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Understanding aquaporins regulation and silicon uptake in carrot (Daucus carota)

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Abstract

Aquaporins play a vital role in uptake and transport of water and many other small solutes in plants. A genome-wide search performed in the carrot genome leads to identification of 47 aquaporins. Subsequent, computational analysis and phylogenetic classification of carrot aquaporins predicted DcNIP2-1 as a silicon transporter. The DcNIP2-1 is a member of NIPIII class of the Nodulin-26 like Intrinsic Protein (NIP) subfamily of aquaporins which is known to regulate uptake of silicon and other metalloids like arsenic and Germanium. Despite having NIP2-1 with functionality defining features like G-S-G-R aromatic/arginine (ar/R) selectivity filter, 108 amino acid spacing between two NPA motif, Mitani’s residue and desired pore morphology, carrot plants found to be silicon poor accumulator. Subsequently, pot-experiments were performed to confirm the uptake of other metalloids, and silicon derived benefits in carrot. Carrot plants were grown with arsenic and with or without silicon supplementation. The results obtained neither showed silicon accumulation, nor any significant benefits to carrot plants under arsenic stress. Similarly, very less accumulation of arsenic was observed in carrot leaves. Such low accumulation of silicon was consistent across different Apiaceae species. The information provided here will be helpful to better understand aquaporin regulation and more particularly silicon uptake and silicon derived benefits in Apiaceae and other plant species.

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Data availability Statement

Data sharing is not applicable to this article as all new created data is already.

contained within this article and the supplementary material of this article.

Code Availability

Not Applicable.

Abbreviations

AQP:

Aquaporins.

PIPs:

Plasma Membrane Intrinsic Proteins.

SIPs:

Small and Basic Intrinsic Intrinsic Proteins.

NIPs:

Nod26-like Intrinsic Proteins.

TIPs:

Tonoplast Intrinsic Proteins.

XIPs:

Uncategorized Intrinsic Proteins.

RPKM:

Reads Per Kilobase of the transcript per Million mapped reads.

GIPs:

GlpF-like Intrinsic Proteins.

HIPs:

Hybrid Intrinsic Proteins.

TM:

Transmembrane helices.

ICP-MS:

Inductively Coupled Plasma Mass Spectroscopty.

FE-SEM:

Field Emission Scanning Electron Microscope.

References

  • Ariani A, Gepts P (2015) Genome-wide identification and characterization of aquaporin gene family in common bean (Phaseolus vulgaris L.). Mol Genet Genomics 290(5):1771–1785

    Article  CAS  PubMed  Google Scholar 

  • Bhat JA et al (2019) Role of silicon in mitigation of heavy metal stresses in crop plants. Plants 8(3):71

    Article  CAS  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(2):306–317

    Article  CAS  PubMed  Google Scholar 

  • Coskun D et al (2019) Si permeability of a deficient Lsi1 aquaporin in tobacco can be enhanced through a conserved residue substitution. Plant Direct 3(8):e00163

    Article  PubMed  PubMed Central  Google Scholar 

  • Deshmukh RK et al (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(4–5):303–315

    Article  CAS  PubMed  Google Scholar 

  • Deshmukh RK et al (2015) A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants. Plant J 83(3):489–500

    Article  CAS  PubMed  Google Scholar 

  • Deshmukh R, Sonah H, Belanger RR (2020) New evidence defining the evolutionary path of aquaporins regulating silicon uptake in land plants. J Exp Bot 71(21):6775–6788

    Article  CAS  PubMed  Google Scholar 

  • di Toppi LS et al (2012) A bifasic response to cadmium stress in carrot: early acclimatory mechanisms give way to root collapse further to prolonged metal exposure. Plant Physiol Biochem 58:269–279

    Article  Google Scholar 

  • Emamverdian A, Ding Y, Xie Y, Sangari S (2018) Silicon mechanisms to ameliorate heavy metal stress in plants. BioMed Research International 2018

  • Farooq MA, Saqib ZA, Akhtar J, Bakhat HF, Pasala R-K, Dietz K-J (2019) Protective role of silicon (Si) against combined stress of salinity and boron (B) toxicity by improving antioxidant enzymes activity in rice. Silicon 11(4):2193–2197

    Article  CAS  Google Scholar 

  • Fryzova R et al (2017) Oxidative stress and heavy metals in plants Reviews of Environmental Contamination and Toxicology, vol 245. Springer, pp 129–156

  • Gao Y et al (2022) Response of glutathione pools to cadmium stress and the strategy to translocate cadmium from roots to leaves (Daucus carota L.). Sci Total Environ 823:153575

    Article  CAS  PubMed  Google Scholar 

  • Gu H-H et al (2011) Mitigation effects of silicon rich amendments on heavy metal accumulation in rice (Oryza sativa L.) planted on multi-metal contaminated acidic soil. Chemosphere 83(9):1234–1240

    Article  CAS  PubMed  Google Scholar 

  • Guan XG et al (2010) NPA motifs play a key role in plasma membrane targeting of aquaporin-4. IUBMB Life 62(3):222–226

    Article  CAS  PubMed  Google Scholar 

  • Johanson U et al (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(4):1358–1369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S, Sohn E, Hamayun M, Yoon J, Lee I (2010) Effect of silicon on growth and salinity stress of soybean plant grown under hydroponic system. Agroforest Syst 80(3):333–340

    Article  Google Scholar 

  • Linke B, Alessandro MS, Galmarini CR, Nothnagel T (2019) Carrot floral development and reproductive biology The Carrot Genome. Springer, pp 27–57

  • Ma JF et al (2006) A silicon transporter in rice. Nature 440(7084):688–691

    Article  CAS  PubMed  Google Scholar 

  • Ma JF et al (2007) An efflux transporter of silicon in rice. Nature 448(7150):209–212

    Article  CAS  PubMed  Google Scholar 

  • Ma JF et al (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proceedings of the National Academy of Sciences 105(29):9931–9935

  • Maurel C, Boursiac Y, Luu D-T, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95(4):1321–1358

    Article  CAS  PubMed  Google Scholar 

  • Peralta-Videa JR, Lopez ML, Narayan M, Saupe G, Gardea-Torresdey J (2009) The biochemistry of environmental heavy metal uptake by plants: implications for the food chain. Int J Biochem Cell Biol 41(8–9):1665–1677

    Article  CAS  PubMed  Google Scholar 

  • Que F et al (2019) Advances in research on the carrot, an important root vegetable in the Apiaceae family. Hortic Res 6(1):1–15

    Article  Google Scholar 

  • Raj A, Mandal J, Kumari PB (2020) Organic amendment can reduce arsenic uptake in wheat. J Pharmacognosy Phytochemistry 9(2):1355–1360

    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(9):1568–1577

    Article  CAS  PubMed  Google Scholar 

  • Seyfferth AL, Fendorf S (2012) Silicate mineral impacts on the uptake and storage of arsenic and plant nutrients in rice (Oryza sativa L.). Environ Sci Technol 46(24):13176–13183

    Article  CAS  PubMed  Google Scholar 

  • Shivaraj S, Deshmukh R, Sonah H, Bélanger RR (2019) Identification and characterization of aquaporin genes in Arachis duranensis and Arachis ipaensis genomes, the diploid progenitors of peanut. BMC Genomics 20(1):222

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  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):1–17

    Article  CAS  Google Scholar 

  • Sudhakaran S et al (2021) Significance of solute specificity, expression, and gating mechanism of tonoplast intrinsic protein during development and stress response in plants. Physiol Plant 172(1):258–274

    Article  CAS  PubMed  Google Scholar 

  • Tahir MA, Rahmatullah T, Aziz M, Ashraf S, Kanwal S, Maqsood MA (2006) Beneficial effects of silicon in wheat (Triticum aestivum L.) under salinity stress. Pak J Bot 38(5):1715–1722

    Google Scholar 

  • Törnroth-Horsefield S et al (2006) Structural mechanism of plant aquaporin gating. Nature 439(7077):688–694

    Article  PubMed  Google Scholar 

  • Uncu AO, Uncu AT (2020) High-throughput simple sequence repeat (SSR) mining saturates the carrot (Daucus carota L.) genome with chromosome-anchored markers. Biotechnol Biotechnol Equip 34(1):1–9

    Article  CAS  Google Scholar 

  • Vaculík M, Lukačová Z, Bokor B, Martinka M, Tripathi DK, Lux A (2020) Alleviation mechanisms of metal (loid) stress in plants by silicon: A review. J Exp Bot 17(21):6744–6757

    Article  Google Scholar 

  • Vishwakarma K, Mishra M, Patil G, Mulkey S, Ramawat N, Pratap Singh V, Deshmukh R, Kumar Tripathi D, Nguyen HT, Sharma S (2019) Avenues of the membrane transport system in adaptation of plants to abiotic stresses. Crit Rev Biotechnol 39(7):861–883

    Article  CAS  PubMed  Google Scholar 

  • Xu Z-S, Tan H-W, Wang F, Hou X-L, Xiong A-S (2014) CarrotDB: a genomic and transcriptomic database for carrot. Database 2014: bau096

  • Zargar SM et al (2017) Aquaporins as potential drought tolerance inducing proteins: towards instigating stress tolerance. J Proteom 169:233–238

    Article  CAS  Google Scholar 

  • Zhao C-X, Shao H-B, Chu L-Y (2008) Aquaporin structure–function relationships: water flow through plant living cells. Colloids Surf B 62(2):163–172

    Article  CAS  Google Scholar 

  • Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167(3):527–533

    Article  CAS  Google Scholar 

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Acknowledgements

Authors are also thankful to the Department of Biotechnology (DBT), India for.

Ramalingaswami fellowship to RD and HS.

Funding

We thank the Department of Biotechnology, Government of India for Ramalingaswami.

Fellowship, and Science and Engineering Research Board (SERB), Department of Science and Technology, Government of India for funding support (CRG/2019/006599) to RD and HS.

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NR and VT compiled the data, performed ICP-MS and FE-SEM analysis. NR, VT, SV, GG, GP, SK and SS wrote first draft of the MS. RD and HS edited and finalized the draft. RD and HS conceptualized the study, drew the conclusions.

Corresponding author

Correspondence to Rupesh Deshmukh.

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Rajora, N., Thakral, V., Geetika et al. Understanding aquaporins regulation and silicon uptake in carrot (Daucus carota). J. Plant Biochem. Biotechnol. 32, 51–62 (2023). https://doi.org/10.1007/s13562-022-00780-7

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  • DOI: https://doi.org/10.1007/s13562-022-00780-7

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