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Research Articles

Vol. 12 No. 2 (2025)

Deciphering the role of sugar transport genes in modulating seed protein content in Chickpea

DOI
https://doi.org/10.14719/pst.7444
Submitted
26 January 2025
Published
19-05-2025 — Updated on 27-05-2025
Versions

Abstract

This study examines the impact of genes unique to sugar metabolism in regulating seed protein content by comparing them across two genotypes, FG212, 20 % (low protein content, LPC) and ICC8397, 30 % (high protein content, HPC) of (Cicer arietinum L.). Genes specific to sugar transport, which promote glycolysis and energy-intensive activities like development and stress responses, are more highly expressed in FG212 despite its low protein content. On the other hand, ICC8397 supports its high protein content by prioritising nitrogen assimilation over carbohydrate metabolism and by expressing more genes linked to nitrogen absorption, such as glutamine synthetase and nitrate reductase. The analysis revealed 17 sugar transport-specific genes, predominantly belonging to the SWEET family, with enhanced expression in FG212, these genes prioritise stress tolerance and glucose metabolism above protein synthesis. Gene ontology and KEGG pathway analysis revealed important biological processes such as hexose transport and carbohydrate metabolism, with genes related to energy balance and sugar distribution showing differential expression. While DNA repair proteins interacted with SWEET genes, suggesting their developmental significance, interaction studies showed that SWEET transporters and transcription factors such as MYB played important roles in stress. The findings of this research are useful in breeding new chickpea cultivars with enhanced SPC and higher nutritional values.

References

  1. 1. Polak R, Phillips EM, Campbell A. Legumes: health benefits and culinary approaches to increase intake. Clin Diabetes. 2015;33(4):198-205. https://doi.org/10.2337/diaclin.33.4.198
  2. 2. Yang T, Wu X, Wang W, Wu Y. Regulation of seed storage protein synthesis in monocot and dicot plants: A comparative review. Mol Plant. 2023;16(1):145-67. https://doi.org/10.1016/j.molp.2022.12.004
  3. 3. Bessada SM, Barreira JC, Oliveira MBP. Pulses and food security: dietary protein, digestibility, bioactive and functional properties. Trends Food Sci Technol. 2019;93:53-68. https://doi.org/10.1016/j.tifs.2019.08.022
  4. 4. Arora J, Kanthaliya B, Joshi A, Meena M, Meena S, Siddiqui MH, et al. Evaluation of total isoflavones in chickpea (Cicer arietinum L.) sprouts germinated under precursors (p-coumaric acid and l-phenylalanine) supplementation. Plants (Basel). 2023;12(15):2823. https://doi.org/10.3390/plants12152823
  5. 5. Oomah BD, Patras A, Rawson A, Singh N, Compos-Vega R. Chemistry of pulses. In: Tiwari BK, Gowen A, McKenna B, editors. Pulse Foods. Academic Press; 2011. p. 9-55. https://doi.org/10.1016/B978-0-12-382018-1.00002-2
  6. 6. Singh C, Kumar R, Sehgal H, Bhati S, Singhal T, Gayacharan, et al. Unclasping potentials of genomics and gene editing in chickpea to fight climate change and global hunger threat. Front Genet. 2023;14:1085024. https://doi.org/10.3389/fgene.2023.1085024
  7. 7. Day DA, Poole PS, Tyerman SD, Rosendahl L. Ammonia and amino acid transport across symbiotic membranes in nitrogen-fixing legume nodules. Cell Mol Life Sci. 2001;58(1):61-71. https://doi.org/10.1007/PL00000778
  8. 8. Lodwig EM, Hosie AH, Bourdes A, Findlay K, Allaway D, Karunakaran R, et al. Amino-acid cycling drives nitrogen fixation in the legume–Rhizobium symbiosis. Nature. 2003;422(6933):722-26. https://doi.org/10.1038/nature01527
  9. 9. Bennetau-Pelissero C. Plant proteins from legumes. Bioactive Molecules in Food. 2019;1:223-66. https://doi.org/10.1007/978-3-319-78030-6_3
  10. 10. Guo K, Yang J, Yu N, Luo L, Wang E. Biological nitrogen fixation in cereal crops: Progress, strategies, and perspectives. Plant Commun. 2023;4(2). https://doi.org/10.1016/j.xplc.2022.100499
  11. 11. Gopal K, Priyadarshini P, Kumar K, Yadava YK, Yadav S, Kohli D, et al. Genome-wide identification and characterization of the amino acid transporter (AAT) genes regulating seed protein content in chickpea (Cicer arietinum L.). Int J Biol Macromol. 2023;252:126324. https://doi.org/10.1016/j.ijbiomac.2023.126324
  12. 12. Nunes-Nesi A, Fernie AR, Stitt M. Metabolic and signaling aspects underpinning the regulation of plant carbon-nitrogen interactions. Mol Plant. 2010;3(6):973-96. https://doi.org/10.1093/mp/ssq049
  13. 13. Baslam M, Mitsui T, Sueyoshi K, Ohyama T. Recent advances in carbon and nitrogen metabolism in C3 plants. Int J Mol Sci. 2020;22(1):318. https://doi.org/10.3390/ijms22010318
  14. 14. Zayed O, Hewedy OA, Abdelmoteleb A, Ali M, Youssef MS, Roumia AF, et al. Nitrogen journey in plants: From uptake to metabolism, stress response, and microbe interaction. Biomolecules. 2023;13(10):1443. https://doi.org/10.3390/biom13101443
  15. 15. Pratelli R, Pilot G. Regulation of amino acid metabolic enzymes and transporters in plants. J Exp Bot. 2014;65(19):5535-56. https://doi.org/10.1093/jxb/eru320
  16. 16. Jan R, Asaf S, Numan M, Lubna, Kim KM. Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy. 2021;11(5):968. https://doi.org/10.3390/agronomy11050968
  17. 17. Reshi ZA, Ahmad W, Lukatkin AS, Javed SB. From Nature to lab: A review of secondary metabolite biosynthetic pathways, environmental influences, and in vitro approaches. Metabolites. 2023;13(8):895. https://doi.org/10.3390/metabo13080895
  18. 18. Matilla AJ. Auxin: Hormonal signal required for seed development and dormancy. Plants. 2020;9(6):705. https://doi.org/10.3390/plants9060705
  19. 19. Sharma S, Kaur P, Gaikwad K. Role of cytokinins in seed development in pulses and oilseed crops: Current status and future perspective. Front Genet. 2022;13:940660. https://doi.org/10.3389/fgene.2022.940660
  20. 20. Kozaki A, Aoyanagi T. Molecular aspects of seed development controlled by gibberellins and abscisic acids. Int J Mol Sci. 2022;23(3):1876. https://doi.org/10.3390/ijms23031876
  21. 21. King CA, Purcell LC. Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiol. 2005;137(4):1389-96. https://doi.org/10.1104/pp.104.056317
  22. 22. Aranjuelo I, Cabrerizo PM, Aparicio-Tejo PM, Arrese-Igor C. Unravelling the mechanisms that improve photosynthetic performance of N2-fixing pea plants exposed to elevated [CO2]. Environ Exp Bot. 2014;99:167-74. https://doi.org/10.1016/j.envexpbot.2013.10.020
  23. 23. Dutta A, Trivedi A, Nath CP, Gupta DS, Hazra KK. A comprehensive review on grain legumes as climate‐smart crops: challenges and prospects. Environ Challenges. 2022;7:100479. https://doi.org/10.1016/j.envc.2022.100479
  24. 24. Ramalingam A, Kudapa H, Pazhamala LT, Weckwerth W, Varshney RK. Proteomics and metabolomics: two emerging areas for legume improvement. Front Plant Sci. 2015;6:1116. https://doi.org/10.3389/fpls.2015.01116
  25. 25. Kumar R, Bohra A, Pandey AK, Pandey MK, Kumar A. Metabolomics for plant improvement: status and prospects. Front Plant Sci. 2017;8:1302. https://doi.org/10.3389/fpls.2017.01302
  26. 26. Liu S, Wang D, Mei Y, Xia T, Xu W, Zhang Y, et al. Overexpression of GmAAP6a enhances tolerance to low nitrogen and improves seed nitrogen status by optimizing amino acid partitioning in soybean. Plant Biotechnol J. 2020;18(8):1749-62. https://doi.org/10.1111/pbi.13338
  27. 27. Grewal SK, Sharma KP, Bharadwaj RD, et al. Characterization of chickpea cultivars and trait specific germplasm for grain protein content and amino acids composition and identification of potential donors for genetic improvement of its nutritional quality. Plant Genetic Resources: Characterization and Utilization. 2022;20(6):383-393. https://doi.org/10.1017/S147926212300028X
  28. 28. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-20. https://doi.org/10.1093/bioinformatics/btu170
  29. 29. Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019;37(8):907-15. https://doi.org/10.1038/s41587-019-0201-4
  30. 30. Varshney RK, Song C, Saxena RK, Azam S, Yu S, Sharpe AG, et al. Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol. 2013;31(3):240-6. https://doi.org/10.1038/nbt.2491
  31. 31. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv preprint arXiv:1303.3997. 2013.
  32. 32. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021;10(2):giab008. https://doi.org/10.1093/gigascience/giab008
  33. 33. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7(3):562–78. https://doi.org/10.1038/nprot.2012.016
  34. 34. Anders S, Huber W. Differential expression analysis for sequence count data. Nat Precedings. 2010;1–11. https://doi.org/10.1186/gb-2010-11-10-r106
  35. 35. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13(8):1194–202. https://doi.org/10.1016/j.molp.2020.06.009
  36. 36. Ge SX, Jung D, Yao R. ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics. 2020;36(8):2628–9. https://doi.org/10.1093/bioinformatics/btz931
  37. 37. Granot D, David-Schwartz R, Kelly G. Hexose kinases and their role in sugar-sensing and plant development. Front Plant Sci. 2013;4:44. https://doi.org/10.3389/fpls.2013.00044
  38. 38. Luo M, Jia M, Pan L, Chen W, Zhou K, Xi W. Sugar transporters PpSWEET9a and PpSWEET14 synergistically mediate peach sucrose allocation from source leaves to fruit. Commun Biol. 2024;7(1):1068. https://doi.org/10.1038/s42003-024-06767-5
  39. 39. Singh J, Thakur JK. Photosynthesis and abiotic stress in plants. In: Biotic and abiotic stress tolerance in plants. 2018. p. 27–46. https://doi.org/10.1007/978-981-10-9029-5_2
  40. 40. Ahmad F, Singh A, Kamal A. Osmoprotective role of sugar in mitigating abiotic stress in plants. In: Protective chemical agents in the amelioration of plant abiotic stress: biochemical and molecular perspectives. 2020. p. 53–70. https://doi.org/10.1002/9781119552154.ch3
  41. 41. Singh J, Das S, Jagadis Gupta K, Ranjan A, Foyer CH, Thakur JK. Physiological implications of SWEETs in plants and their potential applications in improving source–sink relationships for enhanced yield. Plant Biotechnol J. 2023;21(8):1528–41. https://doi.org/10.1111/pbi.13982
  42. 42. Fataftah N, Mohr C, Hajirezaei MR, Wirén NV, Humbeck K. Changes in nitrogen availability lead to a reprogramming of pyruvate metabolism. BMC Plant Biol. 2018;18:1–15. https://doi.org/10.1186/s12870-018-1301-x
  43. 43. Zhang L, Sun S, Liang Y, Li B, Ma S, Wang Z, et al. Nitrogen levels regulate sugar metabolism and transport in the shoot tips of crab apple plants. Front Plant Sci. 2021;12:626149. https://doi.org/10.3389/fpls.2021.626149
  44. 44. Feng W, Xue W, Zhao Z, Shi Z, Wang W, Bai Y, et al. Nitrogen fertilizer application rate affects the dynamic metabolism of nitrogen and carbohydrates in kernels of waxy maize. Front Plant Sci. 2024;15:1416397. https://doi.org/10.3389/fpls.2024.1416397
  45. 45. Du Y, Li W, Geng J, Li S, Zhang W, Liu X, et al. Genome-wide identification of the SWEET gene family in Phaseolus vulgaris L. and their patterns of expression under abiotic stress. J Plant Interact. 2022;17(1):390–403. https://doi.org/10.1080/17429145.2022.2044079
  46. 46. Kumar PV, Mallikarjuna MG, Jha SK, Mahato A, Lal SK, Yathish KR, et al. Unravelling structural, functional, evolutionary and genetic basis of SWEET transporters regulating abiotic stress tolerance in maize. Int J Biol Macromol. 2023;229:539-60. https://doi.org/10.1016/j.ijbiomac.2022.12.326
  47. 47. Tao Y, Cheung LS, Li S, Eom JS, Chen LQ, Xu Y, et al. Structure of a eukaryotic SWEET transporter in a homotrimeric complex. Nature. 2015;527(7577):259-63. https://doi.org/10.1038/nature15391
  48. 48. Ji J, Yang L, Fang Z, Zhang Y, Zhuang M, Lv H, et al. Plant SWEET family of sugar transporters: structure, evolution and biological functions. Biomolecules. 2022;12(2):205. https://doi.org/10.3390/biom12020205
  49. 49. Kang L, Teng Y, Cen Q, Fang Y, Tian Q, Zhang X, et al. Genome-wide identification of R2R3-MYB transcription factor and expression analysis under abiotic stress in rice. Plants. 2022;11(15):1928. https://doi.org/10.3390/plants11151928

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