Personal Information

Principal Investigator

Email:chanhongkim@psc.ac.cn
Personal Web:


Research Direction

Photosynthesis and Stress Signaling


Research Unit

Chanhong Kim

Personal Profile

2020 – Present: Principal Investigator, Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, China
2014 – 2020: Principal Investigator, Shanghai Center for Plant Stress Biology, Chinese Academy of Sciences,
2008 – 2014: Senior Research Associate, Boyce Thompson Institute, Cornell University, USA
2006 – 2008: Senior Research Associate, Institute of Plant Sciences, ETH Zurich, Switzerland
2004 – 2006: Postdoctoral Fellow, Institute of Plant Sciences, ETH Zurich, Switzerland
2000 – 2004: Ph.D., Institute of Plant Sciences, ETH Zurich, Switzerland


Research Work

    The central theme of our research is to unravel the molecular and biochemical regulatory mechanisms behind organelle-to-nucleus retrograde signaling, which is crucial for cellular homeostasis and adaptation to changing environmental conditions. We are particularly focused on how chloroplasts detect environmental fluctuations and relay signals to activate cellular stress responses. Our long-term goal is to decode the chloroplast-generated chemical signals that elicit specific stress responses to various environmental factors, ultimately aiming to enhance crop stress tolerance.




Main Achievements

    As major research accomplishments, our team has identified that the oxidation of tryptophan residues in photosystem II reaction center proteins and specific ROS-sensing chloroplast proteins initiates retrograde signaling from chloroplasts to the nucleus, activating both stress and protective responses in plants (Wang et al., 2016, PNAS; Dogra et al., 2019, Nature Commun.; Dogra et al., 2022, Mol Plant; Lee, Kim. 2024, New Phytol).

    Furthermore, we demonstrated that interactions between chloroplast ROS signaling and plant stress hormones—primarily salicylic acid and jasmonic acid—highlight the role of chloroplasts as complex environmental sensors that integrate multiple stress signals to drive adaptive responses (Li et al., 2020, Plant Cell; Fang et al., 2022, PNAS; Li et al., 2022, Plant Physiology; Lee et al., 2023, Plant Physiol.; Shi et al., 2024, Plant Commun.; Lee et al., 2024, Plant Cell).

    We have also identified potential chloroplast thermosensor proteins that are essential for chloroplast biogenesis and thermal tolerance, particularly during germination. Our ongoing research explores these thermosensors further to elucidate chloroplast’s roles in managing temperature stress during the shift from heterotrophic to photoautotrophic growth.

    We anticipate that our findings will greatly advance our understanding of chloroplast functions in stress responses, providing a robust foundation for enhancing plant resilience and boosting crop yields.



Publications

61. Lee KP, Kim C. Photosynthetic ROS and retrograde signaling pathways. New Phytol. 2024 Sep 17. doi: 10.1111/nph.20134. Online ahead of print. PMID: 39286853 Tansley review.


60. Jiang W, Wang Z, Li Y, Liu X, Ren Y, Li C, Luo S, Singh RM, Li Y, Kim C, Zhao C.FERONIA regulates salt tolerance in Arabidopsis by controlling photorespiratory flux. Plant Cell. 2024 Aug 28:koae246. doi: 10.1093/plcell/koae246. Online ahead of print. PMID: 39197037


59. Wu XX, Mu WH, Li F, Sun SY, Cui CJ, Kim C, Zhou F, Zhang Y. Cryo-EM structures of the plant plastid-encoded RNA polymerase. Cell. 2024 Feb 29;187(5):1127-1144.e21. doi: 10.1016/j.cell.2024.01.026.

58. Shi J, Wang H, Li M, Mi L, Gao Y, Qiang S, Zhang Y, Chen D, Dai X, Ma H, Lu H, Kim C, Chen S. Alternaria TeA toxin activates a chloroplast retrograde signaling pathway to facilitate JA-dependent pathogenicity. Plant Commun. 2023 Dec 4:100775. doi: 10.1016/j.xplc.2023.100775. 


57. Lee KP, Liu K, Kim EY, Medina-Puche L, Dong H, Di M, Singh RM, Li M, Qi S, Meng Z, Cho J, Zhang H, Lozano-Duran R, Kim C. The m6A reader ECT1 drives mRNA sequestration to dampen salicylic acid-dependent stress responses in Arabidopsis.Plant Cell. 2023 Dec 2:koad300. doi: 10.1093/plcell/koad300. 


56. Pan T, Liu Y, Hu X, Li P, Lin C, Tang Y, Tang W, Liu Y, Guo L, Kim C, Fang J, Lin H, Wu Z, Blumwald E, Wang S. Stress-induced endocytosis from chloroplast inner envelope membrane is mediated by CHLOROPLAST VESICULATION but inhibited by GAPC. Cell Rep. 2023 Oct 3;42(10):113208. doi: 10.1016/j.celrep.2023.113208. Online ahead of print.


55. Kato Y, Kuroda H, Ozawa SI, Saito K, Dogra V, Scholz M, Zhang G, Vitry C, Ishikita H, Kim C, Hippler M, Takahashi Y, Sakamoto W. Characterization of Tryptophan Oxidation Affecting D1 Degradation by FtsH in the Photosystem II Quality Control of Chloroplasts. eLife. https://doi.org/10.7554/eLife.88822.1


54. Lee KP, Li M, Li M, Liu K, Medina-Puche L, Qi S, Cui C, Lozano-Duran R, Kim C. Hierarchical regulatory module GENOMES UNCOUPLED1-GOLDEN2-LIKE1/2-WRKY18/40 modulates salicylic acid signaling. Plant Physiol. 2023 Apr 25:kiad251. doi: 10.1093/plphys/kiad251. Online ahead of print.


53. Li M, Kim C. Singlet oxygen in plants: From genesis to signaling. Advances in Botanical Research. 2023. Volume 105, Chapter one (Pages 1-42; https://www.sciencedirect.com/science/article/abs/pii/S0065229622001215)


52. Liu K, Lee KP, Duan J, Kim EY, Singh RM, Di M, Meng Z, Kim C. Cooperative Role of AtRsmD and AtRimM Proteins in Modification and Maturation of 16S rRNA in Plastids. Plant J. 2023 Feb 8. doi: 10.1111/tpj.16135. Online ahead of print.


51. Zhang Z, Zeng W, Zhang W, Li J, Kong D, Zhang L, Wang R, Peng F, Kong Z, Ke Y, Zhang H, Kim C, Zhang H, Botella JR, Zhu JK, Miki D. Insights into the molecular mechanisms of CRISPR/Cas9-mediated gene targeting at multiple loci in Arabidopsis. Plant Physiol. 2022 Sep 15:kiac431. doi: 10.1093/plphys/kiac431. Online ahead of print.


50. Fang J, Li B, Chen LJ, Dogra V, Luo S, Wu W, Wang P, Hwang I, Li HM, Kim C. TIC236 gainof-function mutations unveil the link between plastid division and plastid protein import. Proc Natl Acad Sci U S A. 2022 Mar 15;119(11):e2123353119. doi: 10.1073/pnas.2123353119. Epub 2022 Mar 11.

49. Li M and Kim C. Chloroplast ROS and stress signaling. Plant Comm. 2022, doi:https://doi.org/10.1016/j.xplc.2021.100264.


48. Vivek Dogra, Rahul Mohan Singh, Mengping Li, Mingyue Li, Somesh Singh, and Chanhong Kim. EXECUTER2 modulates the EXECUTER1 signalosome through its singlet oxygen-dependent oxidation. Mol Plant. 2021, DOI:https://doi.org/10.1016/j.molp.2021.12.016


47. Medina-Puche L, Kim C, Lozano-Duran R, Dogra V. Protocol for evaluating protein relocalization from the plasma membrane to chloroplasts. STAR Protoc. 2021 Sep 14;2(4):100816. doi: 10.1016/j.xpro.2021.100816. eCollection 2021 Dec 17.


46. Li M, Lee KP, Liu T, Dogra V, Duan J, Li M, Xing W, Kim C. Antagonistic modules regulate photosynthesis-associated nuclear genes via GOLDEN2-LIKE transcription factors. Plant Physiol. 2021, Dec 24:kiab600. doi: 10.1093/plphys/kiab600. Online ahead of print.


45. Luo S and Kim C. Current Understanding of Temperature Stress-Responsive Chloroplast FtsH Metalloproteases. Int. J. Mol. Sci. 2021, 22, 12106. https://doi.org/10.3390/ijms222212106


44. Niu Q, Song Z, Tang K, Chen L, Wang L, Ban T, Guo Z, Kim C, Zhang H, Duan CG, Zhang H, Zhu JK, Du J, Lang Z. A histone H3K4me1-specific binding protein is required for siRNA accumulation and DNA methylation at a subset of loci targeted by RNA-directed DNA methylation. Nat Commun. 2021 Jun 7;12(1):3367. doi: 10.1038/s41467-021-23637-4.


43. Lv X, Zeng X, Hu H, Chen L, Zhang F, Liu R, Liu Y, Zhou X, Wang C, Wu Z, Kim C, He Y, Du J. Structural insights into the multivalent binding of the Arabidopsis FLOWERING LOCUS T promoter by the CO-NF-Y master transcription factor complex. Plant Cell. 2021. doi: 10.1093/plcell/koab016.


42. Wang F#, Fang J#, Guan K, Luo S, Dogra V, Li B, Ma D, Zhao X, Lee KP, Sun P, Xin J, Liu T, Xing W*, and Kim C *. The Arabidopsis CRUMPLED LEAF protein, a homolog of the cyanobacterial bilin lyase, retains the bilin-binding pocket for a yet unknown function. Plant Journal. 2020. doi: 10.1111/tpj.14974.


41. Li B#, Fang J#, Singh RM, Zi H, Lv S, Liu R, Dogra V*, and Kim C*. FATTY ACID DESATURASE5 Is Required to Induce Autoimmune Responses in Gigantic Chloroplast Mutants of Arabidopsis. Plant Cell. 2020, 10.1105/tpc.20.00016 Highlighted in Plant Cell tpc.00637.2020


40. Medina-Puche L#, Tan H, Dogra V, Wu M, Rosas-Diaz T, Wang L, Ding X, Zhang D, Fu X, Kim C, Lozano-Duran R*. A defence pathway linking plasma membrane and chloroplasts and co-opted by pathogens. Cell. 2020 Aug 20:S0092-8674(20)30885-0. doi: 10.1016/j.cell.2020.07.020.


39. Lee KP#, Liu K, Kim EY, Medina-Puche L, Dong H, Duan J, Li M, Dogra V, Li Y, Lv R, Li Z, Lozano-Duran R, Kim C*. PLANT NATRIURETIC PEPTIDE A and Its Putative Receptor PNP-R2 Antagonize Salicylic Acid-mediated Signaling and Cell Death. Plant Cell. 2020 May 14. pii: tpc.00018.2020. doi: 10.1105/tpc.20.00018.


38. Li Z#, Dogra V#, Lee KP, Li R, Li M, Li M, Kim C*. N-terminal acetylation stabilizes SIGMA FACTOR BINDING PROTEIN 1 involved in salicylic acid-primed cell death. Plant Physiol. May;183(1):358-370. Highlighted in Plant Physiology 2020 May;183(1):35-36.


37. Kim C. ROS-Driven Oxidative Modification: Its Impact on Chloroplast-Nucleus Communication. Front Plant Sci. 2020 Jan 23;10:1729. doi: 10.3389/fpls.2019.01729.


36. Dogra V and Kim C*. Singlet Oxygen Metabolism: From Genesis to Signaling. Front Plant Sci. 2020 Jan 8;10:1640. doi: 10.3389/fpls.2019.01640.


35. Dogra V#, Li M#, Singh S#, Li M, Kim C*. Oxidative post-translational modification of EXECUTER1 is required for sensing singlet oxygen in plastids. Nat Commun. 2019. Doi: 10.1038/s41467-019-10760-6. Recommended in F1000Prime.


34. Dogra V and Kim C*. Chloroplast protein homeostasis is coupled with retrograde signaling. Plant Signaling & Behavior. 2019. doi: 10.1080/15592324.2019.1656037


33. Duan J#, Lee KP#, Dogra V#, Zhang S, Liu K, Caceres-Moreno C, Lv S, Xing W, Kato Y, Sakamoto W, Liu R, Macho AP, Kim C*. Impaired PSII proteostasis promotes retrograde signaling via salicylic acid. Plant Physiol. 2019 Jun 3. pii: pp.00483.2019. doi: 10.1104/pp.19.00483. Recommended in F1000Prime.

32. Dogra V#, Duan J#, Lee KP, Kim C*. Impaired PSII proteostasis trig


gers an UPR-like response in the var2 mutant of Arabidopsis thaliana. J Exp Bot. 2019. pii: erz151. doi: 10.1093/jxb/erz151


31. Pesaresi P and Kim C*. Current understanding of GUN1: a key mediator involved in biogenic retrograde signaling. Plant Cell Rep. 2019. doi: 10.1007/s00299-019-02383-4


30. Lv R#, Li Z#, Li M, Dogra V, Lv S, Liu R, Lee KP*, Kim C*. Uncoupled Expression of Nuclear and Plastid Photosynthesis-Associated Genes Contributes to Cell Death in a Lesion Mimic Mutant. Plant Cell. 2019. 31(1):210-230. doi: 10.1105/tpc.18.00813.


29. Dogra V, Rochaix J-D, Kim C*. Singlet oxygen‐triggered chloroplast‐to‐nucleus retrograde signaling pathways: an emerging perspective. Plant Cell Environ. 2018. 41(8):1727-1738. doi: 10.1111/pce.13332


28. Rochaix JD, Kim C, Apel W. Klaus Apel (1942-2017): a pioneer of photosynthesis research. Photosynth Res. 2018. 137(2):153-159. doi: 10.1007/s11120-018-0488-x


27. Shang-Guan K, Wang M, Htwe NMPS, Li P, Li Y, Qi F, Zhang D, Cao M, Kim C, Weng H, Cen H, Black IM, Azadi P, Carlson RW, Stacey G, Liang Y. Lipopolysaccharides Trigger Two Successive Bursts of Reactive Oxygen Species at Distinct Cellular Locations. Plant Physiol. 2018. 176(3):2543-2556. doi: 10.1104/pp.17.01637


26. Dogra V, Duan J, Lee KP, Lv S, Liu R, Kim C*. FtsH2-Dependent Proteolysis of EXECUTER1 Is Essential in Mediating Singlet Oxygen-Triggered Retrograde Signaling in Arabidopsis thaliana. Front Plant Sci. 2017. 8:1145. doi: 10.3389/fpls.2017.01145.


25. Wang L#, Kim C#, Xu X, Piskurewicz U, Dogra V, Singh S, Mahler H, Apel K. Singlet oxygen- and EXECUTER1-mediated signaling is initiated in grana margins and depends on the protease FtsH2. Proc Natl Acad Sci USA, 2016. 113(26):E3792-800. doi: 10.1073/pnas.1603562113.


24. Chen S#, Kim C#, Lee JM, Lee HA, Fei Z, Wang L, Apel K. Blocking the QB-binding site of photosystem II by tenuazonic acid, a non-host-specific toxin of Alternaria alternata, activates singlet oxygen-mediated and EXECUTER-dependent signalling in Arabidopsis. Plant Cell Environ. 2015 38(6):1069-80. doi: 10.1111/pce.12462.


23. Zhang S, Apel K*, Kim C*. Singlet oxygen-mediated and EXECUTER-dependent signalling and acclimation of Arabidopsis thaliana exposed to light stress. Philos Trans R Soc Lond B Biol Sci. 2014 Mar 3;369(1640):20130227. doi: 10.1098/rstb.2013.0227.


22. Kim C and Apel K. Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity. Photosynth Res. 2013 116(2-3):455-64. doi: 10.1007/s11120-013-9876-4.


21. Kim C and Apel K. 1O2-mediated and EXECUTER-dependent retrograde plastid-to-nucleus signaling in norflurazon-treated seedlings of Arabidopsis thaliana. Mol Plant. 2013. 6(5):1580-91. doi: 10.1093/mp/sst020


20. Kim C and Apel K. Arabidopsis light-dependent NADPH: protochlorophyllide oxidoreductase A (PORA) is essential for normal plant growth and development: an addendum. Plant Mol Biol. 2012. Sep;80(2):237-40. doi: 10.1007/s11103-012-9944-8


19. Kim C, Meskauskiene R, Zhang S, Lee KP, Lakshmanan Ashok M, Blajecka K, Herrfurth C, Feussner I, Apel K. Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signaling pathway. Plant Cell. 2012. 24(7):3026-39. doi: 10.1105/tpc.112.100479


18. Simková K, Kim C, Gacek K, Baruah A, Laloi C, Apel K. The chloroplast division mutant caa33 of Arabidopsis thaliana reveals the crucial impact of chloroplast homeostasis on stress acclimation and retrograde plastid-to-nucleus signaling. Plant J. 2012. 69(4):701-12. doi: 10.1111/j.1365-313X.2011.04825.x


17. Meskauskiene R, Würsch M, Laloi C, Vidi PA, Coll NS, Kessler F, Baruah A, Kim C, Apel K. A mutation in the Arabidopsis mTERF-related plastid protein SOLDAT10 activates retrograde signaling and suppresses 1O2-induced cell death. Plant J. 2009. 60(3):399-410. doi: 10.1111/j.1365-313X.2009.03965.x.


16. Kim C#, Lee KP#, Baruah A, Nater M, Gobel C, Feussner I, Apel K. 1O2-mediated retrograde signaling during late embryogenesis predetermines plastid differentiation in seedlings by recruiting abscisic acid. Proc Natl Acad Sci USA. 2009. 106(24):9920-4. doi: 10.1073/pnas.0901315106.


15. Kim C, Meskauskiene R, Apel K, Laloi C. No single way to understand singlet oxygen signalling in plants. EMBO Rep, 2008. 9(5):435-9. doi: 10.1038/embor.2008.57.


14. Lee KP#, Kim C#, Landgraf F, Apel K. EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA. 2007. 104(24):10270-5.


13. Kim C, Ham H, Apel K. Multiplicity of different cell- and organ-specific import routes for the NADPH-protochlorophyllide oxidoreductases A and B in plastids of Arabidopsis seedlings. Plant J. 2005. 42(3):329-40.


12. Goslings D, Meskauskiene R, Kim C, Lee KP, Nater M, Apel K. Concurrent interactions of heme and FLU with Glu tRNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark- and light-grown Arabidopsis plants. Plant J. 2004. 40(6):957-67.


11. Kim C, Apel K. Substrate-dependent and organ-specific chloroplast protein import in planta. Plant Cell, 2004. 16(1):88-98.


10. Wagner D, Przybyla D, Op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E, Apel K. The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science. 2004 306(5699):1183-5.


9. Huq E, Al-Sady B, Hudson M, Kim C, Apel K, Quail PH. Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science. 2004. 305(5692):1937-41.


8. op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, Feussner I, Nater M, Apel K. Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell. 2003 15(10):2320-32.


7. Lee KP, Kim C, Lee DW, Apel K. TIGRINA d, required for regulating the biosynthesis of tetrapyrroles in barley, is an ortholog of the FLU gene of Arabidopsis thaliana. FEBS Lett. 2003. 553(1-2):119-24.


6. Jang S, Lee B, Kim C, Kim SJ, Yim J, Han JJ, Lee S, Kim SR, An G. The OsFOR1 gene encodes a polygalacturonase-inhibiting protein (PGIP) that regulates floral organ number in rice. Plant Mol Biol. 2003. 53(3):357-69.


5. Lee DW, Kim C, Lee DU. Effect of cultural conditions on the biosynthesis of gagaminine, a potent antioxidant from the roots of Cynanchumwilfordii. Biological & Pharmaceutical Bulletin. 2001 24: 1451-1453


4. Kim C, Jeong D-H, An G. Molecular cloning and characterization of OsLRK1 encoding a putative receptor-like protein kinase from Oryza sativa. Plant Science. 2000 152:17-26


3. Jeon JS, Jang S, Lee S, Nam J, Kim C, Lee SH, Chung YY, Kim SR, Lee YH, Cho YG, An G.Leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell. 2000. 12(6):871-84.


2. Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam J, An K, Han MJ, Sung RJ, Choi HS, Yu JH, Choi JH, Cho SY, Cha SS, Kim S, An G. T-DNA insertional mutagenesis for functional genomics in rice. Plant J. 2000. 22(6):561-70.


1. Jeon JS, Lee S, Jung KH, Jun SH, Kim C, An G. Tissue-preferential expression of a rice alpha-tubulin gene, OsTubA1, mediated by the first intron. Plant Physiol. 2000. 123(3):1005-14.