Advertisement

Study on aquaporins of Setaria italica suggests the involvement of SiPIP3;1 and SiSIP1;1 in abiotic stress response

  • Roshan Kumar Singh
  • Shweta Shweta
  • Mehanathan Muthamilarasan
  • Rekha Rani
  • Manoj PrasadEmail author
Original Article

Abstract

Aquaporins are versatile proteins involved in several biological as well as molecular functions, and they have been extensively studied in various plant systems. Increasing evidences indicate their role in biotic and abiotic stresses, and therefore, studying these proteins in a naturally stress-tolerant crop would provide further insights into the roles of this important protein family. Given this, the present study was performed in foxtail millet (Setaria italica), a model plant for studying biofuel, stress tolerance, and C4 photosynthetic traits. The study identified 12 plasma membrane intrinsic proteins (PIPs), 11 tonoplast intrinsic proteins (TIPs), 13 NOD26-like intrinsic proteins (NIPs), and 3 small basic intrinsic proteins (SIPs) in foxtail millet. The identified proteins and their corresponding genes were characterized using in silico approaches such as chromosomal localization, analysis of gene and protein properties, phylogenetic analysis, promoter analysis, and RNA-seq-derived expression profiling. The candidate genes identified through these analyses were studied for their expression in response to abiotic stresses (dehydration, salinity, and heat) as well as hormone treatments (abscisic acid, methyl jasmonate, and salicylic acid) in two contrasting cultivars of foxtail millet. The study showed that SiPIP3;1 and SiSIP1;1 were differentially expressed in both the cultivars in response to stress and hormone treatments. Overexpression of these genes in a heterologous yeast system also demonstrated that the transgenic cells were able to tolerate dehydration as well as salt stress which suggests the involvement of these proteins in the tolerance mechanism. Overall, the present study provides insights into structure and organization of the aquaporin gene family in foxtail millet and highlights the potential candidate genes for further functional characterizations.

Keywords

Aquaporins Plasma membrane intrinsic proteins (PIPs) Tonoplast intrinsic proteins (TIPs) NOD26-like intrinsic proteins (NIPs) Small basic intrinsic proteins (SIPs) Foxtail millet (Setaria italica

Notes

Acknowledgments

RKS and RR acknowledge the Council of Scientific and Industrial Research and Department of Biotechnology, Government of India, India, respectively, for providing Research Fellowships. SS acknowledges the National Post-Doctoral Fellowship received from DST-SERB, Government of India, India. MM acknowledges the DST INSPIRE Faculty Award from Department of Science & Technology, Government of India, India. The authors are thankful to DBT-eLibrary Consortium (DeLCON) for providing access to the e-resources.

Author’s contributions

Conception and design: MP; experimental analyses: RKS, SS, RR, and MM; interpretation of data: MM and RKS; writing, review and revision of manuscript: MM and RKS; study supervision: MP; all authors have read and approved the final manuscript.

Funding

Authors’ research in this area is supported by the Core Grant of National Institute of Plant Genome Research, New Delhi, India.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10142_2018_653_Fig6_ESM.png (650 kb)
Supplementary Figure S1

Exon-Intron structure of aquaporin genes. (PNG 698 kb)

10142_2018_653_MOESM1_ESM.tif (1.2 mb)
High Resolution Image (TIF 1191 kb)
10142_2018_653_Fig7_ESM.png (108 kb)
Supplementary Figure S2

Sub-cellular localization of aquaporin genes. (PNG 174 kb)

10142_2018_653_MOESM2_ESM.tif (408 kb)
High Resolution Image (TIF 407 kb)
10142_2018_653_Fig8_ESM.png (898 kb)
Supplementary Figure S3

Comparative physical map of aquaporin genes between foxtail millet (Si; Setaria italica) and green foxtail (Sv; Setaria viridis), Brachypodium (Bd; Brachypodium distachyon), sorghum (Sb; Sorghum bicolor), maize (Zm; Zea mays), rice (Os; Oryza sativa) and switchgrass (Panicum virgatum). Each block represents individual chromosome of each organism and the lines denote the corresponding orthologous genes. (JPG 3022 kb)

10142_2018_653_MOESM3_ESM.tif (1.4 mb)
High Resolution Image (TIF 1446 kb)
10142_2018_653_MOESM4_ESM.doc (34 kb)
Supplementary Table S1 List of primers used in the present study. (DOC 34 kb)
10142_2018_653_MOESM5_ESM.xls (48 kb)
Supplementary Table S2 Properties of aquaporin genes identified in foxtail millet. (XLS 48 kb)
10142_2018_653_MOESM6_ESM.xls (268 kb)
Supplementary Table S3 Summary of cis-regulatory elements present in aquaporin genes. (XLS 268 kb)

References

  1. Anderberg HI, Kjellbom P, Johanson U (2012) Annotation of Selaginella moellendorffii major intrinsic proteins and the evolution of the protein family in terrestrial plants. Front Plant Sci 3:33CrossRefGoogle Scholar
  2. 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 66:306–317CrossRefGoogle Scholar
  3. Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764CrossRefGoogle Scholar
  4. Danielson JA, Johanson U (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8:45CrossRefGoogle Scholar
  5. Deokar AA, Tar’an B (2016) Genome-wide analysis of the aquaporin gene family in chickpea (Cicer arietinum L.). Front Plant Sci 7:1802CrossRefGoogle Scholar
  6. Deshmukh RK, Vivancos J, Guérin V, Sonah H, Labbe 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 83:303–315CrossRefGoogle Scholar
  7. 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 83:489–500CrossRefGoogle Scholar
  8. Deshmukh RK, Sonah H, Bélanger RR (2016) Plant aquaporins: genome-wide identification, transcriptomics, proteomics, and advanced analytical tools. Front Plant Sci 7:1896CrossRefGoogle Scholar
  9. Eddy SR (2010) HMMER user’s guide. Available online at: HMMER website: ftp://selab.janelia.org/pub/software/hmmer/CURRENT/Userguide.pdf. Accessed December 28, 2017
  10. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37CrossRefGoogle Scholar
  11. Forrest KL, Bhave M (2007) Major intrinsic proteins (MIPs) in plants: a complex gene family with major impacts on plant phenotype. Funct Integr Genomics 7:263–289CrossRefGoogle Scholar
  12. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein Identification and Analysis Tools on the ExPASy Server. In: Walker JM (ed) The Proteomics Protocols Handbook. Humana Press, New York, USA, pp 571–607Google Scholar
  13. Gomes D, Agasse A, Thiebaud P, Delrot S, Geros H, Chaumont F (2009) Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta 1788:1213–1228CrossRefGoogle Scholar
  14. 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 9:134CrossRefGoogle Scholar
  15. Heymann JB, Engel A (1999) Aquaporins: phylogeny, structure, and physiology of water channels. News Physiol Sci 14:187–193Google Scholar
  16. Hove RM, Ziemann M, Bhave M (2015) Identification and expression analysis of the barley (Hordeum vulgare L.) aquaporin gene family. PLoS One 10:e0128025CrossRefGoogle Scholar
  17. Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297CrossRefGoogle Scholar
  18. 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 579:5814–5820CrossRefGoogle Scholar
  19. 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 126:1358–1369CrossRefGoogle Scholar
  20. Kaldenhoff R, Fischer M (2006) Aquaporins in plants. Acta Physiol 187:169–176CrossRefGoogle Scholar
  21. Kayum MA, Park JI, Nath UK, Biswas MK, Kim HT, Nou IS (2017) Genome-wide expression profiling of aquaporin genes confer responses to abiotic and biotic stresses in Brassica rapa. BMC Plant Biol 17:23CrossRefGoogle Scholar
  22. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645CrossRefGoogle Scholar
  23. Kumar K, Muthamilarasan M, Prasad M (2013) Reference genes for quantitative real-time PCR analysis in the model plant foxtail millet (Setaria italica L.) subjected to abiotic stress conditions. Plant Cell Tissue Organ Cult 115:13–22CrossRefGoogle Scholar
  24. Lee TH, Kim J, Robertson JS, Paterson AH (2017) Plant genome duplication database. Methods Mol Biol 1533:267–277CrossRefGoogle Scholar
  25. Liu Q, Wang H, Zhang Z, Wu J, Feng Y, Zhu Z (2009) Divergence in function and expression of the NOD26-like intrinsic proteins in plants. BMC Genomics 10:313CrossRefGoogle Scholar
  26. Maurel C, Javot H, Lauvergeat V, Gerbeau P, Tournaire C, Santoni V, Heyes J (2002) Molecular physiology of aquaporins in plants. Int Rev Cytol 215:105–148CrossRefGoogle Scholar
  27. Maurel C, Verdoucq L, Luu D-T, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624CrossRefGoogle Scholar
  28. Maurel C, Boursiac Y, Luu D–T, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95:1321–1358CrossRefGoogle Scholar
  29. McGaughey SA, Osborn HL, Chen L, Pegler JL, Tyerman SD, Furbank RT, Byrt CS, Grof CP (2016) Roles of aquaporins in Setaria viridis stem development and sugar storage. Front Plant Sci 7:1815CrossRefGoogle Scholar
  30. Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y (2000) Structural determinants of water permeation through aquaporin–1. Nature 407:599–605CrossRefGoogle Scholar
  31. Muthamilarasan M, Prasad M (2015) Advances in Setaria genomics for genetic improvement of cereals and bioenergy grasses. Theor Appl Genet 128:1–14CrossRefGoogle Scholar
  32. Muthamilarasan M, Prasad M (2017) Genetic determinants of drought stress tolerance in Setaria. In: Doust A, Diao X (eds) Genetics and genomics of Setaria. Plant genetics and genomics: crops and models, vol 19. Springer, Cham, pp 267–289CrossRefGoogle Scholar
  33. Muthamilarasan M, Bonthala VS, Mishra AK, Khandelwal R, Khan Y, Roy R, Prasad M (2014) C2H2 type of zinc finger transcription factors in foxtail millet define response to abiotic stresses. Funct Integr Genomics 14:531–543CrossRefGoogle Scholar
  34. Muthamilarasan M, Bonthala VS, Khandelwal R, Jaishankar J, Shweta S, Nawaz K, Prasad M (2015) Global analysis of WRKY transcription factor superfamily in Setaria identifies potential candidates involved in abiotic stress signaling. Front Plant Sci 6:910Google Scholar
  35. Muthamilarasan M, Dhaka A, Yadav R, Prasad M (2016) Exploration of millet models for developing nutrient rich graminaceous crops. Plant Sci 242:89–97CrossRefGoogle Scholar
  36. Park W, Scheffler BE, Bauer PJ, Campbell BT (2010) Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol 10:142CrossRefGoogle Scholar
  37. Qi X, Xie S, Liu Y, Yi F, Yu J (2013) Genome-wide annotation of genes and noncoding RNAs of foxtail millet in response to simulated drought stress by deep sequencing. Plant Mol Biol 83:459–473CrossRefGoogle Scholar
  38. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378CrossRefGoogle Scholar
  39. Shelden MC, Howitt SM, Kaiser BN, Tyerman SD (2009) Identification and functional characterisation of aquaporins in the grapevine, Vitis vinifera. Funct Plant Biol 36:1065–1078CrossRefGoogle Scholar
  40. 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 7:46137CrossRefGoogle Scholar
  41. Singh RK, Jaishankar J, Muthamilarasan M, Shweta S, Dangi A, Prasad M (2016) Genome-wide analysis of heat shock proteins in C4 model, foxtail millet identifies potential candidates for crop improvement under abiotic stress. Sci Rep 6:32641CrossRefGoogle Scholar
  42. Sonah H, Deshmukh R, Labbé C, Belanger R (2017) Analysis of aquaporins in Brassicaceae species reveals high-level of conservation and dynamic role against biotic and abiotic stress in canola. Sci Rep 7:2771CrossRefGoogle Scholar
  43. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  44. Tyerman SD, Bohnert HJ, Maurel C, Steudle E, Smith JA (1999) Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. J Exp Bot 50:1055–1071Google Scholar
  45. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefGoogle Scholar
  46. Wallace IS, Choi WG, Roberts DM (2006) The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochim Biophys Acta 1758:1165–1175CrossRefGoogle Scholar
  47. Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49CrossRefGoogle Scholar
  48. Yadav CB, Muthamilarasan M, Dangi A, Shweta S, Prasad M (2016) Comprehensive analysis of SET domain gene family in foxtail millet identifies the putative role of SiSET14 in abiotic stress tolerance. Sci Rep 6:32621CrossRefGoogle Scholar
  49. Zhang G, Liu X, Quan Z, Cheng S, Xu X, Pan S, Xie M, Zeng P, Yue Z, Wang W, Tao Y, Bian C, Han C, Xia Q, Peng X, Cao R, Yang X, Zhan D, Hu J, Zhang Y, Li H, Li H, Li N, Wang J, Wang C, Wang R, Guo T, Cai Y, Liu C, Xiang H, Shi Q, Huang P, Chen Q, Li Y, Wang J, Zhao Z, Wang J (2012) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol 30:549–554CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.National Institute of Plant Genome ResearchNew DelhiIndia

Personalised recommendations