Exogenous nitric oxide extends longevity in cut Lilium tigrinum flowers by orchestrating biochemical and molecular aspects
Moonisah Aftab A , Haris Yousuf Lone A , Aijaz A. Wani A , Mohamad Arif Zargar A and Inayatullah Tahir A *A
Abstract
Senescence represents a developmentally orchestrated and precisely regulated cascade of events, culminating in the abscission of plant organs and ultimately leading to the demise of the plant or its constituent parts. In this study, we observed that senescence in cut Lilium tigrinum flowers is induced by elevated ABA levels and the hyperactivation of lipoxygenase (LOX) activity. This cascade increased ROS concentrations, heightened oxidative damage, and disrupted cellular redox equilibrium. This was evidenced by elevated lipid peroxidation, attenuated antioxidant machinery, and reduced membrane stability index (MSI). Despite its known role in delaying flower senescence, the specific biochemical and molecular mechanisms by which nitric oxide (NO) regulates senescence in cut L. tigrinum flowers are not fully elucidated. Specifically, the interactions between NO signaling and ABA metabolism, the regulation of protease activity, and the influence of NO-mediated ROS scavenging, senescence-associated gene expression requires further exploration. Exogenous application of sodium nitroprusside (SNP), a source of NO, mitigated senescence in L. tigrinum cut flowers by upregulating the activity of superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX) and reducing the LOX activity, an indicator of lipid peroxidation. SNP treatment also downregulated the relative expression of senescence-associated gene (SAG12),lipoxygenase 1 (LOX1), and abscisic aldehyde oxidase 3 (AAO3). NO also upregulated defender against apoptotic death 1 (DAD1) expression correlated with minimized protease activity and reduced α-amino acid content in SNP-treated tepals. This regulation was accompanied by increased contents of sugars, proteins and phenols and reduced abscisic acid content, which collectively delayed the senesecence and enhanced the longevity of L. tigrinum cut flowers. This study demonstrates that exogenous SNP application can effectively mitigate senescence in cut L. tigrinum flowers by modulating antioxidant enzyme activities, reducing oxidative stress, and regulating the expression of key senescence-associated genes. This study unravels the complex molecular networks involved in NO-mediated senescence delay, which may lead to the development of innovative approaches for improving flower longevity.
Keywords: AAO3, abscisic acid (ABA), DAD1, LOX1, reactive oxygen species (ROS), SAG12, senescence, sodium nitroprusside.
References
Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121-126.
| Crossref | Google Scholar | PubMed |
Ahmad SS, Tahir I (2017) Regulatory role of phenols in flower development and senescence in the genus Iris. Indian Journal of Plant Physiology 22(1), 135-140.
| Crossref | Google Scholar |
Ahmad P, Raja V, Ashraf M, Wijaya L, Bajguz A, Alyemeni MN (2021) Jasmonic acid (JA) and gibberellic acid (GA3) mitigated Cd-toxicity in chickpea plants through restricted cd uptake and oxidative stress management. Scientific Reports 11(1), 19768.
| Crossref | Google Scholar |
Almeida Trapp M, De Souza GD, Rodrigues-Filho E, Boland W, Mithöfer A (2014) Validated method for phytohormone quantification in plants. Frontiers in Plant Science 5, 417.
| Crossref | Google Scholar |
Arora A, Singh VP (2004) Cysteine protease gene expression and proteolytic activity during floral development and senescence in ethylene-insensitive Gladiolus grandiflora. Journal of Plant Biochemistry and Biotechnology 13(2), 123-126.
| Crossref | Google Scholar |
Asim M, Zhang Y, Sun Y, Guo M, Khan R, Wang XL, Hussain Q, Shi Y (2023) Leaf senescence attributes: the novel and emerging role of sugars as signaling molecules and the overlap of sugars and hormones signaling nodes. Critical Reviews in Biotechnology 43(7), 1092-1110.
| Crossref | Google Scholar | PubMed |
Aziz S, Younis A, Jaskani MJ, Ahmad R (2020) Effect of PGRs on antioxidant activity and phytochemical in delay senescence of lily cut flowers. Agronomy 10(11), 1704.
| Crossref | Google Scholar |
Badiyan D, Wills RBH, Bowyer MC (2004) Use of a nitric oxide donor compound to extend the vase life of cut flowers. HortScience 39(6), 1371-1372.
| Crossref | Google Scholar |
Baseer AQ, Monib AW, Hassand MH, Hejran AB, Sarwari A, Kakar UM, Sediqi S, Rahime M, Sahrai SA, Mahmoud S, Fahmawi SMS, Niazi P (2024) Lifecycle transitions in plant development: ripening, senescence, & cell death. Journal of Pharma Insights and Research 2(2), 169-179.
| Crossref | Google Scholar |
Brouquisse R (2019) Multifaceted roles of nitric oxide in plants. Journal of Experimental Botany 70(17), 4319-4322.
| Crossref | Google Scholar | PubMed |
Bruand C, Meilhoc E (2019) Nitric oxide in plants: pro- or anti-senescence. Journal of Experimental Botany 70(17), 4419-4427.
| Crossref | Google Scholar | PubMed |
Chen G-X, Asada K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant and Cell Physiology 30(7), 987-998.
| Crossref | Google Scholar |
Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162(1), 156-159.
| Crossref | Google Scholar | PubMed |
Choudhary A, Kumar A, Kaur N, Kaur H (2022) Molecular cues of sugar signaling in plants. Physiologia Plantarum 174(1), e13630.
| Crossref | Google Scholar |
Deng Y, Wang C, Huo J, Hu W, Liao W (2019) The involvement of NO in ABA-delayed the senescence of cut roses by maintaining water content and antioxidant enzymes activity. Scientia Horticulturae 247, 35-41.
| Crossref | Google Scholar |
Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany 32(1), 93-101.
| Crossref | Google Scholar |
Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Molecular Plant 8(4), 506-520.
| Crossref | Google Scholar | PubMed |
Dwivedi SK, Arora A, Singh VP, Sairam R, Bhattacharya RC (2016) Effect of sodium nitroprusside on differential activity of antioxidants and expression of SAGs in relation to vase life of gladiolus cut flowers. Scientia Horticulturae 210, 158-165.
| Crossref | Google Scholar |
Eason JR, Johnston JW, de Vré L (2000) Reversal of glyphosate inhibition of Sandersonia aurantiaca flower senescence with aromatic amino acids. Postharvest Biology and Technology 18(1), 81-84.
| Crossref | Google Scholar |
Eason JR, Ryan DJ, Pinkney TT, O’Donoghue EM (2002) Programmed cell death during flower senescence: isolation and characterization of cysteine proteinases from Sandersonia aurantiaca. Functional Plant Biology 29(9), 1055-1064.
| Crossref | Google Scholar | PubMed |
Fancy NN, Bahlmann A-K, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant, Cell & Environment 40(4), 462-472.
| Crossref | Google Scholar | PubMed |
Farooq S, Ul Haq A, Lateef Lone M, Waseem W, Parveen S, Altaf F, Tahir I, Abdullah Alsahli A (2024) “From villain to hero”: harnessing the gaseous grace of nitric oxide for prolonged elegance in Antirrhinum majus L. cut spikes. Journal of King Saud University – Science 36(6), 103217.
| Crossref | Google Scholar |
Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Frontiers in Plant Science 4, 398.
| Crossref | Google Scholar |
Guiboileau A, Sormani R, Meyer C, Masclaux-Daubresse C (2010) Senescence and death of plant organs: nutrient recycling and developmental regulation. Comptes Rendus. Biologies 333(4), 382-391.
| Crossref | Google Scholar | PubMed |
Gupta KJ, Kaladhar VC, Fitzpatrick TB, Fernie AR, Møller IM, Loake GJ (2022) Nitric oxide regulation of plant metabolism. Molecular Plant 15(2), 228-242.
| Crossref | Google Scholar | PubMed |
Han L, Wang Z, Watkins CB, Ma L, He X, Bai C, Wang H, Wang Q, Zuo J, Zheng Y (2024) The regulatory mechanisms of delayed senescence of nitric oxide treatment of hyacinth beans. Postharvest Biology and Technology 207, 112592.
| Crossref | Google Scholar |
Hanson AD, Kende H (1975) Ethylene-enhanced ion and sucrose efflux in morning glory flower tissue. Plant Physiology 55(4), 663-669.
| Crossref | Google Scholar | PubMed |
Hung KT, Kao CH (2003) Nitric oxide counteracts the senescence of rice leaves induced by abscisic acid. Journal of Plant Physiology 160(8), 871-879.
| Crossref | Google Scholar | PubMed |
Hussain A, Shah F, Ali F, Yun B-W (2022) Role of nitric oxide in plant senescence. Frontiers in Plant Science 13, 851631.
| Crossref | Google Scholar |
Iakimova ET, Woltering EJ (2015) Nitric oxide prevents wound-induced browning and delays senescence through inhibition of hydrogen peroxide accumulation in fresh-cut lettuce. Innovative Food Science & Emerging Technologies 30, 157-169.
| Crossref | Google Scholar |
Jayarajan S, Sharma RR (2018) Impact of nitric oxide on shelf life and quality of nectarine (Prunus persica var. nucipersica). Acta Physiologiae Plantarum 40(12), 207.
| Crossref | Google Scholar |
Jones ML (2013) Mineral nutrient remobilization during corolla senescence in ethylene-sensitive and -insensitive flowers. AoB Plants 5, plt023.
| Crossref | Google Scholar |
Jones ML, Chaffin GS, Eason JR, Clark DG (2005) Ethylene–sensitivity regulates proteolytic activity and cysteine protease gene expression in petunia corollas. Journal of Experimental Botany 56(420), 2733-2744.
| Crossref | Google Scholar | PubMed |
Khan M, Ali S, Al Azzawi TNI, Yun B-W (2023) Nitric oxide acts as a key signaling molecule in plant development under stressful conditions. International Journal of Molecular Sciences 24(5), 4782.
| Crossref | Google Scholar |
Kolbert Z, Lindermayr C, Loake GJ (2021) The role of nitric oxide in plant biology: current insights and future perspectives. Journal of Experimental Botany 72(3), 777-780.
| Crossref | Google Scholar | PubMed |
Kop DAMvd, Ruys G, Dees D, Van der Schoot C, Douwe de Boer A, Van Doorn WG (2003) Expression of defender against apoptotic death (DAD-1) in Iris and Dianthus petals. Physiologia Plantarum 117(2), 256-263.
| Crossref | Google Scholar |
Krasylenko YA, Yemets AI, Blume YB (2010) Functional role of nitric oxide in plants. Russian Journal of Plant Physiology 57(4), 451-461.
| Crossref | Google Scholar |
Kumar N, Srivastava GC, Dixit K (2008) Flower bud opening and senescence in roses (Rosa hybrida L.). Plant Growth Regulation 55(2), 81-99.
| Crossref | Google Scholar |
Kumari S, Singh KP, Arora A (2013) Screening of cultivars of cut tuberose (Polianthes tuberosa L.) flower for longer vase life on the basis of membrane stability index. Progressive Horticulture 45(1), 164-168.
| Google Scholar |
Li C, Yu W, Liao W (2022) Role of nitric oxide in postharvest senescence of fruits. International Journal of Molecular Sciences 23(17), 10046.
| Crossref | Google Scholar |
Liao W-B, Zhang M-L, Yu J-H (2013) Role of nitric oxide in delaying senescence of cut rose flowers and its interaction with ethylene. Scientia Horticulturae 155, 30-38.
| Crossref | Google Scholar |
Liu X, Chen S, Du F, Sun L, Huang Q, Gao X, et al. (2023) Insights into adaptive regulation of the leaf-petiole system: strategies for survival of water lily plants under salt stress. International Journal of Molecular Sciences 24(6), 5605.
| Crossref | Google Scholar |
Lone ML, Haq Au, Farooq S, Altaf F, Tahir I (2021) Nitric oxide effectively curtails neck bending and mitigates senescence in isolated flowers of Calendula officinalis L. Physiology and Molecular Biology of Plants 27(4), 835-845.
| Crossref | Google Scholar | PubMed |
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193, 265-275.
| Google Scholar |
Lundberg JO, Weitzberg E (2022) Nitric oxide signaling in health and disease. Cell 185(16), 2853-2878.
| Crossref | Google Scholar | PubMed |
Maccarrone M, Finazzi-Agrò A, Veldink GA, Vliegenthart JFG (1999) Inhibition of plant lipoxygenases by antioxidants, nitric oxide and polyamines. Current Topics in Phytochemistry 2, 163-170.
| Google Scholar |
Manjunatha G, Gupta KJ, Lokesh V, Mur LAJ, Neelwarne B (2012) Nitric oxide counters ethylene effects on ripening fruits. Plant Signaling & Behavior 7(4), 476-483.
| Crossref | Google Scholar | PubMed |
Manuylova EA, Turpaev KT, Pankratova EV (2007) Role of nitric oxide in regulating the expression of histone mRNA. Molecular Biology 41(4), 571-575.
| Crossref | Google Scholar |
Mikulska-Ruminska K, Anthonymuthu TS, Levkina A, Shrivastava I, Kapralov O, Bayir H, Bahar I, Kagan VE (2022) The suppressing role of nitric oxide in the ferroptotic cell death signal transduction. Biophysical Journal 121(3), 188a.
| Crossref | Google Scholar |
Naing AH, Lee K, Kim K-O, Ai TN, Kim CK (2017) Involvement of sodium nitroprusside (SNP) in the mechanism that delays stem bending of different gerbera cultivars. Frontiers in Plant Science 8, 2045.
| Crossref | Google Scholar |
Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. Journal of Biological Chemistry 153(2), 375-380.
| Crossref | Google Scholar |
Nisar S, Dar RA, Bhat AA, Farooq Z, Tahir I (2021) Some important biochemical changes orchestrating flower development and senescence in Nicotiana plumbaginifolia Viv. and Petunia hybrida Vilm. flowers. The Journal of Horticultural Science and Biotechnology 96(6), 759-769.
| Crossref | Google Scholar |
Parveen S, Altaf F, Farooq S, Lone ML, Ul Haq A, Tahir I (2023) The swansong of petal cell death: insights into the mechanism and regulation of ethylene-mediated flower senescence. Journal of Experimental Botany 74(14), 3961-3974.
| Crossref | Google Scholar | PubMed |
Parwez R, Aftab T, Gill SS, Naeem M (2022) Abscisic acid signaling and crosstalk with phytohormones in regulation of environmental stress responses. Environmental and Experimental Botany 199, 104885.
| Crossref | Google Scholar |
Perik RRJ, Razé D, Harkema H, Zhong Y, van Doorn WG (2012) Bending in cut Gerbera jamesonii flowers relates to adverse water relations and lack of stem sclerenchyma development, not to expansion of the stem central cavity or stem elongation. Postharvest Biology and Technology 74, 11-18.
| Crossref | Google Scholar |
Prakash V, Singh VP, Tripathi DK, Sharma S, Corpas FJ (2021) Nitric oxide (NO) and salicylic acid (SA): a framework for their relationship in plant development under abiotic stress. Plant Biology 23, 39-49.
| Crossref | Google Scholar | PubMed |
Procházková D, Wilhelmová N (2011) Nitric oxide, reactive nitrogen species and associated enzymes during plant senescence. Nitric Oxide 24(2), 61-65.
| Crossref | Google Scholar | PubMed |
Raza A, Salehi H, Rahman MA, Zahid Z, Madadkar Haghjou M, Najafi-Kakavand S, Charagh S, Osman HS, Albaqami M, Zhuang Y, Siddique KHM, Zhuang W (2022) Plant hormones and neurotransmitter interactions mediate antioxidant defenses under induced oxidative stress in plants. Frontiers in Plant Science 13, 961872.
| Crossref | Google Scholar |
Rezayian M, Ebrahimzadeh H, Niknam V (2023) Metabolic and physiological changes induced by nitric oxide and its impact on drought tolerance in soybean. Journal of Plant Growth Regulation 42(3), 1905-1918.
| Crossref | Google Scholar |
Rogers HJ (2006) Programmed cell death in floral organs: how and why do flowers die? Annals of Botany 97(3), 309-315.
| Crossref | Google Scholar | PubMed |
Rogers HJ (2013) From models to ornamentals: how is flower senescence regulated? Plant Molecular Biology 82(6), 563-574.
| Crossref | Google Scholar | PubMed |
Rogers HJ (2015) Senescence-associated programmed cell death. In ‘Plant programmed cell death’. (Eds AN Gunawardena, PF McCabe) pp. 203–233. (Springer: Cham, Switzerland) 10.1007/978-3-319-21033-9_9
Rosen H (1957) A modified ninhydrin colorimetric analysis for amino acids. Archives of Biochemistry and Biophysics 67(1), 10-15.
| Crossref | Google Scholar | PubMed |
Sahu SK, Barman K, Singh AK (2020) Nitric oxide application for postharvest quality retention of guava fruits. Acta Physiologiae Plantarum 42, 156.
| Crossref | Google Scholar |
Sairam RK (1994) Effect of moisture stress on physiological activities of two contrasting wheat genotypes. Indian Journal of Experimental Biology 32, 594-597.
| Google Scholar |
Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Comptes Rendus de l’Academie Bulgare des Sciences 51(3), 121–-124.
| Google Scholar |
Shi H, Ye T, Zhu J-K, Chan Z (2014) Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. Journal of Experimental Botany 65(15), 4119-4131.
| Crossref | Google Scholar | PubMed |
Siddiqui MW, Homa F, Lata D, Ahmad MS, Surabhi (2021) Exogenous nitric oxide delays ripening and maintains postharvest quality of pointed gourd during storage. Journal of Plant Growth Regulation 40, 2371-2378.
| Crossref | Google Scholar |
Sun C, Zhang Y, Liu L, Liu X, Li B, Jin C, Lin X (2021) Molecular functions of nitric oxide and its potential applications in horticultural crops. Horticulture Research 8, 71.
| Crossref | Google Scholar |
Suttle JC, Kende H (1978) Ethylene and senescence in petals of Tradescantia. Plant Physiology 62(2), 267-271.
| Crossref | Google Scholar | PubMed |
Swain T, Hillis WE (1959) The phenolic constituents of Prunus domestica. I. – the quantitative analysis of phenolic constituents. Journal of the Science of Food and Agriculture 10(1), 63-68.
| Crossref | Google Scholar |
Tayyab S, Qamar S (1992) A look into enzyme kinetics: some introductory experiments. Biochemical Education 20(2), 118.
| Crossref | Google Scholar |
Ul Haq A, Lateef Lone M, Farooq S, Parveen S, Altaf F, Tahir I, Ingo Hefft D, Ahmad A, Ahmad P (2023) Nitric oxide effectively orchestrates postharvest flower senescence: a case study of Consolida ajacis. Functional Plant Biology 50(2), 97-107.
| Crossref | Google Scholar | PubMed |
van Doorn WG (2004) Is petal senescence due to sugar starvation? Plant Physiology 134(1), 35-42.
| Crossref | Google Scholar | PubMed |
van Doorn WG, Woltering EJ (2008) Physiology and molecular biology of petal senescence. Journal of Experimental Botany 59(3), 453-480.
| Crossref | Google Scholar | PubMed |
Verma N, Tiwari S, Singh VP, Prasad SM (2020) Nitric oxide in plants: an ancient molecule with new tasks. Plant Growth Regulation 90, 1-13.
| Crossref | Google Scholar |
Wagstaff C, Leverentz MK, Griffiths G, Thomas B, Chanasut U, Stead AD, Rogers HJ (2002) Cysteine protease gene expression and proteolytic activity during senescence of Alstroemeria petals. Journal of Experimental Botany 53(367), 233-240 10.1093/jexbot/53.367.233.
| Google Scholar | PubMed |
Wang Y, Loake GJ, Chu C (2013) Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. Frontiers in Plant Science 4, 314.
| Crossref | Google Scholar |
Wang M, Li B, Zhu Y-C, Niu L-J, Jin X, Xu Q-Q, Liao W-B (2015) Effect of exogenous nitric oxide on vegetative and reproductive growth of oriental lily ‘Siberia’. Horticulture, Environment, and Biotechnology 56(5), 677-686.
| Crossref | Google Scholar |
Wojciechowska N, Sobieszczuk-Nowicka E, Bagniewska-Zadworna A (2018) Plant organ senescence – regulation by manifold pathways. Plant Biology 20(2), 167-181.
| Crossref | Google Scholar | PubMed |
Wu X, Yuan J, Wang X, Yu M, Ma R, Yu Z (2021) Synergy of nitric oxide and 1-methylcyclopropene treatment in prolong ripening and senescence of peach fruit. Foods 10(12), 2956.
| Crossref | Google Scholar |
Zeng C-L, Liu L, Xu G-Q (2011) The physiological responses of carnation cut flowers to exogenous nitric oxide. Scientia Horticulturae 127(3), 424-430.
| Crossref | Google Scholar |
Zhao Y, Xi Q, Xu Q, He M, Ding J, Dai Y, Keller NP, Zheng W (2015) Correlation of nitric oxide produced by an inducible nitric oxide synthase-like protein with enhanced expression of the phenylpropanoid pathway in Inonotus obliquus cocultured with Phellinus morii. Applied Microbiology and Biotechnology 99(10), 4361-4372.
| Crossref | Google Scholar | PubMed |
Zhao Y, Zhu X, Hou Y, Wang X, Li X (2020) Postharvest nitric oxide treatment delays the senescence of winter jujube (Zizyphus jujuba Mill. cv. Dongzao) fruit during cold storage by regulating reactive oxygen species metabolism. Scientia Horticulturae 261, 109009.
| Crossref | Google Scholar |
Zhu G, Yin J, Guo X, Chen X, Zhi W, Liu J, Wang Y, Lu H, Jiao X, Zhou G (2019) Gibberellic acid amended antioxidant enzyme and osmotic regulation to improve salt tolerance of okra at early growth stage. International Journal of Agriculture & Biology 22(2), 270-276.
| Google Scholar |