Photosynthetica 2024, 62(4):393-405 | DOI: 10.32615/ps.2024.041

Impact of exogenous rhamnolipids on plant photosynthesis and biochemical parameters under prolonged heat stress

M.A. BOUCHRATI1, 2, S. VILLAUME1, J.F. GUISE1, I. FEUSSNER2, N. VAILLANT-GAVEAU1, †, S. DHONDT-CORDELIER1, †
1 University of Reims Champagne-Ardenne, INRAE, RIBP, USC 1488, 51100 Reims, France
2 Department of Plant Biochemistry, Albrecht-von-Haller-Institute of Plant Sciences and Göttingen Center for Molecular Biosciences (GZMB), Justus-von-Liebig-Weg 11, University of Göttingen, 37077 Göttingen, Germany

High temperatures severely affect plant growth and development leading to major yield losses. These temperatures are expected to increase further due to global warming, with longer and more frequent heat waves. Rhamnolipids (RLs) are known to protect several plants against various pathogens. To date, how RLs act under abiotic stresses is unexplored. In this study, we aimed to investigate whether RLs could modify Arabidopsis thaliana physiology during prolonged heat stress. Measurement of leaf gas exchange and chlorophyll fluorescence showed that heat stress reduces photosynthetic rate through stomatal limitation and reduction of photosystem II yield. Our study reported decreased chlorophyll content and accumulation of soluble sugars and proline in response to heat stress. RLs were shown to have no detrimental effect on photosynthesis and carbohydrate metabolism in all conditions. These results extend the knowledge of plant responses to prolonged heat stress.

Additional key words: chlorophyll fluorescence; gas exchange; photosynthesis; soluble sugars; thermotolerance.

Received: June 14, 2024; Revised: November 18, 2024; Accepted: December 5, 2024; Prepublished online: December 17, 2024; Published: December 19, 2024  Show citation

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BOUCHRATI, M.A., VILLAUME, S., GUISE, J.F., FEUSSNER, I., VAILLANT-GAVEAU, N., & DHONDT-CORDELIER, S. (2024). Impact of exogenous rhamnolipids on plant photosynthesis and biochemical parameters under prolonged heat stress. Photosynthetica, 62(4), 393-405. doi: 10.32615/ps.2024.041
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    References

    1. Abdelrahman M., Ishii T., El-Sayed M., Tran L.-S.P.: Heat sensing and lipid reprograming as a signaling switch for heat stress responses in wheat. - Plant Cell Physiol. 61: 1399-1407, 2020. Go to original source...
    2. Akram M.A., Den N.Z.U., Abbas M.M. et al.: Multifarious role of osmolytes in plants: signaling and defense. - J. Soil Sci. Plant Physiol. 6: 172, 2024.
    3. Alagoz S.M., Lajayer B.A., Ghorbanpour M.: Proline and soluble carbohydrates biosynthesis and their roles in plants under abiotic stresses. - In: Ghorbanpour M., Shahid M.A. (ed.): Plant Stress Mitigators: Types, Techniques and Functions. Pp. 169-185. Academic Press, London 2023. Go to original source...
    4. Ali M.M., Shafique M.W., Gull S. et al.: Alleviation of heat stress in tomato by exogenous application of sulfur. - Horticulturae 7: 21, 2021. Go to original source...
    5. Anderson C.M., Mattoon E.M., Zhang N. et al.: High light and temperature reduce photosynthetic efficiency through different mechanisms in the C4 model Setaria viridis. - Commun. Biol. 4: 1092, 2021. Go to original source...
    6. Anjum N.A., Thangavel P., Rasheed F. et al.: Osmolytes: Efficient oxidative stress-busters in plants. - In: Ansari M.W., Singh A.K., Tuteja N. (ed.): Global Climate Change and Plant Stress Management. Pp. 399-409. John Wiley & Sons, Hoboken 2023. Go to original source...
    7. Canal M.V., Mansilla N., Gras D.E. et al.: Cytochrome c levels affect the TOR pathway to regulate growth and metabolism under energy-deficient conditions. - New Phytol. 241: 2039-2058, 2024. Go to original source...
    8. Carreiras J., Cruz-Silva A., Fonseca B. et al.: Improving grapevine heat stress resilience with marine plant growth-promoting rhizobacteria consortia. - Microorganisms 11: 856, 2023. Go to original source...
    9. Cha J.-Y., Kang S.-H., Ali I. et al.: Humic acid enhances heat stress tolerance via transcriptional activation of Heat-Shock Proteins in Arabidopsis. - Sci. Rep.-UK 10: 15042, 2020. Go to original source...
    10. Chen Y.-E., Liu W.-J., Su Y.-Q. et al.: Different response of photosystem II to short and long-term drought stress in Arabidopsis thaliana. - Physiol. Plantarum 158: 225-235, 2016. Go to original source...
    11. Chen Z., Chen C., Yang Y. et al.: Rhamnolipids supplement in salinized soils improves cotton growth through ameliorating soil properties and modifying rhizosphere communities. - Appl. Soil Ecol. 194: 105174, 2024. Go to original source...
    12. Cordelier S., Crouzet J., Gilliard G. et al.: Deciphering the role of plant plasma membrane lipids in response to invasion patterns: how could biology and biophysics help? - J. Exp. Bot. 73: 2765-2784, 2022. Go to original source...
    13. Crouzet J., Arguelles-Arias A., Dhondt-Cordelier S. et al.: Biosurfactants in plant protection against diseases: Rhamnolipids and lipopeptides case study. - Front. Bioeng. Biotechnol. 8: 1014, 2020. Go to original source...
    14. Demirevska-Kepova K., Holzer R., Simova-Stoilova L., Feller U.: Heat stress effects on ribulose-1,5-bisphosphate carboxylase/oxygenase, Rubisco binding protein and Rubisco activase in wheat leaves. - Biol. Plantarum 49: 521-525, 2005. Go to original source...
    15. Devi P., Awasthi R., Jha U. et al.: Understanding the effect of heat stress during seed filling on nutritional composition and seed yield in chickpea (Cicer arietinum L.). - Sci. Rep.-UK 13: 15450, 2023. Go to original source...
    16. Feng D., Jia X., Yan Z. et al.: Underlying mechanisms of exogenous substances involved in alleviating plant heat stress. - Plant Stress 10: 100288, 2023. Go to original source...
    17. Fortunato S., Lasorella C., Dipierro N. et al.: Redox signaling in plant heat stress response. - Antioxidants 12: 605, 2023. Go to original source...
    18. Gautam H., Fatma M., Sehar Z. et al.: Exogenously-sourced ethylene positively modulates photosynthesis, carbohydrate metabolism, and antioxidant defense to enhance heat tolerance in rice. - Int. J. Mol. Sci. 23: 1031, 2022. Go to original source...
    19. Godínez-Mendoza P.L., Rico-Chávez A.K., Ferrusquía-Jimenez N.I. et al.: Plant hormesis: Revising of the concepts of biostimulation, elicitation and their application in a sustainable agricultural production. - Sci. Total Environ. 894: 164883, 2023. Go to original source...
    20. Guntukula R.: Assessing the impact of climate change on Indian agriculture: Evidence from major crop yields. - J. Public Aff. 20: e2040, 2020. Go to original source...
    21. Guo T., Gull S., Ali M.M. et al.: Heat stress mitigation in tomato (Solanum lycopersicum L.) through foliar application of gibberellic acid. - Sci. Rep.-UK 12: 11324, 2022. Go to original source...
    22. Hu K., Xu S., Gao Y. et al.: Choline chloride and rhamnolipid combined with organic manures improve salinity tolerance, yield, and quality of tomato. - J. Plant Growth Regul. 42: 4118-4130, 2023. Go to original source...
    23. Hu S., Ding Y., Zhu C.: Sensitivity and responses of chloroplasts to heat stress in plants. - Front. Plant Sci. 11: 375, 2020. Go to original source...
    24. IPCC 2022: Climate Change 2022: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Pp. 3056. Cambridge University Press, Cambridge-New York 2022.
    25. Jahan M.S., Shu S., Wang Y. et al.: Melatonin pretreatment confers heat tolerance and repression of heat-induced senescence in tomato through the modulation of ABA- and GA-mediated pathways. - Front. Plant Sci. 12: 650955, 2021. Go to original source...
    26. Jespersen D., Zhang J., Huang B.: Chlorophyll loss associated with heat-induced senescence in bentgrass. - Plant Sci. 249: 1-12, 2016. Go to original source...
    27. Johann P.D., Erkek S., Zapatka M. et al.: A typical teratoid/rhabdoid tumors are comprised of three epigenetic subgroups with distinct enhancer landscapes. - Cancer Cell 29: 379-393, 2016. Go to original source...
    28. Kavi Kishor PB., Suravajhala P., Rathnagiri P., Sreenivasulu N.: Intriguing role of proline in redox potential conferring high temperature stress tolerance. - Front. Plant Sci. 13: 867531, 2022. Go to original source...
    29. Khan A.H., Min L., Ma Y. et al.: High-temperature stress in crops: male sterility, yield loss and potential remedy approaches. - Plant Biotechnol. J. 21: 680-697, 2023. Go to original source...
    30. Kim K., Portis Jr. A.R.: Temperature dependence of photosynthesis in Arabidopsis plants with modifications in Rubisco activase and membrane fluidity. - Plant Cell Physiol. 46: 522-530, 2005. Go to original source...
    31. Kim S.K., Kim Y.C., Lee S. et al.: Insecticidal activity of rhamnolipid isolated from Pseudomonas sp. EP-3 against green peach aphid (Myzus persicae). - J. Agr. Food Chem. 59: 934-938, 2011. Go to original source...
    32. Kreslavski V.D., Khudyakova A.Y., Kosobryukhov A.A. et al.: The effect of short-term heating on photosynthetic activity, pigment content, and pro-/antioxidant balance of A. thaliana phytochrome mutants. - Plants-Basel 12: 867, 2023. Go to original source...
    33. Kumar S., Kaushal N., Nayyar H., Gaur P.: Abscisic acid induces heat tolerance in chickpea (Cicer arietinum L.) seedlings by facilitated accumulation of osmoprotectants. - Acta Physiol. Plant. 34: 1651-1658, 2012. Go to original source...
    34. Lai C.-C., Huang Y.-C., Wei Y.-H., Chang J.-S.: Biosurfactant-enhanced removal of total petroleum hydrocarbons from contaminated soil. - J. Hazard. Mater. 167: 609-614, 2009. Go to original source...
    35. Lakshmi G., Beena R., Soni K.B. et al.: Exogenously applied plant growth regulator protects rice from heat-induced damage by modulating plant defense mechanism. - J. Crop Sci. Biotechnol. 26: 63-75, 2023. Go to original source...
    36. Li Q., Bian Y., Li R. et al.: Chitosan-enhanced heat tolerance associated with alterations in antioxidant defense system and gene expression in creeping bentgrass. - Grass Res. 3: 7, 2023. Go to original source...
    37. Liu G., Zhong H., Yang X. et al.: Advances in applications of rhamnolipids biosurfactant in environmental remediation: A review. - Biotechnol. Bioeng. 115: 796-814, 2018. Go to original source...
    38. Liu Q., Chen C., Chen Y. et al.: Intervention of rhamnolipid improves the rhizosphere microenvironment of cotton in desert saline lands. - Environ. Technol. Innov. 32: 103378, 2023. Go to original source...
    39. Lv W.-T., Lin B., Zhang M., Hua X.-J.: Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. - Plant Physiol. 156: 1921-1933, 2011. Go to original source...
    40. Meng X., Wang N., He H. et al.: Prunus persica transcription factor PpNAC56 enhances heat resistance in transgenic tomatoes. - Plant Physiol. Biochem. 182: 194-201, 2022. Go to original source...
    41. Mo X., Qian J., Liu P. et al.: Exogenous betaine enhances the protrusion vigor of rice seeds under heat stress by regulating plant hormone signal transduction and its interaction network. - Antioxidants 11: 1792, 2022. Go to original source...
    42. Monnier N., Cordier M., Dahi A. et al.: Semipurified rhamnolipid mixes protect Brassica napus against Leptosphaeria maculans early infections. - Phytopathology 110: 834-842, 2020. Go to original source...
    43. Monnier N., Furlan A., Botcazon C. et al.: Rhamnolipids from Pseudomonas aeruginosa are elicitors triggering Brassica napus protection against Botrytis cinerea without physiological disorders. - Front. Plant Sci. 9: 1170, 2018. Go to original source...
    44. Monnier N., Furlan A.L., Buchoux S. et al.: Exploring the dual interaction of natural rhamnolipids with plant and fungal biomimetic plasma membranes through biophysical studies. -Int. J. Mol. Sci. 20: 1009, 2019. Go to original source...
    45. Motta A.M., Donato M., Mobbili G. et al.: Unveiling the mono-rhamnolipid and di-rhamnolipid mechanisms of action upon plasma membrane models. - J. Colloid Interf. Sci. 624: 579-592, 2022. Go to original source...
    46. Mukhtar T., Ali F., Rafique M. et al.: Biochemical characterization and potential of Bacillus safensis strain SCAL1 to mitigate heat stress in Solanum lycopersicum L. - J. Plant Growth Regul. 42: 523-538, 2023. Go to original source...
    47. Nabavi S.M., ©amec D., Tomczyk M. et al.: Flavonoid biosynthetic pathways in plants: Versatile targets for metabolic engineering. - Biotechnol. Adv. 38: 107316, 2020. Go to original source...
    48. Niu Y., Xiang Y.: An overview of biomembrane functions in plant responses to high-temperature stress. - Front. Plant Sci. 9: 915, 2018. Go to original source...
    49. Onlamool T., Saimmai A., Maneerat S.: Antifungal activity of rhamnolipid biosurfactant produced by Pseudomonas aeruginosa A4 against plant pathogenic fungi. - Trends Sci. 20: 6524, 2022. Go to original source...
    50. Park B.-M., Jeong H.-B., Yang E.-Y. et al.: Differential responses of cherry tomatoes (Solanum lycopersicum) to long-term heat stress. - Horticulturae 9: 343, 2023. Go to original source...
    51. Paul P., Mesihovic A., Chaturvedi P. et al.: Structural and functional heat stress responses of chloroplasts of Arabidopsis thaliana. - Genes-Basel 11: 650, 2020. Go to original source...
    52. Perkins-Kirkpatrick S.E., Gibson P.B.: Changes in regional heatwave characteristics as a function of increasing global temperature. - Sci. Rep.-UK 7: 12256, 2017. Go to original source...
    53. Pierre E., Marcelo P., Croutte A. et al.: Impact of rhamnolipids (RLs), natural defense elicitors, on shoot and root proteomes of Brassica napus by a Tandem Mass Tags (TMTs) labeling approach. - Int. J. Mol. Sci. 24: 2390, 2023. Go to original source...
    54. Platel R., Lucau-Danila A., Baltenweck R. et al.: Bioinspired rhamnolipid protects wheat against Zymoseptoria tritici through mainly direct antifungal activity and without major impact on leaf physiology. - Front. Plant Sci. 13: 878272, 2022. Go to original source...
    55. Porcar-Castell A., Pfündel E., Korhonen J.F.J., Juurola E.: A new monitoring PAM fluorometer (MONI-PAM) to study the short- and long-term acclimation of photosystem II in field conditions. - Photosynth. Res. 96: 173-179, 2008. Go to original source...
    56. Prabakaran G., Hoti S.L., Rao H.S.P., Vijjapu S.: Di-rhamnolipid is a mosquito pupicidal metabolite from Pseudomonas fluorescens (VCRC B426). - Acta Trop. 148: 24-31, 2015. Go to original source...
    57. Pshybytko N., Kruk J., Lysenko E. et al.: Heat-induced modifications of photosynthetic electron flows in Hordeum vulgare leaves of different age. - Environ. Exp. Bot. 206: 105151, 2023. Go to original source...
    58. Raja V., Qadir S.U., Alyemeni M.N., Ahmad P.: Impact of drought and heat stress individually and in combination on physio-biochemical parameters, antioxidant responses, and gene expression in Solanum lycopersicum. - 3 Biotech 10: 208, 2020. Go to original source...
    59. Rajendran H.K., Das M., Chandrasekar R. et al.: UiO-66 octahedrons for adsorptive removal of direct blue-6: process optimization, interaction mechanism, and phytotoxicity assessment. - Environ. Sci. Pollut. Res. 30: 114264-114282, 2023. Go to original source...
    60. Rath J.R., Pandey J., Yadav R.M. et al.: Temperature-induced reversible changes in photosynthesis efficiency and organization of thylakoid membranes from pea (Pisum sativum). - Plant Physiol. Biochem. 185: 144-154, 2022. Go to original source...
    61. Rehman A., Khan I., Farooq M.: Secondary metabolites mediated reproductive tolerance under heat stress in plants. - J. Plant Growth Regul. 43: 2993-3011, 2024. Go to original source...
    62. Robineau M., Le Guenic S., Sanchez L. et al.: Synthetic mono-rhamnolipids display direct antifungal effects and trigger an innate immune response in tomato against Botrytis cinerea. -Molecules 25: 3108, 2020. Go to original source...
    63. Ru C., Hu X., Chen D. et al.: Photosynthetic, antioxidant activities, and osmoregulatory responses in winter wheat differ during the stress and recovery periods under heat, drought, and combined stress. - Plant Sci. 327: 111557, 2023. Go to original source...
    64. Salehi F., Rahnama A., Meskarbashee M. et al.: Physiological and metabolic changes of safflower (Carthamus tinctorius L.) cultivars in response to terminal heat stress. - J. Plant Growth Regul. 42: 6585-6600, 2023. Go to original source...
    65. Samtani H., Sharma A., Khurana J.P., Khurana P.: Thermosensing in plants: Deciphering the mechanisms involved in heat sensing and their role in thermoresponse and thermotolerance. -Environ. Exp. Bot. 203: 105041, 2022. Go to original source...
    66. Sanchez L., Courteaux B., Hubert J. et al.: Rhamnolipids elicit defense responses and induce disease resistance against biotrophic, hemibiotrophic, and necrotrophic pathogens that require different signaling pathways in Arabidopsis and highlight a central role for salicylic acid. - Plant Physiol. 160: 1630-1641, 2012. Go to original source...
    67. Schellenberger R., Crouzet J., Nickzad A. et al.: Bacterial rhamnolipids and their 3-hydroxyalkanoate precursors activate Arabidopsis innate immunity through two independent mechanisms. - PNAS 118: e2101366118, 2021. Go to original source...
    68. Shaffique S., Khan M.A., Wani S.H. et al.: A review on the role of endophytes and plant growth promoting rhizobacteria in mitigating heat stress in plants. - Microorganisms 10: 1286, 2022. Go to original source...
    69. Sharma A., Kumar V., Shahzad B. et al.: Photosynthetic response of plants under different abiotic stresses: a review. - J. Plant Growth Regul. 39: 509-531, 2020. Go to original source...
    70. Sharma S., Singh V., Tanwar H. et al.: Impact of high temperature on germination, seedling growth and enzymatic activity of wheat. - Agriculture 12: 1500, 2022. Go to original source...
    71. Sihag P., Kumar U., Sagwal V. et al.: Effect of terminal heat stress on osmolyte accumulation and gene expression during grain filling in bread wheat (Triticum aestivum L.). - Plant Genome 17: e20307, 2024. Go to original source...
    72. Singh A., Kumar A., Yadav S., Singh I.K.: Reactive oxygen species-mediated signaling during abiotic stress. - Plant Gene 18: 100173, 2019. Go to original source...
    73. Singh M., Kumar J., Singh S. et al.: Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. - Rev. Environ. Sci. Biotechnol. 14: 407-426, 2015. Go to original source...
    74. Smith A., Gentile B.R., Xin Z., Zhao D.: The effects of heat stress on male reproduction and tillering in Sorghum bicolor. - Food Energ. Secur. 12: e510, 2023. Go to original source...
    75. Soberón-Chávez G., Lépine F., Déziel E.: Production of rhamnolipids by Pseudomonas aeruginosa. - Appl. Microbiol. Biot. 68: 718-725, 2005. Go to original source...
    76. Stone P.: The effects of heat stress on cereal yield and quality. -In: Basra A. (ed.): Crop Responses and Adaptations to Temperature Stress. Pp. 243-291. CRC Press, Boca Raton 2023. Go to original source...
    77. Su F., Gilard F., Guérard F. et al.: Spatio-temporal responses of Arabidopsis leaves in photosynthetic performance and metabolite contents to Burkholderia phytofirmans PsJN. - Front. Plant Sci. 7: 403, 2016. Go to original source...
    78. Su Y., Huang Y., Dong X. et al.: Exogenous methyl jasmonate improves heat tolerance of perennial ryegrass through alteration of osmotic adjustment, antioxidant defense, and expression of jasmonic acid-responsive genes. - Front. Plant Sci. 12: 664519, 2021. Go to original source...
    79. Suzuki N.: Fine tuning of ROS, redox and energy regulatory systems associated with the functions of chloroplasts and mitochondria in plants under heat stress. - Int. J. Mol. Sci. 24: 1356, 2023. Go to original source...
    80. Suzuki N., Mittler R.: Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction. -Physiol. Plantarum 126: 45-51, 2006. Go to original source...
    81. Tafesse E.G., Warkentin T.D., Bueckert R.A.: Canopy architecture and leaf type as traits of heat resistance in pea. - Field Crop. Res. 241: 107561, 2019. Go to original source...
    82. Todorov D.T., Karanov E.N., Smith A.R., Hall M.A.: Chlorophyllase activity and chlorophyll content in wild type and eti5 mutant of Arabidopsis thaliana subjected to low and high temperatures. - Biol. Plantarum 46: 633-636, 2003. Go to original source...
    83. Varnier A.-L., Sanchez L., Vatsa P. et al.: Bacterial rhamnolipids are novel MAMPs conferring resistance to Botrytis cinerea in grapevine. - Plant Cell Environ. 32: 178-193, 2009. Go to original source...
    84. von Caemmerer S., Farquhar G.D.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. - Planta 153: 376-387, 1981. Go to original source...
    85. Wahid A.: Physiological implications of metabolite biosynthesis for net assimilation and heat-stress tolerance of sugarcane (Saccharum officinarum) sprouts. - J. Plant Res. 120: 219-228, 2007. Go to original source...
    86. Wahid A., Gelani S., Ashraf M., Foolad M.R.: Heat tolerance in plants: an overview. - Environ. Exp. Bot. 61: 199-223, 2007. Go to original source...
    87. Wang L., Ma K.-B., Lu Z.-G. et al.: Differential physiological, transcriptomic and metabolomic responses of Arabidopsis leaves under prolonged warming and heat shock. - BMC Plant Biol. 20: 86, 2020. Go to original source...
    88. Wang Q.-L., Chen J.-H., He N.-Y., Guo F.-Q.: Metabolic reprogramming in chloroplasts under heat stress in plants. - Int. J. Mol. Sci. 19: 849, 2018. Go to original source...
    89. Wang W., Xie Y., Liu C., Jiang H.: The exogenous application of brassinosteroids confers tolerance to heat stress by increasing antioxidant capacity in soybeans. - Agriculture 12: 1095, 2022. Go to original source...
    90. Wang X., Altaf M.A., Hao Y. et al.: Effect of heat stress on root architecture, photosynthesis, and antioxidant profile of water spinach (Ipomoea aquatica Forsk) seedlings. - Horticulturae 9: 923, 2023. Go to original source...
    91. Wassie M., Zhang W., Zhang Q. et al.: Exogenous salicylic acid ameliorates heat stress-induced damages and improves growth and photosynthetic efficiency in alfalfa (Medicago sativa L.). - Ecotox. Environ. Safe. 191: 110206, 2020. Go to original source...
    92. Wedler M., Pinto J.G., Hochman A.: More frequent, persistent, and deadly heat waves in the 21st century over the Eastern Mediterranean. - Sci. Total Environ. 870: 161883, 2023. Go to original source...
    93. Xalxo R., Yadu B., Chandra J. et al.: Alteration in carbohydrate metabolism modulates thermotolerance of plant under heat stress. - In: Wani S.H., Kumar V. (ed.): Heat Stress Tolerance in Plants: Physiological, Molecular and Genetic Perspectives. Pp. 77-115. John Wiley & Sons, Hoboken 2020. Go to original source...
    94. Yang D., Li Y., Shi Y. et al.: Exogenous cytokinins increase grain yield of winter wheat cultivars by improving stay-green characteristics under heat stress. - PLoS ONE 11: e0155437, 2016. Go to original source...
    95. Zahra N., Hafeez M.B., Ghaffar A. et al.: Plant photosynthesis under heat stress: Effects and management. - Environ. Exp. Bot. 206: 105178, 2023. Go to original source...
    96. Zhang L., Chang Q., Hou X. et al.: The effect of high-temperature stress on the physiological indexes, chloroplast ultrastructure, and photosystems of two herbaceous peony cultivars. - J. Plant Growth Regul. 42: 1631-1646, 2023a. Go to original source...
    97. Zhang X., Yang Z., Wang L. et al.: The effects of plant growth-promoting rhizobacteria on plants under temperature stress: A meta-analysis. - Rhizosphere 28: 100788, 2023b. Go to original source...
    98. Zhang Z., Lan M., Han X. et al.: Response of ornamental pepper to high-temperature stress and role of exogenous salicylic acid in mitigating high temperature. - J. Plant Growth Regul. 39: 133-146, 2020. Go to original source...
    99. Zhao C., Liu B., Piao S. et al.: Temperature increase reduces global yields of major crops in four independent estimates. - PNAS 114: 9326-9331, 2017. Go to original source...
    100. Zhao F., Wang B., Yuan M., Ren S.: Comparative study on antimicrobial activity of mono-rhamnolipid and di-rhamnolipid and exploration of cost-effective antimicrobial agents for agricultural applications. - Microb. Cell Fact. 21: 221, 2022. Go to original source...
    101. Zhao J., Lu Z., Wang L., Jin B.: Plant responses to heat stress: physiology, transcription, noncoding RNAs, and epigenetics. -Int. J. Mol. Sci. 22: 117, 2021. Go to original source...
    102. Zulfiqar F., Ashraf M.: Proline alleviates abiotic stress induced oxidative stress in plants. - J. Plant Growth Regul. 42: 4629-4651, 2023. Go to original source...

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