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Overexpression of the tomato pathogenesis-related gene SlPR-1.9 confers increased tolerance to salt stress in Arabidopsis thaliana

Year 2024, Volume: 37 Issue: 3, 147 - 154, 06.12.2024
https://doi.org/10.29136/mediterranean.1556782

Abstract

Pathogenesis-related (PR) proteins are essential components of plant defense mechanisms, responding to both biotic and abiotic stresses. Among these, PR-1 proteins feature a CAP (Cysteine-rich secretory proteins, Antigen 5, and Pathogenesis-related 1) domain, which is crucial for immune responses and pathogen defense due to its ability to stabilize protein structures and interact with various molecules. This study investigated the role of the tomato PR-1 gene SlPR-1.9 in enhancing salt tolerance in Arabidopsis thaliana. The gene’s coding sequence was cloned and transferred into Arabidopsis to create SlPR-1.9 overexpression lines. These transgenic lines, alongside wild-type plants, were exposed to salt stress (150 mM NaCl) to assess their tolerance. Morphological analysis revealed that the transgenic lines demonstrated greater resilience to salt stress compared to wild-type plants, with less severe leaf curling and color changes. Additionally, lower proline accumulation, a stress marker, in the transgenic lines indicated an enhanced adaptive response. Bioinformatics analysis of the protein encoded by SlPR-1.9, A0A3Q7HSC4, suggested a strong interaction with galactolipase. Expression analysis showed that SlPR-1.9 was mainly expressed in roots and during early fruit development, suggesting a significant role in root physiology and stress response. These findings indicate that overexpression of SlPR-1.9 can improve plant tolerance to salt stress, offering potential applications for enhancing crop resilience to environmental challenges.

Supporting Institution

Akdeniz University

Thanks

This study was supported by Akdeniz University Scientific Research Projects Coordination Unit grant no. FYL-2022-5900. MAA is thankful for the financial support provided by the Fulbright Visiting Scholar Grant from the Turkish Fulbright Commission.

References

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  • Akbudak MA, Yildiz S, Filiz E (2020) Pathogenesis related protein-1 (PR-1) genes in tomato (Solanum lycopersicum L.): Bioinformatics analyses and expression profiles in response to drought stress. Genomics 112(6): 4089-4099.
  • Ali S, Mir ZA, Tyagi A, Bhat JA, Chandrashekar N, Papolu PK, Rawat S, Grover A (2017) Identification and comparative analysis of Brassica juncea pathogenesis-related genes in response to hormonal, biotic and abiotic stresses. Acta Physiol Plant 39(12): 268.
  • Almeida-Silva F, Venancio TM (2022) Pathogenesis-related protein 1 (PR-1) genes in soybean: Genome-wide identification, structural analysis and expression profiling under multiple biotic and abiotic stresses. Gene 809: 146013.
  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1): 205-207.
  • Bhattacharya A (2022) Lipid Metabolism in Plants Under Low-Temperature Stress: A Review | SpringerLink. Physiological processes in plants under low temperature stress: 409-516.
  • Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Current Opinion in Plant Biology 3(2): 117-124.
  • Douce R, Joyard J (1980) 12 - Plant Galactolipids. In: Lipids: Structure and Function (Stumpf PK, Ed.). Academic Press, pp. 321-362.
  • Ghosh UK, Islam MN, Siddiqui MN, Cao X, Khan M a. R (2022) Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms. Plant Biology 24(2): 227-239.
  • Gibbs GM, Roelants K, O’Bryan MK (2008) The CAP Superfamily: Cysteine-Rich Secretory Proteins, Antigen 5, and Pathogenesis-Related 1 Proteins—Roles in Reproduction, Cancer, and Immune Defense. Endocrine Reviews 29(7): 865-897.
  • Goyal RK, Fatima T, Topuz M, Bernadec A, Sicher R, Handa AK, Mattoo AK (2016) Pathogenesis-Related Protein 1b1 (PR1b1) Is a Major Tomato Fruit Protein Responsive to Chilling Temperature and Upregulated in High Polyamine Transgenic Genotypes. Front Plant Sci 7: 901.
  • Himmelbach A, Zierold U, Hensel G, Riechen J, Douchkov D, Schweizer P, Kumlehn J (2007) A Set of Modular Binary Vectors for Transformation of Cereals. Plant Physiology 145(4): 1192-1200.
  • Hong JK, Hwang BK (2005) Functional Characterization of PR-1 Protein, β-1,3-Glucanase and Chitinase Genes During Defense Response to Biotic and Abiotic Stresses in Capsicum annuum. The Plant Pathology Journal 21(3): 195-206.
  • Kasap M, Akbudak MA (2024) Domates Pr-1 Genlerinin Soğuk Stresi Altındaki İfade Profilleri. In: 8th International Cukurova Agriculture and Veterinary Congress.
  • Khan R, Zhou P, Ma X, Zhou L, Wu Y, Ullah Z, Wang S (2019) Transcriptome Profiling, Biochemical and Physiological Analyses Provide New Insights towards Drought Tolerance in Nicotiana tabacum L. Genes 10(12): 1041.
  • Lee H-J, Park OK (2019) Lipases associated with plant defense against pathogens. Plant Science 279: 51-58.
  • Liu Y, Qi Y, Zhang A, Wu H, Liu Z, Ren X (2019) Molecular cloning and functional characterization of AcGST1, an anthocyanin-related glutathione S-transferase gene in kiwifruit (Actinidia chinensis). Plant Mol Biol 100(4): 451-465.
  • Liu T, Chen T, Kan J, Yao Y, Guo D, Yang Y, Ling X, Wang J, Zhang B (2022) The GhMYB36 transcription factor confers resistance to biotic and abiotic stress by enhancing PR1 gene expression in plants. Plant Biotechnology Journal 20(4): 722-735.
  • Loon LC van, Martijn Rep, Corné MJ Pieterse (2006) Significance of Inducible Defense-related Proteins in Infected Plants. Annu Rev Phytopathol 44(1): 135-162.
  • Milne TJ, Abbenante G, Tyndall JDA, Halliday J, Lewis RJ (2003) Isolation and Characterization of a Cone Snail Protease with Homology to CRISP Proteins of the Pathogenesis-related Protein Superfamily *. Journal of Biological Chemistry 278(33): 31105-31110.
  • Moellering ER, Benning C (2011) Galactoglycerolipid metabolism under stress: a time for remodeling. Trends in Plant Science 16(2): 98-107.
  • Prihatna C, Barbetti MJ, Barker SJ (2018) A Novel Tomato Fusarium Wilt Tolerance Gene. Front Microbiol 9.
  • Roca Paixão JF, Gillet F-X, Ribeiro TP, Bournaud C, Lourenço-Tessutti IT, Noriega DD, Melo BP de, Almeida-Engler J de, Grossi-de-Sa MF (2019) Improved drought stress tolerance in Arabidopsis by CRISPR/dCas9 fusion with a Histone AcetylTransferase. Sci Rep 9(1): 8080.
  • Sarowar S, Kim YJ, Kim EN, Kim KD, Hwang BK, Islam R, Shin JS (2005) Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep 24(4): 216-224.
  • Sels J, Mathys J, De Coninck BMA, Cammue BPA, De Bolle MFC (2008) Plant pathogenesis-related (PR) proteins: A focus on PR peptides. Plant Physiology and Biochemistry 46(11): 941-950.
  • Singhal P, Jan AT, Azam M, Haq QMR (2016) Plant abiotic stress: a prospective strategy of exploiting promoters as alternative to overcome the escalating burden. Frontiers in Life Science 9(1): 52-63.
  • Szklarczyk D, Gable AL, Nastou KC, Lyon D, Kirsch R, Pyysalo S, Doncheva NT, Legeay M, Fang T, Bork P, Jensen LJ, von Mering C (2021) The STRING database in 2021: customizable protein–protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Research 49(D1): D605-D612.
  • Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485(7400): 635-641.
  • Wang J, Mao X, Wang R, Li A, Zhao G, Zhao J, Jing R (2019a) Identification of wheat stress-responding genes and TaPR-1-1 function by screening a cDNA yeast library prepared following abiotic stress. Sci Rep 9(1): 141.
  • Wang K, Durrett TP, Benning C (2019b) Functional diversity of glycerolipid acylhydrolases in plant metabolism and physiology. Progress in Lipid Research 75: 100987.
  • Wani SH, Dutta T, Neelapu NRR, Surekha C (2017) Transgenic approaches to enhance salt and drought tolerance in plants. Plant Gene 11: 219-231.
  • Yeats C, Bentley S, Bateman A (2003) New Knowledge from Old: In silico discovery of novel protein domains in Streptomyces coelicolor. BMC Microbiol 3(1): 3.
  • Yu L, Zhou C, Fan J, Shanklin J, Xu C (2021) Mechanisms and functions of membrane lipid remodeling in plants. The Plant Journal 107(1): 37-53.

Overexpression of the tomato pathogenesis-related gene SlPR-1.9 confers increased tolerance to salt stress in Arabidopsis thaliana

Year 2024, Volume: 37 Issue: 3, 147 - 154, 06.12.2024
https://doi.org/10.29136/mediterranean.1556782

Abstract

References

  • Ahuja I, Kissen R, Bones AM (2012) Phytoalexins in defense against pathogens. Trends in Plant Science 17(2): 73-90.
  • Akbudak MA, Yildiz S, Filiz E (2020) Pathogenesis related protein-1 (PR-1) genes in tomato (Solanum lycopersicum L.): Bioinformatics analyses and expression profiles in response to drought stress. Genomics 112(6): 4089-4099.
  • Ali S, Mir ZA, Tyagi A, Bhat JA, Chandrashekar N, Papolu PK, Rawat S, Grover A (2017) Identification and comparative analysis of Brassica juncea pathogenesis-related genes in response to hormonal, biotic and abiotic stresses. Acta Physiol Plant 39(12): 268.
  • Almeida-Silva F, Venancio TM (2022) Pathogenesis-related protein 1 (PR-1) genes in soybean: Genome-wide identification, structural analysis and expression profiling under multiple biotic and abiotic stresses. Gene 809: 146013.
  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1): 205-207.
  • Bhattacharya A (2022) Lipid Metabolism in Plants Under Low-Temperature Stress: A Review | SpringerLink. Physiological processes in plants under low temperature stress: 409-516.
  • Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Current Opinion in Plant Biology 3(2): 117-124.
  • Douce R, Joyard J (1980) 12 - Plant Galactolipids. In: Lipids: Structure and Function (Stumpf PK, Ed.). Academic Press, pp. 321-362.
  • Ghosh UK, Islam MN, Siddiqui MN, Cao X, Khan M a. R (2022) Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms. Plant Biology 24(2): 227-239.
  • Gibbs GM, Roelants K, O’Bryan MK (2008) The CAP Superfamily: Cysteine-Rich Secretory Proteins, Antigen 5, and Pathogenesis-Related 1 Proteins—Roles in Reproduction, Cancer, and Immune Defense. Endocrine Reviews 29(7): 865-897.
  • Goyal RK, Fatima T, Topuz M, Bernadec A, Sicher R, Handa AK, Mattoo AK (2016) Pathogenesis-Related Protein 1b1 (PR1b1) Is a Major Tomato Fruit Protein Responsive to Chilling Temperature and Upregulated in High Polyamine Transgenic Genotypes. Front Plant Sci 7: 901.
  • Himmelbach A, Zierold U, Hensel G, Riechen J, Douchkov D, Schweizer P, Kumlehn J (2007) A Set of Modular Binary Vectors for Transformation of Cereals. Plant Physiology 145(4): 1192-1200.
  • Hong JK, Hwang BK (2005) Functional Characterization of PR-1 Protein, β-1,3-Glucanase and Chitinase Genes During Defense Response to Biotic and Abiotic Stresses in Capsicum annuum. The Plant Pathology Journal 21(3): 195-206.
  • Kasap M, Akbudak MA (2024) Domates Pr-1 Genlerinin Soğuk Stresi Altındaki İfade Profilleri. In: 8th International Cukurova Agriculture and Veterinary Congress.
  • Khan R, Zhou P, Ma X, Zhou L, Wu Y, Ullah Z, Wang S (2019) Transcriptome Profiling, Biochemical and Physiological Analyses Provide New Insights towards Drought Tolerance in Nicotiana tabacum L. Genes 10(12): 1041.
  • Lee H-J, Park OK (2019) Lipases associated with plant defense against pathogens. Plant Science 279: 51-58.
  • Liu Y, Qi Y, Zhang A, Wu H, Liu Z, Ren X (2019) Molecular cloning and functional characterization of AcGST1, an anthocyanin-related glutathione S-transferase gene in kiwifruit (Actinidia chinensis). Plant Mol Biol 100(4): 451-465.
  • Liu T, Chen T, Kan J, Yao Y, Guo D, Yang Y, Ling X, Wang J, Zhang B (2022) The GhMYB36 transcription factor confers resistance to biotic and abiotic stress by enhancing PR1 gene expression in plants. Plant Biotechnology Journal 20(4): 722-735.
  • Loon LC van, Martijn Rep, Corné MJ Pieterse (2006) Significance of Inducible Defense-related Proteins in Infected Plants. Annu Rev Phytopathol 44(1): 135-162.
  • Milne TJ, Abbenante G, Tyndall JDA, Halliday J, Lewis RJ (2003) Isolation and Characterization of a Cone Snail Protease with Homology to CRISP Proteins of the Pathogenesis-related Protein Superfamily *. Journal of Biological Chemistry 278(33): 31105-31110.
  • Moellering ER, Benning C (2011) Galactoglycerolipid metabolism under stress: a time for remodeling. Trends in Plant Science 16(2): 98-107.
  • Prihatna C, Barbetti MJ, Barker SJ (2018) A Novel Tomato Fusarium Wilt Tolerance Gene. Front Microbiol 9.
  • Roca Paixão JF, Gillet F-X, Ribeiro TP, Bournaud C, Lourenço-Tessutti IT, Noriega DD, Melo BP de, Almeida-Engler J de, Grossi-de-Sa MF (2019) Improved drought stress tolerance in Arabidopsis by CRISPR/dCas9 fusion with a Histone AcetylTransferase. Sci Rep 9(1): 8080.
  • Sarowar S, Kim YJ, Kim EN, Kim KD, Hwang BK, Islam R, Shin JS (2005) Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep 24(4): 216-224.
  • Sels J, Mathys J, De Coninck BMA, Cammue BPA, De Bolle MFC (2008) Plant pathogenesis-related (PR) proteins: A focus on PR peptides. Plant Physiology and Biochemistry 46(11): 941-950.
  • Singhal P, Jan AT, Azam M, Haq QMR (2016) Plant abiotic stress: a prospective strategy of exploiting promoters as alternative to overcome the escalating burden. Frontiers in Life Science 9(1): 52-63.
  • Szklarczyk D, Gable AL, Nastou KC, Lyon D, Kirsch R, Pyysalo S, Doncheva NT, Legeay M, Fang T, Bork P, Jensen LJ, von Mering C (2021) The STRING database in 2021: customizable protein–protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Research 49(D1): D605-D612.
  • Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485(7400): 635-641.
  • Wang J, Mao X, Wang R, Li A, Zhao G, Zhao J, Jing R (2019a) Identification of wheat stress-responding genes and TaPR-1-1 function by screening a cDNA yeast library prepared following abiotic stress. Sci Rep 9(1): 141.
  • Wang K, Durrett TP, Benning C (2019b) Functional diversity of glycerolipid acylhydrolases in plant metabolism and physiology. Progress in Lipid Research 75: 100987.
  • Wani SH, Dutta T, Neelapu NRR, Surekha C (2017) Transgenic approaches to enhance salt and drought tolerance in plants. Plant Gene 11: 219-231.
  • Yeats C, Bentley S, Bateman A (2003) New Knowledge from Old: In silico discovery of novel protein domains in Streptomyces coelicolor. BMC Microbiol 3(1): 3.
  • Yu L, Zhou C, Fan J, Shanklin J, Xu C (2021) Mechanisms and functions of membrane lipid remodeling in plants. The Plant Journal 107(1): 37-53.
There are 33 citations in total.

Details

Primary Language English
Subjects Plant Biotechnology in Agriculture
Journal Section Makaleler
Authors

Kubra Yildiz 0000-0002-2958-7058

M. Aydin Akbudak 0000-0002-1397-4678

Publication Date December 6, 2024
Submission Date September 27, 2024
Acceptance Date October 24, 2024
Published in Issue Year 2024 Volume: 37 Issue: 3

Cite

APA Yildiz, K., & Akbudak, M. A. (2024). Overexpression of the tomato pathogenesis-related gene SlPR-1.9 confers increased tolerance to salt stress in Arabidopsis thaliana. Mediterranean Agricultural Sciences, 37(3), 147-154. https://doi.org/10.29136/mediterranean.1556782
AMA Yildiz K, Akbudak MA. Overexpression of the tomato pathogenesis-related gene SlPR-1.9 confers increased tolerance to salt stress in Arabidopsis thaliana. Mediterranean Agricultural Sciences. December 2024;37(3):147-154. doi:10.29136/mediterranean.1556782
Chicago Yildiz, Kubra, and M. Aydin Akbudak. “Overexpression of the Tomato Pathogenesis-Related Gene SlPR-1.9 Confers Increased Tolerance to Salt Stress in Arabidopsis Thaliana”. Mediterranean Agricultural Sciences 37, no. 3 (December 2024): 147-54. https://doi.org/10.29136/mediterranean.1556782.
EndNote Yildiz K, Akbudak MA (December 1, 2024) Overexpression of the tomato pathogenesis-related gene SlPR-1.9 confers increased tolerance to salt stress in Arabidopsis thaliana. Mediterranean Agricultural Sciences 37 3 147–154.
IEEE K. Yildiz and M. A. Akbudak, “Overexpression of the tomato pathogenesis-related gene SlPR-1.9 confers increased tolerance to salt stress in Arabidopsis thaliana”, Mediterranean Agricultural Sciences, vol. 37, no. 3, pp. 147–154, 2024, doi: 10.29136/mediterranean.1556782.
ISNAD Yildiz, Kubra - Akbudak, M. Aydin. “Overexpression of the Tomato Pathogenesis-Related Gene SlPR-1.9 Confers Increased Tolerance to Salt Stress in Arabidopsis Thaliana”. Mediterranean Agricultural Sciences 37/3 (December 2024), 147-154. https://doi.org/10.29136/mediterranean.1556782.
JAMA Yildiz K, Akbudak MA. Overexpression of the tomato pathogenesis-related gene SlPR-1.9 confers increased tolerance to salt stress in Arabidopsis thaliana. Mediterranean Agricultural Sciences. 2024;37:147–154.
MLA Yildiz, Kubra and M. Aydin Akbudak. “Overexpression of the Tomato Pathogenesis-Related Gene SlPR-1.9 Confers Increased Tolerance to Salt Stress in Arabidopsis Thaliana”. Mediterranean Agricultural Sciences, vol. 37, no. 3, 2024, pp. 147-54, doi:10.29136/mediterranean.1556782.
Vancouver Yildiz K, Akbudak MA. Overexpression of the tomato pathogenesis-related gene SlPR-1.9 confers increased tolerance to salt stress in Arabidopsis thaliana. Mediterranean Agricultural Sciences. 2024;37(3):147-54.

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