Responses of hazelnut shell–derived carbon nanodots to drought stress in wheat (Triticum aestivum L.): relationships with photosynthetic performance and phenolic composition

Öz

Drought is one of the major stress factors causing substantial yield losses in wheat production, and current agricultural practices often remain insufficient to enhance stress tolerance. In recent years, carbon nanodots have emerged as innovative nanomaterials in plant stress due to their high biocompatibility, low toxicity, and strong antioxidant properties. Carbon nanodots synthesized from phenolic-rich lignocellulosic wastes offer an economically and environmentally sustainable approach. In this context, although hazelnut shell, characterized by its high carbon and phenolic content, represents an ideal raw material, no study has investigated how carbon nanodots derived from this material modulate physiological and metabolic responses to drought stress in wheat. This study aimed to determine the holistic effects of hazelnut shell–derived carbon nanodots on gas exchange, PSII photochemistry, and phenolic metabolism of wheat seedlings exposed to PEG-induced drought stress. Wheat seedlings were treated with HNS-CNDs for 72 hours, followed by 48 hours of 10% PEG stress. Compared with PEG alone, the HNS-CND+PEG treatment increased photosynthetic rate by 83.8%, transpiration by 61.4%, stomatal conductance by 96.2%, and intercellular CO₂ concentration by 69.4%. Chlorophyll fluorescence measurements revealed increases of 6.7% in Fv/Fm and 12.3% in ΦPSII, whereas NPQ decreased by 52.8%. Phenolic analyses showed increases of 33.5% in gallic acid, 12.5% in pyrogallol, and 5.3% in (–)-epicatechin, along with decreases of 25.1% in vanillic acid, 59.7% in p-coumaric acid, 80% in chlorogenic acid, 48.8% in rutin, 20.6% in quercetin, and 22% in baicalein. Overall, the findings demonstrate that HNS-CNDs significantly enhance drought tolerance in wheat by restructuring photosynthetic capacity, stabilizing PSII photochemistry, and redirecting phenolic flux toward more energy-efficient antioxidant compounds.

Anahtar Kelimeler

• Carbondot
• photochemical efficiency
• antioxidant
• wheat

Fındık kabuğu kökenli karbon nanodotlarının buğday (Triticum aestivum L.) da kuraklık toleransına etkileri: fotosentez kapasitesi ve fenolik bileşiminin iyileştirilmesi

Öz

Kuraklık, buğday üretiminde ciddi verim kayıplarına yol açan başlıca stres faktörlerinden biridir ve mevcut tarımsal uygulamalar bitkinin stres dayanıklılığını artırmada çoğu zaman yetersiz kalmaktadır. Son yıllarda karbon nanodotlar, yüksek biyouyumlulukları, düşük toksisiteleri ve güçlü antioksidan özellikleri nedeniyle bitki stresine dikkat çeken yenilikçi nanomateryaller hâline gelmiştir. Fenolik açıdan zengin lignoselülozik atıklardan sentezlenen karbon nanodotların ekonomik ve çevresel açıdan sürdürülebilir bir yaklaşım sunmaktadır. Bu bağlamda, yüksek karbon ve fenolik içeriğiyle öne çıkan fındık kabuğu ideal bir hammadde olmasına rağmen, bu materyalden üretilen karbon nanodotların buğdayda kuraklık stresine yönelik fizyolojik ve metabolik yanıtları nasıl düzenlediğine ilişkin literatürde herhangi bir çalışma bulunmamaktadır. Bu çalışma, fındık kabuğu kökenli karbon nanodotların (HNS-CND) PEG ile oluşturulan kuraklık stresi altında buğday fidelerinin gaz değişimi, PSII fotokimyası ve fenolik metabolizması üzerindeki bütüncül etkilerini belirlemeyi amaçlamıştır. Buğday fidelerine 72 saat boyunca HNS-CND uygulanmış, ardından 48 saat %10 PEG stresi uygulanmıştır. HNS-CND+PEG uygulaması, PEG’e kıyasla fotosentetik hızı %83.8, transpirasyonu %61.4, stoma iletkenliğini %96.2 ve hücresel CO₂ konsantrasyonunu %69.4 oranında artırmıştır. Klorofil floresans ölçümleri, Fv/Fm ve ΦPSII’nin sırasıyla %6.7 ve %12.3 arttığını, NPQ’nun ise %52.8 azaldığını göstermiştir. Fenolik analizler, gallik asitte %33.5, pirogallolde %12.5 ve (–)-epicatechin’de %5.3 artış; vanilik asitte %25.1, p-kumarik asitte %59.7, klorojenik asitte %80, rutin’de %48.8, quersetin’de %20.6 ve baikaleinde %22 azalma göstermiştir. HNS-CND’lerin fotosentetik kapasiteyi yeniden yapılandırarak, PSII fotokimyasını stabilize ederek ve fenolik akışı enerji açısından daha verimli antioksidanlara yönlendirerek buğdayda kuraklık toleransını belirgin şekilde artırdığını göstermektedir.

Anahtar Kelimeler

• Karbondot
• fotokimyasal verimlilik
• antioksidan
• buğday

Kaynakça

1. S.M. Rodrigues, P. Demokritou, N. Dokoozlian, C.O. Hendren, B. Karn, M.S. Mauter, G.V. Lowry, Nanotechnology for sustainable food production: promising opportunities and scientific challenges, Environ Sci Nano, 4, 2017, 767–781
2. N.M. Alabdallah, M.M. Hasan, Plant-based green synthesis of silver nanoparticles and its effective role in abiotic stress tolerance in crop plants, Saudi J Biol Sci, 28(10), 2021, 5631–5639
3. M.K. Hasan, L. Kumar, Yield trends and variabilities explained by climatic change in coastal and non-coastal areas of Bangladesh, Sci Total Environ, 795, 2021, 148814
4. B.E. Genç, Global Politics of Food Security, Master’s Thesis, Middle East Technical University, 2022
5. M. Mortimore, Adapting to drought in the Sahel: lessons for climate change, Wiley Interdiscip Rev Clim Change, 1(1), 2010, 134–143
6. B. Sharma, L. Yadav, A. Shrestha, S. Shrestha, M. Subedi, S. Subedi, J. Shrestha, Drought stress and its management in wheat (Triticum aestivum L.): a review, Agric Sci Technol, 14(1), 2022
7. M.F. Seleiman, N. Al-Suhaibani, N. Ali, M. Akmal, M. Alotaibi, Y. Refay, M.L. Battaglia, Drought stress impacts on plants and different approaches to alleviate its adverse effects, Plants, 10(2), 2021, 259
8. U. Sahin, M. Ekinci, S. Ors, M. Turan, S. Yildiz, E. Yildirim, Effects of salinity and drought on physiological and biochemical traits of cabbage, Sci Hortic, 240, 2018, 196–204

9. M.F. Quartacci, C. Pinzino, C.L. Sgherri, F. Navari-Izzo, Lipid composition and protein dynamics in thylakoids of wheat cultivars differently sensitive to drought, Plant Physiol, 108(1), 1995, 191–197
10. C.A. Jaleel, P. Manivannan, A. Wahid, M. Farooq, H.J. Al-Juburi, R. Somasundaram, R. Panneerselvam, Drought stress plants: morphological characteristics and pigments composition, Int J Agric Biol, 11, 2009, 100–105
11. D.E. Rao, K.V. Chaitanya, Morphological and physiological responses of soybean cultivars to drought stress, J Crop Sci Biotechnol, 22, 2019, 355–362
12. M.U. Hassan, M. Aamer, M.U. Chattha, T. Haiying, B. Shahzad, L. Barbanti, The critical role of zinc in plants facing drought stress, Agriculture, 10(9), 2020, 396
13. A. Rasheed, H. Li, M.M. Tahir, A. Mahmood, M. Nawaz, A.N. Shah, Z. Wu, Role of nanoparticles in plant biochemical, physiological and molecular responses under drought stress: a review, Front Plant Sci, 13, 2022, 976179
14. A. Michalak, Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress, Pol J Environ Stud, 15(4), 2006
15. I. Sperdouli, M. Moustakas, Differential response of photosystem II photochemistry in young and mature leaves of Arabidopsis thaliana to the onset of drought stress, Acta Physiol Plant, 34(4), 2012, 1267–1276
16. J. Flexas, J. Bota, F. Loreto, G. Cornic, T.D. Sharkey, Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants, Plant Biol, 6(3), 2004, 269–279
17. R. Nair, S.H. Varghese, B.G. Nair, T. Maekawa, Y. Yoshida, D.S. Kumar, Nanoparticulate material delivery to plants, Plant Sci, 179(3), 2010, 154–163
18. N.A. Anjum, S.S. Gill, A.C. Duarte, E. Pereira, Oxidative stress biomarkers and antioxidant defense in plants exposed to metallic nanoparticles, Nanomaterials and Plant Potential, Springer International Publishing, Cham, 2019
19. M. Inam, I. Attique, M. Zahra, A.K. Khan, M. Hahim, C. Hano, S. Anjum, Metal oxide nanoparticles and plant secondary metabolism: unraveling the game-changer nano-elicitors, Plant Cell Tissue Organ Cult, 155(2), 2023, 327–344
20. H. Ventribout-Rodríguez, Circular Biobased Synthesis of Carbon Nano Dots for Agricultural Applications, 2025
21. S. Venkataraman, A.K. Sundramoorthy, Waste-derived carbon nanomaterials for electrochemical applications: toward a circular and sustainable future, RSC Adv, 16(1), 2026, 733–747
22. B. Guo, G. Liu, W. Li, C. Hu, B. Lei, J. Zhuang, M. Zheng, Y. Liu, The role of carbon dots in the life cycle of crops, Ind Crops Prod, 187, 2022, 115427
23. C. Ozfidan-Konakci, E. Yildiztugay, B. Arikan-Abdulveli, F.N. Alp-Turgut, C. Baslak, M. Yıldırım, The characterization of plant-derived carbon dots and their responses on chlorophyll a fluorescence kinetics, radical accumulation in guard cells, cellular redox state and antioxidant system in chromium-stressed Lactuca sativa, Chemosphere, 356, 2024, 141937
24. F. Chen, N. Yang, X. Huang, J. Lin, H. Zhang, X. Zhang, Y. Liu, W. Li, B. Lei, Carbon dots alleviate photoinhibition and enhance photosynthesis in Chlorella pyrenoidosa, Chem Eng J, in press, 2025
25. Q. Chen, X. Cao, X. Nie, Y. Li, T. Liang, L. Ci, Alleviation role of functional carbon nanodots for tomato growth and soil environment under drought stress, J Hazard Mater, 423, 2022, 127260
26. M. Ge, Y. Wang, X. Liu, J. Zhang, L. Chen, H. Wang, Y. Liu, Carbon dots promote tomato growth and yield via photosynthesis enhancement and leaf senescence delay, J Plant Physiol, 302, 2025, 154981
27. H. Salehi, B. Miras-Moreno, A. Chehregani Rad, Y. Pii, T. Mimmo, S. Cesco, L. Lucini, Relatively low dosages of CeO₂ nanoparticles in the solid medium induce adjustments in the secondary metabolism and ionomic balance of bean (Phaseolus vulgaris L.) roots and leaves, J Agric Food Chem, 68(1), 2019, 67–76
28. E. Nourozi, B. Hosseini, R. Maleki, B. Abdollahi Mandoulakani, Iron oxide nanoparticles: a novel elicitor to enhance anticancer flavonoid production and gene expression in Dracocephalum kotschyi hairy-root cultures, J Sci Food Agric, 99(14), 2019, 6418–6430
29. K.M. Al Nooh, A.M. Salim, W.S. Faizy, M.K. Musa, D.T.A. Al-Heetimi, Synergistic effects of plant growth regulators and Fe₃O₄ nanoparticles on in vitro organogenesis and bioactive compound production in Hypericum perforatum, BMC Plant Biol, 25, 2025, 1335
30. Q. Wang, S. Xu, L. Zhong, X. Zhao, L. Wang, Effects of zinc oxide nanoparticles on growth, development, and flavonoid synthesis in Ginkgo biloba, Int J Mol Sci, 24(21), 2023, 15775
31. B. Gheisary, M. Fattahi, Selenium and zinc oxide nanoparticles stimulate product quality, phenolic content, antioxidant activity, and shikonin production in Italian bugloss (Echium italicum L.) plantlets under in vitro conditions, BMC Plant Biol, 25, 2025, 1465
32. B. Zhang, L.P. Zheng, W.Y. Li, J.W. Wang, Stimulation of artemisinin production in Artemisia annua hairy roots by Ag–SiO₂ core–shell nanoparticles, Curr Nanosci, 9(3), 2013, 363–370
33. M. Comotto, A.A. Casazza, B. Aliakbarian, V. Caratto, M. Ferretti, P. Perego, Influence of TiO₂ nanoparticles on growth and phenolic compounds production in photosynthetic microorganisms, Sci World J, 2014, 961437
34. S. Samadi, M.J. Saharkhiz, M. Azizi, L. Samiei, M. Ghorbanpour, Exposure to single-walled carbon nanotubes differentially affects in vitro germination, biochemical and antioxidant properties of Thymus daenensis Celak seedlings, BMC Plant Biol, 23(1), 2023, 579
35. S. Samadi, M.J. Saharkhiz, M. Azizi, L. Samiei, M. Ghorbanpour, Multi-walled carbon nanotubes stimulate growth, redox reactions and biosynthesis of antioxidant metabolites in Thymus daenensis Celak in vitro, Chemosphere, 249, 2020, 126069
36. C. Liné, F. Manent, A. Wolinski, E. Flahaut, C. Larue, Comparative study of response of four crop species exposed to carbon nanotube contamination in soil, Chemosphere, 274, 2021, 129854
37. D.L. McGehee, M.H. Lahiani, F. Irin, M.J. Green, M.V. Khodakovskaya, Multiwalled carbon nanotubes dramatically affect the fruit metabolome of exposed tomato plants, ACS Appl Mater Interfaces, 9(38), 2017, 32430–32435
38. TUIK, Türkiye İstatistik Kurumu, Bitkisel Üretim İstatistikleri 2022: Meyve ürünleri, içecek ve baharat bitkileri üretim miktarları – hazelnut production in shell, 2022
39. A. Gümrükçüoğlu, Doğal atık ürünlerden fındık kabuğundan karbon nano noktaların sentezi ve analitik özelliklerinin incelenmesi, Doctoral Thesis, Karadeniz Teknik University, Institute of Science, 2022
40. L. Yan, Y. Shi, Effect of drought stress on growth and development in winter wheat with Aquasorb-fertilizer, Adv J Food Sci Technol, 5(11), 2013, 1502–1504
41. E. Yildirim, İ. Güvenç, M. Turan, A. Karatas, Effect of foliar urea application on quality, growth, mineral uptake and yield of broccoli (Brassica oleracea L. var. italica), Plant Soil Environ, 53(3), 2007, 120–128
42. M. Demiralay, Exogenous acetone O-(4-chlorophenylsulfonyl) oxime alleviates Cd stress in maize, Physiol Mol Biol Plants, 28, 2022, 2069–2083
43. H. Nar, A. Saglam, R. Terzi, Z. Várkonyi, A. Kadioglu, Leaf rolling and PSII efficiency under drought in Ctenanthe setosa, Photosynthetica, 47, 2009, 429–436
44. Y.E. Chen, H.T. Mao, N. Wu, A. Khan, A.M.U. Din, C.B. Ding, Photosynthetic apparatus tolerance to Cd stress in rice cultivars, Acta Physiol Plant, 41(12), 2019, 1–13
45. G.H. Krause, E. Weis, Chlorophyll fluorescence and photosynthesis: the basics, Annu Rev Plant Biol, 42, 1991, 313–349
46. O. Van Kooten, J.F.H. Snel, The use of chlorophyll fluorescence nomenclature in plant stress physiology, Photosynth Res, 25, 1990, 147–150
47. B. Genty, J.M. Briantais, N.R. Baker, Quantum yield and quenching of chlorophyll fluorescence, Biochim Biophys Acta, 990, 1989, 87–92
48. A. Uysal, G. Zengin, Y. Durak, A. Aktumsek, Screening for antioxidant and antimutagenic properties of extracts from Centaurea pterocaula as well as their enzyme inhibitory potentials, Marmara Pharm J, 20, 2016, 232–242
49. İ. Akbulut, E. Gürbüz, A. Rayman Ergün, T. Baysal, Drying of apricots treated with Ginkgo biloba plant extract and determination of the quality properties, J Adv Res Nat Appl Sci, 7(1), 2021, 145–159
50. T. Seal, Quantitative HPLC analysis of phenolic acids, flavonoids and ascorbic acid in four different solvent extracts of two wild edible leaves, Sonchus arvensis and Oenanthe linearis, J Appl Pharm Sci, 6(2), 2016, 157–166
51. Y. Alan, Chemical changes of potential probiotic Lactiplantibacillus plantarum and Lactobacillus pentosus starter cultures in natural Gemlik type black olive fermentation, Food Chem, 434, 2023, 137472
52. W. Cheng, X. Wang, H. Hu, Closed-loop enhancement of plant photosynthesis via biomass-derived carbon dots in biohybrids, Commun Mater, 6, 2025, 40
53. Z. Ji, A. Sheardy, Z. Zeng, W. Zhang, H. Chevva, K. Allado, Z. Yin, J. Wei, Tuning the functional groups on carbon nanodots and antioxidant studies, Molecules, 24(1), 2019, 152
54. P. Ashkavand, M. Zarafshar, M. Tabari, J. Mirzaie, A. Nikpour, S.K. Bordbar, G.G. Striker, Application of SiO₂ nanoparticles as pretreatment alleviates the impact of drought on the physiological performance of Prunus mahaleb (Rosaceae), Bol Soc Argent Bot, 53(2), 2018, 1–10
55. M. El-Zohri, N.A. Al-Wadaani, S.O. Bafeel, Foliar-applied green zinc oxide nanoparticles alleviate drought-induced oxidative stress in tomato, Plants, 10(11), 2021, 2400
56. Z. Kaleem, S. Ali, K. Zhang, A. Manan, A. Shahzad, A.E. Mohammed, W. Zhou, Optimal nanocopper enhances cadmium tolerance in Brassica napus by regulating nutritional homeostasis, antioxidant defense, chelation capacity, and cellular changes, J Plant Growth Regul, 2025, 1–17
57. K. Abinaya, K. Raja, P.S. Sathya Moorthy, A. Senthil, K. Chandrakumar, Enhancing drought tolerance in blackgram (Vigna mungo L. Hepper) through physiological and biochemical modulation by peanut shell carbon dots, Sci Rep, 15(1), 2025, 5475
58. K. Maxwell, G.N. Johnson, Chlorophyll fluorescence—a practical guide, J Exp Bot, 51(345), 2000, 659–668
59. M. Kaleem, A.A. Shah, S. Usman, W. Xu, A.A. Alsahli, MgO nanoparticles improve drought resilience in coriander, ACS Omega, 10(30), 2025, 32813–32828
60. P. Rai-Kalal, A. Jajoo, Seed nanopriming by silicon oxide improves drought tolerance in wheat, Environ Exp Bot, 186, 2021, 104436
61. Z. Karimian, L. Samiei, ZnO nanoparticles efficiently enhance drought tolerance in Dracocephalum kotschyi through altering physiological, biochemical and elemental contents, Front Plant Sci, 14, 2023, 1063618
62. A. Sharma, B. Shahzad, A. Rehman, R. Bhardwaj, M. Landi, B. Zheng, Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress, Molecules, 24(13), 2019, 2452
63. O. Chen, L. Deng, C. Ruan, L. Yi, K. Zeng, Pichia galeiformis induces resistance in postharvest citrus by activating the phenylpropanoid biosynthesis pathway, J Agric Food Chem, 69(8), 2021, 2619–2631
64. Y. Li, R. Xu, J. Qi, S. Lei, Q. Han, C. Ma, H. Wang, Transcriptional and metabolic mechanism of carbon dots enhancing rice growth and resistance by promoting root development, bioRxiv, 2024
65. V. Martinez, T.C. Mestre, F. Rubio, A. Girones-Vilaplana, D.A. Moreno, R. Mittler, R.M. Rivero, Accumulation of flavonols over hydroxycinnamic acids favors oxidative damage protection under abiotic stress, Front Plant Sci, 7, 2016, 838
66. S. Munné-Bosch, K. Schwarz, L. Alegre, Enhanced formation of α-tocopherol and highly oxidized abietane diterpenes in water-stressed rosemary plants, Plant Physiol, 121(3), 1999, 1047–1052
67. P. Rampino, S. Pataleo, C. Gerardi, G. Mita, C. Perrotta, Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes, Plant Cell Environ, 29(12), 2006, 2143–2152
68. Y. Xu, L. Liang, G. Lisak, Blue-emissive antioxidant carbon dots enhance drought resistance of pea (Pisum sativum L.), ACS Appl Mater Interfaces, 16, 2024, 39090-39103
69. M.U. Zia, P.T. Sambasivam, D. Chen, S.A. Bhuiyan, R. Ford, Q. Li, A carbon dot toolbox for managing biotic and abiotic stresses in crop production systems, EcoMat, 6, 2024, e12451.