Physiological, Morphological and Biochemical Responses of Exogenous Hydrogen Sulfide in Salt-Stressed Tomato Seedlings
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials and Experimental Set-Up
2.2. H2S Treatment
2.3. Salinity Treatment
2.4. Analysis and Measurements
2.4.1. Plant Growth Parameters
2.4.2. Chlorophyll Content
2.4.3. Leaf Relative Water Content (LRWC), Electrolyte Leakage (EL) and Photosynthetic Properties
2.4.4. Hydrogen Peroxide (H2O2), Malondialdehyde (MDA), Sucrose and Proline Content
2.4.5. Catalase (CAT), Peroxidase (POD) and Superoxide Dismutase (SOD) Enzyme Activities
2.4.6. Hormone Content
2.4.7. Mineral Element Content
2.4.8. Statistical Analysis
3. Results
3.1. Plant Growth Parameters
3.2. LRWC, EL and Chlorophyll Content
3.3. Photyosynthetic Activity
3.4. H2O2, MDA, Sucrose and Proline Content
3.5. CAT, SOD and POD Enzyme Activity
3.6. Hormones and Mineral Contents
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Zhu, J.K. Plant salt tolerance. Trends Plant Sci. 2001, 6, 66–71. [Google Scholar] [CrossRef] [PubMed]
- Tuteja, N. Mechanisms of high salinity tolerance in plants. Meth. Enzymol. 2007, 428, 419–438. [Google Scholar] [CrossRef]
- Negrao, S.; Schmöckel, S.M.; Tester, M. Evaluating physiological responses of plants to salinity stress. Ann. Bot. 2017, 119, 1–11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Munns, R.; Termaat, A. Whole-plant responses to salinity. Aust. J. Plant Physiol. 1986, 13, 143–160. [Google Scholar] [CrossRef]
- Zhu, J.K. Plant Salt Stress; John Wiley & Sons, Ltd: Hoboken, NJ, USA, 2007; Available online: www.els.net (accessed on 3 January 2023).
- Munns, R.; Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 2008, 59, 651–681. [Google Scholar] [CrossRef] [Green Version]
- Parida, A.K.; Das, A.B. Salt tolerance and salinity effect on plants: A review. Ecotox. Environ. Safe. 2005, 60, 324–349. [Google Scholar] [CrossRef]
- Yildirim, E.; Turan, M.; Guvenc, I. Effect of foliar salicylic acid applications on growth, chlorophyll, and mineral content of cucumber grown under salt stress. J. Plant Nutr. 2008, 31, 593–612. [Google Scholar] [CrossRef]
- Kalaji, H.M.; Govindjee, B.K.; Koscielniakd, J.; Zük-Gołaszewska, K. Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ. Exp. Bot. 2011, 73, 64–72. [Google Scholar] [CrossRef]
- Khodarahmpour, Z.; Ifar, M.; Motamedi, M. Effects of NaCl salinity on maize (Zea mays L.) at germination and early seedling stage. Afr. J. Biotechnol. 2012, 11, 298–304. [Google Scholar] [CrossRef] [Green Version]
- Al-Zubaidi, A.H.A. Effects of salinity stress on growth and yield of two varieties of eggplant under greenhouse condition. Res. Crops 2018, 19, 436–440. [Google Scholar] [CrossRef]
- Ors, S.; Ekinci, M.; Yildirim, E.; Sahin, U.; Turan, M.; Dursun, A. Interactive effects of salinity and drought stress on photosynthetic characteristics and physiology of tomato (Lycopersicon esculentum L.) seedlings. S. Afr. J. Bot. 2021, 137, 335–339. [Google Scholar] [CrossRef]
- Shahzad, B.; Rehman, A.; Tanveer, M.; Wang, L.; Park, S.K.; Ali, A. Salt stress in brassica: Effects, tolerance mechanisms, and management. J. Plant Growth Regul. 2022, 41, 781–795. [Google Scholar] [CrossRef]
- Yildirim, E.; Ekinci, M.; Turan, M.; Dursun, A.; Kul, R.; Parlakova, F. Roles of glycine betaine in mitigating deleterious effect of salt stress on lettuce (Lactuca sativa L.). Arch. Agron. Soil Sci. 2015, 61, 1673–1689. [Google Scholar] [CrossRef]
- Shams, M.; Ekinci, M.; Ors, S.; Turan, M.; Agar, G.; Kul, R.; Yildirim, E. Nitric oxide mitigates salt stress effects of pepper seedlings by altering nutrient uptake, enzyme activity and osmolyte accumulation. Physiol. Mol. Biol. Plants 2019, 25, 1149–1161. [Google Scholar] [CrossRef] [PubMed]
- Ekinci, M.; Kocaman, A.; Argin, S.; Turan, M.; Dadasoglu, F.; Yildirim, E. Rhizobacteria alleviate the adverse effects of salt stress on seedling growth of Capsicum annuum L. by modulating the antioxidant enzyme activity and mineral uptake. Taiwania 2021, 66, 287–297. [Google Scholar] [CrossRef]
- Turan, M.; Ekinci, M.; Kul, R.; Boynueyri, F.G.; Yildirim, E. Mitigation of salinity stress in cucumber seedlings by exogenous hydrogen sulfide. J. Plant Res. 2022, 135, 517–529. [Google Scholar] [CrossRef]
- Jiang, J.L.; Tian, Y.; Li, L.; Yu, M.; Hou, R.P.; Ren, X.M. H2S alleviates salinity stress in cucumber by maintaining the Na+/K+ balance and regulating H2S metabolism and oxidative stress response. Front. Plant Sci. 2019, 10, 678. [Google Scholar] [CrossRef] [Green Version]
- Dawood, M.F.; Sohag, A.A.M.; Tahjib-Ul-Arif, M.; Latef, A.A.H.A. Hydrogen sulfide priming can enhance the tolerance of artichoke seedlings to individual and combined saline-alkaline and aniline stresses. Plant Physiol. Biochem. 2021, 159, 347–362. [Google Scholar] [CrossRef]
- Yu, L.X.; Zhang, C.J.; Shang, H.Q.; Wang, X.F.; Min, W.E.I.; Yang, F.J.; Shi, Q.H. Exogenous hydrogen sulfide enhanced antioxidant capacity, amylase activities and salt tolerance of cucumber hypocotyls and radicles. J. Integr. Agric. 2013, 12, 445–456. [Google Scholar] [CrossRef]
- Raju, A.D.; Prasad, S.M. Hydrogen sulfide implications on easing NaCl induced toxicity in eggplant and tomato seedlings. Plant Physiol. Biochem. 2021, 164, 173–184. [Google Scholar] [CrossRef]
- Ding, H.; Han, Q.; Ma, D.; Hou, J.; Huang, X.; Wang, C.; Xie, Y.; Kang, G.; Guo, T. Characterizing physiological and proteomic analysis of the action of H2S to mitigate drought stress in young seedling of wheat. Plant Mol. Biol. Rep. 2018, 36, 45–57. [Google Scholar] [CrossRef]
- Ding, H.; Ma, D.; Huang, X.; Hou, J.; Wang, C.; Xie, Y.; Wang, Y.; Qin, H.; Guo, T. Exogenous hydrogen sulfide alleviates salt stress by improving antioxidant defenses and the salt overly sensitive pathway in wheat seedlings. Acta Physiol. Plant. 2019, 41, 123. [Google Scholar] [CrossRef]
- Zhang, H.; Tang, J.; Liu, X.P.; Wang, Y.; Yu, W.; Peng, W.Y.; Fang, F.; Ma, D.F.; Wei, Z.J.; Hu, L.Y. Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine Max. J. Integr. Plant Biol. 2009, 51, 1086–1094. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Wang, M.J.; Hu, L.Y.; Wang, S.H.; Hu, K.D.; Bao, L.J.; Luo, J.P. Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russ. J. Plant Physiol. 2010, 57, 532–539. [Google Scholar] [CrossRef]
- Chen, J.; Wu, F.; Wang, W.; Zheng, C.; Lin, G.; Dong, X.; He, J.; Pei, Z.; Zheng, H. Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiolredox modification in Spinacia oleracea seedlings. J. Exp. Bot. 2011, 62, 4481–4493. [Google Scholar] [CrossRef] [Green Version]
- Lisjak, M.; Teklic, T.; Wilson, I.D.; Wood, M.E.; Whiteman, M.; Hancock, J.T. Hydrogen sulfide effects on stomatal apertures. Plant Signal. Behav. 2011, 6, 1444–1446. [Google Scholar] [CrossRef] [Green Version]
- Shen, Y.; Wang, W.; Zhang, W.; Zhu, L.; Li, B. Hydrogen sulfide facilitating enhancement of antioxidant ability and maintainance of fruit quality of kiwifruits during low-temperatures storage. Trans CSAE 2015, 31, 367–372. [Google Scholar]
- Christou, A.; Filippou, P.; Manganaris, G.; Fotopoulos, V. Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol. 2014, 14, 42. [Google Scholar] [CrossRef] [Green Version]
- Duan, B.; Ma, Y.; Jiang, M.; Yang, F.; Ni, L.; Lu, W. Improvement of photosynthesis in rice (Oryza sativa L.) as a result of an increase in stomatal aperture and density by exogenous hydrogen sulfide treatment. Plant Growth Regul. 2015, 75, 33–44. [Google Scholar] [CrossRef]
- Li, Z.G.; Ding, X.J.; Du, P.F. Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J. Plant Physiol. 2013, 170, 741–747. [Google Scholar] [CrossRef]
- Hu, K.D.; Bai, G.S.; Li, W.J.; Yan, H.; Hu, L.Y.; Li, Y.H.; Zhang, H. Sulfur dioxide promotes germination and plays an antioxidant role in cadmium-stressed wheat seeds. Plant Growth Regul. 2015, 75, 271–280. [Google Scholar] [CrossRef]
- Ekinci, M.; Yildirim, E.; Turan, M. Ameliorating effects of hydrogen sulfide on growth, physiological and biochemical characteristics of eggplant seedlings under salt stress. S. Afr. J. Bot. 2021, 143, 79–89. [Google Scholar] [CrossRef]
- Ayers, R.S.; Westcott, D.W. Water quality evaluation. In Managing Saline Water for İrrigation; Springer: Berlin/Heidelberg, Germany, 1976; pp. 400–431. [Google Scholar]
- Scholberg, J.M.S.; Locascio, S.J. Growth response of snap bean and tomato as affected by salinity and irrigation method. HortScience 1999, 34, 259–264. [Google Scholar] [CrossRef] [Green Version]
- Cuartero, J.; Fernández-Muňoz, R. Tomato and salinity. Sci. Hortic. 1999, 78, 83–125. [Google Scholar] [CrossRef]
- Loudari, A.; Benadis, C.; Naciri, R.; Soulaimani, A.; Zeroual, Y.; Gharous, M.E.; Kalji, H.M.; Oukarroum, A. Salt stress affects mineral nutrition in shoots and roots and chlorophyll a fluorescence of tomato plants grown in hydroponic culture. J. Plant Interact. 2020, 15, 398–405. [Google Scholar] [CrossRef]
- Macedo, W.R.; Araújo, D.K.; e Castro, P.R.D.C. Unravelling the physiologic and metabolic action of thiamethoxam on rice plants. Pestic. Biochem. Phys. 2013, 107, 244–249. [Google Scholar] [CrossRef]
- Witham, F.H.; Blaydes, D.F. Exercises in Plant Physiology Paperback; Prindle Weber & Schmidt: Belmont, CA, USA, 1971. [Google Scholar]
- Ors, S.; Ekinci, M.; Yildirim, E.; Sahin, U. Changes in gas exchange capacity and selected physiological properties of squash seedlings (Cucurbita pepo L.) under well-watered and drought stress conditions. Arch. Agron. Soil Sci. 2016, 62, 1700–1710. [Google Scholar] [CrossRef]
- Liu, S.; Dong, Y.; Xu, L.; Kong, J. Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings. Plant Growth Regul. 2014, 73, 67–78. [Google Scholar] [CrossRef]
- Cakmak, I.; Horst, W.J. Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol. Plant. 1991, 83, 463–468. [Google Scholar] [CrossRef]
- Velikova, V.; Yordanov, I.; Edreva, A. Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Sci. 2000, 151, 59–66. [Google Scholar] [CrossRef]
- Wu, X.; Zhu, W.; Zhang, H.; Ding, H.; Zhang, H.J. Exogenous nitric oxide protects against salt-induced oxidative stress in the leaves from two genotypes of tomato (Lycopersicom esculentum Mill.). Acta Physiol. Plant. 2011, 33, 1199–1209. [Google Scholar] [CrossRef]
- Bates, L.S.; Waldren, R.P.; Teare, I.D. Rapid determination of free proline for waterstress studies. Plant Soil 1973, 39, 205–207. [Google Scholar] [CrossRef]
- Angelini, R.; Manes, F.; Federico, R. Spatial an functional correlation between daimine- oxsidase and peroxidase activities and their dependence upon deetilation and wounding in chick-pea. Planta 1990, 182, 89–96. [Google Scholar] [CrossRef] [PubMed]
- Angelini, R.; Federico, R. Histochemical evidence of polyamine oxidation and generation of hydrogen- peroxide in the cell wall. J. Plant Physiol. 1989, 135, 212–217. [Google Scholar] [CrossRef]
- Battal, P.; Tileklioglu, B. The effects of different mineral nutrients on the levels of cytokinins in maize (Zea mays L.). Turk. J. Bot. 2001, 25, 123–130. [Google Scholar]
- Kuraishi, S.; Tasaki, K.; Sakurai, N.; Sadatoku, K. Changes in levels of cytokinins in etiolated squash seedlings after illumination. Plant Cell Physiol. 1991, 32, 585–591. [Google Scholar] [CrossRef]
- Turan, M.; Ekinci, M.; Yıldırım, E.; Güneş, A.; Karagöz, K.; Kotan, R.; Dursun, A. Plant growth-promoting rhizobacteria improved growth, nutrient, and hormone content of cabbage (Brassica oleracea) seedlings. Turk. J. Agric. For. 2014, 38, 327–333. [Google Scholar] [CrossRef]
- Mertens, D. AOAC Official Method 922.02. Plants preparation of laboratuary sample. In Official Methods of Analysis, 18th ed.; Horwitz, W., Latimer, G.W., Eds.; AOAC-International Suite: Gaitherburg, MD, USA, 2005; pp. 1–2, Chapter 3. [Google Scholar]
- Mertens, D. AOAC Official Method 975.03. Metal in plants and pet foods. In Official Methods of Analysis, 18th ed.; Horwitz, W., Latimer, G.W., Eds.; AOACInternational Suite: Gaitherburg, MD, USA, 2005; pp. 3–4, Chapter 3. [Google Scholar]
- SPSS Inc. SPSS® 18.0 Base User’s Guide; Prentice Hall: Chicago, IL, USA, 2010. [Google Scholar]
- Qados, A.M.A. Effect of salt stress on plant growth and metabolism of bean plant Vicia faba (L.). J. Saudi Soc. Agric. Sci. 2011, 10, 7–15. [Google Scholar] [CrossRef] [Green Version]
- Deng, Y.Q.; Bao, J.; Yuan, F.; Liang, X.; Feng, Z.T.; Wang, B.S. Exogenous hydrogen sulfide alleviates salt stress in wheat seedlings by decreasing Na content. Plant Growth Regul. 2016, 79, 391–399. [Google Scholar] [CrossRef]
- Liu, H.; Wang, J.; Liu, J.; Liu, T.; Xue, S. Hydrogen sulfide (H2S) signaling in plant development and stress responses. Abiotech 2021, 2, 32–63. [Google Scholar] [CrossRef]
- Tanveer, K.; Gilani, S.; Hussain, Z.; Ishaq, R.; Adeel, M.; Ilyas, N. Effect of salt stress on tomato plant and the role of calcium. J. Plant Nutr. 2020, 43, 28–35. [Google Scholar] [CrossRef]
- Acosta-Motos, J.R.; Ortuño, M.F.; Bernal-Vicente, A.; Diaz-Vivancos, P.; Sanchez-Blanco, M.J.; Hernandez, J.A. Plant responses to salt stress: Adaptive mechanisms. Agron 2017, 7, 18. [Google Scholar] [CrossRef]
- Ahmed, I.M.; Dai, H.; Zheng, W.; Cao, F.; Zhang, G.; Sun, D.; Wu, F. Genotypic differences in physiological characteristics in the tolerance to drought and salinity combined stress between Tibetan wild and cultivated barley. Plant Physiol. Biochem. 2013, 63, 49–60. [Google Scholar] [CrossRef] [PubMed]
- Mostofa, M.G.; Saegusa, D.; Fujita, M.; Tran, L.S.P. Hydrogen sulfide regulates salt tolerance in rice by maintaining Na/K balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Front. Plant Sci. 2015, 6, 1055. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shan, C.; Liu, H.; Zhao, L.; Wang, X. Effects of exogenous hydrogen sulfide on the redox states of ascorbate and glutathione in maize leaves under salt stress. Biol. Plant. 2014, 58, 169–173. [Google Scholar] [CrossRef]
- Shin, Y.K.; Bhandari, S.R.; Cho, M.C.; Lee, J.G. Evaluation of chlorophyll fluorescence parameters and proline content in tomato seedlings grown under different salt stress conditions. Hortic. Environ. Biotechnol. 2020, 61, 433–443. [Google Scholar] [CrossRef]
- Sarwar, M.; Anjum, S.; Ali, Q.; Alam, M.W.; Haider, M.S.; Mehboob, W. Triacontanol modulates salt stress tolerance in cucumber by altering the physiological and biochemical status of plant cells. Sci. Rep. 2021, 11, 24504. [Google Scholar] [CrossRef]
- Wei, M.Y.; Liu, J.Y.; Li, H.; Hu, W.J.; Shen, Z.J.; Qiao, F.; Zhu, C.Q.; Chen, J.; Liu, X.; Zheng, H.L. Proteomic analysis reveals the protective role of exogenous hydrogen sulfide against salt stress in rice seedlings. Nitric Oxide 2021, 111, 14–30. [Google Scholar] [CrossRef]
- Sun, Y.; Ma, C.; Kang, X.; Zhang, L.; Wang, J.; Zheng, S.; Zhang, T. Hydrogen sulfide and nitric oxide are involved in melatonin-induced salt tolerance in cucumber. Plant Physiol. Biochem. 2021, 167, 101–112. [Google Scholar] [CrossRef]
- Li, Y. Physiological responses of tomato seedlings (Lycopersicon esculentum) to salt stress. Mod. Appl. Sci. 2009, 3, 171–176. [Google Scholar] [CrossRef] [Green Version]
- Shahba, Z.; Baghizadeh, A.; Vakili, S.M.A.; Yazdanpanah, A.; Yosefi, M. The salicylic acid effect on the tomato (Lycopersicum esculentum Mill.) sugar, protein and proline contents under salinity stress (NaCl). J. Biophys. Struct. Biol. 2010, 2, 35–41. [Google Scholar]
- Wei, G.Q.; Zhang, W.W.; Cao, H.; Yue, S.S.; Li, P.; Yang, H.Q. Effects hydrogen sulfide on the antioxidant system and membrane stability in mitochondria of Malus hupehensis under NaCl stress. Biol. Plant. 2019, 63, 228–236. [Google Scholar] [CrossRef]
- Kusvuran, S.; Kiran, S.; Ellialtioglu, S.S. Antioxidant enzyme activities and abiotic stress tolerance relationship in vegetable crops. In Abiotic and Biotic Stress in Plants, Recent Advances and Future Perspectives; IntechOpen: London, UK, 2016; pp. 481–506. [Google Scholar] [CrossRef]
- Sun, Y.D.; Luo, W.R. Effects of exogenous hydrogen sulphide on seed germination and seedling growth of cucumber (Cucumis sativus) under sodium bicarbonate stress. Seed Sci. Technol. 2014, 42, 126–131. [Google Scholar] [CrossRef]
- Raza, A.; Tabassum, J.; Mubarik, M.S.; Anwar, S.; Zahra, N.; Sharif, Y.; Hafeez, M.B.; Zhang, C.; Corpas, F.J.; Chen, H. Hydrogen sulfide: An emerging component against abiotic stress in plants. Plant Biol. 2021, 24, 540–558. [Google Scholar] [CrossRef]
- Fahad, S.; Hussain, S.; Matloob, A.; Khan, F.A.; Khaliq, A.; Saud, S.; Hassan, S.; Shan, D.; Khan, F.; Ullah, N.; et al. Phytohormones and plant responses to salinity stress: A review. Plant Growth Regul. 2015, 75, 391–404. [Google Scholar] [CrossRef]
- Huang, D.; Huo, J.; Liao, W. Hydrogen sulfide: Roles in plant abiotic stress response and crosstalk with other signals. Plant Sci. 2021, 302, 110733. [Google Scholar] [CrossRef]
- Liu, H.; Xue, S. Interplay between hydrogen sulfide and other signaling molecules in the regulation of guard cell signaling and abiotic/biotic stress response. Plant Commun. 2021, 2, 100179. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Zhou, H.; Zhou, M.; Ge, Z.; Zhang, F.; Foyer, C.H.; Yuan, X.; Xie, Y. The coordination of guard-cell autonomous ABA synthesis and DES1 function in situ regulates plant water deficit responses. J. Adv. Res. 2021, 27, 191–197. [Google Scholar] [CrossRef] [PubMed]
- Li, Z.G.; Xiang, R.H.; Wang, J.Q. Hydrogen sulfide–phytohormone interaction in plants under physiological and stress conditions. J. Plant Growth Regul. 2021, 40, 2476–2484. [Google Scholar] [CrossRef]
- Mei, Y.; Chen, H.; Shen, W.; Huang, L. Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings. BMC Plant Biol. 2017, 17, 162. [Google Scholar] [CrossRef]
- Fang, T.; Cao, Z.; Li, J.; Shen, W.; Huang, L. Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato. Plant Physiol. Biochem. 2014, 76, 44–51. [Google Scholar] [CrossRef] [PubMed]
- Khan, M.N.; Siddiqui, M.H.; Mukherjee, S.; Alamri, S.; Al-Amri, A.A.; Alsubaie, Q.D.; Al-Munqedhi, B.M.; Ali, H.M. Calcium-hydrogen sulfide crosstalk during K deficient NaCl stress operates through regulation of Na/H antiport and antioxidative defense system in mung bean roots. Plant Physiol. Biochem. 2021, 159, 211–225. [Google Scholar] [CrossRef] [PubMed]
- Srivastava, V.; Chowdhary, A.A.; Verma, P.K.; Mehrotra, S.; Mishra, S. Hydrogen sulfide-mediated mitigation and its integrated signaling crosstalk during salinity stress. Physiol. Plant. 2022, 174, e13633. [Google Scholar] [CrossRef] [PubMed]
Salt | Treatment | Plant Height | Stem Diameter | Leaf Number | Leaf Area | Chlorophyll Reading Value |
---|---|---|---|---|---|---|
cm | Mm | Number plant−1 | cm2 plant−1 | SPAD | ||
SI | T1 | 22.17 b | 7.27 ab | 9.67 a | 784.91 a | 52.80 ab |
TII | 23.33 a | 7.09 ab | 9.00 b | 803.20 a | 52.40 ab | |
TIII | 23.17 ab | 7.06 b | 9.00 b | 783.10 a | 52.07 ab | |
TIV | 23.67 ab | 7.31 ab | 9.17 b | 777.96 a | 52.30 ab | |
TV | 22.67 ab | 7.32 a | 8.83 b | 776.02 a | 53.77 a | |
SII | T1 | 14.83 ef | 5.24 de | 6.83 e | 257.90 cde | 40.80 f |
TII | 17.00 c | 5.81 c | 7.50 cd | 464.85 b | 49.00 c | |
TIII | 16.58 cd | 5.80 c | 7.67 c | 324.60 c | 49.50 c | |
TIV | 16.33 cd | 5.90 c | 7.83 c | 325.05 bc | 48.90 c | |
TV | 15.67 de | 5.38 d | 7.17 de | 303.04 cd | 50.97 bc | |
SIII | T1 | 13.33 h | 4.56 g | 6.33 f | 200.90 e | 41.90 f |
TII | 14.33 fgh | 5.23 de | 7.00 e | 244.42 de | 45.07 de | |
TIII | 14.58 fg | 4.93 f | 6.83 f | 302.49 cd | 45.77 de | |
TIV | 15.00 ef | 5.05 ef | 6.17 f | 198.97 e | 42.83 ef | |
TV | 13.67 gh | 5.04 ef | 7.02 e | 253.46 cde | 45.33 de |
Salt | Treatment | Plant Fresh Weight | Root Fresh Weight | Plant Dry Weight | Root Dry Weight |
---|---|---|---|---|---|
g plant−1 | |||||
SI | T1 | 29.80 c | 9.25 c | 3.75 d | 0.57 b |
TII | 35.23 a | 10.98 b | 4.67 a | 0.62 b | |
TIII | 32.96 ab | 11.52 a | 4.11 b | 0.61 b | |
TIV | 31.02 bc | 11.43 a | 3.93 c | 0.75 a | |
TV | 30.93 bc | 10.91 b | 3.92 c | 0.70 a | |
SII | T1 | 10.87 de | 2.29 e | 1.31 f | 0.20 cd |
TII | 13.40 d | 3.23 d | 1.67 e | 0.24 c | |
TIII | 12.81 d | 3.45 d | 1.62 e | 0.24 c | |
TIV | 8.99 ef | 3.27 d | 1.63 e | 0.25 c | |
TV | 13.62 d | 3.47 d | 1.59 e | 0.25 c | |
SIII | T1 | 6.04 f | 1.61 f | 0.84 h | 0.16 d |
TII | 7.81 f | 2.15 e | 1.06 g | 0.18 d | |
TIII | 8.32 ef | 2.28 e | 1.05 g | 0.17 d | |
TIV | 7.65 f | 2.07 e | 1.00 g | 0.17 d | |
TV | 8.65 ef | 2.30 e | 1.14 g | 0.18 d |
Salt | Treatment | IAA | ABA | GA | SA | Cytokinin | Zeatin | Jasmonic Acid |
---|---|---|---|---|---|---|---|---|
ng mg tissue−1 | ng g DW−1 | |||||||
SI | T1 | 2.35 c | 214.28 h | 1.44 fg | 8.38 fgh | 15.95 ef | 4.17 g | 13.01 ij |
TII | 2.81 b | 185.49 hi | 2.06 de | 12.36 de | 16.32 ef | 5.49 f | 30.21 f | |
TIII | 2.87 b | 145.40 i | 3.02 c | 20.26 c | 31.59 c | 8.16 cd | 36.54 de | |
TIV | 3.38 a | 129.74 i | 3.90 b | 23.95 b | 38.71 b | 13.51 b | 67.36 b | |
TV | 3.41 a | 128.97 i | 4.40 a | 31.60 a | 44.09 a | 22.12 a | 75.52 a | |
SII | T1 | 0.66 h | 1033.01 b | 1.15 gh | 5.67 hi | 12.29 h | 2.28 i | 9.74 jk |
TII | 0.85 gh | 426.44 e | 1.63 ef | 7.07 gh | 8.84 i | 4.14 g | 18.95 h | |
TIII | 1.29 f | 290.57 fg | 2.14 d | 9.16 fg | 15.50 f | 6.24 ef | 27.82 f | |
TIV | 1.43 f | 234.50 gh | 1.94 de | 10.67 ef | 16.98 e | 6.67 e | 40.09 d | |
TV | 2.01 d | 235.19 gh | 2.80 c | 13.37 de | 19.02 d | 8.75 c | 49.71 c | |
SIII | T1 | 0.30 i | 1475.72 a | 0.33 i | 3.02 i | 7.14 j | 1.41 i | 7.21 k |
TII | 0.78 gh | 857.85 c | 4.42 a | 3.86 i | 8.30 ij | 2.52 hi | 12.20 j | |
TIII | 0.93 g | 637.27 d | 0.86 h | 7.36 gh | 9.41 i | 3.61 gh | 16.36 hi | |
TIV | 1.75 e | 329.70 f | 1.18 fgh | 9.35 fg | 12.30 h | 4.19 g | 23.70 g | |
TV | 2.18 cd | 345.60 f | 1.32 fgh | 14.83 d | 13.97 g | 7.16 de | 35.01 e |
Salt | Treatment | N | P | K | Ca | Mg | S | Na | Zn | Fe | Mn | Cu | B | Cl |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
% | mg kg−1 | |||||||||||||
SI | T1 | 3.04 d | 0.36 a | 2.62 e | 2.15 d | 0.32 f | 0.25 ab | 178.78 gh | 46.88 e | 35.10 f | 28.19 d | 16.23 e | 18.19 d | 3.56 h |
TII | 3.72 a | 0.35 b | 2.77 d | 2.31 c | 0.34 e | 0.25 ab | 183.01 g | 56.56 d | 33.23 g | 22.79 e | 18.39 d | 17.33 e | 3.38 h | |
TIII | 3.42 c | 0.36 a | 2.88 c | 2.49 b | 0.43 c | 0.24 b | 164.50 i | 76.06 c | 48.57 d | 30.60 c | 25.83 b | 19.52 c | 2.67 h | |
TIV | 3.52 bc | 0.34 c | 3.06 b | 2.64 a | 0.52 a | 0.25 ab | 170.29 hi | 93.72 b | 70.47 b | 34.34 b | 24.44 c | 20.76 b | 2.00 h | |
TV | 3.57 b | 0.37 a | 3.25 a | 2.49 b | 0.51 a | 0.26 a | 179.74 gh | 96.47 a | 80.40 a | 44.26 a | 28.42 a | 23.92 a | 1.89 h | |
SII | T1 | 1.40 i | 0.10 g | 1.41 k | 0.97 j | 0.14 i | 0.13 e | 275.89 b | 5.58 n | 16.89 j | 6.43 k | 2.41 kl | 6.84 l | 196.05 c |
TII | 2.25 e | 0.33 c | 2.55 f | 1.42 g | 0.25 g | 0.14 e | 182.12 g | 9.48 l | 23.12 i | 7.60 j | 3.02 k | 7.73 j | 183.15 d | |
TIII | 1.83 fg | 0.24 f | 1.88 i | 1.73 e | 0.32 f | 0.15 d | 199.24 ef | 17.39 j | 33.69 g | 15.57 h | 7.07 i | 10.27 g | 172.20 f | |
TIV | 1.95 f | 0.26 e | 1.96 h | 1.69 e | 0.45 b | 0.17 c | 207.73 e | 25.24 h | 32.71 g | 16.70 g | 11.53 g | 9.25 h | 166.65 e | |
TV | 1.84 fg. | 0.27 e | 2.05 g | 1.54 f | 0.51 a | 0.13 e | 161.04 i | 39.83 f | 50.62 c | 23.36 e | 15.50 e | 11.18 f | 132.25 f | |
SIII | T1 | 1.22 j | 0.10 g | 1.00 m | 0.72 k | 0.10 j | 0.09 g | 379.08 a | 4.62 n | 12.73 k | 6.08 k | 1.99 l | 5.74 m | 325.05 a |
TII | 1.97 f | 0.26 e | 1.81 j | 1.12 i | 0.20 h | 0.09 g | 229.74 cd | 7.85 m | 17.43 j | 7.17 j | 2.83 kl | 6.49 l | 208.95 b | |
TIII | 1.61 h | 0.26 e | 1.34 l | 1.28 h | 0.24 g | 0.10 g | 220.93 d | 14.40 k | 25.39 h | 14.72 i | 5.84 j | 8.61 i | 181.65 d | |
TIV | 1.77 g | 0.29 d | 1.40 kl | 1.25 h | 0.34 e | 0.12 f | 231.67 c | 20.90 i | 24.65 h | 15.79 h | 9.53 h | 7.76 j | 168.45 f | |
TV | 1.70 gh | 0.30 d | 1.46 k | 1.60 f | 0.38 d | 0.13 e | 196.82 f | 32.98 g | 38.15 e | 22.09 f | 12.81 f | 9.38 h | 121.77 g |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yildirim, E.; Ekinci, M.; Turan, M.; Ors, S.; Dursun, A. Physiological, Morphological and Biochemical Responses of Exogenous Hydrogen Sulfide in Salt-Stressed Tomato Seedlings. Sustainability 2023, 15, 1098. https://doi.org/10.3390/su15021098
Yildirim E, Ekinci M, Turan M, Ors S, Dursun A. Physiological, Morphological and Biochemical Responses of Exogenous Hydrogen Sulfide in Salt-Stressed Tomato Seedlings. Sustainability. 2023; 15(2):1098. https://doi.org/10.3390/su15021098
Chicago/Turabian StyleYildirim, Ertan, Melek Ekinci, Metin Turan, Selda Ors, and Atilla Dursun. 2023. "Physiological, Morphological and Biochemical Responses of Exogenous Hydrogen Sulfide in Salt-Stressed Tomato Seedlings" Sustainability 15, no. 2: 1098. https://doi.org/10.3390/su15021098