Abstract
Water deficiency is a threat to food security and limits the yield of vegetables, including arugula (Eruca sativa Mill.). Despite the increasing use of amino acid-based bioregulators to mitigate water stress, the effects of carnitine as a water deficit mitigation agent have not yet been elucidated. Here, the effects of different carnitine concentrations on the morphophysiology of arugula plants under different water deficit conditions were evaluated. Plants were irrigated to 100%, 80%, 60%, or 20% field capacity (FC) with water alone (control) or water with carnitine at concentrations of 100 µM or 100 mM. Forty days after sowing, the photosynthetic pigment content, gas exchange, chlorophyll a fluorescence, electrolyte leakage, relative water content, and growth parameters were measured. The application of 100 µM carnitine to well-watered plants (80%-FC) and plants under moderate water stress (60%-FC) resulted in greater photosynthetic plasticity, as demonstrated by the unaltered maximum quantum yield of photosystem II. However, under severe water deficit (20%-FC), plants treated with carnitine exhibited a reduced maximum quantum yield of photosystem II, indicating damage to photosystem II. Application of 100 µM carnitine increased the shoot biomass of arugula plants exposed to 80%-FC conditions and reduced electrolyte leakage in plants receiving 60%-FC irrigation. In contrast, 100 mM carnitine was toxic to arugula, hampering overall plant growth. The results suggest that low carnitine concentrations have the potential to mitigate the effects of moderate water stress on arugula, maintain membrane integrity and photosynthetic plasticity, and enhance shoot growth, which indicates this amino acid as a promising biostimulant in plants.
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References
Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image Processing with ImageJ. Biophotonics Int 11:36–42
AGRITEMPO Dados meteorológicos. https://www.agritempo.gov.br/agritempo/jsp/PesquisaClima/index.jsp?siglaUF=PB. Accessed 10 Feb 2022. Bananeiras
Aissani N, Urgeghe PP, Oplos C, Saba M, Tocco G, Petretto GL, Caboni P (2015) Nematicidal activity of the volatilome of Eruca sativa on Meloidogyne incognita. J Agric Food Chem 63:6120–6125. https://doi.org/10.1021/acs.jafc.5b02425
Akino A, Soorianathasundaram K, Paramaguru P, Jeyakumar P, Muthulakshmi P (2021) Bioregulators induced modulation of leaf physiological attributes and severity of papaya ring spot viral disease symptom expression in papaya. Madras Agric J 108:123–131
Bajji M, Kinet JM, Lutts S (2002) The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul 36:61–70. https://doi.org/10.1023/A:1014732714549
Bakhshandeh E, Pirdashti H, Vahabinia F, Gholamhossieni M (2020) Quantification of the effect of environmental factors on seed germination and seedling growth of eruca (Eruca sativa) using mathematical models. J Plant Growth Regul 39:190–204. https://doi.org/10.1007/s00344-019-09974-1
Barr HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficit in leaves. Aust J Biol Sci 15:413–428. https://doi.org/10.1071/BI9620413
Bista DR, Heckathorn SA, Jayawardena DM, Mishra S, Boldt JK (2018) Effects of drought on nutrient uptake and the levels of nutrient-uptake proteins in roots of drought-sensitive and -tolerant grasses. Plants 7:1–16. https://doi.org/10.3390/plants7020028
Bourdin B, Adenier H, Perrin Y (2007) Carnitine is associated with fatty acid metabolism in plants. Plant Physiol Biochem 45:926–931. https://doi.org/10.1016/j.plaphy.2007.09.009
Cai F, Na MI, Ji RP, Zhao XL, Shi KQ, Yang Y, Zhang H, Zhang YS (2017) Effects of drought stress and subsequent rewatering on major physiological parameters of spring maize during the key growth periods. J Appl Ecol 28:3643–3652
Charrier A, Rippa S, Yu A, Nguyen PJ, Renou JP, Perrin Y (2012) The effect of carnitine on Arabidopsis development and recovery in salt stress conditions. Planta 235:123–135. https://doi.org/10.1007/s00425-011-1499-4
Correia CCSA, Cunha FF, Mantovani EC, Silva DJH, Dias SHB, Sousa Ferreira T (2019) Irrigation of arugula cultivars in the region of Zona da Mata Mineira. Semin Cienc Agrar 40:1101–1114. https://doi.org/10.5433/1679-0359.2019v40n3p1101
Cruz CD (2016) Genes Software-extended and integrated with the R, Matlab and Selegen. Acta Sci Agron 38:547–552
Dayanand CD, Krishnamurthy N, Ashakiran S, Shashidhar KN (2011) Carnitine: a novel health factor—an overview. Int J Phar Biomed Res 2:79–89
Fechner J, Kaufmann M, Herz C, Eisenschmidt D, Lamy E, Kroh LW, Hanschen FS (2018) The major glucosinolate hydrolysis product in rocket (Eruca sativa Mill.), sativin, is 1,3-hiazepane-2-thione: elucidation of structure, bioactivity, and stability compared to other rocket isothiocyanates. Food Chem 261:57–65. https://doi.org/10.1016/j.foodchem.2018.04.023
Fiaz K, Malik SA, Younis U, Danish S, Raza Shah MH, Niaz S (2014) Drought impact on Pb/Cd toxicity remediated by biochar in Brassica campestris. J Soil Sci Plant Nutr 14:845–854. https://doi.org/10.4067/S0718-95162014005000067
Forde BG, Roberts MR (2014) Glutamate receptor-like channels in plants: a role as amino acid sensors in plant defence? F1000Prime Rep. https://doi.org/10.12703/P6-3
Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100. https://doi.org/10.1104/pp.110.166181
Garg G, Sharma V (2014) Eruca sativa (L.): botanical description, crop improvement, and medicinal properties. J Herbs Spices Med Plants 20:171–182. https://doi.org/10.1080/10496475.2013.848254
Hachemi A, Ali OS, Belghazi T, Lahrouni A, El Mercht S, El Hassan C, El Messoussi S (2021) Effect of hydric and light stress on biomass, nutrient uptake and enzymatic antioxidants of Argania spinosa seedlings. Arch Biol Sci 73:145–153. https://doi.org/10.2298/ABS201220010H
Henschel JM, Dantas EFO, Azevedo Soares V, Santos SK, Santos LWO, Dias TJ, Batista DS (2022) Salicylic acid mitigates the effects of mild drought stress on radish (Raphanus sativus) growth. Funct Plant Biol. https://doi.org/10.1071/FP22040
Huang B, Su J, Zhang G, Luo X, Wang H, Gao Y, Ma G, Wang J, Cai D, Zhang X, Huang B (2017) Screening for Eruca genotypes tolerant to polyethylene glycol-simulated drought stress based on the principal component and cluster analyses of seed germination and early seedling growth. Plant Genet Res 15:187–193. https://doi.org/10.1017/S1479262115000519
Hussain HA, Hussain S, Khaliq A, Ashraf U, Anjum SA, Men S, Wang L (2018) Chilling and drought stresses in crop plants: implications, cross talk, and potential management opportunities. Front Plant Sci 9:1–21. https://doi.org/10.3389/fpls.2018.00393
Jaafar NS, Jaafar IS (2019) Eruca sativa Linn: Pharmacognostical and pharmacological properties and pharmaceutical preparations. Asian J Pharm Clin Res 12:39–45
Jacques F, Rippa S, Perrin Y (2018) Physiology of L-carnitine in plants in light of the knowledge in animals and microorganisms. Plant Sci 274:432–440. https://doi.org/10.1016/j.plantsci.2018.06.020
Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Łukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102. https://doi.org/10.1007/s11738-016-2113-y
Kaur G, Asthir B (2017) Molecular responses to drought stress in plants. Biol Plant 61:201–209. https://doi.org/10.1007/s10535-016-0700-9
Khan S, Yu H, Li Q, Gao Y, Sallam BN, Wang H, Liu P, Jiang W (2019) Exogenous application of amino acids improves the growth and yield of lettuce by enhancing photosynthetic assimilation and nutrient availability. Agronomy 9:266. https://doi.org/10.3390/agronomy9050266
Khan MN, AlZuaibr FM, Al-Huqail AA, Siddiqui MH, Ali HM, Al-Muwayhi MA, Al-Haque HN (2018) Hydrogen sulfide-mediated activation of O-acetylserine (thiol) lyase and L/D-cysteine desulfhydrase enhance dehydration tolerance in Eruca sativa Mill. Int J Mol Sci 19:3981. https://doi.org/10.3390/ijms19123981
Khazaei Z, Estaji A (2020) Effect of foliar application of ascorbic acid on sweet pepper (Capsicum annuum) plants under drought stress. Acta Physiol Plant 42:1–12. https://doi.org/10.1007/s11738-020-03106-z
Khoobchandani M, Ojeswi BK, Ganesh N, Srivastava MM, Gabbanini S, Matera R, Valgimigli L (2010) Antimicrobial properties and analytical profile of traditional Eruca sativa seed oil: comparison with various aerial and root plant extracts. Food Chem 120:217–224. https://doi.org/10.1016/j.foodchem.2009.10.011
Latowski D, Kuczyńska P, Strzałka K (2011) Xanthophyll cycle—a mechanism protecting plants against oxidative stress. Redox Rep 16:78–90. https://doi.org/10.1179/174329211X13020951739938
Lee DK, Jung H, Jang G, Jeong JS, Kim YS, Ha SH, Choi Y, Kim JK (2016) Overexpression of the OsERF71 transcription factor alters rice root structure and drought resistance. Plant Physiol 172:575–588. https://doi.org/10.1104/pp.16.00379
Lopes LS, Nobre DAC, Macedo WR (2019) Effect of foliar application of 24-epibrassinolide and salicylic acid on common bean plants grown under drought stress. Emir J Food Agric 31:635–644. https://doi.org/10.9755/ejfa.2019.v31.i8.1996
Merwad ARM, Desoky ESM, Rady MM (2018) Response of water deficit-stressed Vigna unguiculata performances to silicon, proline or methionine foliar application. Sci Hortic 228:132–144. https://doi.org/10.1016/j.scienta.2017.10.008
Mumtaz MW, Mukhtar H, Dilawer UA, Hussain SM, Hussain M, Iqbal M, Adnan A, Nisar J (2016) Biocatalytic transesterification of Eruca sativa oil for the production of biodiesel. Biocatal Agric Biotechnol 5:162–167. https://doi.org/10.1016/j.bcab.2016.01.003
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Nguyen PJ, Rippa S, Rossez Y, Perrin Y (2016) Acylcarnitines participate in developmental processes associated to lipid metabolism in plants. Planta 243:1011–1022
Oney-Birol S (2019) Exogenous L-carnitine promotes plant growth and cell division by mitigating genotoxic damage of salt stress. Sci Rep 9:17229
Özden E, Memiş N, Gökdaş Z, Çatikkaş E, Demir İ (2020) Seed vigour evaluation of rocket (Eruca sativa Mill.) seed lots. J Inst Sci Tech 10:1486–1493
Rippa S, Zhao Y, Merlier F, Charrier A, Perrin Y (2012) The carnitine biosynthetic pathway in Arabidopsis thaliana shares similar features with the pathway of mammals and fungi. Plant Physiol Biochem 60:109–114
Salem HS, Pudza M, Yihdego Y (2022) Water strategies and water–food Nexus: challenges and opportunities towards sustainable development in various regions of the world. Sustain Water Resour Manag 8:114. https://doi.org/10.1007/s40899-022-00676-3
Santos RP, Cruz ACF, Iarema L, Kuki KN, Otoni WC (2008) Protocolo para extração de pigmentos foliares em porta-enxertos de videira micropropagados. Rev Ceres 55:356–364
Santos SK, Soares VA, Dantas EFO, Santos LWO, Gomes DS, Henschel JM, Batista DS (2022) Exogenous carnitine application enhances the growth of culantro (Eryngium foetidum) plants. Vegetos. https://doi.org/10.1007/s42535-022-00438-8
Sienkiewicz-Cholewa U, Sumisławska J, Sacała E, Dziągwa-Becker M, Kieloch R (2018) Influence of silicon on spring wheat seedlings under salt stress. Acta Physiol Plant 40:1–8. https://doi.org/10.1007/s11738-018-2630-y
Soares VA, Dantas EFO, Santos SK, Santos LWO, Dias TJ, Henschel JM, Batista DS (2022) Effect of salicylic acid on the growth and biomass partitioning in water-stressed radish plants. Vegetos. https://doi.org/10.1007/s42535-022-00381-8
Sohag AAM, Tahjib-Ul-Arif M, Brestic M, Afrin S, Sakil MA, Hossain MT, Hossain MA (2020) Exogenous salicylic acid and hydrogen peroxide attenuate drought stress in rice. Plant Soil Environ 66:7–13
Sun Y, Wang C, Chen HY, Ruan H (2020) Response of plants to water stress: a meta-analysis. Front Plant Sci 11:1–8. https://doi.org/10.3389/fpls.2020.00978
Sun S, Yao X, Liu X, Qiao Z, Liu Y, Li X, Jiang X (2022) Brassinolide can improve drought tolerance of maize seedlings under drought stress: by inducing the photosynthetic performance, antioxidant capacity and ZmMYB gene expression of maize seedlings. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-022-00796-x
Tsimilli-Michael M (2020) Revisiting JIP-test: an educative review on concepts, assumptions, approximations, definitions and terminology. Photosynthetica 58:275–292
Turk H, Erdal S, Dumlupinar R (2020) Carnitine-induced physio-biochemical and molecular alterations in maize seedlings in response to cold stress. Arch Agron Soil Sci 66:925–941. https://doi.org/10.1080/03650340.2019.1647336
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/S0176-1617(11)81192-2
Zafar-Pashanezhad M, Shahbazi E, Golkar P, Shiran B (2020) Genetic variation of Eruca sativa L. genotypes revealed by agro-morphological traits and ISSR molecular markers. Ind Crops Prod 145:1–9. https://doi.org/10.1016/j.indcrop.2019.111992
Zhang Z, Cao B, Gao S, Xu K (2019) Grafting improves tomato drought tolerance through enhancing photosynthetic capacity and reducing ROS accumulation. Protoplasma 256:1013–1024. https://doi.org/10.1007/s00709-019-01357-3
Zhang RR, Wang YH, Li T, Tan GF, Tao JP, Su XJ, Xu ZS, Tian YS, Xiong AS (2021) Effects of simulated drought stress on carotenoid contents and expression of related genes in carrot taproots. Protoplasma 258:379–390. https://doi.org/10.1007/s00709-020-01570-5
Zulfiqar F, Ashraf M (2021) Bioregulators: unlocking their potential role in regulation of the plant oxidative defense system. Plant Mol Biol 105:11–41. https://doi.org/10.1007/s11103-020-01077-w
Zulfiqar F, Younis A, Abideen Z, Francini A, Ferrante A (2019) Bioregulators can improve biomass production, photosynthetic efficiency, and ornamental quality of Gazania rigens L. Agronomy 9:773. https://doi.org/10.3390/agronomy9110773
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We would like to thank Editage (www.editage.com) for English language editing.
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This study was funded by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil), FAPESQ/UFPB (Fundação de Apoio à Pesquisa do Estado da Paraíba/Universidade Federal da Paraíba), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior), and the Public Call n. 03 Produtividade em Pesquisa PROPESQ/PRPG/UFPB—Proposal code PVO13257-2020. Conselho Nacional de Desenvolvimento Científico e Tecnológico,Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, PROPESQ/PRPG/UFPB, PVO13257-2020, Diego Silva Batista
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SKS, DSG, JMH, and DSB designed the study. VAS, EFOD, SKS, LWOS, DSG, and JMH conducted the experiments. SKS, DSG, VAS, EFOD, LWOS, JMH, and DSB collected and analyzed the data. SKS, DSG, VAS, EFOD, JMH, and DSB contributed to the design and interpretation of the study and the writing of the paper. All authors have read and approved the final version of the manuscript.
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dos Santos, S.K., da Silva Gomes, D., dos Santos, L.W.O. et al. Exogenous Carnitine Mitigates the Deleterious Effects of Mild-Water Stress on Arugula by Modulating Morphophysiological Responses. J Plant Growth Regul 42, 4073–4082 (2023). https://doi.org/10.1007/s00344-022-10868-y
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DOI: https://doi.org/10.1007/s00344-022-10868-y