Abstract
The dynamics and distribution of endogenous cytokinins (CKs), gibberellic (GA3) and salicylic (SA) acids in wheat (Triticum aestivum L., ‘Podolyanka’) and spelt wheat (Triticum spelta L., ‘Frankenkorn’) plants was analyzed using HPLC–MS. Fourteen-day-old plants that had been exposed to short-term heat stress (+ 40 °C, 2 h) and 21-day-old plants after recovery were studied. Heat stress induced rapid changes, both specific and nonspecific, in hormone levels and distribution. The level of GA3 decreased in the shoots and roots of both winter and spelt wheat. A reduction in SA content was observed in wheat, while an increase was observed in spelt. The pool of CKs significantly increased in wheat, while in spelt—it decreased more than twofold. After recovery, an increase in GA3 content occurred in both species, but not to the levels measured in control plants. More active accumulation of GA3 was observed in the roots. The content of SA in the shoots of wheat continued to decrease, while in the roots it increased. In spelt, hormone concentration decreased, but it remained higher than in 21-day-old control plants. In shoots of both plants the pool of CKs decreased, while in wheat roots it did not change, and in spelt roots it decreased. The total CKs content in stressed wheat plants was twice as high as in spelt. In general, we established significant hormonal fluctuations, which indicate a direct involvement of endogenous cytokinins, gibberellic and salicylic acids in wheat and spelt response to heat stress. Screening of stress-resistant genotypes of cereals may benefit from quantitation of CKs, GA3, and SA.
Similar content being viewed by others
Abbreviations
- GA3 :
-
Gibberellic acid
- SA:
-
Salicylic acid
- CKs:
-
Cytokinins
- iP:
-
Isopentenyladenine
- iPa:
-
Isopentenyladenosine
- t-Z:
-
trans-Zeatin
- t-ZR:
-
trans-Zeatin riboside
- t-ZOG:
-
trans-Zeatin-O-glucoside
- HPLC–MS:
-
High-performance liquid chromatography-mass spectrometry
- ROS:
-
Reactive oxygen species
- FW:
-
Fresh weight
- DW:
-
Dry weight
References
Abhinandan K, Skori L, Stanic M, Hickerson NMN, Jamshed M, Samuel MA (2018) Abiotic stress signaling in wheat—an inclusive overview of hormonal interactions during abiotic stress responses in wheat. Front Plant Sci 9:734. https://doi.org/10.3389/fpls.2018.00734
Abid M, Ali S, Qi LK, Zahoor R, Tian Z, Jiang D, Snider JL, Dai T (2018) Physiological and biochemical changes during drought and recovery periods at tillering and jointing stages in wheat (Triticum aestivum L.). Sci Rep 8:1–15. https://doi.org/10.1038/s41598-018-21441-7
Ansari O, Azadi MS, Sharif-Zadeh F, Younesi L (2013) Effect of hormone priming on germination characteristics and enzyme activity of mountain rye (Secale montanum) seeds under drought stress conditions. J Stress Physiol Biochem 9(3):61–71
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190. https://doi.org/10.1007/s11099-013-0021-6
Asif M, Jamil HMA, Hayat MT, Mahmood Q, Ali S (2019) Use of phytohormones to improve abiotic stress tolerance in wheat. In: Hasanuzzaman M, Nahar K, Hossain M (eds) Wheat Production in changing environments. Springer, Singapore, pp 465–479. https://doi.org/10.1007/978-981-13-6883-7_18
Babenko LM, Hospodarenko HM, Rozhkov RV, Pariy YF, Pariy MF, Babenko AV, Kosakivska IV (2018) Triticum spelta: origin, biological characteristics and perspectives for use in breeding and agriculture. Regul Mech Biosyst 9(2):250–257. https://doi.org/10.15421/021837
Brestic M, Zivcak M, Hauptvoge P, Misheva S, Kocheva K, Yang X, Li X, Allakhverdiev S (2018) Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions. Photosynth Res 136(2):245–255. https://doi.org/10.1007/s11120-018-0486-z
Cheikh N, Jones RJ (1994) Disruption of maize kernel growth and development by heat stress (role of cytokinin/abscisic acid balance). Plant Physiol 106(1):45–51. https://doi.org/10.1104/pp.106.1.45
Chen YE, Cui JM, Li GX, Yuan M, Zhang ZW, Yuan S, Zhang HY (2016) Effect of salicylic acid on the antioxidant system and photosystem II in wheat seedlings. Biol Plant 60:139–147. https://doi.org/10.1007/s10535-015-0564-4
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217(1):67–75. https://doi.org/10.1242/jeb.089938
Cortleven A, Leuendorf JE, Frank M, Pezzetta D, Bolt S, Schmülling T (2019) Cytokinin action in response to abiotic and biotic stresses in plants. Plant Cell Environ 42:998–1018. https://doi.org/10.1111/pce.13494
Dobrá J, Černý M, Štorchová H, Dobrev P, Skalák J, Jedelský PL, Lukšanová H, Gaudinová A, Pešek B, Malbeck J, Vanek T, Brzobohatý B, Vanková R (2015) The impact of heat stress targeting on the hormonal and transcriptomic response in Arabidopsis. Plant Sci 231:52–61. https://doi.org/10.1016/j.plantsci.2014.11.005f
Escarnot E, Jacquemin J-M, Agneessens R, Paquot M (2012) Comparative study of the content and profiles of macronutrients in spelt and wheat, a review. Biotechnol Agron Soc Environ 16(2):243–256
Farkhutdinov RG, Kudoyarova GR, Veselov SY, Valke R (1997) Influence of temperature increase on evapotranspiration rate and cytokinin content in wheat seedlings. Biol Plant 39:289–291. https://doi.org/10.1023/A:1000627916005
Farooq M, Bramley H, Palta JA, Siddique KHM (2011) Heat stress in wheat during reproductive and grain-filling phases. Crit Rev Plant Sci 30:491–507. https://doi.org/10.1080/07352689.2011.615687
Gantait S, Sinniah UR, Ali MN, Sahu NC (2015) Gibberellins—a multifaceted hormone in plant growth regulatory network. Curr Protein Pept Sci 16:406–412. https://doi.org/10.2174/1389203716666150330125439
Gupta NK, Gupta S, Shukla DS, Deshmukh PS (2003) Differential responses of BA injection on yield and specific grain growth in contrasting genotypes of wheat (Triticum aestivum L.). Plant Growth Regul 40:201–205. https://doi.org/10.1023/A:1025023822806
Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17:172–179. https://doi.org/10.1016/j.tplants.2011.12.005
Hamayun M, Khan SA, Shinwari ZK, Khan AL (2010) Effect of polyethylene glycol induced drought stress on physio-hormonal attributes of soybean. Pak J Bot 42(2):977–986
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684. https://doi.org/10.3390/ijms14059643
Hönig M, Plíhalová L, Husičková A, Nisler J, Doležal K (2018) Role of cytokinins in senescence, antioxidant defence and photosynthesis. Int J Mol Sci 19:4045. https://doi.org/10.3390/ijms19124045
Hosseini SM, Poustini K, Ahmadi A (2008) Effects of foliar application of BAP on source and sink strength in four six-rowed barley (Hordeum vulgare L.) cultivars. Plant Growth Regul 54:231–239. https://doi.org/10.1007/s10725-007-9245-4
Janda M, Ruelland E (2015) Magical mystery tour: salicylic acid signaling. Environ Exp Bot 114:117–128. https://doi.org/10.1016/j.envexpbot.2014.07.003
Janda T, Khalil R, Tajti J, Pal M, Darko E (2019) Responses of young wheat plants to moderate heat stress. Acta Physiol Plant 41:137. https://doi.org/10.1007/s11738-019-2930-x
Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2015) Salicylic acid in plant salinity stress signalling and tolerance. J Plant Growth Regul 75:25–40. https://doi.org/10.1007/s10725-015-0028-z
Kang GZ, Li G, Guo T (2014) Molecular mechanism of salicylic acid induced abiotic stress tolerance in higher plants. Acta Physiol Plant 36:2287–2297. https://doi.org/10.1007/s11738-014-1603-z
Khan MI, Iqbal N, Masood A, Per TS, Khan AN (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8(11):e26374. https://doi.org/10.4161/psb.26374
Khan MI, Fatma M, Per TS et al (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462. https://doi.org/10.3389/fpls.2015.00462
Kieber JJ, Schaller GE (2018) Cytokinin signaling in plant development. Development 145:dev149344. https://doi.org/10.1242/dev.149344
Kosakivska IV, Voytenko LV, Likhnyovskiy RV (2016) Peculiarities of cytokinin accumulation and distribution in Triticum aestivum L. seedlings under temperature stresses. J Stress Physiol Biochem 12(2):32–38
Kosakivska IV, Voytenko LV, Vasyuk VA, Shcherbatiuk MM (2019) Effect of zinc on growth and phytohormones accumulation in Triticum aestivum L. priming with abscisic acid. Dopov Nac Akad Nauk Ukr 11:93–99. https://doi.org/10.15407/dopovidi2019.11.093
Kosakivska IV, Shcherbatiuk MM, Voytenko LV (2020) Profiling of hormones in plant tissues: history, modern approaches, use in biotechnology. Biotechnol Acta 13(4):14–25. https://doi.org/10.15407/biotech13.04.014
Kumar D (2014) Salicylic acid signaling in disease resistance. Plant Sci 228:127–134. https://doi.org/10.1016/j.plantsci.2014.04.014
Lacko-Bartošová M, Korczyk-Szabó J, Ražný R (2010) Triticum spelta—a specialty grain for ecological farming systems. Res J Agric Sci 42(1):143–147
Larkindale J, Huang B (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J Plant Physiol 161(4):405–413. https://doi.org/10.1078/0176-1617-01239
Li H, Torres-Garcia J, Latrasse D, Benhamed M, Schilderink S, Zhou W, Kulikova O, Hirt Y, Bisseling T (2017) Plant-specific histone deacetylases HDT1/2 regulate GIBBERELLIN 2-OXIDASE2 expression to control Arabidopsis root meristem cell number. Plant Cell 29(9):2183–2196. https://doi.org/10.1105/tpc.17.00366
Lynch JP, Chimungu JG, Brown KM (2014) Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement. J Exp Bot 65:6155–6166. https://doi.org/10.1093/jxb/eru162
Minguet GE, Alabadi D, Blázquez MA (2014) Gibberellin implication in plant growth and stress responses. In: Tran L-SP, Pal S (eds) Phytohormones: a window to metabolism, signaling and biotechnological application. Springer, New York, pp 119–161. https://doi.org/10.1007/978-1-4939-0491-4_5
Morgun VV, Dubrovna OV, Morgun BV (2016) Modern biotechnologies of obtaining stress-resistant wheat plants. Fiziol Rast Genet 48(3):196–214. https://doi.org/10.15407/frg2016.03.196
Nadolska-Orczyk A, Rajchel IK, Orczyk W, Gasparis S (2017) Major genes determining yield-related traits in wheat and barley. Theor Appl Genet 130:1081–1098. https://doi.org/10.1007/s00122-017-2880-x
Narayanan S (2018) Effects of high temperature stress and traits associated with tolerance in wheat. J Sci 2(3):177–186. https://doi.org/10.15406/oajs.2018.02.00067
Prerostova S, Dobrev PI, Kramna B, Gaudinova A, Knirsch V, Spichal L, Zatloukal M, Vankova R (2020) Heat acclimation and inhibition of cytokinin degradation positively affect heat stress tolerance of Arabidopsis. Front Plant Sci 11:87. https://doi.org/10.3389/fpls.2020.00087
Sawada H, Shim I, Usui K (2006) Induction of benzoicacid-2-hydroxylase and salicylic acid biosynthesis: Modulation by salt stress in rice seedlings. Plant Sci 171:263–270. https://doi.org/10.1016/j.plantsci.2006.03.020
Sponsel VM, Hedden P (2010) Gibberellin biosynthesis and inactivation. In: Davies PJ (ed) Plant hormones. Springer, Dordrecht, pp 63–94. https://doi.org/10.1007/978-1-4020-2686-7_4
Todorova D, Genkov T, Vaseva-Gemisheva I, Alexieva V, Karanov E, Smith A, Hall M (2005) Effect of temperature stress on the endogenous cytokinin content in Arabidopsis thaliana (L.) Heynh plants. Acta Physiol Plant 27:13–18. https://doi.org/10.1007/s11738-005-0031-5
Van Emden H (2008) Statistics for terrified biologists. Wiley-Blackwell, Oxford
Veselov DS, Kudoyarova GR, Kudryakova NV, Kusnetsov VV (2017) Role of cytokinins in stress resistance of plants. Russ J Plant Physiol 64:15–27. https://doi.org/10.1134/S1021443717010162
Wang X, Cai J, Jiang D, Liu F, Dai T, Cao W (2011) Pre-anthesis high-temperature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat. J Plant Physiol 168:585–593. https://doi.org/10.1016/j.jplph.2010.09.016
Wang HQ, Liu P, Zhang JW, Zhao B, Ren BZ (2020) Endogenous hormones inhibit differentiation of young ears in maize (Zea mays L.) under heat stress. Front Plant Sci 11:533046. https://doi.org/10.3389/fpls.2020.533046
Wu C, Cui K, Wang W, Li Q, Fahad S, Hu Q, Huang J, Nie L, Mohapatra PK, Peng S (2017) Heat-induced cytokinin transportation and degradation are associated with reduced panicle cytokinin expression and fewer spikelets per panicle in rice. Front Plant Sci 8:371. https://doi.org/10.3389/fpls.2017.00371
Zhan A, Schneider H, Lynch J (2015) Reduced lateral root branching density improves drought tolerance in maize. Plant Physiol 168:1603–1615. https://doi.org/10.1104/pp.15.00187
Acknowledgements
The publication contains the results of research conducted within the project funded by the National Academy of Sciences of Ukraine № III-82-17.454 “Phytohormonal system of new genotypes of T. aestivum L. and its wild precursors under the action of extreme climatic factors” (2017–2021).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Rights and permissions
About this article
Cite this article
Kosakivska, I.V., Vasyuk, V.A., Voytenko, L.V. et al. Changes in hormonal status of winter wheat (Triticum aestivum L.) and spelt wheat (Triticum spelta L.) after heat stress and in recovery period. CEREAL RESEARCH COMMUNICATIONS 50, 821–830 (2022). https://doi.org/10.1007/s42976-021-00206-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42976-021-00206-5