Abstract
Lettuce (Lactuca sativa L.) prefers cool environments, and high temperatures affect its yield and quality. Polyamines (PAs) have a mitigating effect on plant abiotic stresses. The effect of exogenous spermidine (Spd) on the osmoregulatory substances and stomata of seedlings of the non-heat-tolerant lettuce variety ‘Bei San 3’ under high temperature stress was investigated at 35 °C/30 °C (day/night) under spray treatment with Spd. The results showed that exogenous Spd increased the total fresh weight, root-to-shoot ratio, leaf length, leaf width, root volume, and root surface area of lettuce under high temperature stress and reduced levels of malondialdehyde. The endogenous polyamine content was changed, and endogenous spermidine (Spd) and putrescine (Put) were increased. The accumulation of six organic osmoregulatory substances was promoted, resulting in enhanced betaine aldehyde dehydrogenase (BADH), choline monooxygenase (CMO), proline catalase pyrroline-5-carboxylate synthase (P5CS), ornithine aminotransferase (OAT), and pyrroline-5-carboxylate reductase (P5CR) activity. The production and activity of the degrading enzymes proline dehydrogenase (PDH) and proline oxidase (POX) were inhibited, and the activity of glutamic acid decarboxylase (GAD), the key enzyme of γ-aminobutyric (GABA), was suppressed. In addition, exogenous Spd increased the contents of Ca, K, Fe, Mn, Zn, and NO3− ions in lettuce leaves under high temperature stress, promoted K+ efflux and Ca2+ influx, and reduced the relative stomatal aperture. In summary, exogenous Spd mitigates lettuce injury caused by high temperature stress by increasing the content of osmoregulatory substances and altering stomatal morphology.
Similar content being viewed by others
Data Availability
All data and material generated or used during the study appear in the submitted article.
Code Availability
None.
References
Alcázar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2007) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876. https://doi.org/10.1007/s10529-006-9179-3
Alcázar R, Bueno M, Tiburcio AF (2020) Polyamines: small amines with large effects on plant abiotic stress tolerance. Cells-Basel 9(11):2373. https://doi.org/10.3390/cells9112373
Al-Yasi H, Attia H, Alamer K, Hassan F, Ali E, Elshazly S, Siddique KHM, Hessini K (2020) Impact of drought on growth, photosynthesis, osmotic adjustment, and cell wall elasticity in Damask rose. Plant Physiol Biochem 150:133–139. https://doi.org/10.1016/j.plaphy.2020.02.038
An ZF, Li CY, Zhang LX, Alva AK (2012) Role of polyamines and phospholipase D in maize (Zea mays L.) response to drought stress. S Afr J Bot 83:145–150. https://doi.org/10.1016/j.sajb.2012.08.009
Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317. https://doi.org/10.1007/s007260170046
Bano C, Amist N, Singh NB (2020) Role of polyamines in plants abiotic stress tolerance: advances and future prospects. Plant Life Chang Environ. https://doi.org/10.1016/B978-0-12-818204-8.00021-7
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/bf00018060
Blum A (2017) Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ 40:4–10. https://doi.org/10.1111/pce.12800
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Bukharov AF, Baleev DN, Soldatenko AV, Musaev FB, Kezimana P, Priyatkin NS (2021) Impacts of high temperature on embryonic growth and seed germination of dill (Anethum graveolens). Seed Sci Technol 49:7–17
Burnet M, Lafontaine PJ, Hanson AD (1995) Assay, purification, and partial characterization of choline monooxygenase from spinach. Plant Physiol 108:581–588. https://doi.org/10.1104/pp.108.2.581
Cai QS, He LF, Zen XC, Yu BJ, Xie YF (2021) Plant physiology. China Agricultural University Press, Beijing
Cekic FO, Goren-Saglam N, Torun H, Yigit E, Unal D (2018) Gamma-amino butyric acid metabolism under high temperature stress in two lichen species. Appl Ecol Environ Res 16:5529–5538
Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257. https://doi.org/10.1016/s1369-5266(02)00255-8
Chen WL, Yang WJ, Lo HF, Yeh DM (2014) Physiology, anatomy, and cell membrane thermostability selection of leafy radish (Raphanus sativus var. oleiformis Pers.) with different tolerance under heat stress. Sci Hortic 179:367–375. https://doi.org/10.1016/j.scienta.2014.10.003
Chen L, Liu L, Lu B, Ma T, Jiang D, Li J, Zhang K, Sun H, Zhang Y, Bai Z, Li C (2020) Exogenous melatonin promotes seed germination and osmotic regulation under salt stress in cotton (Gossypium hirsutum L.). PLoS ONE 15:e0228241. https://doi.org/10.1371/journal.pone.0228241
ElSayed AI, Rafudeen MS, El-hamahmy MAM, Odero DC, Hossain MS (2018) Enhancing antioxidant systems by exogenous spermine and spermidine in wheat (Triticum aestivum) seedlings exposed to salt stress. Funct Plant Biol 45:745–759. https://doi.org/10.1071/fp17127
Fan W, Zhang M, Zhang H, Zhang P (2012) Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. PLoS ONE 7:e37344. https://doi.org/10.1371/journal.pone.0037344
Fernandez O, Béthencourt L, Quero A, Sangwan RS, Clément C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417. https://doi.org/10.1016/j.tplants.2010.04.004
Fu W, Li P, Wu Y (2012) Effects of different light intensities on chlorophyll fluorescence characteristics and yield in lettuce. Sci Hortic 135:45–51. https://doi.org/10.1016/j.scienta.2011.12.004
Fu Y Y, Gu QQ, Dong Q, Zhang ZH, Lin C, Hu WM, Pan RH, Guan YJ, Hu J (2019) Spermidine enhances heat tolerance of rice seeds by modulating endogenous starch and polyamine metabolism. Molecules 24:1395. https://doi.org/10.3390/molecules24071395
Gomathi R, Shiyamala S, Vasantha S, Johnson DE, Janani PK (2013) Kinetics of metabolism in sugarcane (Saccharum officinarum L.) under heat stress. Indian J Plant Physiol 18(1):41–47. https://doi.org/10.1007/s40502-013-0011-5
Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307. https://doi.org/10.1007/bf02374789
Han Y, Chen Z, Lv S, Ning K, Ji X, Liu X, Wang Q, Liu R, Fan S, Zhang X (2016) MADS-box genes and gibberellins regulate bolting in lettuce (Lactuca sativa L.). Front Plant Sci 7:1889. https://doi.org/10.3389/fpls.2016.01889
Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553. https://doi.org/10.1046/j.1365-3040.1998.00309.x
Hasanuzzaman M, Nahar K, Alam M, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14(5):9643–9684. https://doi.org/10.3390/ijms14059643
Hasanuzzaman M, Alhaithloul HAS, Parvin K, Bhuyan MHB, Tanveer M, Mohsin SM, Nahar K, Soliman MH, Mahmud JA, Fujita M (2019) Polyamine action under metal/metalloid stress: regulation of biosynthesis, metabolism, and molecular interactions. Int J Mol Sci 20(13):3215. https://doi.org/10.3390/ijms20133215
Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466. https://doi.org/10.4161/psb.21949
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611. https://doi.org/10.1007/s004250050524
Hu X, Li D, Qiao Y, Song Q, Guan Z, Qiu K, Cao J, Huang L (2020) Salt tolerance mechanism of a hydrocarbon-degrading strain: salt tolerance mediated by accumulated betaine in cells. J Hazard Mater 392:122326. https://doi.org/10.1016/j.jhazmat.2020.122326
Huang AH, Cavalieri AJ (1979) Proline oxidase and water stress-induced proline accumulation in spinach leaves. Plant Physiol 63:531–535. https://doi.org/10.1104/pp.63.3.531
Huang B, Xu Q (2000) Root growth and nutrient element status of creeping bentgrass cultivars differing in heat tolerance as influenced by supraoptimal shoot and root temperatures. J Plant Nutr 23:979–990. https://doi.org/10.1080/01904160009382075
Imran M, Khan MA, Shahzad R, Bilal S, Lee IJ (2021) Melatonin ameliorates thermotolerance in soybean seedling through balancing redox homeostasis and modulating antioxidant defense. Phytohormones Polyamines Biosynthesi Mol 26(17):5116. https://doi.org/10.3390/molecules26175116
Jia YX, Sun J, Guo SR, Li J, Hu XH, Wang SP (2010) Effect of root-applied spermidine on growth and respiratory metabolism in roots of cucumber (Cucumis sativus) seedlings under hypoxia. Russ J Plant Physiol 57:648–655. https://doi.org/10.1134/s1021443710050079
Jia CH, Yu XJ, Zhang M, Liu ZG, Zou P, Ma J, Xu YC (2020) Application of melatonin-enhanced tolerance to high-temperature stress in cherry radish (Raphanus sativus L. var. radculus pers). J Plant Growth Regul 39:631–640. https://doi.org/10.1007/s00344-019-10006-1
Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722. https://doi.org/10.1093/pcp/pch083
Kasukabe Y, He L, Watakabe Y, Otani M, Shimada T, Tachibana S (2006) Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase. Plant Biotechnol 23:75–83. https://doi.org/10.5511/plantbiotechnology.23.75
Lee JG, Choi CS, Jang YA, Jang SW, Lee SG, Um YC (2013) Effects of air temperature and air flow rate control on the tipburn occurrence of leaf lettuce in a closed-type plant factory system. Hortic Environ Biotechnol 54:303–310. https://doi.org/10.1007/s13580-013-0031-0
Li F, Chen X (2017) Response of over~summer hydroponic lettuce to nutrient solution temperature control. Agric Sci Technol 18:1072–1075
Li J, Wang MH, Guo SR, Wang SP, Wang MH (2006) Effect of exogenous spermidine on polyamine content and antioxidant enzyme activities in roots of cucumber seedlings under root-zone hypoxia stress. Chin J Plant Ecol 30:118–123
Li S, Li F, Wang J, Zhang WEN, Meng Q, Chen THH, Murata N, Yang X (2011) Glycinebetaine enhances the tolerance of tomato plants to high temperature during germination of seeds and growth of seedlings. Plant Cell Environ 34:1931–1943. https://doi.org/10.1111/j.1365-3040.2011.02389.x
Li ZG, Ding XJ, Du PF (2013) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:741–747. https://doi.org/10.1016/j.jplph.2012.12.018
Li L, Gu W, Li J, Li C, Xie T, Qu D, Meng Y, Li C, Wei S (2018) Exogenously applied spermidine alleviates photosynthetic inhibition under drought stress in maize (Zea mays L.) seedlings associated with changes in endogenous polyamines and phytohormones. Plant Physiol Biochem 129:35–55. https://doi.org/10.1016/j.plaphy.2018.05.017
Li CJ, Liu R, Han YY, Hao JH, Liu CJ, Fan SX (2019) Effects of exogenousspermidineat on growth and antioxidant activityof lettuce under high temperature stress. J Beijing Univ Agric 34:56–61
Liu P, Li MJ (2016) Experiments of plant physiology. Science Press, Beijing
Liu K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1326. https://doi.org/10.1104/pp.124.3.1315
Loka DA, Oosterhuis DM, Baxevanos D, Noulas C, Hu W (2020) Single and combined effects of heat and water stress and recovery on cotton (Gossypium hirsutum L.) leaf physiology and sucrose metabolism. Plant Physiol Biochem 148:166–179. https://doi.org/10.1016/j.plaphy.2020.01.015
MacRobbie EAC (1988) Control of ion fluxes in stomatal guard cells. Bot Acta 101:140–148. https://doi.org/10.1111/j.1438-8677.1988.tb00025.x
Martin-Tanguy J (2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul 34:135–148. https://doi.org/10.1023/a:1013343106574
Martins LD, Tomaz MA, Lidon FC, DaMatta FM, Ramalho JC (2014) Combined effects of elevated [CO2] and high temperature on leaf mineral balance in Coffea spp. plants. Clim Chang 126:365–379. https://doi.org/10.1007/s10584-014-1236-7
Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997. https://doi.org/10.1126/science.1098704
Mickelbart MV, Boine B (2020) Glycinebetaine enhances osmotic adjustment of ryegrass under cold temperatures. Agronomy 10:210. https://doi.org/10.3390/agronomy10020210
Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environ Exp Bot 112:44–54. https://doi.org/10.1016/j.envexpbot.2014.12.001
Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Mahmud J-A, Suzuki T, Fujita M (2017) Insights into spermine-induced combined high temperature and drought tolerance in mung bean: osmoregulation and roles of antioxidant and glyoxalase system. Protoplasma 254:445–460. https://doi.org/10.1007/s00709-016-0965-z
Ning K, Han Y, Chen Z, Luo C, Wang S, Zhang W, Li L, Zhang X, Fan S, Wang Q (2019) Genome-wide analysis of MADS-box family genes during flower development in lettuce. Plant Cell Environ 42:1868–1881. https://doi.org/10.1111/pce.13523
Niu JH, Anjum SA, Wang R, Li JH, Liu MR, Song JX, Zohaib A, Lv J, Wang SG, Zong XF (2016) Exogenous application of brassinolide can alter morphological and physiological traits of Leymus chinensis (trin.) tzvelev under room and high temperatures. Chilean J Agric Res 76(1):27–33. https://doi.org/10.4067/S0718-58392016000100004
Okuda N, Toriyama K, Miya Y, Yanagi T, Yamaguchi K, Tanaka M (2014) Effect of end-of-day light irradiation using LED light sources on the growth of lettuce under a high temperature. Environ Control Biol 52:73–77. https://doi.org/10.2525/ecb.52.73
Pál M, Szalai G, Janda T (2015) Speculation: polyamines are important in abiotic stress signaling. Plant Sci 237:16–23. https://doi.org/10.1016/j.plantsci.2015.05.003
Pandey S, Zhang W, Assmann SM (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581:2325–2336. https://doi.org/10.1016/j.febslet.2007.04.008
Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling. Front Plant Sci 5:154. https://doi.org/10.3389/fpls.2014.00154
Qin XH, Li HB, Li P, Zhang GS (2015) Soilless culture technique. Chongqing University Press, ChongQing
Ramani HR, Mandavia MK, Dave RA, Bambharolia RP, Silungwe H, Garaniya NH (2017) Biochemical and physiological constituents and their correlation in wheat (Triticum aestivum L.) genotypes under high temperature at different development stages. Int J Plant Physiol Biochem 9:1–8. https://doi.org/10.5897/ijppb2015.0240
Rasheed R, Wahid A, Farooq M, Hussain I, Basra SMA (2011) Role of proline and glycinebetaine pretreatments in improving heat tolerance of sprouting sugarcane (Saccharum sp.) buds. Plant Growth Regul 65:35–45. https://doi.org/10.1007/s10725-011-9572-3
Rena AB, Splittstoesser WE (1975) Proline dehydrogenase and pyrroline-5-carboxylate reductase from pumpkin cotyledons. Phytochemistry 14:657–661. https://doi.org/10.1016/0031-9422(75)83010-x
Richard AK (2007) Global warming is changing the world. Science 316:188–190. https://doi.org/10.1126/science.316.5822.188
Sadok W, Lopez JR, Smith KP (2020) Transpiration increases under high-temperature stress: potential mechanisms, trade-offs and prospects for crop resilience in a warming world. Plant Cell Environ. https://doi.org/10.1111/pce.13970
Sang QQ, Shu S, Shan X, Guo SR, Sun J (2016) Effects of exogenous spermidine on antioxidant system of tomato seedlings exposed to high temperature stress. Russ J Plant Physiol 63:645–655. https://doi.org/10.1134/s1021443716050113
Sang QQ, Shan X, An YH, Shu S, Sun J, Guo SR (2017) Proteomic analysis reveals the positive effect of exogenous spermidine in tomato seedlings’ response to high-temperature stress. Front Plant Sci 8:120. https://doi.org/10.3389/fpls.2017.00120
Scott RH, Strasheim A (1975) Determination of trace elements in plant materials by inductively coupled plasma optical emission spectrometry. Anal Chim Acta 76(1):71–78. https://doi.org/10.1016/S0003-2670(01)81986-3
Seher Y, Filiz O, Melike B (2013) Gamma-amino butyric acid, glutamate dehydrogenase and glutamate decarboxylase levels in phylogenetically divergent plants. Plant Syst Evol 299:403–412. https://doi.org/10.1007/s00606-012-0730-5
Shu S, Chen L, Lu W, Sun J, Guo S, Yuan Y, Li J (2014) Effects of exogenous spermidine on photosynthetic capacity and expression of Calvin cycle genes in salt-stressed cucumber seedlings. J Plant Res 127:763–773. https://doi.org/10.1007/s10265-014-0653-z
Sita K, Kumar V (2020) Role of gamma amino butyric acid (GABA) against abiotic stress tolerance in legumes: a review. Plant Physiol Rep 25:654–663. https://doi.org/10.1007/s40502-020-00553-1
Sun J, Lu N, Xu HJ, Maruo T, Guo SR (2016) Root zone cooling and exogenous spermidine root-pretreatment promoting Lactuca sativa L. growth and photosynthesis in the high-temperature season. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00368
Sun H, Luo M, Zhou X, Zhou Q, Sun Y, Ge W, Wei B, Cheng S, Ji S (2019) Exogenous glycine betaine treatment alleviates low temperature-induced pericarp browning of ‘Nanguo’ pears by regulating antioxidant enzymes and proline metabolism. Food Chem 306:125626. https://doi.org/10.1016/j.foodchem.2019.125626
Sun H, Luo M, Zhou X, Zhou Q, Sun Y, Ge W, Wei B, Cheng S, Ji S (2020a) Exogenous glycine betaine treatment alleviates low temperature-induced pericarp browning of ‘Nanguo’ pears by regulating antioxidant enzymes and proline metabolism. Food Chem 306:125626. https://doi.org/10.1016/j.foodchem.2019.125626
Sun H, Zhou X, Zhou Q, Zhao Y, Kong X, Luo M, Ji S (2020b) Disorder of membrane metabolism induced membrane instability plays important role in pericarp browning of refrigerated ‘Nanguo’ pears. Food Chem 320:126684. https://doi.org/10.1016/j.foodchem.2020.126684
Tonhati R, Mello SC, Momesso P, Pedroso RM (2020) L-proline alleviates heat stress of tomato plants grown under protected environment. Sci Hortic 268:109370. https://doi.org/10.1016/j.scienta.2020.109370
Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759. https://doi.org/10.1007/s00726-008-0061-6
Wahid A, Close TJ (2007) Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol Plant 51:104–109. https://doi.org/10.1007/s10535-007-0021-0
Wang XH, Wang SJ, Chen Z, Gong B, Wang XF, Win M, Shi QH, Li Y, Yang FJ (2016) Effects of exogenous polyamines on nitrate tolerance in cucumber. Russ J Plant Physiol 63:549–557. https://doi.org/10.1134/s1021443716040166
Wang SY, Shi XC, Liu FQ, Pedro L (2021) Effects of exogenous methyl jasmonate on quality and preservation of postharvest fruits: a review. Food Chem. https://doi.org/10.1016/j.foodchem.2021.129482
Yan S, McLamore ES, Dong S, Gao H, Taguchi M, Wang N, Zhang T, Su X, Shen Y (2015) The role of plasma membrane H +-ATP ase in jasmonate-induced ion fluxes and stomatal closure in Arabidopsis thaliana. Plant J 83:638–649. https://doi.org/10.1111/tpj.12915
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514. https://doi.org/10.1042/bj0570508
Yu Y, Li X, Sun J, Zhang X, Xu T, Zhang J, Li Z, Chen S (2016) Heat shock responses in Populus euphratica cell cultures: important role of crosstalk among hydrogen peroxide, calcium and potassium. Plant Cell Tissue Organ Cult 125:215–230. https://doi.org/10.1007/s11240-016-0940-6
Zhang G, Bown AW (1997) The rapid determination of γ-aminobutyric acid. Phytochemistry 44:1007–1009. https://doi.org/10.1016/s0031-9422(96)00626-7
Zhang R, Guo X, Zhang Y, Tian C (2020) Influence of modified atmosphere treatment on post-harvest reactive oxygen metabolism of pomegranate peels. Nat Prod Res 34:740–744. https://doi.org/10.1080/14786419.2018.1497027
Zhao GC, Xie MX, Wang YC, Li JY (2017) Molecular mechanisms underlying γ-aminobutyric acid (GABA) accumulation in giant embryo rice seeds. J Agric Food Chem 65:4883–4889. https://doi.org/10.1021/acs.jafc.7b00013
Zhou ZH, Wang Y, Ye XY, Li ZG (2018) Signaling molecule hydrogen sulfide improves seed germination and seedling growth of maize (Zea mays L.) under high temperature by inducing antioxidant system and osmolyte biosynthesis. Front Plant Sci 9:1288. https://doi.org/10.3389/fpls.2018.01288
Zhou R, Hu QJ, Pu Q, Chen MX, Zhu XR, Gao C, Zhou GX, Liu LJ, Wang ZQ, Yang JC, Zhang JH, Cao YY (2020) Spermidine enhanced free polyamine levels and expression of polyamine biosynthesis enzyme gene in rice spikelets under heat tolerance before heading. Sci Rep-UK. https://doi.org/10.1038/s41598-020-64978-2
Zhu Y, Huang L, Zheng YP, Hao LH, Jiang GB, Wang HX, Li GZ, Zhang ZC (2016) Effects of high temperatures on leaf stomatal traits and gas exchanges of highbush blueberries. J Fruit Sci 33:444–456
Acknowledgements
We thank American Journal Experts (AJE) for English language editing. This manuscript was edited for English language by American Journal Experts (AJE). We thank Xin He and Wenjing Sun from Beijing University of Agriculture for determination of lettuce endogenous polyamines.
Funding
This work was supported by the National Key Research and Development Program of China (2016YFD0201010), the Beijing Innovation Consortium of Agriculture Research System (BAIC07), and the Science and Technology Program of the Beijing Municipal Education Commission (KM201910020012).
Author information
Authors and Affiliations
Contributions
HH participated in the investigation and writing of the original draft; YH participated in the resources and writing, reviewing, and editing of the manuscript; JH participated in the writing, reviewing, and editing of the manuscript; XQ participated in the writing, reviewing, and editing of the manuscript; CL participated in the conceptualization, writing, reviewing, and editing of the manuscript, and funding acquisition; SF participated in the conceptualization and funding acquisition.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Handling Editor: Peter Hedden.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Huang, H., Han, Y., Hao, J. et al. Exogenous Spermidine Modulates Osmoregulatory Substances and Leaf Stomata to Alleviate the Damage to Lettuce Seedlings Caused by High Temperature Stress. J Plant Growth Regul 42, 1236–1255 (2023). https://doi.org/10.1007/s00344-022-10625-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-022-10625-1