzaki T, Yi XH, Eswara J, Bouley R, McKee M, Brown D (2007) Heat shock protein 70 interacts with aquaporin-2 and regulates its trafficking. J Biol Chem 282:28721–28732

    Article  PubMed  CAS  Google Scholar 

  • Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96

    Article  CAS  Google Scholar 

  • Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto T, Lian HL, Su WA, Tanaka D, Liu C, Iwasaki I, Kitagawa Y (2009) Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice. Plant Cell Physiol 50:216–229

    Article  PubMed  CAS  Google Scholar 

  • Maurel C (1997) Aquaporins and water permeability of plant membranes. Annu Rev Plant Physiol Plant Mol Biol 48:399–429

    Article  PubMed  CAS  Google Scholar 

  • Maurel C, Javot H, Lauvergeat V, Gerbeau P, Tournaire C, Santoni V, Heyes J (2002) Molecular physiology of aquaporins in plants. Int Rev Cytol 215:105–148

    Article  PubMed  CAS  Google Scholar 

  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624

    Article  PubMed  CAS  Google Scholar 

  • Mendonca AG, Alves RJ, Pereira-Leal JB (2011) Loss of genetic redundancy in reductive genome evolution. PLoS Comput Biol 7:e1001082

    Article  PubMed  CAS  Google Scholar 

  • Mihara M, Itoh T, Izawa T (2010) SALAD database: a motif-based database of protein annotations for plant comparative genomics. Nucleic Acids Res 38:D835–D842

    Article  PubMed  CAS  Google Scholar 

  • Miki D, Itoh R, Shimamoto K (2005) RNA silencing of single and multiple members in a gene family of rice. Plant Physiol 138:1903–1913

    Article  PubMed  CAS  Google Scholar 

  • Miller EW, Dickinson BC, Chang CJ (2010) Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc Natl Acad Sci USA 107:15681–15686

    Article  PubMed  CAS  Google Scholar 

  • Mitani-Ueno N, Yamaji N, Zhao FJ, Ma JF (2011) The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J Exp Bot 62:4391–4398

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150:1368–1379

    Article  PubMed  CAS  Google Scholar 

  • Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35:D883–D887

    Article  PubMed  CAS  Google Scholar 

  • Pandey S, Bhandari H, Hardy B (2007) Economic costs of drought and rice farmers’ coping mechanisms: a cross-country comparative analysis. International Rice Research Institute, Los Baños, p 203

    Google Scholar 

  • Pang Y, Li L, Ren F, Lu P, Wei P, Cai J, Xin L, Zhang J, Chen J, Wang X (2010) Overexpression of the tonoplast aquaporin AtTIP5;1 conferred tolerance to boron toxicity in Arabidopsis. J Genet Genomics 37(389–397):381–382

    Google Scholar 

  • Postaire O, Tournaire-Roux C, Grondin A, Boursiac Y, Morillon R, Schaffner AR, Maurel C (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiol 152:1418–1430

    Article  PubMed  CAS  Google Scholar 

  • Preston GM, Agre P (1991) Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc Natl Acad Sci USA 88:11110–11114

    Article  PubMed  CAS  Google Scholar 

  • Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ (2002) From genome to function: the Arabidopsis aquaporins. Genome Biol 3: RESEARCH0001

  • Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

    Article  PubMed  CAS  Google Scholar 

  • Rouard M, Guignon V, Aluome C, Laporte MA, Droc G, Walde C, Zmasek CM, Perin C, Conte MG (2011) GreenPhylDB v2.0: comparative and functional genomics in plants. Nucleic Acids Res 39:D1095–D1102

    Article  PubMed  CAS  Google Scholar 

  • Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411:134–193

    Article  PubMed  CAS  Google Scholar 

  • Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46:1568–1577

    Article  PubMed  CAS  Google Scholar 

  • Sakurai J, Ahamed A, Murai M, Maeshima M, Uemura M (2008) Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant Cell Physiol 49:30–39

    Article  PubMed  CAS  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  PubMed  CAS  Google Scholar 

  • Soto G, Alleva K, Mazzella MA, Amodeo G, Muschietti JP (2008) AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea. FEBS Lett 582:4077–4082

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Torres GAM, Gimenes MA, de Rosa Jr VE, Quecini V (2007) Identifying water stress-response mechanisms in citrus by in silico transcriptome analysis. Genet Mol Biol 30:888–905

    Article  CAS  Google Scholar 

  • van der Schoot C, Paul LK, Paul SB, Rinne PL (2011) Plant lipid bodies and cell–cell signaling: a new role for an old organelle? Plant Signal Behav 6:1732–1738

    Article  PubMed  Google Scholar 

  • Weaver CD, Shomer NH, Louis CF, Roberts DM (1994) Nodulin 26, a nodule-specific symbiosome membrane protein from soybean, is an ion channel. J Biol Chem 269:17858–17862

    PubMed  CAS  Google Scholar 

  • Weig A, Deswarte C, Chrispeels MJ (1997) The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol 114:1347–1357

    Article  PubMed  CAS  Google Scholar 

  • Yamaji N, Ma JF (2009) A transporter at the node responsible for intervascular transfer of silicon in rice. Plant Cell 21:2878–2883

    Article  PubMed  CAS  Google Scholar 

  • Yamaji N, Mitatni N, Ma JF (2008) A transporter regulating silicon distribution in rice shoots. Plant Cell 20:1381–1389

    Article  PubMed  CAS  Google Scholar 

  • Yu X, Peng YH, Zhang MH, Shao YJ, Su WA, Tang ZC (2006) Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery. Cell Res 16:599–608

    Article  PubMed  Google Scholar 

  • Zardoya R, Villalba S (2001) A phylogenetic framework for the aquaporin family in eukaryotes. J Mol Evol 52:391–404

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Next-Generation BioGreen 21 Program of South Korea (PJ008079 and PJ008173) to KHJ and a Young Scientist Program through the National Research Foundation of Korea (Grant no. 20120003801) to KHJ.

Author information

Authors and Affiliations

  1. Department of Plant Molecular Systems Biotechnology and Crop Biotech Institute, Kyung Hee University, Yongin, 446-701, Korea

    Minh Xuan Nguyen, Sunok Moon & Ki-Hong Jung

Authors
  1. Minh Xuan Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sunok Moon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ki-Hong Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ki-Hong Jung.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1 Chromosomal distribution of 34 rice aquaporin genes. Red boxes denote a new member (JPEG 1311 kb)

Fig. S2 The phylogenetic tree of rice aquaporin proteins (JPEG 1231 kb)

Fig. S3 The phylogenomic data of the rice aquaporins with orthologs from Arabidopsis and maize (EPS 3828 kb)

425_2013_1918_MOESM4_ESM.jpg

Fig. S4 Anatomical expression of rice aquaporin genes using 1150 Affymetrix and 209 Agilent 44 K arrays. A black bar denotes an indica cultivar and a grey bar a japonica cultivar (JPEG 1598 kb)

Table S1 Detailed information for 34 rice aquaporin genes (XLSX 12 kb)

425_2013_1918_MOESM6_ESM.docx

Table S2 Primer sequences for RT-PCR and real-time PCR of aquaporin genes and genes functionally associated with aquaporins, used in Figs. 2, 4, and 5 (DOCX 19 kb)

Table S3 Detailed comparison of microarrays used for Fig. 3 (XLSX 34 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nguyen, M.X., Moon, S. & Jung, KH. Genome-wide expression analysis of rice aquaporin genes and development of a functional gene network mediated by aquaporin expression in roots. Planta 238, 669–681 (2013). https://doi.org/10.1007/s00425-013-1918-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-013-1918-9

Keywords

Search

Navigation