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Physiologia plantarum
2024 May-Jun;176 (3): e14379.

Enhancing drought tolerance in chilli pepper through AdDjSKI-mediated modulation of ABA sensitivity, photosynthetic preservation, and ROS scavenging.

Mallesham Bulle, Ajay Kumar Venkatapuram, Md Mezanur Rahman, Kotab A Attia, Arif Ahmed Mohammed, Sadanandam Abbagani, P B Kirti
Author Information
  1. Mallesham Bulle: Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, Telangana, India. ORCID
  2. Ajay Kumar Venkatapuram: International Centre for Genetic Engineering and Biotechnology, Aruna Asaf Ali Marg, New Delhi, India.
  3. Md Mezanur Rahman: Department of Agroforestry and Environment, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh.
  4. Kotab A Attia: Department of Biochemistry, College of Science, King Saud University, Riyadh, Riyadh, Saudi Arabia.
  5. Arif Ahmed Mohammed: Department of Biochemistry, College of Science, King Saud University, Riyadh, Riyadh, Saudi Arabia.
  6. Sadanandam Abbagani: Plant Biotechnology Research Unit, Department of Biotechnology, Kakatiya University, Warangal, Telangana, India.
  7. P B Kirti: Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, Telangana, India.
PMID: 38853306 DOI: 10.1111/ppl.14379

Abstract

Drought stress threatens the productivity of numerous crops, including chilli pepper (Capsicum annuum). DnaJ proteins are known to play a protective role against a wide range of abiotic stresses. This study investigates the regulatory mechanism of the chloroplast-targeted chaperone protein AdDjSKI, derived from wild peanut (Arachis diogoi), in enhancing drought tolerance in chilli peppers. Overexpressing AdDjSKI in chilli plants increased chlorophyll content, reflected in the maximal photochemical efficiency of photosystem II (PSII) (Fv/Fm) compared with untransformed control (UC) plants. This enhancement coincided with the upregulated expression of PSII-related genes. Our subsequent investigations revealed that transgenic chilli pepper plants expressing AdDjSKI showed reduced accumulation of superoxide and hydrogen peroxide and, consequently, lower malondialdehyde levels and decreased relative electrolyte leakage percentage compared with UC plants. The mitigation of ROS-mediated oxidative damage was facilitated by heightened activities of antioxidant enzymes, including superoxide dismutase, catalase, ascorbate peroxidase, and peroxidase, coinciding with the upregulation of the expression of associated antioxidant genes. Additionally, our observations revealed that the ectopic expression of the AdDjSKI protein in chilli pepper plants resulted in diminished ABA sensitivity, consequently promoting seed germination in comparison with UC plants under different concentrations of ABA. All of these collectively contributed to enhancing drought tolerance in transgenic chilli plants with improved root systems when compared with UC plants. Overall, our study highlights AdDjSKI as a promising biotechnological solution for enhancing drought tolerance in chilli peppers, addressing the growing global demand for this economically valuable crop.

References

  1. Able, A. J. 2003. Role of reactive oxygen species in the response of barley to necrotrophic pathogens. Protoplasma, 221, 137���143.
  2. Aebi, H. 1984. [13] Catalase in vitro. Methods in enzymology. Academic Press; pp. 121���126. Vol. 105.
  3. Ahmed, I., Yadav, D., Shukla, P. & Kirti, P.B. 2018. Heterologous expression of Brassica juncea annexin, AnnBj2 confers salt tolerance and ABA insensitivity in transgenic tobacco seedlings. Functional & integrative genomics, 18, 569���579.
  4. Ali, F., Wang, Q., Fazal, A., Wang, L.���J., Song, S., Kong, M.���J., Mahmood, T. & Lu, S. 2022. The DnaJ���like zinc finger protein ORANGE promotes proline biosynthesis in drought���stressed Arabidopsis seedlings. International Journal of Molecular Sciences, 23, 3907.
  5. Anjum, S. A., Farooq, M., Xie, X.���Y., Liu, X.���J. & Ijaz, M. F. 2012. Antioxidant defense system and proline accumulation enables hot pepper to perform better under drought. Scientia Horticulturae, 140, 66���73.
  6. Aqeel, M., Khalid, N., Nazir, A., Irshad, M. K., Hakami, O., Basahi, M. A., Alamri, S., Hashem, M. & Noman, A. 2023. Foliar application of silver nanoparticles mitigated nutritional and biochemical perturbations in chilli pepper fertigated with domestic wastewater. Plant Physiology and Biochemistry, 194, 470���479.
  7. Bates, L. S., Waldren, R. A. & Teare, I. 1973. Rapid determination of free proline for water���stress studies. Plant and soil, 39, 205���207.
  8. Batiha, G. E.���S., Alqahtani, A., Ojo, O. A., Shaheen, H. M., Wasef, L., Elzeiny, M., Ismail, M., Shalaby, M., Murata, T. & Zaragoza���Bastida, A. 2020. Biological properties, bioactive constituents, and pharmacokinetics of some Capsicum spp. and capsaicinoids. International journal of molecular sciences, 21, 5179.
  9. Brocard, I. M., Lynch, T. J. & Finkelstein, R. R. 2002. Regulation and role of the Arabidopsis abscisic acid���insensitive 5 gene in abscisic acid, sugar, and stress response. Plant Physiology, 129, 1533���1543.
  10. Bulle, M., Yarra, R. & Abbagani, S. 2016. Enhanced salinity stress tolerance in transgenic chilli pepper (Capsicum annuum L.) plants overexpressing the wheat antiporter (TaNHX2) gene. Molecular Breeding, 36, 1���12.
  11. Cai, G. & Ahmed, M. A. 2022. The role of root hairs in water uptake: recent advances and future perspectives. Journal of experimental botany, 73, 3330���3338.
  12. Caplan, A. J., Cyr, D. M. & Douglas, M. 1993. Eukaryotic homologues of Escherichia coli dnaJ: a diverse protein family that functions with hsp70 stress proteins. Molecular biology of the cell, 4, 555���563.
  13. Chauhan, P. K., Upadhyay, S. K., Rajput, V. D., Dwivedi, P., Minkina, T. & Wong, M. H. 2024. Fostering plant growth performance under drought stress using rhizospheric microbes, their gene editing, and biochar. Environmental Geochemistry and Health, 46, 41.
  14. Chavan, S. G., He, X., Maier, C., Alagoz, Y., Anwar, S., Chen, Z.���H., Ghannoum, O., Cazzonelli, C. I. & Tissue, D. T. 2023. An energy���saving glasshouse film reduces seasonal, and cultivar dependent Capsicum yield due to light limited photosynthesis. Annals of Agricultural Sciences, 68, 21���35.
  15. Chen, T., Lin, T., Li, H., Lu, T., Li, J., Huang, W., Sun, H., Jiang, X., Zhang, J. & Yan, A. 2018. Heat shock protein 40 (HSP40) in pacific white shrimp (Litopenaeus vannamei): molecular cloning, tissue distribution and ontogeny, response to temperature, acidity/alkalinity and salinity stresses, and potential role in ovarian development. Frontiers in physiology, 9, 1784.
  16. Choudhury, F. K., Rivero, R. M., Blumwald, E. & Mittler, R. 2017. Reactive oxygen species, abiotic stress and stress combination. The Plant Journal, 90, 856���867.
  17. Clark, R. & Lee, S.���H. 2016. Anticancer properties of capsaicin against human cancer. Anticancer research, 36, 837���843.
  18. Collin, A., Daszkowska���Golec, A., Kurowska, M. & Szarejko, I. 2020. Barley ABI5 (Abscisic Acid INSENSITIVE 5) is involved in abscisic acid���dependent drought response. Frontiers in Plant Science, 11, 1138.
  19. Das, K. & Roychoudhury, A. 2014. Reactive oxygen species (ROS) and response of antioxidants as ROS���scavengers during environmental stress in plants. Frontiers in environmental science, 2, 53.
  20. Diao, M., Ma, L., Wang, J., Cui, J., Fu, A. & Liu, H.���Y. 2014. Selenium promotes the growth and photosynthesis of tomato seedlings under salt stress by enhancing chloroplast antioxidant defense system. Journal of plant growth regulation, 33, 671���682.
  21. Ding, F., Li, F. & Zhang, B. 2022. A plastid���targeted heat shock cognate 70���kDa protein confers osmotic stress tolerance by enhancing ROS scavenging capability. Frontiers in Plant Science, 13, 1012145.
  22. Dionisio���Sese, M. L. & Tobita, S. 1998. Antioxidant responses of rice seedlings to salinity stress. Plant science, 135, 1���9.
  23. Fan, C.���Y., Lee, S. & Cyr, D. M. 2003. Mechanisms for regulation of Hsp70 function by Hsp40. Cell stress & chaperones, 8, 309.
  24. Feller, U. 2016. Drought stress and carbon assimilation in a warming climate: Reversible and irreversible impacts. Journal of plant physiology, 203, 84���94.
  25. Finkelstein, R. R., Gampala, S. S. & Rock, C. D. 2002. Abscisic acid signaling in seeds and seedlings. The plant cell, 14, S15���S45.
  26. Gautam, R., Meena, R. K., Rampuria, S., Shukla, P. & Kirti, P. 2023. Ectopic expression of DnaJ type���I protein homolog of Vigna aconitifolia (VaDJI) confers ABA insensitivity and multiple stress tolerance in transgenic tobacco plants. Frontiers in Plant Science, 14.
  27. Georgopoulos, C. P., Lundquist���Heil, A., Yochem, J. & Feiss, M. 1980. Identification of the E. coli dnaJ gene product. Molecular and General Genetics MGG, 178, 583���588.
  28. Goffin, L. & Georgopoulos, C. 1998. Genetic and biochemical characterization of mutations affecting the carboxy���terminal domain of the Escherichia coli molecular chaperone DnaJ. Molecular microbiology, 30, 329���340.
  29. Gupta, A., Rico���Medina, A. & Ca��o���Delgado, A. I. 2020. The physiology of plant responses to drought. Science, 368, 266���269.
  30. Hennessy, F., Boshoff, A. & Blatch, G. L. 2005. Rational mutagenesis of a 40 kDa heat shock protein from Agrobacterium tumefaciens identifies amino acid residues critical to its in vivo function. The international journal of biochemistry & cell biology, 37, 177���191.
  31. Inskeep, W. P. & Bloom, P. R. 1985. Extinction coefficients of chlorophyll a and b in N, N���dimethylformamide and 80% acetone. Plant physiology, 77, 483���485.
  32. Jacobsen, J. V., Pearce, D. W., Poole, A. T., Pharis, R. P. & Mander, L. N. 2002. Abscisic acid, phaseic acid and gibberellin contents associated with dormancy and germination in barley. Physiologia Plantarum, 115, 428���441.
  33. Jariteh, M., Ebrahimzadeh, H., Niknam, V., Mirmasoumi, M. & Vahdati, K. 2015. Developmental changes of protein, proline and some antioxidant enzymes activities in somatic and zygotic embryos of Persian walnut (Juglans regia L.). Plant Cell, Tissue and Organ Culture (PCTOC), 122, 101���115.
  34. Ke, D., Sun, G. & Wang, Z. 2007. Effects of superoxide radicals on ACC synthase activity in chilling���stressed etiolated mungbean seedlings. Plant Growth Regulation, 51, 83���91.
  35. Kishor, P. B. K., Tiozon, R. N., Fernie, A. R. & Sreenivasulu, N. 2022. Abscisic acid and its role in the modulation of plant growth, development, and yield stability. Trends in Plant Science.
  36. Kong, F., Deng, Y., Wang, G., Wang, J., Liang, X. & Meng, Q. 2014. LeCDJ1, a chloroplast DnaJ protein, facilitates heat tolerance in transgenic tomatoes. Journal of integrative plant biology, 56, 63���74.
  37. Kopta, T., Sekara, A., Pokluda, R., Ferby, V. & Caruso, G. 2020. Screening of chilli pepper genotypes as a source of capsaicinoids and antioxidants under conditions of simulated drought stress. Plants, 9, 364.
  38. Kushiro, T., Okamoto, M., Nakabayashi, K., Yamagishi, K., Kitamura, S., Asami, T., Hirai, N., Koshiba, T., Kamiya, Y. & Nambara, E. 2004. The Arabidopsis cytochrome P450 CYP707A encodes ABA 8������hydroxylases: key enzymes in ABA catabolism. The EMBO journal, 23, 1647���1656.
  39. Liao, Y., Zou, H.���F., Wei, W., Hao, Y.���J., Tian, A.���G., Huang, J., Liu, Y.���F., Zhang, J.���S. & Chen, S.���Y. 2008. Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta, 228, 225���240.
  40. Lim, C. W., Han, S.���W., Hwang, I. S., Kim, D. S., Hwang, B. K. & Lee, S. C. 2015. The pepper lipoxygenase CaLOX1 plays a role in osmotic, drought and high salinity stress response. Plant and Cell Physiology, 56, 930���942.
  41. Lim, C. W. & Lee, S. C. 2014. Functional roles of the pepper MLO protein gene, CaMLO2, in abscisic acid signaling and drought sensitivity. Plant molecular biology, 85, 1���10.
  42. Liu, J. Z. & Whitham, S. A. 2013. Overexpression of a soybean nuclear localized type���III DnaJ domain���containing HSP40 reveals its roles in cell death and disease resistance. The plant journal, 74, 110���121.
  43. Luo, X., Bai, X., Sun, X., Zhu, D., Liu, B., Ji, W., Cai, H., Cao, L., Wu, J. & Hu, M. 2013. Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signalling. Journal of experimental botany, 64, 2155���2169.
  44. Lutz, M., Hern��ndez, J. & Henr��quez, C. 2015. Phenolic content and antioxidant capacity in fresh and dry fruits and vegetables grown in Chile. CyTA���Journal of Food, 13, 541���547.
  45. Meng, Y.���C., Zhang, H.���F., Pan, X.���X., Chen, N., Hu, H.���F., Haq, S. U., Khan, A. & Chen, R.���G. 2021. CaDHN3, a pepper (Capsicum annuum L.) dehydrin gene enhances the tolerance against salt and drought stresses by reducing ROS accumulation. International Journal of Molecular Sciences, 22, 3205.
  46. Metze, D., Schnecker, J., Canarini, A., Fuchslueger, L., Koch, B. J., Stone, B. W., Hungate, B. A., Hausmann, B., Schmidt, H. & Schaumberger, A. 2023. Microbial growth under drought is confined to distinct taxa and modified by potential future climate conditions. Nature Communications, 14, 5895.
  47. Miransari, M. & Smith, D. 2014. Plant hormones and seed germination. Environmental and experimental botany, 99, 110���121.
  48. Mittova, V., Volokita, M., Guy, M. & Tal, M. 2000. Activities of SOD and the ascorbate���glutathione cycle enzymes in subcellular compartments in leaves and roots of the cultivated tomato and its wild salt���tolerant relative Lycopersicon pennellii. Physiologia plantarum, 110, 42���51.
  49. Moore, C. E., Meacham���Hensold, K., Lemonnier, P., Slattery, R. A., Benjamin, C., Bernacchi, C. J., Lawson, T. & Cavanagh, A. P. 2021. The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems. Journal of experimental botany, 72, 2822���2844.
  50. Muddarsu, V. & Manivannan, S. 2017. In vitro screening of Chilli (Capsicum annuum L.) cultivars for drought tolerance. Chem Sci Rev Lett, 6, 2636���2644.
  51. Murashige, T. & Skoog, F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia plantarum, 15, 473���497.
  52. Naresh, P., Rao, V., Reddy, L., Reddy, A., Venkatachalapathi, V. & Reddy, M. 2016. Genetic analysis for fruit biochemical traits (capsaicinoids and carotenoids) and dry fruit yield in chilli (Capsicum annuum L.). Industrial crops and products, 94, 920���931.
  53. Naves, E. R., De ��vila Silva, L., Sulpice, R., Ara��jo, W. L., Nunes���Nesi, A., Peres, L. E. & Zs��g��n, A. 2019. Capsaicinoids: pungency beyond Capsicum. Trends in plant science, 24, 109���120.
  54. Rahman, M. M., Mostofa, M. G., Das, A. K., Anik, T. R., Keya, S. S., Ahsan, S., Khan, M. A. R., Ahmed, M., Rahman, M. A. & Hossain, M. M. 2022. Ethanol positively modulates photosynthetic traits, antioxidant defense and osmoprotectant levels to enhance drought acclimatization in soybean. Antioxidants, 11, 516.
  55. Rahman, M. M., Mostofa, M. G., Rahman, M. A., Islam, M. R., Keya, S. S., Das, A. K., Miah, M. G., Kawser, A. R., Ahsan, S. & Hashem, A. 2019. Acetic acid: A cost���effective agent for mitigation of seawater���induced salt toxicity in mung bean. Scientific reports, 9, 15186.
  56. Rampuria, S., Bag, P., Rogan, C. J., Sharma, A., Gassmann, W. & Kirti, P. 2018. Pathogen���induced AdDjSKI of the wild peanut, Arachis diogoi, potentiates tolerance of multiple stresses in E. coli and tobacco. Plant Science, 272, 62���74.
  57. Ruggiero, A., Landi, S., Punzo, P., Possenti, M., Van Oosten, M. J., Costa, A., Morelli, G., Maggio, A., Grillo, S. & Batelli, G. 2019. Salinity and ABA seed responses in pepper: expression and interaction of ABA core signaling components. Frontiers in plant science, 10, 304.
  58. Sadef, Y., Javed, T., Javed, R., Mahmood, A., Alwahibi, M. S., Elshikh, M. S., Abdelgawwa, M. R., Alhaji, J. H. & Rasheed, R. A. 2022. Nutritional status, antioxidant activity and total phenolic content of different fruits and vegetables' peels. Plos one, 17, e0265566.
  59. Sah, S. K., Reddy, K. R. & Li, J. 2016. Abscisic acid and abiotic stress tolerance in crop plants. Frontiers in plant science, 7, 571.
  60. Shinozaki, K. & Yamaguchi���Shinozaki, K. 1997. Gene expression and signal transduction in water���stress response. Plant physiology, 115, 327.
  61. Singh, A., Jha, S. K., Bagri, J. & Pandey, G. K. 2015. ABA inducible rice protein phosphatase 2C confers ABA insensitivity and abiotic stress tolerance in Arabidopsis. PloS one, 10, e0125168.
  62. Tang, C., Xie, J., Lv, J., Li, J., Zhang, J., Wang, C. & Liang, G. 2021. Alleviating damage of photosystem and oxidative stress from chilling stress with exogenous zeaxanthin in pepper (Capsicum annuum L.) seedlings. Plant Physiology and Biochemistry, 162, 395���409.
  63. Taofiq, O., Gonz��lez���Param��s, A. M., Barreiro, M. F. & Ferreira, I. C. 2017. Hydroxycinnamic acids and their derivatives: Cosmeceutical significance, challenges and future perspectives, a review. Molecules, 22, 281.
  64. Uknes, S. J. & Ho, T.���H. D. 1984. Mode of action of abscisic acid in barley aleurone layers: abscisic acid induces its own conversion to phaseic acid. Plant physiology, 75, 1126���1132.
  65. Vijay, A., Kumar, A., Islam, K., Momo, J. & Ramchiary, N. 2023. Functional genomics to understand the tolerance mechanism against biotic and abiotic stresses in Capsicum species. Transcriptome Profiling. Elsevier.
  66. Wan, H., Yuan, W., Ruan, M., Ye, Q., Wang, R., Li, Z., Zhou, G., Yao, Z., Zhao, J. & Liu, S. 2011. Identification of reference genes for reverse transcription quantitative real���time PCR normalization in pepper (Capsicum annuum L.). Biochemical and biophysical research communications, 416, 24���30.
  67. Wang, G., Cai, G., Kong, F., Deng, Y., Ma, N. & Meng, Q. 2014. Overexpression of tomato chloroplast���targeted DnaJ protein enhances tolerance to drought stress and resistance to Pseudomonas solanacearum in transgenic tobacco. Plant Physiology and Biochemistry, 82, 95���104.
  68. Wang, G., Cai, G., Xu, N., Zhang, L., Sun, X., Guan, J. & Meng, Q. 2019. Novel DnaJ protein facilitates thermotolerance of transgenic tomatoes. International Journal of Molecular Sciences, 20, 367.
  69. Wang, K., Liu, H., Mei, Q., Yang, J., Ma, F. & Mao, K. 2023a. Characteristics of bHLH transcription factors and their roles in the abiotic stress responses of horticultural crops. Scientia Horticulturae, 310, 111710.
  70. Wang, P., Liu, W. C., Han, C., Wang, S., Bai, M. Y. & Song, C. P. 2023b. Reactive oxygen species: multidimensional regulators of plant adaptation to abiotic stress and development. Journal of Integrative Plant Biology.
  71. Widuri, L. I., Lakitan, B., Sakagami, J., Yabuta, S., Kartika, K. & Siaga, E. 2020. Short���term drought exposure decelerated growth and photosynthetic activities in chili pepper (Capsicum annuum L.). Annals of Agricultural Sciences, 65, 149���158.
  72. Yang, Y., Guang, Y., Wang, F., Chen, Y., Yang, W., Xiao, X., Luo, S. & Zhou, Y. 2021. Characterization of phytochrome���interacting factor genes in pepper and functional analysis of CaPIF8 in cold and salt stress. Frontiers in Plant Science, 12, 746517.
  73. Yu, L., Chen, X., Wang, Z., Wang, S., Wang, Y., Zhu, Q., Li, S. & Xiang, C. 2013. Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiology, 162, 1378���1391.
  74. Zargar, S. M., Gupta, N., Nazir, M., Mahajan, R., Malik, F. A., Sofi, N. R., Shikari, A. B. & Salgotra, R. 2017. Impact of drought on photosynthesis: Molecular perspective. Plant gene, 11, 154���159.
  75. Zhao, H., Nie, K., Zhou, H., Yan, X., Zhan, Q., Zheng, Y. & Song, C. P. 2020. ABI5 modulates seed germination via feedback regulation of the expression of the PYR/PYL/RCAR ABA receptor genes. New Phytologist, 228, 596���608.
  76. Zhu, Z., Xu, X., Cao, B., Chen, C., Chen, Q., Xiang, C., Chen, G. & Lei, J. 2015. Pyramiding of AtEDT1/HDG11 and Cry2Aa2 into pepper (Capsicum annuum L.) enhances drought tolerance and insect resistance without yield decrease. Plant Cell, Tissue and Organ Culture (PCTOC), 120, 919���932.

MeSH Term

Capsicum
Photosynthesis
Reactive Oxygen Species
Plants, Genetically Modified
Droughts
Abscisic Acid
Plant Proteins
Arachis
Gene Expression Regulation, Plant
Photosystem II Protein Complex
Chlorophyll
Antioxidants
Molecular Chaperones
Drought Resistance

Chemicals

Reactive Oxygen Species
Abscisic Acid
Plant Proteins
Photosystem II Protein Complex
Chlorophyll
Antioxidants
Molecular Chaperones
Journal Article
Article has an altmetric score of 4

Word Cloud

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