OsCERK1 Interacts with OsHPP08 to Regulate Copper Uptake and Blast Resistance in Rice
Received date: 2024-09-18
Accepted date: 2025-01-23
Online published: 2025-04-14
The cell surface receptor chitin elicitor receptor kinase 1 (CERK1) is a well-known component of plant immunity. OsCERK1 is involved in regulating copper (Cu) uptake in rice, though the underlying mechanisms remain elusive. In this study, we identified proteins interacting with OsCERK1 and uncovered a novel heavy metal-associated domain-containing protein, OsHPP08. Our findings demonstrate that OsCERK1 phosphorylated and stabilized OsHPP08. Through structural analysis using AlphaFold, a yeast sensitivity assay of the Cu uptake-deficient yeast mutant, and Cu level measurements in oshpp08 mutants and overexpression plants (OsHPP08OE), we revealed that OsHPP08 facilitated Cu uptake. Additionally, rice seedling infection assays demonstrated that OsHPP08 positively contributed to blast resistance, with both OsCERK1 and OsHPP08 being essential for Cu-modulated blast resistance. Further analyses suggested that OsCERK1 and OsHPP08 likely enhanced blast resistance by regulating the antioxidant system and increasing H2O2 accumulation. In conclusion, OsCERK1 promoted Cu uptake by stabilizing OsHPP08, and together they contributed to Cu-modulated blast resistance, likely through the modulation of reactive oxygen species accumulation. These findings deepen our understanding of the intricate interplay between biotic and abiotic signals in rice.
Chen Ya, Liu Zhiquan, Yang Linyin, Wu Fujie, Cao Zijian, Shi Huanbin, Qiu Jiehua, Kou Yanjun . OsCERK1 Interacts with OsHPP08 to Regulate Copper Uptake and Blast Resistance in Rice[J]. Rice Science, 2025 , 32(2) : 203 -216 . DOI: 10.1016/j.rsci.2025.02.001
| [1] | Ao Y, Li Z Q, Feng D R, et al. 2014. OsCERK1 and OsRLCK176 play important roles in peptidoglycan and chitin signaling in rice innate immunity. Plant J, 80(6): 1072-1084. |
| [2] | Bi G Z, Hu M, Fu L, et al. 2022. The cytosolic thiol peroxidase PRXIIB is an intracellular sensor for H2O2 that regulates plant immunity through a redox relay. Nat Plants, 8(10): 1160-1175. |
| [3] | Cao H W, Zhao Y N, Liu X S, et al. 2022. A metal chaperone OsHIPP16 detoxifies cadmium by repressing its accumulation in rice crops. Environ Pollut, 311: 120058. |
| [4] | Chen G Q, Xiong S. 2021. OsHIPP24 is a copper metallochaperone which affects rice growth. J Plant Biol, 64(2): 145-153. |
| [5] | Chen Y, Liu Z Q, Meng S, et al. 2022. OsCERK1 contributes to cupric oxide nanoparticles induced phytotoxicity and basal resistance against blast by regulating the anti-oxidant system in rice. J Fungi, 9(1): 36. |
| [6] | Choudhary R C, Kumaraswamy R V, Kumari S, et al. 2017. Cu-chitosan nanoparticle boost defense responses and plant growth in maize (Zea mays L.). Sci Rep, 7(1): 9754. |
| [7] | Chowdhury A R, Kumar R, Mahanty A, et al. 2024. Inhibitory role of copper and silver nanocomposite on important bacterial and fungal pathogens in rice (Oryza sativa). Sci Rep, 14(1): 1779. |
| [8] | Colangelo E P, Guerinot M L. 2006. Put the metal to the petal: Metal uptake and transport throughout plants. Curr Opin Plant Biol, 9(3): 322-330. |
| [9] | de Abreu-Neto J B, Turchetto-Zolet A C, de Oliveira L F V, et al. 2013. Heavy metal-associated isoprenylated plant protein (HIPP): Characterization of a family of proteins exclusive to plants. FEBS J, 280(7): 1604-1616. |
| [10] | Dykema P E, Sipes P R, Marie A, et al. 1999. A new class of proteins capable of binding transition metals. Plant Mol Biol, 41(1): 139-150. |
| [11] | Espinoza C, Liang Y, Stacey G. 2017. Chitin receptor CERK 1 links salt stress and chitin-triggered innate immunity in Arabidopsis. Plant J, 89(5): 984-995. |
| [12] | Feng S J, Liu X S, Cao H W, et al. 2021. Identification of a rice metallochaperone for cadmium tolerance by an epigenetic mechanism and potential use for clean up in wetland. Environ Pollut, 288: 117837. |
| [13] | Hayafune M, Berisio R, Marchetti R, et al. 2014. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc Natl Acad Sci USA, 111(3): E404-E413. |
| [14] | Kennedy P H, Alborzian Deh Sheikh A, Balakar M, et al. 2024. Post-translational modification-centric base editor screens to assess phosphorylation site functionality in high throughput. Nat Methods, 21(6): 1033-1043. |
| [15] | Khan I U, Rono J K, Zhang B Q, et al. 2019. Identification of novel rice (Oryza sativa) HPP and HIPP genes tolerant to heavy metal toxicity. Ecotoxicol Environ Saf, 175: 8-18. |
| [16] | Khan I U, Rono J K, Liu X S, et al. 2020. Functional characterization of a new metallochaperone for reducing cadmium concentration in rice crop. J Clean Prod, 272: 123152. |
| [17] | Li Z Y, Wei X J, Tong X H, et al. 2022. The OsNAC23-Tre6P- SnRK1a feed-forward loop regulates sugar homeostasis and grain yield in rice. Mol Plant, 15(4): 706-722. |
| [18] | Liu B, Li J F, Ao Y, et al. 2012. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell, 24(8): 3406-3419. |
| [19] | Liu Z Q, Qiu J H, Shen Z N, et al. 2023. The E3 ubiquitin ligase OsRGLG5 targeted by the Magnaporthe oryzae effector AvrPi9 confers basal resistance against rice blast. Plant Commun, 4(5): 100626. |
| [20] | Maidment J H R, Franceschetti M, Maqbool A, et al. 2021. Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense. J Biol Chem, 296: 100371. |
| [21] | Park C H, Chen S B, Shirsekar G, et al. 2012. The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. Plant Cell, 24(11): 4748-4762. |
| [22] | Priya M, Venkatesan R, Deepa S, et al. 2023. Green synthesis, characterization, antibacterial, and antifungal activity of copper oxide nanoparticles derived from Morinda citrifolia leaf extract. Sci Rep, 13(1): 18838. |
| [23] | Qiu J H, Chen Y, Liu Z Q, et al. 2023. The application of zinc oxide nanoparticles: An effective strategy to protect rice from rice blast and abiotic stresses. Environ Pollut, 331: 121925. |
| [24] | Raffaele S, Bayer E, Lafarge D, et al. 2009. Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell, 21(5): 1541-1555. |
| [25] | Rono J K, Sun D, Yang Z M. 2022. Metallochaperones: A critical regulator of metal homeostasis and beyond. Gene, 822: 146352. |
| [26] | Shi H B, Meng S, Qiu J H, et al. 2021. MoWhi2 regulates appressorium formation and pathogenicity via the MoTor signalling pathway in Magnaporthe oryzae. Mol Plant Pathol, 22(8): 969-983. |
| [27] | Shi Y, Jiang N, Wang M T, et al. 2023. OsHIPP17 is involved in regulating the tolerance of rice to copper stress. Front Plant Sci, 14: 1183445. |
| [28] | Song H D, Lin B R, Huang Q L, et al. 2021. The Meloidogyne graminicola effector MgMO289 targets a novel copper metallochaperone to suppress immunity in rice. J Exp Bot, 72(15): 5638-5655. |
| [29] | Tehseen M, Cairns N, Sherson S, et al. 2010. Metallochaperone- like genes in Arabidopsis thaliana. Metallomics, 2(8): 556-564. |
| [30] | Tsuda K, Katagiri F. 2010. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol, 13(4): 459-465. |
| [31] | Wang C, Wang G, Zhang C, et al. 2017. OsCERK1-mediated chitin perception and immune signaling requires receptor-like cytoplasmic kinase 185 to activate an MAPK cascade in rice. Mol Plant, 10(4): 619-633. |
| [32] | Wang J W, Li Y, Zhang Y X, et al. 2013. Molecular cloning and characterization of a Brassica juncea yellow stripe-like gene, BjYSL7, whose overexpression increases heavy metal tolerance of tobacco. Plant Cell Rep, 32(5): 651-662. |
| [33] | Wintz H, Fox T, Wu Y Y, et al. 2003. Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem, 278(48): 47644-47653. |
| [34] | Xiong S, Kong X H, Chen G Q, et al. 2023. Metallochaperone OsHIPP9 is involved in the retention of cadmium and copper in rice. Plant Cell Environ, 46(6): 1946-1961. |
| [35] | Xu L, Wang J Z, Xiao Y, et al. 2022. Structural insight into chitin perception by chitin elicitor receptor kinase 1 of Oryza sativa. J Integr Plant Biol, 65(1): 235-248. |
| [36] | Yamaguchi K, Imai K, Akamatsu A, et al. 2012. SWAP70 functions as a Rac/Rop guanine nucleotide-exchange factor in rice. Plant J, 70(3): 389-397. |
| [37] | Yang C, Liu R, Pang J H, et al. 2021. Poaceae-specific cell wall- derived oligosaccharides activate plant immunity via OsCERK1 during Magnaporthe oryzae infection in rice. Nat Commun, 12(1): 2178. |
| [38] | Yeon J, Park A R, Nguyen H T T, et al. 2022. Inhibition of oomycetes by the mixture of maleic acid and copper sulfate. Plant Dis, 106(3): 960-965. |
| [39] | Yuan M, Chu Z H, Li X H, et al. 2010. The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution. Plant Cell, 22(9): 3164-3176. |
| [40] | Zhang B Q, Liu X S, Feng S J, et al. 2020. Developing a cadmium resistant rice genotype with OsHIPP29 locus for limiting cadmium accumulation in the paddy crop. Chemosphere, 247: 125958. |
| [41] | Zhang C, He J M, Dai H L, et al. 2021. Discriminating symbiosis and immunity signals by receptor competition in rice. Proc Natl Acad Sci USA, 118(16): e2023738118. |
| [42] | Zhang X, Liu Y, Yuan G X, et al. 2024. The synthetic NLR RGA5HMA5 requires multiple interfaces within and outside the integrated domain for effector recognition. Nat Commun, 15(1): 1104. |
| [43] | Zhang Y Y, Chen K, Zhao F J, et al. 2018. OsATX1 interacts with heavy metal P1B-type ATPases and affects copper transport and distribution. Plant Physiol, 178(1): 329-344. |
| [44] | Zhao Y N, Wang M Q, Li C, et al. 2022. The metallochaperone OsHIPP56 gene is required for cadmium detoxification in rice crops. Environ Exp Bot, 193: 104680. |
| [45] | Zheng T H, Sun J, Zhou S R, et al. 2019. Post-transcriptional regulation of Ghd7 protein stability by phytochrome and OsGI in photoperiodic control of flowering in rice. New Phytol, 224(1): 306-320. |
| [46] | Zschiesche W, Barth O, Daniel K, et al. 2015. The zinc-binding nuclear protein HIPP 3 acts as an upstream regulator of the salicylate-dependent plant immunity pathway and of flowering time in Arabidopsis thaliana. New Phytol, 207(4): 1084-1096. |
/
| 〈 |
|
〉 |