Skip to main content
Log in

Understanding the role of SWEET genes in fruit development and abiotic stress in pomegranate (Punica granatum L.)

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

The Sugar Will Eventually Be Exported Transporters (SWEET), consisting of the MtN3 and salvia domain, are sugar transporters having an active role in diverse activities in plants such as pollen nutrition, phloem loading, nectar secretion, reproductive tissue development, and plant-pathogen interaction. The SWEET genes have been characterized only in a few fruit crop species.

Methods and results

In this study, a total of 15 SWEET genes were identified in the pomegranate (Punica granatum) genome. The gene structure, transmembrane (TM) helices, domain architecture, and phylogenetic relationships of these genes were evaluated using computational approaches. Genes were further classified as Semi-SWEETs or SWEETs based on the TM domains. Similarly, pomegranate, Arabidopsis, rice, and soybean SWEETs were studied together to classify into major groups. In addition, analysis of RNAseq transcriptome data was performed to study SWEEET gene expression dynamics in different tissue. The expression suggests that SWEETs are mostly expressed in pomegranate peel. In addition, PgSWEET13 was found to be differentially expressed under high salinity stress in pomegranate. Further, quantitative PCR analysis confirmed the expression of four candidate genes in leaf and stem tissues.

Conclusion

The information provided here will help to understand the role of SWEET genes in fruit development and under abiotic stress conditions in pomegranate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All the data provided as electronic supplementary material along with the article.

References

  1. Patil G, Valliyodan B, Deshmukh R, Prince S, Nicander B, Zhao M, Sonah H, Song L, Lin L, Chaudhary J (2015) Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. BMC Genomics 16:520

    Article  PubMed  PubMed Central  Google Scholar 

  2. Lanjie Z, Jinbo Y, Wei C, Yan L, Youjun L, Yan G, Junyi W, Li Y, Ziyang L, Zhang Y (2018) A genome-wide analysis of SWEET gene family in cotton and their expressions under different stresses. J Cotton Res 1:7

    Article  Google Scholar 

  3. Kühn C, Grof CP (2010) Sucrose transporters of higher plants. Curr Opin Plant Biol 13:287–297

    Article  Google Scholar 

  4. Ayre BG (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 4:377–394

    Article  CAS  PubMed  Google Scholar 

  5. Slewinski TL (2011) Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: a physiological perspective. Mol Plant 4:641–662

    Article  CAS  PubMed  Google Scholar 

  6. Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML, Qu X-Q, Guo W-J, Kim J-G, Underwood W, Chaudhuri B (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Yuan M, Wang S (2013) Rice MtN3/saliva/SWEET family genes and their homologs in cellular organisms. Mol Plant 6:665–674

    Article  CAS  PubMed  Google Scholar 

  8. Feng C-Y, Han J-X, Han X-X, Jiang J (2015) Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato. Gene 573:261–272

    Article  CAS  PubMed  Google Scholar 

  9. Mizuno H, Kasuga S, Kawahigashi H (2016) The sorghum SWEET gene family: stem sucrose accumulation as revealed through transcriptome profiling. Biotechnol Biofuels 9:127

    Article  PubMed  PubMed Central  Google Scholar 

  10. Hu LP, Zhang F, Song SH, Tang XW, Hui XU, Liu GM, Yaqin WA, He HJ (2017) Genome-wide identification, characterization, and expression analysis of the SWEET gene family in cucumber. J Integr Agric 16(7):1486–1501

    Article  CAS  Google Scholar 

  11. Gao Y, Wang ZY, Kumar V, Xu XF, Yuan DP, Zhu XF, Li TY, Jia B, Xuan YH (2018) Genome-wide identification of the SWEET gene family in wheat. Gene 642:284–292

    Article  CAS  PubMed  Google Scholar 

  12. Doidy J, Vidal U, Lemoine R (2019) Sugar transporters in Fabaceae, featuring SUT MST and SWEET families of the model plant Medicago truncatula and the agricultural crop Pisum sativum. PLoS ONE 14:e0223173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Xuan YH, Hu YB, Chen L-Q, Sosso D, Ducat DC, Hou B-H, Frommer WB (2013) Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proc Natl Acad Sci 110:E3685–E3694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chen L-Q, Qu X-Q, Hou B-H, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–211

    Article  CAS  PubMed  Google Scholar 

  15. Chardon F, Bedu M, Calenge F, Klemens PA, Spinner L, Clement G, Chietera G, Léran S, Ferrand M, Lacombe B (2013) Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr Biol 23:697–702

    Article  CAS  PubMed  Google Scholar 

  16. Guo W-J, Nagy R, Chen H-Y, Pfrunder S, Yu Y-C, Santelia D, Frommer WB, Martinoia E (2014) SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol 164:777–789

    Article  CAS  PubMed  Google Scholar 

  17. Klemens PA, Patzke K, Deitmer J, Spinner L, Le Hir R, Bellini C, Bedu M, Chardon F, Krapp A, Neuhaus HE (2013) Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol 163:1338–1352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Eom J-S, Chen L-Q, Sosso D, Julius BT, Lin I, Qu X-Q, Braun DM, Frommer WB (2015) SWEETs, transporters for intracellular and intercellular sugar translocation. Curr Opin Plant Biol 25:53–62

    Article  CAS  PubMed  Google Scholar 

  19. Guan Y-F, Huang X-Y, Zhu J, Gao J-F, Zhang H-X, Yang Z-N (2008) RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol 147:852–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Chen LQ (2014) SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol 201:1150–1155

    Article  CAS  PubMed  Google Scholar 

  21. Denancé N, Szurek B, Noël LD (2014) Emerging functions of nodulin-like proteins in non-nodulating plant species. Plant Cell Physiol 55:469–474

    Article  PubMed  Google Scholar 

  22. Streubel J, Pesce C, Hutin M, Koebnik R, Boch J, Szurek B (2013) Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol 200:808–819

    Article  CAS  PubMed  Google Scholar 

  23. Zaka A, Grande G, Coronejo T, Quibod IL, Chen C-W, Chang S-J, Szurek B, Arif M, Cruz CV, Oliva R (2018) Natural variations in the promoter of OsSWEET13 and OsSWEET14 expand the range of resistance against Xanthomonas oryzae pv. oryzae. PLoS ONE 13:e0203711

    Article  PubMed  PubMed Central  Google Scholar 

  24. Sonnewald U (2011) SWEETS–the missing sugar efflux carriers. Front Plant Sci 2:7

    Article  PubMed  PubMed Central  Google Scholar 

  25. Lin IW, Sosso D, Chen L-Q, Gase K, Kim S-G, Kessler D, Klinkenberg PM, Gorder MK, Hou B-H, Qu X-Q (2014) Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature 508:546

    Article  CAS  PubMed  Google Scholar 

  26. Oliva R, Ji C, Atienza-Grande G, Huguet-Tapia JC, Perez-Quintero A, Li T, Eom J-S, Li C, Nguyen H, Liu B (2019) Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat Biotechnol 37:1344–1350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Vats S, Kumawat S, Kumar V, Patil GB, Joshi T, Sonah H, Sharma TR, Deshmukh R (2019) Genome editing in plants: exploration of technological advancements and challenges. Cells 8:1386

    Article  CAS  PubMed Central  Google Scholar 

  28. Varshney RK, Godwin ID, Mohapatra T, Jones JD, McCouch SR (2019) A SWEET solution to rice blight. Nat Biotechnol 37:1280–1282

    Article  CAS  PubMed  Google Scholar 

  29. Ben-Simhon Z, Judeinstein S, Nadler-Hassar T, Trainin T, Bar-Ya’akov I, Borochov-Neori H, Holland D (2011) A pomegranate (Punica granatum L.) WD40-repeat gene is a functional homologue of Arabidopsis TTG1 and is involved in the regulation of anthocyanin biosynthesis during pomegranate fruit development. Planta 234:865–881

    Article  CAS  PubMed  Google Scholar 

  30. Yuan Z, Fang Y, Zhang T, Fei Z, Han F, Liu C, Liu M, Xiao W, Zhang W, Wu S (2018) The pomegranate (Punica granatum L.) genome provides insights into fruit quality and ovule developmental biology. Plant Biotechnol J 16:1363–1374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Luo X, Li H, Wu Z, Yao W, Zhao P, Cao D, Yu H, Li K, Poudel K, Zhao D (2019) The pomegranate (Punica granatum L.) draft genome dissects genetic divergence between soft-and hard-seeded cultivars. Plant Biotechnol J 18:955

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In: Nucleic acids symposium series. Information Retrieval Ltd, London, pp 95–98

  33. El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Qureshi M, Richardson LJ, Salazar GA, Smart A (2018) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432

    Article  PubMed Central  Google Scholar 

  34. Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64:643–651

    Article  CAS  PubMed  Google Scholar 

  35. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  38. 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

    Article  PubMed  PubMed Central  Google Scholar 

  39. Sellami S, Le Hir R, Thorpe MR, Vilaine F, Wolff N, Brini F, Dinant S (2019) Salinity effects on sugar homeostasis and vascular anatomy in the stem of the Arabidopsis thaliana inflorescence. Int J Mol Sci 20:3167

    Article  CAS  PubMed Central  Google Scholar 

  40. Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557–564

    Article  PubMed  Google Scholar 

  41. Qin G, Xu C, Ming R, Tang H, Guyot R, Kramer EM, Hu Y, Yi X, Qi Y, Xu X (2017) The pomegranate (Punica granatum L.) genome and the genomics of punicalagin biosynthesis. Plant J 91:1108–1128

    Article  CAS  PubMed  Google Scholar 

  42. Zheng Q-M, Tang Z, Xu Q, Deng X-X (2014) Isolation, phylogenetic relationship and expression profiling of sugar transporter genes in sweet orange (Citrus sinensis). Plant Cell Tissue Org Cult (PCTOC) 119:609–624

    Article  CAS  Google Scholar 

  43. Jia B, Zhu XF, Pu ZJ, Duan YX, Hao LJ, Zhang J, Chen L-Q, Jeon CO, Xuan YH (2017) Integrative view of the diversity and evolution of SWEET and SemiSWEET sugar transporters. Front Plant Sci 8:2178

    Article  PubMed  PubMed Central  Google Scholar 

  44. Anjali A, Fatima U, Manu M, Ramasamy S, Senthil-Kumar M (2020) Structure and regulation of SWEET transporters in plants: an update. Plant Physiol Biochem

  45. Zhang R, Niu K, Ma H (2020) Identification and expression analysis of the SWEET gene family from Poa pratensis under abiotic stresses. DNA Cell Biol 39:1606

    Article  CAS  PubMed  Google Scholar 

  46. Baker RF, Leach KA, Braun DM (2012) SWEET as sugar: new sucrose effluxers in plants. Mol Plant 5:766–768

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Authors are thankful to the Department of Biotechnology (DBT), India for the Ramalingaswami fellowship to HS; Council of Scientific and Industrial Research (CSIR) for Shyama Prasad Mukherjee Fellowship (SPMF) to SV, and Junior Research Fellowship (JRF) to YS and VK; University Grants Commission (UGC) for JRF to SK, SS, and GR. The authors are also thankful to Dr. SM Shivaraj for his help in English improvement and valuable suggestions.

Funding

Department of Biotechnology (DBT), India; Science and Engineering Research Board (SERB), Department of Science and Technology, Government of India.

Author information

Authors and Affiliations

Authors

Contributions

SK performed qPCR analysis and transcriptome profiling, wrote the first draft of the MS; YS, SV, SS, SS, and RM, contributed in drafting and data analysis, GR, VK, and NR, performed computational analysis, HS conceptualize the study, supervised and finalized the draft.

Corresponding author

Correspondence to Rupesh Deshmukh.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

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.

11033_2021_6961_MOESM1_ESM.tif

Supplementary file1 (TIF 26384 kb) Supplementary Figure 1 Phylogenetic tree of SWEET genes identified in Punica granatum. The clade I, clade II, clade III, and clade IV is marked in red, purple, blue, and green, respectively. Pomegranate SWEETs is abbreviated as Pg.

11033_2021_6961_MOESM2_ESM.tif

Supplementary file2 (TIF 26390 kb) Supplementary Figure 2 Conserved motifs in the protein sequences of 15 SWEETs identified in the pomegranate genome (PgSWEETs). The conserved motifs were identified by the MEME server (http://meme-suite.org/).

Supplementary file3 (XLSX 9 kb) Supplementary Table 1 Details of Primers used for Quantitative Real-Time PCR (qPCR)

11033_2021_6961_MOESM4_ESM.xlsx

Supplementary file4 (XLSX 9 kb) Supplementary Table 2 Details of Blastp results performed using BioEdit showing highest bit score against respective queries from Arabidopsis thaliana, Glycine max, and Oryza sativa

11033_2021_6961_MOESM5_ESM.xlsx

Supplementary file5 (XLSX 9 kb) Supplementary Table 3 Conserved domain analysis of identified Pomegranate SWEET using NCBI conserved Domain Search

11033_2021_6961_MOESM6_ESM.xlsx

Supplementary file6 (XLSX 10 kb) Supplementary Table 4 Biosequence analysis of Pomegranate SWEET using profile hidden Markov Models (HMMER) (https://www.ebi.ac.uk/Tools/hmmer/)

11033_2021_6961_MOESM7_ESM.xlsx

Supplementary file7 (XLSX 9 kb) Supplementary Table 5 Transmembrane domain identified by using TMHMM and SOSUI servers in Pomegranate SWEET

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumawat, S., Sharma, Y., Vats, S. et al. Understanding the role of SWEET genes in fruit development and abiotic stress in pomegranate (Punica granatum L.). Mol Biol Rep 49, 1329–1339 (2022). https://doi.org/10.1007/s11033-021-06961-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-021-06961-2

Keywords

Navigation