Research Progress in NO Regulating Seed Dormancy and Germination

doi:10.13560/j.cnki.biotech.bull.1985.2025-1040

Abstract

Abstract:

Seeds are recognized as the “chips” of agricultural production, and their germination, as the starting point of a crop’s life cycle, directly determines seedling emergence quality as well as crop yield and quality. Nitric oxide (NO), a key gaseous signaling molecule, has emerged as a research frontier in plant biology due to its central role in regulating seed dormancy and germination. This review systematically summarizes the current progress in this field, elucidating the primary synthesis and metabolic pathways of NO in plants and their homeostatic regulation. It focuses on dissecting the signal transduction mechanisms of NO, particularly its molecular basis for coordinately regulating key nodes of seed dormancy and germination through crosstalk with hormonal and reactive oxygen species (ROS) signaling networks as well as through post-translational modifications. Although significant progress has been achieved, several important scientific issues in this area still remain to be deeply explored. At the basic research level, future efforts should further be on resolving the spatiotemporal specificity of NO synthesis and signaling within different seed tissues and germination stages, utilizing multi-omics technologies to systematically identify downstream modification targets of NO and clarify their functions. Additionally, elucidating the molecular mechanisms underlying the integration of NO signaling with environmental signals such as light and temperature is essential. At the applied level, novel green seed treatment technologies based on NO can be developed to enhance seed germination performance and seedling resistance to stress under adverse conditions. Furthermore, exploring genetic or biotechnological approaches to modulate endogenous NO synthesis and metabolism pathways in seeds could improve crop germination traits, offering new strategies for breeding crop varieties with uniform emergence and enhanced stress resistance. By systematically synthesizing the regulatory mechanisms of NO in seed dormancy and germination, this review aims to provide a theoretical foundation for a deeper understanding of the molecular regulatory network governing the initiation of seed life, while also offering new insights for the development of key technologies to enhance crop seed quality and innovate stress-resilient cultivation models.

Key words: NO, seed dormancy, seed germination, regulatory mechanism, signal transduction

WANG Hong-yang, QIU Yan-hong, WANG De-xin, XIA Yang, MENG Shu-chun, XU Xiu-lan, ZHANG Hai-jun. Research Progress in NO Regulating Seed Dormancy and Germination[J]. Biotechnology Bulletin, 2026, 42(6): 164-174.

Figures/Tables 4

Fig. 1 Biosynthesis and scavenging of NOThe left side of the dashed line shows the synthesis process of NO, while the right side illustrates the scavenging process of NO. NR: Nitrate reductase (e.g., AtNIA1/2); mETC: mitochondrial electron transport chain; GSNO: S-nitrosoglutathione; NO2-FAs: nitro fatty acids; NO-Mela: N-nitrosomelatonin; GSSG: glutathione disulfide; ONOO-: peroxynitrite

Fig. 2 Role of NO and phytohormones interaction in synergistically regulating seed dormancy and germinationNO promotes seed germination and breaks dormancy by antagonizing ABA biosynthesis and signaling, while concurrently activating the biosynthesis and signaling pathways of GA, JA, and ethylene. CYP707A: Cytochrome P450, Family 707, Subfamily A; NCED: nine-cis-epoxycarotenoid dioxygenase; PYR/PYL/RCAR: PYRABACTIN RESISTANCE1 (PYR1)/PYR1-LIKE (PYL)/REGULATORY COMPONENTS OF ABA RECEPTORS (RCAR) ; PP2C: type 2C protein phosphatases; SnRKs: SNF1-related protein kinase; ABI5: ABSCISIC ACID INSENSITIVE 5; GAox: GA oxidase; RGL2: REPRESSOR OF GA-LIKE2; ACS: S-adenosyl-L-methionine methylthioadenosine-lyase; ACO: ACC oxidase; ETR: ethylene resistant 1; CTR1: constitutive triple response 1; EIN2: ETHYLENE INSENSITIVE2; AOS: allene oxide synthase. The seed schematic represents a general model, and the illustrated NO-mediated mechanisms are operative in both monocot (e.g., rice) and dicot (e.g., Arabidopsis) species

Table 1 Types of protein post-translational modifications (PTMs) directly mediated by NO

PTM类型 Category	修饰蛋白 Protein	修饰位点 Modification sites	功能描述 Function description	参考文献 Reference
S-亚硝基化 S-nitrosylation	APX， GR， DHAR	—	激活抗坏血酸-谷胱甘肽循环中的抗氧化酶活性，提高顽拗型种子的脱水耐受性	［56］
	ABI5	Cys153	S-亚硝基化后，E3连接酶介导其降解，从而促进种子萌发	［57］
	SnRK2.2/ SnRK2.3	Cys137	抑制激酶活性，阻断ABA信号传递，促进种子萌发	［58］
	GSNOR1	—	高温胁迫诱导GSNOR1发生S-亚硝基化修饰并促使其降解，稳定ABI5蛋白导致种子热休眠	［62］
	GADPH	Cys154	诱导蛋白寡聚化，加速细胞死亡和种子老化	［60］
	HFR	Cys164	高温诱导HFR1 S-亚硝基化促使其降解，激活PIF1靶向的SOM基因表达，改变GA与ABA代谢平衡，抑制种子萌发	［61］
	MYB30	Cys49	NO介导MYB30 S-亚硝基化增强MYB30的转录活性，促进CYP707A2表达，降低ABA含量。打破种子休眠、促进萌发	［59］
酪氨酸硝化 Tyrosine nitration	储藏蛋白	—	促进储藏蛋白降解，为胚轴伸长提供必需的氨基酸与维生素，为种子萌发提供能量	［13］
酪氨酸硝化 Tyrosine nitration	PYR/PYL/RCAR	—	硝化使ABA受体失活，限制ABA信号传导	［64］

Fig. 3 Agricultural application potential of NOIn agricultural practice, NO modulates gene expression and post-translational modifications, thereby reshaping hormonal balance, scavenging oxidative damage, maintaining membrane integrity, and reprogramming energy metabolism. These coordinated actions collectively break seed dormancy, promote germination, and ultimately enhance seed resistance to stress and maintain long-term vigor

References 73

[1]	Sajeev N, Koornneef M, Bentsink L. A commitment for life: Decades of unraveling the molecular mechanisms behind seed dormancy and germination [J]. Plant Cell, 2024, 36(5): 1358-1376.
[2]	Hubert B, Leprince O, Buitink J. Sleeping but not defenceless: seed dormancy and protection [J]. J Exp Bot, 2024, 75(19): 6110-6124.
[3]	Matilla AJ. Current insights into weak seed dormancy and pre-harvest sprouting in crop species [J]. Plants, 2024, 13(18): 2559.
[4]	Koshland DE. The molecule of the year [J]. 1992, 258(5090): 1861.
[5]	Gupta KJ, Yadav N, Kumari A, et al. New insights into nitric oxide biosynthesis underpin lateral root development [J]. Mol Plant, 2024, 17(5): 691-693.
[6]	Ciacka K, Staszek P, Sobczynska K, et al. Nitric oxide in seed biology [J]. Int J Mol Sci, 2022, 23(23): 14951.
[7]	León J, Costa-Broseta Á. Present knowledge and controversies, deficiencies, and misconceptions on nitric oxide synthesis, sensing, and signaling in plants [J]. Plant Cell Environ, 2020, 43(1): 1-15.
[8]	Jack Q Wilkinson NMC. Identification of the Arabidopsis CHL3 gene as the nitrate reductase structural gene NIA2 [J]. Plant Cell, 1991, 3(5): 461-471.
[9]	Desikan R, Griffiths R, Hancock J, et al. A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana [J]. Proc Natl Acad Sci USA, 2002, 99(25): 16314-16318.
[10]	Lozano-Juste J, León J. Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis [J]. Plant Physiol, 2010, 152(2): 891-903.
[11]	Gupta KJ, Kaladhar VC, Fitzpatrick TB, et al. Nitric oxide regulation of plant metabolism [J]. Mol Plant, 2022, 15(2): 228-242.
[12]	Astier J, Gross I, Durner J. Nitric oxide production in plants: an update [J]. J Exp Bot, 2018, 69(14): 3401-3411.
[13]	Krasuska U, Ciacka K, Orzechowski S, et al. Modification of the endogenous NO level influences apple embryos dormancy by alterations of nitrated and biotinylated protein patterns [J]. Planta, 2016, 244(4): 877-891.
[14]	Modolo LV, Augusto O, Almeida IMG, et al. Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae [J]. FEBS Lett, 2005, 579(17): 3814-3820.
[15]	Bethke PC, Badger MR, Jones RL. Apoplastic synthesis of nitric oxide by plant tissues [J]. Plant Cell, 2004, 16(2): 332-341.
[16]	Corpas FJ, González-Gordo S, Palma JM. NO source in higher plants: present and future of an unresolved question [J]. Trends Plant Sci, 2022, 27(2): 116-119.
[17]	Karpinska B, Foyer CH. Superoxide signalling and antioxidant processing in the plant nucleus [J]. J Exp Bot, 2024, 75(15): 4599-4610.
[18]	Ciacka K, Krasuska U, Otulak-Kozieł K, et al. Dormancy removal by cold stratification increases glutathione and S-nitrosoglutathione content in apple seeds [J]. Plant Physiol Biochem, 2019, 138: 112-120.
[19]	Berger A, Boscari A, Puppo A, et al. Nitrate reductases and hemoglobins control nitrogen-fixing symbiosis by regulating nitric oxide accumulation [J]. J Exp Bot, 2021, 72(3): 873-884.
[20]	Liu YY, Liu ZY, Wu XT, et al. Role of protein S-nitrosylation in plant growth and development [J]. Plant Cell Rep, 2024, 43(8): 204.
[21]	Fuentes-Terrón A, Latter R, Madden S, et al. Destined for destruction: The role of methionine aminopeptidases and plant cysteine oxidases in N-degron formation [J]. Plant Physiol, 2024, 197(1): kiae667.
[22]	Gibbs DJ, Md Isa N, Movahedi M, et al. Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors [J]. Mol Cell, 2014, 53(3): 369-379.
[23]	Sedlářová M, Jedelská T, Lebeda A, et al. Progress in plant nitric oxide studies: implications for phytopathology and plant protection [J]. Int J Mol Sci, 2025, 26(5): 2087.
[24]	Naaz S, Pande A, Laxmi A. Nitric oxide-mediated thermomemory: a new perspective on plant heat stress resilience [J]. Front Plant Sci, 2025, 16: 1525336.
[25]	Kumar D, Ohri P. Say “NO” to plant stresses: Unravelling the role of nitric oxide under abiotic and biotic stress [J]. Nitric Oxide, 2023, 130: 36-57.
[26]	Wong A, Tian XC, Yang YX, et al. Identification of potential nitric oxide-sensing proteins using the H-NOX motif [J]. Mol Plant, 2021, 14(2): 195-197.
[27]	Zhao X, Cao HN, Liu Y, et al. A new plant guanosine cyclase ZjGC found from jujube regulates growth and development via endogenous hormones [J]. Front Plant Sci, 2025, 16: 1633496.
[28]	Fejes G, Bodor T, Szőllősi R, et al. Nitric oxide as an integral element in priming-induced tolerance and plant stress memory [J]. J Exp Bot, 2025, 76(13): 3669-3685.
[29]	Zhang Y, Wang RR, Wang XD, et al. Nitric oxide regulates seed germination by integrating multiple signalling pathways [J]. Int J Mol Sci, 2023, 24(10): 9052.
[30]	Sekita MC, dos Santos Dias DCF, Pinheiro DT, et al. Nitric oxide in physiological potential and biochemical mechanisms of pea seeds under water deficit [J]. J Seed Sci, 2022, 44: e202244016.
[31]	杨小环, 杨婧怡, 王子然, 等. 六价铬对红芸豆种子萌发和幼苗生长的毒害作用及外源NO的缓解效应 [J]. 中国生态农业学报: 中英文, 2024, 32(8): 1366-1376.
	Yang XH, Yang JY, Wang ZR, et al. Toxic effect of hexavalent chromium on seed germination and seedling growth of red kidney bean and the alleviation effect of exogenous NO [J]. Chin J Eco Agric, 2024, 32(8): 1366-1376.
[32]	王志科, 王金成. 外源NO对NaCl胁迫下玉米种子萌发和幼苗生理特性的影响 [J]. 山东农业科学, 2025, 57(2): 78-83.
	Wang ZK, Wang JC. Effects of exogenous nitric oxide on seed germination and seedling physiological characteristics of maize under NaCl stress [J]. Shandong Agric Sci, 2025, 57(2): 78-83.
[33]	吴建飞, 黄茵, 温天旺, 等. 硝普钠浸种对铜胁迫下棉花种子萌发和幼苗抗氧化系统及铜离子吸收分配的影响 [J]. 农业环境科学学报, 2025, 44(1): 31-40.
	Wu JF, Huang Y, Wen TW, et al. Effects of seed presoaking with sodium nitroprussiate on cotton seed germination, antioxidant system, and copper ion uptake and distribution under copper stress [J]. J Agro Environ Sci, 2025, 44(1): 31-40.
[34]	Liu FF, Qiao XH, Yang T, et al. Nitric oxide promoted the seed germination of Cynanchum auriculatum under cadmium stress [J]. Agronomy, 2024, 14(1): 86.
[35]	尹美强, 王栋, 王金荣, 等. 外源一氧化氮对盐胁迫下高粱种子萌发及淀粉转化的影响 [J]. 中国农业科学, 2019, 52(22): 4119-4128.
	Yin MQ, Wang D, Wang JR, et al. Effects of exogenous nitric oxide on seed germination and starch transformation of sorghum seeds under salt stress [J]. Sci Agric Sin, 2019, 52(22): 4119-4128.
[36]	Shu K, Liu XD, Xie Q, et al. Two faces of one seed: hormonal regulation of dormancy and germination [J]. Mol Plant, 2016, 9(1): 34-45.
[37]	Sano N, Marion-Poll A. ABA metabolism and homeostasis in seed dormancy and germination [J]. Int J Mol Sci, 2021, 22(10): 5069.
[38]	Xu JR, Lu XF, Liu YZ, et al. Interaction between ABA and NO in plants under abiotic stresses and its regulatory mechanisms [J]. Front Plant Sci, 2024, 15: 1330948.
[39]	Liu YG, Shi L, Ye NH, et al. Nitric oxide-induced rapid decrease of abscisic acid concentration is required in breaking seed dormancy in Arabidopsis [J]. New Phytol, 2009, 183(4): 1030-1042.
[40]	Andryka-Dudek P, Ciacka K, Wiśniewska A, et al. Nitric oxide-induced dormancy removal of apple embryos is linked to alterations in expression of genes encoding ABA and JA biosynthetic or transduction pathways and RNA nitration [J]. Int J Mol Sci, 2019, 20(5): 1007.
[41]	Wang PC, Du YY, Hou YJ, et al. Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1 [J]. Proc Natl Acad Sci USA, 2015, 112(2): 613-618.
[42]	Iqbal N, Umar S, Khan NA, et al. Crosstalk between abscisic acid and nitric oxide under heat stress: exploring new vantage points [J]. Plant Cell Rep, 2021, 40(8): 1429-1450.
[43]	Kępczyński J, Wójcik A, Dziurka M. NO-mediated dormancy release of Avena fatua caryopses is associated with decrease in abscisic acid sensitivity, content and ABA/GAs ratios [J]. Planta, 2023, 257(6): 101.
[44]	Bethke PC, Libourel IGL, Aoyama N, et al. The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy [J]. Plant Physiol, 2007, 143(3): 1173-1188.
[45]	Nagel M, Alqudah AM, Bailly M, et al. Novel loci and a role for nitric oxide for seed dormancy and preharvest sprouting in barley [J]. Plant Cell Environ, 2019, 42(4): 1318-1327.
[46]	Carrillo-Barral N, Matilla AJ, Iglesias-Fernández R, et al. Nitrate-induced early transcriptional changes during imbibition in non-after-ripened Sisymbrium officinale seeds [J]. Physiol Plant, 2013, 148(4): 560-573.
[47]	Zhao CH, Zhang Y, Yang L. Integrating physiology, transcriptome, and metabolomics reveals the potential mechanism of nitric oxide concentration-dependent regulation of embryo germination in Sorbus pohuashanensis [J]. Plants, 2025, 14(3): 344.
[48]	Gniazdowska A, Krasuska U, Bogatek R. Dormancy removal in apple embryos by nitric oxide or cyanide involves modifications in ethylene biosynthetic pathway [J]. Planta, 2010, 232(6): 1397-1407.
[49]	Gniazdowska A, Dobrzyńska U, Babańczyk T, et al. Breaking the apple embryo dormancy by nitric oxide involves the stimulation of ethylene production [J]. Planta, 2007, 225(4): 1051-1057.
[50]	Sami A, Rehman S, Tanvir MA, et al. Assessment of the germination potential of Brassica oleracea seeds treated with karrikin 1 and cyanide, which modify the ethylene biosynthetic pathway [J]. J Plant Growth Regul, 2021, 40(3): 1257-1269.
[51]	Jacobsen JV, Barrero JM, Hughes T, et al. Roles for blue light, jasmonate and nitric oxide in the regulation of dormancy and germination in wheat grain (Triticum aestivum L.) [J]. Planta, 2013, 238(1): 121-138.
[52]	Bailly C. The signalling role of ROS in the regulation of seed germination and dormancy [J]. Biochem J, 2019, 476(20): 3019-3032.
[53]	Ye TT, Ma TX, Chen Y, et al. The role of redox-active small molecules and oxidative protein post-translational modifications in seed aging [J]. Plant Physiol Biochem, 2024, 213: 108810.
[54]	EL-MAAROUF-BOUTEAU H, Sajjad Y, Bazin J, et al. Reactive oxygen species, abscisic acid and ethylene interact to regulate sunflower seed germination [J]. Plant Cell Environ, 2015, 38(2): 364-374.
[55]	Yiğit İ, Atici Ö. Seed priming with nitric oxide mitigates exogenous methylglyoxal toxicity by restoring glyoxalase and antioxidant systems in germinating maize (Zea mays L.) seeds [J]. Cereal Res Commun, 2022, 50(4): 811-820.
[56]	Liu YG, Ye NH, Liu R, et al. H₂O₂ mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination [J]. J Exp Bot, 2010, 61(11): 2979-2990.
[57]	Ciacka K, Tyminski M, Gniazdowska A, et al. Nitric oxide as a remedy against oxidative damages in apple seeds undergoing accelerated ageing [J]. Antioxidants, 2021, 11(1): 70.
[58]	Lin W, Shang JX, Li XY, et al. Nitric oxide regulates multiple signal pathways in plants via protein S-nitrosylation [J]. Curr Issues Mol Biol, 2025, 47(6): 407.
[59]	Bai XG, Yang LM, Tian MH, et al. Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation [J]. PLoS One, 2011, 6(6): e20714.
[60]	Albertos P, Romero-Puertas MC, Tatematsu K, et al. S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth [J]. Nat Commun, 2015, 6: 8669.
[61]	Wang PC, Zhu JK, Lang ZB. Nitric oxide suppresses the inhibitory effect of abscisic acid on seed germination by S-nitrosylation of SnRK2 proteins [J]. Plant Signal Behav, 2015, 10(6): e1031939.
[62]	Zhao HY, Ma L, Shen JL, et al. S-nitrosylation of the transcription factor MYB30 facilitates nitric oxide-promoted seed germination in Arabidopsis [J]. Plant Cell, 2024, 36(2): 367-382.
[63]	Zeng MY, He YQ, Gao X, et al. Characteristics and functions of glyceraldehyde 3-phosphate dehydrogenase S-nitrosylation during controlled aging of elm and Arabidopsis seeds [J]. J Exp Bot, 2021, 72(20): 7020-7034.
[64]	Ying SB, Yang WJ, Li P, et al. Phytochrome B enhances seed germination tolerance to high temperature by reducing S-nitrosylation of HFR1 [J]. EMBO Rep, 2022, 23(10): e54371.
[65]	Wei WJ, Hu YL, Yang WJ, et al. S-nitrosoglutathion reductase activity modulates the thermotolerance of seeds germination by controlling ABI5 stability under high temperature [J]. Phyton Int J Exp Bot, 2021, 90(4): 1075-1087.
[66]	León J. Protein tyrosine nitration in plant nitric oxide signaling [J]. Front Plant Sci, 2022, 13: 859374.
[67]	Castillo MC, Lozano-Juste J, González-Guzmán M, et al. Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants [J]. Sci Signal, 2015, 8(392): ra89.
[68]	Vollár M, Feigl G, Oláh D, et al. Nitro-oleic acid in seeds and differently developed seedlings of Brassica napus L [J]. Plants, 2020, 9(3): 406.
[69]	Sun CL, Zhang YX, Liu LJ, et al. Molecular functions of nitric oxide and its potential applications in horticultural crops [J]. Hortic Res, 2021, 8(1): 71.
[70]	Wang RR, Wang MF, Yang L. Antagonistic effects of nitric oxide and far-red light on Sorbus pohuashanensis embryo germination [J]. J Plant Growth Regul, 2025. .
[71]	Liu SJ, Song SH, Wang WQ, et al. De novo assembly and characterization of germinating lettuce seed transcriptome using Illumina paired-end sequencing [J]. Plant Physiol Biochem, 2015, 96: 154-162.
[72]	Pande A, Mun BG, Methela NJ, et al. Heavy metal toxicity in plants and the potential NO-releasing novel techniques as the impending mitigation alternatives [J]. Front Plant Sci, 2022, 13: 1019647.
[73]	Ciacka K, Krasuska U, Staszek P, et al. Effect of nitrogen reactive compounds on aging in seed [J]. Front Plant Sci, 2020, 11: 101