Assessing Heat Tolerance in Creeping Bentgrass Lines Based on Physiological Responses
Abstract
:1. Introduction
2. Results
3. Materials and Methods
3.1. Growth and Treatment Conditions
3.2. Measurements
3.2.1. Physiological Measurements
3.2.2. Biochemical Measurements
3.3. Statistical Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Fry, J.; Huang, B. Applied Turfgrass Science and Physiology; John Wiley & Sons: Hoboken, NJ, USA, 2004. [Google Scholar]
- Turgeon, A.J.N. Turfgrass Management, 5th ed.; Prentice Hall: Upper Saddle River, NJ, USA, 1999; Volume 4, p. 225. [Google Scholar]
- Pachauri, R.K.; Meyer, L. Climate Change 2014 Synthesis Report-Summary for Policymakers; Intergovernmental Panel on Climate Change (IPCC): Geneva, Switzerland, 2014. [Google Scholar]
- Zhou, Y.; Yin, M.; Liu, F. First Report of Summer Patch of Creeping Bentgrass Caused by Magnaporthiopsis poae in Southeastern China. Plant Dis. 2022, 106, 1527. [Google Scholar] [CrossRef]
- O’Brien, P.; Hartwiger, C. A time to change: The ultradwarf bermudagrass putting green golf model is solid in the southern USA. USGA Green Sect. Record. Febr. 2011, 25, 8. [Google Scholar]
- Mansoor, S.; Ali Wani, O.; Lone, J.K.; Manhas, S.; Kour, N.; Alam, P.; Ahmad, A.; Ahmad, P. Reactive Oxygen Species in Plants: From Source to Sink. Antioxidants 2022, 11, 225. [Google Scholar] [CrossRef]
- Huang, B.R.; DaCosta, M.; Jiang, Y.W. Research Advances in Mechanisms of Turfgrass Tolerance to Abiotic Stresses: From Physiology to Molecular Biology. Crit. Rev. Plant Sci. 2014, 33, 141–189. [Google Scholar] [CrossRef]
- Alam, M.N.; Yang, L.; Yi, X.; Wang, Q.; Robin, A.H.K. Role of melatonin in inducing the physiological and biochemical processes associated with heat stress tolerance in tall fescue (Festuca arundinaceous). J. Plant Growth Regul. 2022, 41, 2759–2768. [Google Scholar] [CrossRef]
- Jespersen, D.; Xu, C.P.; Huang, B.R. Membrane Proteins Associated with Heat-Induced Leaf Senescence in a Cool-Season Grass Species. Crop Sci. 2015, 55, 837–850. [Google Scholar] [CrossRef]
- Balfagón, D.; Sengupta, S.; Gómez-Cadenas, A.; Fritschi, F.B.; Azad, R.K.; Mittler, R.; Zandalinas, S.I. Jasmonic acid is required for plant acclimation to a combination of high light and heat stress. Plant Physiol. 2019, 181, 1668–1682. [Google Scholar] [CrossRef] [Green Version]
- Li, H.; Xu, H.; Zhang, P.; Gao, M.; Wang, D.; Zhao, H. High temperature effects on D1 protein turnover in three wheat varieties with different heat susceptibility. Plant Growth Regul. 2017, 81, 1–9. [Google Scholar] [CrossRef]
- Møller, I.M.; Kristensen, B.K. Protein oxidation in plant mitochondria as a stress indicator. Photochem. Photobiol. Sci. 2004, 3, 730–735. [Google Scholar] [CrossRef]
- Du, H.; Wang, Z.; Huang, B. Differential responses of warm-season and cool-season turfgrass species to heat stress associated with antioxidant enzyme activity. J. Am. Soc. Hortic. Sci. 2009, 134, 417–422. [Google Scholar] [CrossRef]
- Li, Z.; Zeng, W.; Cheng, B.; Xu, J.; Han, L.; Peng, Y. Turf Quality and Physiological Responses to Summer Stress in Four Creeping Bentgrass Cultivars in a Subtropical Zone. Plants 2022, 11, 665. [Google Scholar] [CrossRef]
- Jespersen, D.; Meyer, W.; Huang, B. Physiological traits and genetic variations associated with drought and heat tolerance in creeping bentgrass. Int. Turfgrass Soc. Res. J 2013, 12, 459–464. [Google Scholar]
- Liu, X.; Huang, B. Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Sci. 2000, 40, 503–510. [Google Scholar] [CrossRef]
- Zhou, R.; Yu, X.; Kjær, K.H.; Rosenqvist, E.; Ottosen, C.-O.; Wu, Z. Screening and validation of tomato genotypes under heat stress using Fv/Fm to reveal the physiological mechanism of heat tolerance. Environ. Exp. Bot. 2015, 118, 1–11. [Google Scholar] [CrossRef]
- Pirdashti, H.; Sarvestani, Z.T.; Bahmanyar, M.A. Comparison of physiological responses among four contrast rice cultivars under drought stress conditions. World Acad. Sci. Eng. Technol. 2009, 49, 52–53. [Google Scholar]
- Zhang, X.; Gao, Y.; Zhuang, L.; Hu, Q.; Huang, B. Phosphatidic acid and hydrogen peroxide coordinately enhance heat tolerance in tall fescue. Plant Biol. 2021, 23, 142–151. [Google Scholar] [CrossRef]
- Strasser, R.J.; Srivastava, A.; Tsimilli-Michael, M. The fluorescence transient as a tool to characterize and screen photosynthetic samples. Probing Photosynth. Mech. Regul. Adapt. 2000, 1, 445–483. [Google Scholar]
- Küpper, H.; Benedikty, Z.; Morina, F.; Andresen, E.; Mishra, A.; Trtílek, M. Analysis of OJIP chlorophyll fluorescence kinetics and QA reoxidation kinetics by direct fast imaging. Plant Physiol. 2019, 179, 369–381. [Google Scholar] [CrossRef] [Green Version]
- Stirbet, A.; Lazár, D.; Kromdijk, J. Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica 2018, 56, 86–104. [Google Scholar] [CrossRef]
- Zushi, K.; Kajiwara, S.; Matsuzoe, N. Chlorophyll a fluorescence OJIP transient as a tool to characterize and evaluate response to heat and chilling stress in tomato leaf and fruit. Sci. Hortic. 2012, 148, 39–46. [Google Scholar] [CrossRef]
- Snider, J.L.; Thangthong, N.; Pilon, C.; Virk, G.; Tishchenko, V. OJIP-fluorescence parameters as rapid indicators of cotton (Gossypium hirsutum L.) seedling vigor under contrasting growth temperature regimes. Plant Physiol. Biochem. 2018, 132, 249–257. [Google Scholar] [CrossRef] [PubMed]
- Virk, G.; Snider, J.L.; Chee, P.; Jespersen, D.; Pilon, C.; Rains, G.; Roberts, P.; Kaur, N.; Ermanis, A.; Tishchenko, V. Extreme temperatures affect seedling growth and photosynthetic performance of advanced cotton genotypes. Ind. Crops Prod. 2021, 172, 114025. [Google Scholar] [CrossRef]
- Strauss, A.; Krüger, G.; Strasser, R.; Van Heerden, P. Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient OJIP. Environ. Exp. Bot. 2006, 56, 147–157. [Google Scholar] [CrossRef]
- Jespersen, D.; Ma, X.; Bonos, S.A.; Belanger, F.C.; Raymer, P.; Huang, B.J.C.S. Association of SSR and candidate gene markers with genetic variations in summer heat and drought performance for creeping bentgrass. Crop Sci. 2018, 58, 2644–2656. [Google Scholar] [CrossRef]
- Krans, J.V.; Morris, K. Determining a profile of protocols and standards used in the visual field assessment of turfgrasses: A survey of national turfgrass evaluation program-sponsored university scientists. Appl. Turfgrass Sci. 2007, 4, 1–16. [Google Scholar] [CrossRef] [Green Version]
- Karcher, D.E.; Richardson, M.D. Digital image analysis in turfgrass research. Turfgrass Biol. Use Manag. 2013, 56, 1133–1149. [Google Scholar] [CrossRef]
- Wellburn, A.R. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 1994, 144, 307–313. [Google Scholar] [CrossRef]
- Blum, A.; Ebercon, A.J.C.S. Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci. 1981, 21, 43–47. [Google Scholar] [CrossRef]
- Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- Hodges, D.M.; DeLong, J.M.; Forney, C.F.; Prange, R.K. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 1999, 207, 604–611. [Google Scholar] [CrossRef]
- Irigoyen, J.; Einerich, D.; Sánchez-Díaz, M. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiol. Plant. 1992, 84, 55–60. [Google Scholar] [CrossRef]
- Allakhverdiev, S.I.; Kreslavski, V.D.; Klimov, V.V.; Los, D.A.; Carpentier, R.; Mohanty, P. Heat stress: An overview of molecular responses in photosynthesis. Photosynth. Res. 2008, 98, 541–550. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.; Huang, B. Heat-induced leaf senescence and hormonal changes for thermal bentgrass and turf-type bentgrass species differing in heat tolerance. J. Am. Soc. Hortic. Sci. 2007, 132, 185–192. [Google Scholar] [CrossRef] [Green Version]
- Xu, C.P.; Huang, B.R. Comparative Analysis of Proteomic Responses to Single and Simultaneous Drought and Heat Stress for Two Kentucky Bluegrass Cultivars. Crop Sci. 2012, 52, 1246–1260. [Google Scholar] [CrossRef]
- Hu, L.; Bi, A.; Hu, Z.; Amombo, E.; Li, H.; Fu, J. Antioxidant metabolism, photosystem II, and fatty acid composition of two tall fescue genotypes with different heat tolerance under high temperature stress. Front. Plant Sci. 2018, 9, 1242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wahid, A.; Gelani, S.; Ashraf, M.; Foolad, M. Heat tolerance in plants: An overview. Environ. Exp. Bot. 2007, 61, 199–223. [Google Scholar] [CrossRef]
- Jespersen, D.; Zhang, J.; Huang, B.R. Chlorophyll loss associated with heat-induced senescence in bentgrass. Plant Sci. 2016, 249, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Rossi, S.; Burgess, P.; Jespersen, D.; Huang, B.J.C.S. Heat-induced leaf senescence associated with Chlorophyll metabolism in Bentgrass lines differing in heat tolerance. Crop Sci. 2017, 57 (Suppl. S1), S-169–S-178. [Google Scholar] [CrossRef]
- Taiz, L.; Zeiger, E. Plant Physiology, 5th ed.; The Sinauer Associates: Sunderland, MA, USA, 2006. [Google Scholar]
- Zhang, L.; Chang, Q.; Hou, X.; Wang, J.; Chen, S.; Zhang, Q.; Wang, Z.; Yin, Y.; Liu, J. The Effect of high-temperature stress on the physiological indexes, chloroplast ultrastructure, and photosystems of two herbaceous peony cultivars. J. Plant Growth Regul. 2022, 41, 1–16. [Google Scholar] [CrossRef]
- Chen, S.; Yang, J.; Zhang, M.; Strasser, R.J.; Qiang, S. Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise OJIP. Environ. Exp. Bot. 2016, 122, 126–140. [Google Scholar] [CrossRef]
- Chen, L.-S.; Cheng, L. Photosystem 2 is more tolerant to high temperature in apple (Malus domestica Borkh.) leaves than in fruit peel. Photosynthetica 2009, 47, 112–120. [Google Scholar] [CrossRef]
- Sharma, D.K.; Andersen, S.B.; Ottosen, C.O.; Rosenqvist, E. Wheat cultivars selected for high Fv/Fm under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter. Physiol. Plant. 2015, 153, 284–298. [Google Scholar] [CrossRef] [PubMed]
- Huang, B.R.; Liu, X.Z.; Xu, Q.Z. Supraoptimal soil temperatures induced oxidative stress in leaves of creeping bentgrass cultivars differing in heat tolerance. Crop Sci. 2001, 41, 430–435. [Google Scholar] [CrossRef]
- Li, F.F.; Zhan, D.; Xu, L.X.; Han, L.B.; Zhang, X.Z. Antioxidant and Hormone Responses to Heat Stress in Two Kentucky Bluegrass Cultivars Contrasting in Heat Tolerance. J. Am. Soc. Hortic. Sci. 2014, 139, 587–596. [Google Scholar] [CrossRef]
- Gulen, H.; Eris, A. Effect of heat stress on peroxidase activity and total protein content in strawberry plants. Plant Sci. 2004, 166, 739–744. [Google Scholar] [CrossRef]
- Ayub, M.; Ashraf, M.Y.; Kausar, A.; Saleem, S.; Anwar, S.; Altay, V.; Ozturk, M. Growth and physio-biochemical responses of maize (Zea mays L.) to drought and heat stresses. Plant Biosyst.-Int. J. Deal. All Asp. Plant Biol. 2021, 155, 535–542. [Google Scholar] [CrossRef]
- Huffaker, R. Proteolytic activity during senescence of plants. New Phytol. 1990, 116, 199–231. [Google Scholar] [CrossRef]
- Callis, J.J.T.P.C. Regulation of protein degradation. Plant Cell. 1995, 7, 845. [Google Scholar] [CrossRef] [Green Version]
- He, Y.; Huang, B. Protein changes during heat stress in three Kentucky bluegrass cultivars differing in heat tolerance. Crop Sci. 2007, 47, 2513–2520. [Google Scholar] [CrossRef]
- Huang, B.R.; Rachmilevitch, S.; Xu, J.C. Root carbon and protein metabolism associated with heat tolerance. J. Exp. Bot. 2012, 63, 3455–3465. [Google Scholar] [CrossRef] [Green Version]
- Parsell, D.; Lindquist, S. The function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins. Annu. Rev. Genet. 1993, 27, 437–496. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.; Huang, B. Differential protein expression for geothermal Agrostis scabra and turf-type Agrostis stolonifera differing in heat tolerance. Environ. Exp. Bot. 2008, 64, 58–64. [Google Scholar] [CrossRef]
- Roberts, I.N.; Caputo, C.; Criado, M.V.; Funk, C. Senescence-associated proteases in plants. Physiol. Plant. 2012, 145, 130–139. [Google Scholar] [CrossRef] [PubMed]
- Ferguson, D.L.; Guikema, J.A.; Paulsen, G.M.J.P.P. Ubiquitin pool modulation and protein degradation in wheat roots during high temperature stress. Plant Physiol. 1990, 92, 740–746. [Google Scholar] [CrossRef]
- Duff, D.T.; Beard, J.B. Supraoptimal Temperature Effects upon Agrostis palustris: Part II. Influence on Carbohydrate Levels, Photosynthetic Rate, and Respiration Rate. Physiol. Plant. 1974, 32, 18–22. [Google Scholar] [CrossRef]
- Du, H.; Wang, Z.; Yu, W.; Liu, Y.; Huang, B. Differential metabolic responses of perennial grass Cynodon transvaalensis×Cynodon dactylon (C4) and Poa Pratensis (C3) to heat stress. Physiol. Plant. 2011, 141, 251–264. [Google Scholar] [CrossRef]
- Wahid, A.; Close, T.J.B.P. Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol. Plant. 2007, 51, 104–109. [Google Scholar] [CrossRef]
Parameter † | p Value | ||||||
---|---|---|---|---|---|---|---|
Date (D) | Temperature (T) | Line (L) | D × T | D × L | L × T | D × T × L | |
TQ | <0.0001 | 0.0004 | <0.0001 | <0.0001 | <0.0001 | <0.0001 | <0.0001 |
Percent green cover | <0.0001 | 0.0025 | <0.0001 | <0.0001 | 0.0002 | <0.0001 | <0.0001 |
EL | <0.0001 | 0.0064 | <0.0001 | <0.0001 | 0.0400 | <0.0001 | 0.1994 |
Total chlorophyll content | <0.0001 | 0.0004 | 0.0044 | <0.0001 | 0.4223 | <0.0001 | 0.7669 |
MDA content | <0.0001 | 0.0004 | 0.0016 | <0.0001 | 0.5540 | 0.0006 | 0.7585 |
Total protein content | <0.0001 | 0.0316 | 0.0002 | <0.0001 | 0.7554 | 0.0001 | 0.0102 |
ABS/CSm | <0.0001 | 0.0008 | 0.0002 | <0.0001 | 0.8551 | 0.0001 | 0.6623 |
TRo/CSm | <0.0001 | 0.0004 | <0.0001 | <0.0001 | 0.7140 | <0.0001 | 0.4652 |
ETo/CSm | <0.0001 | 0.0005 | 0.0002 | <0.0001 | 0.8837 | <0.0001 | 0.7059 |
TRo/ABS | <0.0001 | 0.0010 | <0.0001 | <0.0001 | <0.0001 | <0.0001 | <0.0001 |
DIo/ABS | <0.0001 | 0.001 | <0.0001 | <0.0001 | <0.0001 | <0.0001 | <0.0001 |
ETo/ABS | <0.0001 | 0.0025 | <0.0001 | <0.0001 | 0.1282 | <0.0001 | 0.0608 |
REo/ABS | <0.0001 | 0.0572 | 0.4620 | 0.0834 | 1.0000 | 0.1614 | 1.0000 |
ESC | \ | 0.0097 | 0.3803 | \ | \ | 0.9539 | \ |
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Fan, Q.; Jespersen, D. Assessing Heat Tolerance in Creeping Bentgrass Lines Based on Physiological Responses. Plants 2023, 12, 41. https://doi.org/10.3390/plants12010041
Fan Q, Jespersen D. Assessing Heat Tolerance in Creeping Bentgrass Lines Based on Physiological Responses. Plants. 2023; 12(1):41. https://doi.org/10.3390/plants12010041
Chicago/Turabian StyleFan, Qianqian, and David Jespersen. 2023. "Assessing Heat Tolerance in Creeping Bentgrass Lines Based on Physiological Responses" Plants 12, no. 1: 41. https://doi.org/10.3390/plants12010041
APA StyleFan, Q., & Jespersen, D. (2023). Assessing Heat Tolerance in Creeping Bentgrass Lines Based on Physiological Responses. Plants, 12(1), 41. https://doi.org/10.3390/plants12010041