
Chloroplast-Derived Reactive Oxygen Species Dynamics Mediate Jasmonic Acid-Induced Drought Tolerance in Rice
Received date: 2026-01-13
Accepted date: 2026-03-11
Online published: 2026-04-01
Beyond their central role in photosynthesis and plant productivity, chloroplasts are emerging as key regulators of plant responses and tolerance to abiotic stress. However, the molecular mechanisms linking chloroplastic reactive oxygen species (ROS) metabolism to stress adaptation remain poorly understood. Here, we show that knockout of OsJAZ9, a repressor of jasmonic acid (JA) signaling, enhances JA response and drought tolerance in rice by suppressing cellular ROS accumulation. Time-lapse visualization of subcellular ROS dynamics revealed that stress-induced ROS accumulation was initiated in chloroplasts and subsequently propagated to the cytoplasm. Notably, loss of OsJAZ9 markedly suppressed chloroplastic ROS accumulation, resulting in reduced cellular ROS levels under stress conditions. Consistently, either JA treatment or overexpression of the JA-responsive chloroplastic ROS scavenger OsFeSOD3 was sufficient to attenuate chloroplastic ROS accumulation and enhance drought tolerance in rice. Furthermore, two-year agronomic field analyses showed that osjaz9 knockout rice exhibited improved grain yield, particularly under drought stress conditions. Together, our findings identify chloroplast-derived ROS dynamics as a pivotal molecular link between JA signaling and rice stress tolerance and highlight OsJAZ9 as a promising molecular target for developing high-yielding, stress-tolerant rice cultivars.
Key words: jasmonic acid; OsJAZ9; abiotic stress; reactive oxygen species; chloroplast; rice
Jiwoong Jung , Deok Hyun Seo , Youngdae Yoon , Geupil Jang . Chloroplast-Derived Reactive Oxygen Species Dynamics Mediate Jasmonic Acid-Induced Drought Tolerance in Rice[J]. Rice Science, 2026 , 33(4) : 531 -544 . DOI: 10.1016/j.rsci.2026.03.005
| [1] | Apel K, Hirt H. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol, 55: 373-399. |
| [2] | Aslam M M, Rashid M A R, Siddiqui M A, et al. 2022. Recent insights into signaling responses to cope drought stress in rice. Rice Sci, 29(2): 105-117. |
| [3] | Awan S A, Khan I, Rizwan M, et al. 2021. Exogenous abscisic acid and jasmonic acid restrain polyethylene glycol-induced drought by improving the growth and antioxidative enzyme activities in pearl millet. Physiol Plant, 172(2): 809-819. |
| [4] | Benitez-Alfonso Y, Soanes B K, Zimba S, et al. 2023. Enhancing climate change resilience in agricultural crops. Curr Biol, 33(23): R1246-R1261. |
| [5] | Bonifacio A, Martins M O, Ribeiro C W, et al. 2011. Role of peroxidases in the compensation of cytosolic ascorbate peroxidase knockdown in rice plants under abiotic stress. Plant Cell Environ, 34(10): 1705-1722. |
| [6] | Bournonville C F G, Díaz-Ricci J C. 2011. Quantitative determination of superoxide in plant leaves using a mondified NBT staining method. Phytochem Anal, 22(3): 268-271. |
| [7] | Chen L G, Song Y, Li S J, et al. 2012. The role of WRKY transcription factors in plant abiotic stresses. Biochim Biophys Acta: Gene Regul Mech, 1819(2): 120-128. |
| [8] | Chini A, Fonseca S, Fernández G, et al. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature, 448: 666-671. |
| [9] | Cordeiro A M, Figueiredo D D, Tepperman J, et al. 2016. Rice phytochrome-interacting factor protein OsPIF14 represses OsDREB1B gene expression through an extended N-box and interacts preferentially with the active form of phytochrome B. Biochim Biophys Acta: Gene Regul Mech, 1859(2): 393-404. |
| [10] | de Vos K, Janssens C, Jacobs L, et al. 2023. Rice availability and stability in Africa under future socio-economic development and climatic change. Nat Food, 4(6): 518-527. |
| [11] | Del Río L A. 2015. ROS and RNS in plant physiology: An overview. J Exp Bot, 66(10): 2827-2837. |
| [12] | Deng H Y, Li Q, Cao R Z, et al. 2023. Overexpression of SmMYC2 enhances salt resistance in Arabidopsis thaliana and Salvia miltiorrhiza hairy roots. J Plant Physiol, 280: 153862. |
| [13] | Ekanayake I J, de Datta S K, Steponkus P L. 1989. Spikelet sterility and flowering response of rice to water stress at anthesis. Ann Bot, 63(2): 257-264. |
| [14] | Finkel T, Holbrook N J. 2000. Oxidants, oxidative stress and the biology of ageing. Nature, 408: 239-247. |
| [15] | Gebrechorkos S H, Sheffield J, Vicente-Serrano S M, et al. 2025. Warming accelerates global drought severity. Nature, 642: 628-635. |
| [16] | Ghosh S, Kanwar P, Jha G. 2017. Alterations in rice chloroplast integrity, photosynthesis and metabolome associated with pathogenesis of Rhizoctonia solani. Sci Rep, 7: 41610. |
| [17] | Guan Q J, Liao X, He M L, et al. 2017. Tolerance analysis of chloroplast OsCu/Zn-SOD overexpressing rice under NaCl and NaHCO3 stress. PLoS One, 12(10): e0186052. |
| [18] | Gupta A S, Heinen J L, Holaday A S, et al. 1993a. Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc Natl Acad Sci USA, 90(4): 1629-1633. |
| [19] | Gupta A S, Webb R P, Holaday A S, et al. 1993b. Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiol, 103(4): 1067-1073. |
| [20] | Hou X L, Lee L Y C, Xia K F, et al. 2010. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell, 19(6): 884-894. |
| [21] | Ikeda A, Ueguchi-Tanaka M, Sonoda Y, et al. 2001. slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell, 13(5): 999-1010. |
| [22] | Jang G, Lee S, Um T Y, et al. 2016. Genetic chimerism of CRISPR/ Cas9-mediated rice mutants. Plant Biotechnol Rep, 10(6): 425-435. |
| [23] | Jang G, Yoon Y, Choi Y D. 2020. Crosstalk with jasmonic acid integrates multiple responses in plant development. Int J Mol Sci, 21(1): 305. |
| [24] | Jeong J S, Kim Y S, Redillas M C F R, et al. 2013. OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant Biotechnol J, 11(1): 101-114. |
| [25] | Jin G C, Qi J F, Zu H Y, et al. 2023. Jasmonate-mediated gibberellin catabolism constrains growth during herbivore attack in rice. Plant Cell, 35(10): 3828-3844. |
| [26] | Khan M I R, Kumari S, Nazir F, et al. 2023. Defensive role of plant hormones in advancing abiotic stress-resistant rice plants. Rice Sci, 30(1): 15-35. |
| [27] | Kim H, Seomun S, Yoon Y, et al. 2021. Jasmonic acid in plant abiotic stress tolerance and interaction with abscisic acid. Agronomy, 11(9): 1886. |
| [28] | Kim J, Jang G. 2025. ALB7 regulates chloroplast development by controlling the PEP-dependent expression of chloroplast genes. Plant Biotechnol Rep, 19(4): 363-372. |
| [29] | Li L L, Zhang H H, Yang Z H, et al. 2022. Independently evolved viral effectors convergently suppress DELLA protein SLR1-mediated broad-spectrum antiviral immunity in rice. Nat Commun, 13(1): 6920. |
| [30] | Li P, Li X W, Jiang M. 2021. CRISPR/Cas9-mediated mutagenesis of WRKY3 and WRKY4 function decreases salt and Me-JA stress tolerance in Arabidopsis thaliana. Mol Biol Rep, 48(8): 5821-5832. |
| [31] | Li Z, Rosa L, Gorelick S. 2025. Severe floods significantly reduce global rice yields. Sci Adv, 11(46): eadx7799. |
| [32] | Liao Z G, Yu H, Duan J B, et al. 2019. SLR1 inhibits MOC1 degradation to coordinate tiller number and plant height in rice. Nat Commun, 10(1): 2738. |
| [33] | Lim C W, Han S W, Hwang I S, et al. 2015. The pepper lipoxygenase CaLOX1 plays a role in osmotic, drought and high salinity stress response. Plant Cell Physiol, 56(5): 930-942. |
| [34] | Llorente B, Segretin M E, Giannini E, et al. 2021. Homecoming: Rewinding the reductive evolution of the chloroplast genome for increasing crop yields. Nat Commun, 12(1): 6734. |
| [35] | Lu Y Z, Feng Z, Bian L Y, et al. 2010. miR398 regulation in rice of the responses to abiotic and biotic stresses depends on CSD1 and CSD2 expression. Funct Plant Biol, 38(1): 44-53. |
| [36] | Maruta T, Tanouchi A, Tamoi M, et al. 2010. Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol, 51(2): 190-200. |
| [37] | Miller G, Suzuki N, Ciftci-Yilmaz S, et al. 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ, 33(4): 453-467. |
| [38] | Mittler R. 2017. ROS are good. Trends Plant Sci, 22(1): 11-19. |
| [39] | Mittler R, Zandalinas S I, Fichman Y, et al. 2022. Reactive oxygen species signalling in plant stress responses. Nat Rev Mol Cell Biol, 23(10): 663-679. |
| [40] | Mur L A J, Kenton P, Draper J. 2005. In planta measurements of oxidative bursts elicited by avirulent and virulent bacterial pathogens suggests that H2O2 is insufficient to elicit cell death in tobacco. Plant Cell Environ, 28(4): 548-561. |
| [41] | Myouga F, Hosoda C, Umezawa T, et al. 2008. A hetero complex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell, 20(11): 3148-3162. |
| [42] | Panda D, Mishra S S, Behera P K. 2021. Drought tolerance in rice: Focus on recent mechanisms and approaches. Rice Sci, 28(2): 119-132. |
| [43] | Park D, Jang J, Seo D H, et al. 2024. Bacillus velezensis GH1-13 enhances drought tolerance in rice by reducing the accumulation of reactive oxygen species. Front Plant Sci, 15: 1432494. |
| [44] | Pnueli L, Liang H J, Rozenberg M, et al. 2003. Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J, 34(2): 187-203. |
| [45] | Queval G, Issakidis-Bourguet E, Hoeberichts F A, et al. 2007. Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell death. Plant J, 52(4): 640-657. |
| [46] | Rao M V, Lee H, Creelman R A, et al. 2000. Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell, 12(9): 1633-1646. |
| [47] | Seo D H, Jang J, Park D, et al. 2024. PEP-ASSOCIATED PROTEIN 3 regulates rice tiller formation and grain yield by controlling chloroplast biogenesis. Plant Physiol, 194(2): 805-818. |
| [48] | Seo D H, Jung J, Jang G. 2026. OsFeSOD3 functions as an enzymatic component of the PEP complex, bifunctionally regulating chloroplastic ROS metabolism and chloroplast biogenesis in rice. Plant Biotechnol J, 24(4): 2475-2491. |
| [49] | Seo J S, Joo J, Kim M J, et al. 2011. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J, 65(6): 907-921. |
| [50] | Sheard L B, Tan X, Mao H B, et al. 2010. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature, 468: 400-405. |
| [51] | Shim J S, Park S H, Lee D K, et al. 2021. The rice GLYCINE-RICH PROTEIN 3 confers drought tolerance by regulating mRNA stability of ROS scavenging-related genes. Rice, 14(1): 31. |
| [52] | Singh P, Pokharia C, Shah K. 2021. Exogenous peroxidase mitigates cadmium toxicity, enhances rhizobial population and lowers root knot formation in rice seedlings. Rice Sci, 28(2): 166-177. |
| [53] | Surendran U, Raja P, Jayakumar M, et al. 2021. Use of efficient water saving techniques for production of rice in India under climate change scenario: A critical review. J Clean Prod, 309: 127272. |
| [54] | Thines B, Katsir L, Melotto M, et al. 2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature, 448: 661-665. |
| [55] | Tran B L, Tseng W C, Chen C C. 2025. Climate change impacts on crop yields across temperature rise thresholds and climate zones. Sci Rep, 15(1): 23424. |
| [56] | Wang G L, Long Y F, Jin X Y, et al. 2024. SbMYC2 mediates jasmonic acid signaling to improve drought tolerance via directly activating SbGR1 in sorghum. Theor Appl Genet, 137(3): 72. |
| [57] | Wang P T, Liu W C, Han C, et al. 2024. Reactive oxygen species: Multidimensional regulators of plant adaptation to abiotic stress and development. J Integr Plant Biol, 66(3): 330-367. |
| [58] | Wang W M, Xie Z Z, Wu Y Y, et al. 2024. The JA-OsJAZ6-DELLA module controls the tillering and drought stress response in rice. Environ Exp Bot, 222: 105776. |
| [59] | Wasternack C, Song S S. 2017. Jasmonates: Biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J Exp Bot, 68(6): 1303-1321. |
| [60] | Wellburn A R. 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(3): 307-313. |
| [61] | Yoon Y, Seo D H, Shin H, et al. 2020. The role of stress-responsive transcription factors in modulating abiotic stress tolerance in plants. Agronomy, 10(6): 788. |
| [62] | Zhang H M, Zhu J H, Gong Z Z, et al. 2022. Abiotic stress responses in plants. Nat Rev Genet, 23(2): 104-119. |
| [63] | Zhang Y, Su J B, Duan S, et al. 2011. A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods, 7(1): 30. |
| [64] | Zhuang Y, Wei M, Ling C C, et al. 2021. EGY3 mediates chloroplastic ROS homeostasis and promotes retrograde signaling in response to salt stress in Arabidopsis. Cell Rep, 36(2): 109384. |
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