Role of sulfur in pyrroline-5-carboxylate synthase (P5CS) gene expression, proline accumulation, and antioxidant enzyme activity of wheat under water deficit conditions

Document Type : Research Paper

Authors

Department of Agronomy and Crop Breeding, Faculty of Agriculture, Ilam University, Ilam,I. R. Iran

Abstract

Sulfur (S) plays a crucial role in plant growth and development and serves numerous biological functions in plants. To investigate the role of sulfur in drought stress protection, two experiments were conducted under greenhouse and growth ‎chamber conditions in 2021 Also, to evaluate ‎the influence of foliar application of sulfur on the expression of Pyrroline-5-carboxylate synthase, )P5CS)‎, proline concentration, and antioxidant enzyme activities‎, the plants of wheat Sardari and Ivan cultivars were exposed to two levels of water regimes. Plants under well-watered irrigation and drought stress conditions showed different P5CS expression levels and accumulated proline. The P5CS expression level in the Ivan cultivar was significantly increased by foliar application of S, while the same application had no significant effect on P5CS expression in the Sardari cultivar. Plants exposed to drought stress and foliar-sprayed with S showed a higher proline accumulation The activities of antioxidant enzymes, including peroxidase (POD), catalase, ‎glutathione peroxidase (GP), and glutathione reductase , were increased by 134 %, 40.4 %,  45.4 %, and 77.4 %, respectively, in plants exposed to drought stress. POD and GR ‎were ‎significantly increased‎ by 19.6 % and 51.8 %, respectively, ‎due to S application. Drought-induced plants that were foliar-sprayed with S exhibited a significantly lower rate of ion leakage and higher leaf-relative water content than those of control plants. Based on the results of the present research, it was revealed that S substantially enhances the expression rate of the P5CS gene, leading to proline accumulation, and activates defense reactions in water-stressed wheat.

Keywords

Main Subjects

Article Title [Persian]

نقش سولفور در بیان ژن پرولین-5-کربوکسیلیت سنتاز (P5CS)، تجمع پرولین و فعالیت آنزیم‌های آنتی‌اکسیدانتی گندم در شرایط تنش کمبود آب

Authors [Persian]

  • زهره کریمی
  • محمدجواد زارع
  • آرش فاضلی
  • بتول زارعی
گروه زراعت و اصلاح نباتات دانشکده کشاورزی دانشگاه ایلام، ایلام، ج. ا. ایران
Abstract [Persian]

سولفور نقش کلیدی در رشد و نمو گیاه دارد و در بسیاری از کارکردهای زیستی گیاه مورد استفاده قرار می­گیرد. برای بررسی نقش سولفور در حفاظت گیاه در مقابل تنش خشکی، دو آزمایش در شرایط گلخانه و اتاقک رشد در سال 1399 انجام شد. همچنین برای ارزیابی تاثیر محلول پاشی با عنصر سولفور بر بیان ژنهای مرتبط با ساخت پرولین(پرولین-5-کربوکسیلات سنتاز، (P5CS)، تجمع پرولین،  و فعالیت های آنتی_اکسیدانتی، گیاهان دو رقم  سرداری و ایوان  گندم در معرض دو سطح رژیم آبی قرار گرفتند.  گیاهان در معرض تنش آبی در مقایسه با کیاهانی که تحت آبیاری مطلوب قرار گرفته بودند سطوح مختلف بیان ژن  P5CSو تجمع پرولین را نشان دادند. هرچند محلول پاشی با گوگرد منجر به تغییر معنی دار در بیان ژن P5CS در رقم سرداری نگردید اما موجب افزایش معنی دار سطح بیان این ژن در رقم ایوان گردید. اعمال تنش آبی همراه با محلول‌پاشی سولفور موجب تجمع بیشتر پرولین گردید. اعمال تنش خشکی موجب افزایش فعالیت آنزیمهای آنتی اکسدانتی شامل پراکسیداز، کاتالاز، گلوتاتیون پراکسیداز و گلاتاتیون ریدوکتاز به ترتیب به میزان 134، 40/4، 54/4 و 77/4 درصد گردید. پراکسیداز ‏و گلاتاتیون ریدوکتاز در اثر کاربرد سولفور به ترتیب به میزان 19/6 و 51/8 درصد افزایش معنی دار داشتند.گیاهان محلول پاشی شده با سولفور از نشت یونی کمتر و میزان بیشتر محتوای آب نسبی برگ نسبت به گیاهان شاهد برخوردار بودند. بر اساس نتایج این تحقیق مشخص گردید که سولفور موجب افزایش  معنی دار بیان ژن P5CS و تجمع  بیشتر پرولین  گردید. همچنین گوگرد موجب فعال سازی واکنش­های دفاعی مرتبط با اثرات سوء تنش کم آبی در گندم گردید.

Keywords [Persian]

  • آنزیم های آنتی اکسیدانتی
  • پرولین
  • پیرولین-5-کربوکسیلیت سینتاز
  • سولفور

References

Ahmad, N., Malagoli, M., Wirtz, M., & Ruediger, H. (2016). Drought stress in maize causes differential acclimation responses of glutathione and sulfur metabolism in leaves and roots. BMC Plant Biology, 16(1), 247.
https://doi.org/10.1186/s12870-016-0940-z
Arianmehr, M., Karimi, N., & Souri, Z. (2022). Exogenous supplementation of sulfur (S) and reduced glutathione (GSH) alleviates arsenic toxicity in shoots of Isatis cappadocica Desv. and Erysimum allionii L. Environmental Science and Pollution Research  29(42), 64205-64214.
https://doi.org/10.1007/s11356-022-19477-4
Arnon, D. I. (1949). Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiology, 24, 1-5.
https://doi.org/10.1104/pp.24.1.1
Arteaga, S., Yabor, L., Díez, M. J., Prohens, J., Boscaiu, M., & Vicente, Ó. (2020). The use of proline in screening for tolerance to drought and salinity in common bean (Phaseolus vulgaris L.) Genotypes. Agronomy, 10, 817.‎
https://doi.org/10.3390/agronomy10060817
Astolfi, S., & Zuchi, S. (2013). Adequate S supply protects barley plants from adverse effects of salinity stress by increasing thiol contents. Acta Physiologiae Plantarum, 35, 175-181. https://doi.org/10.1007/s11738-012-1060-5
Aula, L., Dhillon, J. S., Omara, P., Wehmeyer, G. B., Freeman, K. W., & Raun, W. R. (2019). World sulfur use efficiency for cereal crops. Agronomy Journal, 111, 2485-2492.
https://doi.org/10.2134/agronj2019.02.0095
Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water stress studies. Plant and Soil, 39, 205-207.
https://doi.org/10.1007/BF00018060
Blake-Kalff, M. M. A., Hawkesford, M. J., Zhao, F. J., & McGrath, S. P. (2000). Diagnosing sulfur deficiency in field-grown oilseed rape (Brassica napus L) and wheat (Triticum aestivum L). Plant and Soil, 225, 95-107.
https://doi.org/10.1023/A:1026503812267
Chance, B., & Maehly, A. C. (1955). Assay of catalase and peroxidase. Methods in Enzymology, 2, 764-775.
https://doi.org/10.1016/S0076-6879(55)02300-8
Curtis, T. Y., Raffan, S., Wan, Y., King, R., Gonzalez-Uriarte, A., Halford, N. G. (2019). Contrasting ‎gene expression patterns in grain of high and low asparagine wheat genotypes in response to sulphur supply. BMC Genomics, 1, 628. https://doi.org/10.1186/s12864-019-5991-8
Das, U., Rahman, M. A., Ela, E. J., Lee, K. W., & Kabir, A. H. (2021). Sulfur triggers glutathione and phytochelatin accumulation causing excess Cd bound to the cell wall of roots in alleviating Cd-toxicity in alfalfa. Chemosphere, 262, 128361.
https://doi.org/10.1016/j.chemosphere.2020.128361
Fatma, M., Asgher, M., Masood, A., & Khan, N. A. (2014). Excess sulfur supplementation improves photosynthesis and growth in mustard under salt stress through increased production of glutathione. Environmental and Experimental Botany, 107, 55-63.
https://doi.org/10.1016/j.envexpbot.2014.05.008
Foyer, C. H., & Halliwell, B. (1976). Presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. Planta, 133, 21-25.
https://doi.org/10.1007/BF00386001
Furlan A. L., Bianucci, E., Giordano, W., Castro, S., & Becker, D. F. (2020). Proline metabolic dynamics and implications in drought tolerance of peanut plants. Plant Physiology and Biochemistry, 151, 566-578.
https://doi.org/10.1016/j.plaphy.2020.04.010
Gilbert, S. M., Clarkson, D.T., Cambridge, M., Lambers, H., & Hawkesford, M. J. (1997).  SO₄²⁻ deprivation has an early effect on the content of ribulose-1,5-biphosphate carboxylase/oxygenase ‎and photosynthesis in young leaves of wheat. Plant Physiology, 115, 1231-1239.‎
https://doi.org/ 10.1104/pp.115.3.1231
Borpatragohain,  P., Rose, T. J., Liu, L., Barkla, B. J., Raymond, C. A., & King, G. J. (2019). Remobilization and fate of sulphur in mustard. Annals of Botany, 124, 471-480.
https://doi.org/10.1093/aob/mcz101
Hare, P. D., &‎ Cress, W. A. ‎(1997). Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation, 21, 79-102.
https://doi.org/10.1023/A:1005703923347
Hasan, H., Uzma, Gul, A., Amir, R., Ali, M., Kubra, G., Khan, F., Yousaf, S., Ajmal, K. B., Naseer, H., Khan, W., & Keyani, R. (2020). Role of osmoprotectants and drought tolerance in wheat. In Ozturk, M. and Gul, A. (Eds), Climate change and food security with emphasis on wheat (‎pp: 207-216). Academic Press.
https://doi.org/10.1016/B978-0-12-819527-7.00013-3
Hasanuzzaman, M., Nahar, K., Rahman, A., Al Mahmud, J., Alharby, H. F., & Fujita, M. (2018). Exogenous glutathione attenuates lead-induced oxidative stress in wheat by improving antioxidant defense and physiological mechanisms. Journal of Plant Interactions, 13, 203-212.
https://doi.org/10.1080/17429145.2018.1458913
Jamshidi Goharrizi, K., Baghizadeh, A., Afroushteh, M., Amirmahani, F., & Ghotbzadeh Kermani, S. (2020). Effects of salinity stress on proline content and expression of Δ1-pyrroline-5-carboxylate synthase and vacuolar-type H+ subunit E genes in wheat. Plant Genetic Resources, 18, 334-342.
https://doi.org/10.1017/S1479262120000350
 Jamshidi Goharrizi, K., Baghizadeh, A., Karami, S., Nazari, M., & Afroushteh, M. (2023). Expression of the W36, P5CS, P5CR, MAPK3, and MAPK6 genes and proline content in bread wheat genotypes under drought stress. Cereal Research Communications, 51, 545-556.
https://doi.org/10.1007/s42976-022-00331-9
Lee, B. R., Zaman, R., Avice, J. C., Ourry, A., & Kim, T. H. (2016). Sulfur use efficiency is a significant determinant of drought stress tolerance in relation to photosynthetic activity in Brassica napus cultivars. Frontiers in Plant Science, 7, Article 459.
https://doi.org/10.3389/fpls.2016.00459
Li, C., Wang, P., van der Ent, A., Cheng, M., Jiang, H., Lund Read, T., Lombi, E., Tang, C., de Jonge, M. D., Menzies, N. W., & Kopittke, P. M. (2019). Absorption of foliar-applied Zn in sunflower (Helianthus annuus): importance of the cuticle, stomata and trichomes. Annals of Botany, 123, 57-68.
https://doi.org/10.1093/aob/mcy135
Li, L., Yi, H., Liu, X., & Qi, H. (2021). Sulfur dioxide enhance drought tolerance of wheat seedlings through H2S signaling. Ecotoxicology and Environmental Safety, 207, 111248.
https://doi.org/10.1016/j.ecoenv.2020.111248
Li, Q., Gao, Y., & Yang, A. (2020). Sulfur homeostasis in plants. International Journal of Molecular Sciences, 21, 8926.
https://doi.org/10.3390/ijms21238926
Luck, H. (1974). Catalase. In Bergmeyer, H. U. (Ed), Methods in enzymatic analysis V2 (pp. 885-894). New York and London: Academic Press.
http://dx.doi.org/10.1016/B978-0-12-395630-9.50158-4
Lunde, C., Zygadlo, A., Simonsen, H. T., Nielsen, P. L., Blennow, A., & Haldrup, A. (2008). Sulfur starvation in rice: The effect on photosynthesis, carbohydrate metabolism, and oxidative stress protective pathways. Physiologia Plantarum, 134, 508-521.
https://doi.org/10.1111/j.1399-3054.2008.01159.x
Lutts, S., Kint, J., & Bouharmont, J. (1996). NaCl-induced senescence in leaves of rice (Oriza sativa L.) cultivars differing in salinity resistance. Annals of Botany, 78, 389-398.
https://doi.org/10.1006/anbo.1996.0134
Maghsoudi, K., Emam, Y., Niazi, A., Pessarakli, M., & Arvin, M. J. (2018). P5CS expression level and proline accumulation in the sensitive and tolerant wheat cultivars under control and drought stress conditions in the presence/absence of silicon and salicylic acid. Journal of Plant Interactions, 13, 461-471. https://doi.org/10.1080/17429145.2018.1506516
Meena, M., Divyanshu, K., Kumar, S., Swapnil, P., Zehra, A., Shukla, V., Yadav, M., & Upadhyay, R. S. (2019). Regulation of L-proline biosynthesis, signal transduction, transport, accumulation and its vital role in plants during variable environmental conditions. Heliyon, 5 (12), e02952.
https://doi.org/10.1016/j.heliyon.2019.e02952
Mirdoraghi, M., Behpouri, A., & Bijanzade, E. (2022). Evaluating the effects of genotype mixture and stress tolerant indices in durum wheat (Triticum durum Desf.) under drought stress. Iran Agricultural Research, 41, 83-94.
https://doi.org/10.22099/iar.2022.42353.1469
Muneer, S., Lee, B. R., Kim, K. Y., Park, S. H., Zhang, Q., & Kim, T. H. (2014). Involvement of sulphur‎nutrition in modulating iron deficiency responses in photosynthetic organelles of oilseed ‎rape (Brassica napus L.). Photosynthesis Research, 119, 319-329.
https://doi.org/10.1007/s11120-013-9953-8
Mwadzingeni, L., Shimelis, H., Tesfay, S., & Tsilo, T. J. (2016). Screening of bread wheat genotypes for drought tolerance using phenotypic and proline analyses. Frontier in Plant Science, 7, Article 1276.
https://doi.org/10.3389/fpls.2016.01276
Nadeem, M., Ali, M., Kubra, G., Fareed, A., Hasan, H., Khursheed, A., Gul, A., Amir, R., Fatima, N., & Khan, S. U. (2020). Role of osmoprotectants in salinity tolerance in wheat. In Ozturk, M. and Gul A. (Eds), Climate change and food security with emphasis on wheat (‎pp: 93-106). Academic Press. https://doi.org/10.1016/B978-0-12-819527-7.00006-6
Narayan, O. P., Kumar, P. A., Yadav, B. K., Dua, M., & Johri, A. K. (2023). ‎Sulfur ‎nutrition and its role in plant growth and development. Plant Signaling and Behavior, 7, 2030082.
https://doi.org/10.1080/15592324.2022.2030082
Nardino, M., Perin, E. C., Aranha, B. C., Carpes, S. T., Fontoura, B. H., de Sousa, D. J. P., & Freitas, D. S. (2022). Understanding drought response mechanisms in wheat and multi-trait selection. PLoS One, 17, e0266368.
 https://doi.org/10.1371/journal.pone.0266368
Nxele, X., Klein, A., & Ndimba, B. K. (2017). Drought and salinity stress alters ROS accumulation, water retention, and osmolyte content in sorghum plants. South African Journal of Botany, 108, 261-266. https://doi.org/10.1016/j.sajb.2016.11.003
Qayyum, A., Al Ayoubi, S., Sher, A., Bibi, Y., Ahmad, S., Shen, Z., & Jenks, M. A. (2021). Improvement in drought tolerance in bread wheat is related to an improvement in osmolyte production, antioxidant enzyme activities, and gaseous exchange. Saudi Journal of Biological Sciences, 28, 5238-5249.
https://doi.org/10.1016/j.sjbs.2021.05.040
Raffan, S., Oddy, J., Halford, N. G. (2020). The Sulphur response in wheat grain and ‎its implications for acrylamide formation and food safety. International Journal of Molecular ‎Sciences, 21, 3876.‎
https://doi.org/10.3390/ijms21113876
Resurreccion, A.P., Makino, A., Bennett, J., & Mae, T. (2001). Effects of sulfur nutrition on the growth and photosynthesis of rice. Soil Science and Plant Nutrition, 47(3), 611-620.
https://doi.org/10.1080/00380768.2001.10408424
Ritchie, S. W., Nguyen, H. T., & Holaday, A. S. (1990). Leaf water content and gas‐exchange parameters of two wheat genotypes differing in drought resistance. Crop Science, 30, 105-111.
https://doi.org/10.2135/cropsci1990.0011183X003000010025x
Rotruck, J. T., Pope, A. L., Ganther, H. E., Swanson, A. B., Hafeman, D. G., & Hoekstra, W. G. (1973). Selenium: Biochemical role as a component of glutathione peroxidase. Science, 179, 588-590.
https://doi.org/10.1126/science.179.4073.588
Salvagiotti, F., Castellarín, J. M., Miralles, D. J., & Pedrol, H. M. (2009). Sulfur fertilization improves nitrogen use efficiency in wheat by increasing nitrogen uptake. Field Crops Research.113, 170-177.
https://doi.org/10.1016/j.fcr.2009.05.003
Samanta, S., Singh, A., & ‎Roychoudhury A. (2020). Involvement of sulfur in the regulation of abiotic stress tolerance in plants. In Roychoudhury, A., and ‎Tripathi D. K. (Eds), Protective chemical agents in the amelioration of plant abiotic stress: Biochemical and Molecular Perspectives.(pp 437-466). John Wiley and Sons Ltd.
Scherer, H. W. (2001). Sulphur in crop production. European Journal of Agronomy, 14, 81-111.
https://doi.org/10.1016/S1161-0301(00)00082-4
Schonfeld, M. A., Johnson, R. C., Carver, B. F., & Mornhinweg, D. W. (1988). Water relations in winter wheat as drought resistance indicators. Crop Science, 28, 526-531.
https://doi.org/10.2135/cropsci1988.0011183X002800030021x
Shafiq, B. A., Nawaz, F., Majeed, S., Aurangzaib, M., Al Mamun, A., Ahsan, M., Ahmad, K. S., ‎Shehzad, M. A., Ali, M., Hashim, S., & ‎Haq, T. U. (2021).‎ Sulfate-based fertilizers regulate nutrient uptake, photosynthetic gas exchange, and enzymatic antioxidants to increase sunflower growth ‎and yield under drought stress. Journal of Plant Nutrition and Soil Science, 21, 2229-2241. https://doi.org/10.1007/s42729-021-00516-x
Shah, S. H., Parrey, Z. A., Islam, S., Tyagi, A., Ahmad, A., & Mohammad, F. (2022). Exogenously applied sulphur improves growth, photosynthetic efficiency, enzymatic activities, mineral nutrient contents, yield and quality of Brassica juncea L. Sustainability, 14(21), 14441. 
https://doi.org/10.3390/su142114441
Szabados, L., Kovács, H., Zilberstein, A., & Bouchereau, A. (2011). Plants in extreme environments: Importance of protective compounds in tress tolerance. In Turkan, I. (Ed.), Advances in Botanical Research, 57, (‎pp: 105-150). Academic Press
https://doi.org/10.1016/B978-0-12-387692-8.00004-7
Ullah, A., Al-Busaidi, W. M., Al-Sadi, A. M., & Farooq, M. (2022). Bread wheat genotypes accumulating free proline and phenolics can better tolerate drought stress through sustained rate of photosynthesis. Journal of Soil Science and Plant Nutrition, 22, 165-176.
https://doi.org/10.1007/s42729-021-00641-7
Usmani M. M., Nawaz F., Majeed, S., Shehzad, M. A., Ahmad, K.  S., Akhtar, G., Aqib, M., Shabbir, R. N. (2020). Sulfate-‎mediated drought tolerance in maize involves regulation at physiological and biochemical levels. Seintefic ‎Report, 10, 1147.
https://doi.org/10.1038/s41598-020-58169-2
Vendruscolo, E. C. G., Schuster, I., Pileggi, M., Scapim, C. A., Molinari, H. B. C., Marur, C. J., & Vieira, L. G. E. (2007). Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. Journal of Plant Physiology, 164, 1367-1376.
https://doi.org/10.1016/j.jplph.2007.05.001
Vuković, R., Čamagajevac, I. Š., Vuković, A., Šunić, K., Begović, L., Mlinarić, S., Sekulić, R., Sabo, N., & Španić, V. (2022). Physiological, biochemical and molecular response of different winter wheat varieties under drought stress at germination and seedling growth stage. Antioxidants (Basel), 11(4), 693.
https://doi.org/10.3390/antiox11040693
Zhai, C. Z., Zhao, L., Yin, L. J., Chen, M., Wang, Q. Y., Li, L. C., Xu, Z. S., & Ma, Y. Z. (2013). Two wheat glutathione peroxidase genes whose products are located in chloroplasts improve salt and H2O2 tolerances in Arabidopsis. PLoS One, 8, e73989. https://doi.org/10.1371/journal.pone.0073989
Zarea, M.  J., & Karimi, N. (2023). Zinc-regulated P5CS and sucrose transporters SUT1B expression to enhance drought stress tolerance in wheat. Journal of Plant Growth Regulation, 42, 5831-5841. https://doi.org/10.1007/s00344-023-10968-3
Zhao, F. J., Hawkesford, M. J., & McGrath, S. P. (1999) Sulphur assimilation and effects on yield and quality of wheat. Journal of Cereal Science, 30, 1-17.
https://doi.org/10.1006/jcrs.1998.0241
Iran Agricultural Research
Volume 42, Issue 1
June 2023
Pages 83-98

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