Skip to main content
SpringerLink
Log in

Deciphering the Role of Aquaporins Under Different Abiotic Stress Conditions in Watermelon (Citrullus lanatus)

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Aquaporins (AQPs) play essential roles in various physiological processes by regulating the transport of water and various uncharged small solutes, like carbon dioxide, urea, and metalloids, including silicon (Si). In the present study, 35 AQPs were identified in the watermelon (Citrullus lanatus) genome and subsequently analyzed to understand their role and regulation during various abiotic stress conditions. For a better understanding of solute specificity, gene and protein structure of Citrullus lanatus AQPs (ClaAPQs) various computational tools were used. Based on the selectivity filters ClaNIP2-1 was characterized as Si transporter. Transcriptomics analysis revealed the expression of ClaAQPs under drought stress and during fruit development. In addition, differential expression of AQPs during drought, cold, salinity, and methyl jasmonate stress was observed with gene expression evaluated by quantitative real-time PCR (qRT-PCR). Interestingly, the expression of ClaTIP1-1 and ClaPIP2-4 was found to be increased during both cold and salinity stresses. In the early stages of stress, increased expression of ClaNIP2-1 and ClaPIP1-2 and ClaTIP1-1 was observed. The expression of ClaPIP1-2 was significantly increased at least once during methyl jasmonate, drought, salinity, and cold stress. The findings indicate that PIPs particularly ClaPIP1-2 and ClaPIP2-4 play a significant role in stress response. The information presented here will provide the fundamental basis of AQP-mediated transport system in watermelon and closely related Cucurbitaceae species.

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

Similar content being viewed by others

References

  • Afzal Z, Howton T, Sun Y, Mukhtar MS (2016) The roles of aquaporins in plant stress responses. J Dev Biol 4:9

    PubMed  PubMed Central  Google Scholar 

  • Alexandersson E, Fraysse L, Sjövall-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

    CAS  PubMed  Google Scholar 

  • Arvidsson S, Kwasniewski M, Riaño-Pachón DM, Mueller-Roeber B (2008) QuantPrime–a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinformatics 9:465

    PubMed  PubMed Central  Google Scholar 

  • Bienert GP, Bienert MD, Jahn TP, Boutry M, Chaumont F (2011) Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J 66:306–317

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    CAS  PubMed  Google Scholar 

  • de Paula Santos Martins C, Pedrosa AM, Du D, Goncalves LP, Yu Q, Gmitter FG Jr, Costa MGC (2015) Genome-wide characterization and expression analysis of major intrinsic proteins during abiotic and biotic stresses in sweet orange (Citrus sinensis L. Osb.). PLoS ONE 10:01387

    Google Scholar 

  • Deshmukh R, Bélanger RR (2016) Molecular evolution of aquaporins and silicon influx in plants. Funct Ecol 30:1277–1285

    Google Scholar 

  • Deshmukh RK, Vivancos J, Guérin V, Sonah H, Labbé C, Belzile F, Bélanger RR (2013) Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Mol Biol 83:303–315

    CAS  PubMed  Google Scholar 

  • Deshmukh RK, Vivancos J, Ramakrishnan G, Guérin V, Carpentier G, Sonah H, Labbé C, Isenring P, Belzile FJ, Bélanger RR (2015) A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants. Plant J 83:489–500

    CAS  PubMed  Google Scholar 

  • Deshmukh RK, Sonah H, Bélanger RR (2016) Plant Aquaporins: genome-wide identification, transcriptomics, proteomics, and advanced analytical tools. Front Plant Sci 7:1896

    PubMed  PubMed Central  Google Scholar 

  • Flexas J, Ribas-Carbó M, Hanson DT, Bota J, Otto B, Cifre J, McDowell N, Medrano H, Kaldenhoff R (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2in vivo. Plant J 48:427–439

    CAS  PubMed  Google Scholar 

  • Guerriero G, Deshmukh R, Sonah H, Sergeant K, Hausman J-F, Lentzen E, Valle N, Siddiqui KS, Exley C (2019) Identification of the aquaporin gene family in Cannabis sativa and evidence for the accumulation of silicon in its tissues. Plant Sci 287:110167

    CAS  PubMed  Google Scholar 

  • Guo S, Zhang J, Sun H, Salse J, Lucas WJ, Zhang H, Zheng Y, Mao L, Ren Y, Wang Z (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 45:51

    CAS  PubMed  Google Scholar 

  • Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol 9:134

    PubMed  PubMed Central  Google Scholar 

  • Hachez C, Heinen RB, Draye X, Chaumont F (2008) The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. Plant Mol Biol 68:337

    CAS  PubMed  Google Scholar 

  • Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucleic acids symposium series. [London]: Information Retrieval Ltd., c1979-c2000., pp. 95-98.

  • Heymann JB, Engel A (1999) Aquaporins: phylogeny, structure, and physiology of water channels. Physiology 14:187–193

    CAS  Google Scholar 

  • Hove RM, Bhave M (2011) Plant aquaporins with non-aqua functions: deciphering the signature sequences. Plant Mol Biol 75:413–430

    CAS  PubMed  Google Scholar 

  • Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao GJB (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    PubMed  PubMed Central  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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jung JS, Preston GM, Smith BL, Guggino WB, Agre P (1994) Molecular structure of the water channel through aquaporin CHIP. The Hourglass Model J Biol Chem 269:14648–14654

    CAS  PubMed  Google Scholar 

  • Kapilan R, Vaziri M, Zwiazek JJ (2018) Regulation of aquaporins in plants under stress. Biol Res 51:1–11

    Google Scholar 

  • Karle S, Kumar K, Srivastava S, Suprasanna P (2020) Cloning, in silico characterization and expression analysis of TIP subfamily from rice (Oryza sativa L.). Gene 761:145043

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar N, Kumawat S, Khatri P, Singla P, Tandon G, Bhatt V, Shinde S, Patil GB, Sonah H, Deshmukh R (2020) Understanding aquaporin transport system in highly stress-tolerant and medicinal plant species Jujube (Ziziphus jujuba Mill.). J Biotechnol 324:103–111

    CAS  PubMed  Google Scholar 

  • Kumawat S, Khatri P, Ahmed A, Vats S, Kumar V, Jaswal R, Wang Y, Xu P, Mandlik R, Shivaraj S (2020) Understanding aquaporin transport system, silicon and other metalloids uptake and deposition in bottle gourd (Lagenaria siceraria). J Hazard Mater 409:124598

    PubMed  Google Scholar 

  • Kumawat S, Aggarwal B, Rana N, Mandlik R, Mehra A, Shivaraj S, Sonah H, Deshmukh R (2021) Identification of aquaporins and deciphering their role under salinity stress in pomegranate (Punica granatum). J Plant Biochem Biotechnol 30:930–942

    CAS  Google Scholar 

  • Kurowska MM, Daszkowska-Golec A, Gajecka M, Kościelniak P, Bierza W, Szarejko I (2020) Methyl jasmonate affects photosynthesis efficiency, expression of HvTIP genes and nitrogen homeostasis in barley. Int J Mol Sci 21:4335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SH, Zwiazek JJ (2019) Regulation of water transport in Arabidopsis by methyl jasmonate. Plant Physiol Biochem 139:540–547

    CAS  PubMed  Google Scholar 

  • Li D-D, Tai F-J, Zhang Z-T, Li Y, Zheng Y, Wu Y-F, Li X-B (2009) A cotton gene encodes a tonoplast aquaporin that is involved in cell tolerance to cold stress. Gene 438:26–32

    CAS  PubMed  Google Scholar 

  • Li G, Santoni V, Maurel C (2014) Plant aquaporins: roles in plant physiology. Biochim Biophys Acta 1840:1574–1582

    CAS  PubMed  Google Scholar 

  • Liu H-Y, Yu X, Cui D-Y, Sun M-H, Sun W-N, Tang Z-C, Kwak S-S, Su W-A (2007) The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Res 17:638

    CAS  PubMed  Google Scholar 

  • Lopez D, Amira MB, Brown D, Muries B, Brunel-Michac N, Bourgerie S, Porcheron B, Lemoine R, Chrestin H, Mollison E (2016) The Hevea brasiliensis XIP aquaporin subfamily: genomic, structural and functional characterizations with relevance to intensive latex harvesting. Plant Mol Biol 91:375–396

    CAS  PubMed  Google Scholar 

  • Ma JF (2010) Silicon transporters in higher plants MIPs and their role in the exchange of metalloids. Adv Exp Med Biol 679:99–109

    CAS  PubMed  Google Scholar 

  • Mandlik R, Thakral V, Raturi G, Shinde S, Nikolić M, Tripathi DK, Sonah H, Deshmukh R (2020) Significance of silicon uptake, transport, and deposition in plants. J Exp Bot 71:6703–6718

    CAS  PubMed  Google Scholar 

  • Mandlik R, Singla P, Kumawat S, Khatri P, Ansari W, Singh A, Sharma Y, Singh A, Solanke A, Nadaf A, Sonah H, Deshmukh R (2021) Understanding aquaporin regulation defining silicon uptake and role in arsenic, antimony and germanium stress in pigeonpea (Cajanus cajan). Environ Pollut 294:118606

    PubMed  Google Scholar 

  • Maurel C (2007) Plant aquaporins: novel functions and regulation properties. FEBS Lett 581:2227–2236

    CAS  PubMed  Google Scholar 

  • Mitani-Ueno N, Yamaji N, Zhao F-J, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385

    CAS  PubMed  Google Scholar 

  • Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ (2001) From genome to function: the Arabidopsis aquaporins. Genome Biol 3(1):1–17

    Google Scholar 

  • Raturi G, Sharma Y, Rana V, Thakral V, Myaka B, Salvi P, Singh M, Dhar H, Deshmukh R (2021) Exploration of silicate solubilizing bacteria for sustainable agriculture and silicon biogeochemical cycle. Plant Physiol Biochem 166:827–838

    CAS  PubMed  Google Scholar 

  • Reddy PS, Rao TSRB, Sharma KK, Vadez V (2015) Genome-wide identification and characterization of the aquaporin gene family in Sorghum bicolor (L.). Plant Gene 1:18–28

    CAS  Google Scholar 

  • Rios JJ, Martínez-Ballesta MC, Ruiz JM, Blasco B, Carvajal M (2017) Silicon-mediated improvement in plant salinity tolerance: the role of aquaporins. Front Plant Sci 8:948

    PubMed  PubMed Central  Google Scholar 

  • Roy SW, Penny D (2006) Patterns of intron loss and gain in plants: intron loss–dominated evolution and genome-wide comparison of O. sativa and A. thaliana. Mol Biol Evol 24:171–181

    PubMed  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

    CAS  PubMed  Google Scholar 

  • Sánchez-Romera B, Ruiz-Lozano JM, Zamarreño ÁM, García-Mina JM, Aroca R (2016) Arbuscular mycorrhizal symbiosis and methyl jasmonate avoid the inhibition of root hydraulic conductivity caused by drought. Mycorrhiza 26:111–122

    PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shivaraj SM, Deshmukh RK, Rai R, Bélanger R, Agrawal PK, Dash PK (2017) Genome-wide identification, characterization, and expression profile of aquaporin gene family in flax (Linum usitatissimum). Sci Rep 7:46137

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shivaraj S, Mandlik R, Bhat JA, Raturi G, Elbaum R, Alexander L, Tripathi DK, Deshmukh R, Sonah H (2021) Outstanding questions on the beneficial role of silicon in crop plants. Plant Cell Physiol 63(1):4–18

    Google Scholar 

  • Singh RK, Deshmukh R, Muthamilarasan M, Rani R, Prasad M (2020) Versatile roles of aquaporin in physiological processes and stress tolerance in plants. Plant Physiol Biochem 149:178–189

    CAS  PubMed  Google Scholar 

  • Sonah H, Zhang X, Deshmukh RK, Borhan MH, Fernando W, Bélanger RR (2016) Comparative transcriptomic analysis of virulence factors in Leptosphaeria maculans during compatible and incompatible interactions with canola. Front Plant Sci 7:1784

    PubMed  PubMed Central  Google Scholar 

  • Sonah H, Deshmukh RK, Labbé C, Bélanger RR (2017) Analysis of aquaporins in Brassicaceae species reveals high-level of conservation and dynamic role against biotic and abiotic stress in canola. Sci Rep 7:1–17

    CAS  Google Scholar 

  • Sugaya S, Ohshima I, Gemma H, Iwahori S (2003) Expression analysis of genes encoding aquaporins during the development of peach fruit. Acta Hort 618:363–370

    CAS  Google Scholar 

  • Sun H, Guo J, Duan Y, Zhang T, Huo H, Gong H (2017) Isolation and functional characterization of CsLsi1, a silicon transporter gene in Cucumis sativus. Physiol Plant 159:201–214

    CAS  PubMed  Google Scholar 

  • Tang H, Yu Q, Li Z, Liu F, Su W, Zhang C, Ling H, Luo J, Su Y, Que Y (2021) A PIP-mediated osmotic stress signaling cascade plays a positive role in the salt tolerance of sugarcane. BMC Plant Biol 21:589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tzfadia O, Diels T, De Meyer S, Vandepoele K, Aharoni A, de Peer V, Y.J.F.i.p.s., (2016) CoExpNetViz: comparative co-expression networks construction and visualization tool. Front Plant Sci 6:1194

    PubMed  PubMed Central  Google Scholar 

  • Verma G, Srivastava D, Narayan S, Shirke PA, Chakrabarty D (2020) Exogenous application of methyl jasmonate alleviates arsenic toxicity by modulating its uptake and translocation in rice (Oryza sativa L.). Ecotoxicol Environ Saf 201:110735

    CAS  PubMed  Google Scholar 

  • Wang Y, Zhao Z, Liu F, Sun L, Hao F (2020) Versatile roles of aquaporins in plant growth and development. Int J Mol Sci 21:9485

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Mo Y, Yang X, Zhang H, Wang Y, Li H, Wei C, Zhang X (2016) Transcriptome profiling of watermelon root in response to short-term osmotic stress. PLoS ONE 11:e0166314

    PubMed  PubMed Central  Google Scholar 

  • Zhang J, John UP, Wang Y, Li X, Gunawardana D, Polotnianka RM, Spangenberg GC, Nan Z (2011) Targeted mining of drought stress-responsive genes from EST resources in Cleistogenes songorica. J Plant Physiol 168:1844–1851

    CAS  PubMed  Google Scholar 

  • Zhang DY, Ali Z, Wang CB, Xu L, Yi JX, Xu ZL, Liu XQ, He XL, Huang YH, Khan IA (2013) Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.). PLoS ONE 8:e56312

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Schraut D, Hartung W, Schäffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. J Exp Bot 56:2971–2981

    CAS  PubMed  Google Scholar 

  • Zou Z, Gong J, Huang Q, Mo Y, Yang L, Xie, G.J.P.o., (2015) Gene structures, evolution, classification and expression profiles of the aquaporin gene family in castor bean (Ricinus communis L.). PLoS ONE 10:e0141022

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the Department of Biotechnology (DBT), Government of India (GoI) for the Ramalingaswami Fellowship Award and Grant BT/PR32853/AGIII/103/1159/2019 to HS and RD and the Science and Engineering Research Board (SERB), India, Department of Science and Technology (DST), Government of India (GoI), for research grant CRG/2019/006599 awarded to HS and RD.

Author information

Authors and Affiliations

  1. Department of Agriculture Biotechnology, National Agri-Food Biotechnology Institute (NABI), Sector-81(Knowledge city), P.O. Manauli, SAS Nagar, Mohali, Punjab, 140306, India

    Gaurav Raturi, Surbhi Kumawat, Rushil Mandlik, Deepak Duhan, Vandana Thakral, Sreeja Sudhakaran, Humira Sonah & Rupesh Deshmukh

  2. Department of Biotechnology, Panjab University, Chandigarh, India

    Gaurav Raturi, Surbhi Kumawat, Rushil Mandlik, Vandana Thakral & Sreeja Sudhakaran

  3. ICAR - Central Institute for Arid Horticulture, Bikaner, India

    Chet Ram

Authors
  1. Gaurav Raturi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Surbhi Kumawat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rushil Mandlik
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Deepak Duhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vandana Thakral
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sreeja Sudhakaran
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chet Ram
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Humira Sonah
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rupesh Deshmukh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

R.D., C.R., and H.S. designed the study and perform final editing. G.R., S.K., and R.M. performed the experiments. G.R., and S.K., analyzed the data, prepared figures, and wrote the manuscript. All the authors contributed to finalizing the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Rupesh Deshmukh.

Additional information

Handling Editor: Golam Jalal Ahammed .

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 499 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Raturi, G., Kumawat, S., Mandlik, R. et al. Deciphering the Role of Aquaporins Under Different Abiotic Stress Conditions in Watermelon (Citrullus lanatus). J Plant Growth Regul 42, 3137–3149 (2023). https://doi.org/10.1007/s00344-022-10776-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-022-10776-1

Keywords

Search

Navigation