Plant Metal Stress Biology
National Key Laboratory of Plant Molecular Genetics
Chao-Feng Huang
Personal Profile
Research Work
Acid soils, which cover approximately 30% of the world’s total land area and up to 50% of potentially arable land, pose significant challenges to agriculture due to the increased availability of protons and certain metals. These metals, including aluminum (Al), manganese (Mn), iron (Fe), and cadmium (Cd), can exert toxic effects on plant growth or lead to Cd contamination in crop edible parts. Of particular concern is Al toxicity, which is a major limitation for plant production on acid soils. Our research focuses on several key areas:
1. Aluminum Resistance Mechanisms: We aim to decipher the molecular mechanisms underlying plant resistance to Al toxicity, with a specific focus on the sensing and signaling pathways that plants activate in response to Al stress.
2. Manganese Transport, Utilization, and Detoxification: We are investigating the processes by which plants transport and utilize Mn, an essential micronutrient that is critical for plant growth. Additionally, we are examining the mechanisms by which plants detoxify excess Mn, which can become toxic and inhibit plant growth in acid soil environments.
3. Mitigating Cadmium Accumulation in Rice: We are exploring strategies to reduce Cd accumulation in rice grains, particularly through manipulation of Mn transporters, to ensure food safety and crop quality.
4. Plant Tolerance to Acid Soil Stress: Our research also extends to understanding the mechanisms that enable plants to tolerate proton toxicity and the Fe toxicity induced by low phosphate availability in acid soils.
Our goal is develop a comprehensive understanding of these mechanisms to improve crop productivity and sustainability in acid soil environments.
Main Achievements
Publications
2024
43. Fan N, Li XB, Xie WX, Wei X, Fang Q, Xu JY, and Huang CF* (2024) Modulation of external and internal aluminum resistance by ALS3-dependent STAR1-mediated promotion of STOP1 degradation. New Phytologist https://doi: 10.1111/nph.19985.
42. Cao HR, Zhang M, Zhu X, Bai ZM, Ma YQ, Huang CF, and Yang ZB* (2024) The RAE1-STOP1-GL2-RHD6 module regulates the ALMT1-dependent aluminum resistance in Arabidopsis. Nature Communications 15: 6294.
41. Huang CF* (2024) Connecting calcium signaling with boron transport: the crucial role of CPK10 protein kinase. New Phytologist 243: 1633-1635.
40. Zeng WJ#, Huang H#, Lin XQ, Zhu C, Kosami KI, Huang CF, Zhang HM, Duan CG, Zhu JK, and Miki Daisuke* (2024) Role of DEMETER in regulating DNA methylation in vegetative tissues and pathogen resistance. Journal of Integrative Plant Biology 64: 691-706.
39. Wei X#, Zhu YF#, Xie WX, Ren WW, Zhang Y, Zhang H, Dai SJ, and Huang CF* (2024) H2O2 negatively regulates aluminum resistance via oxidation and degradation of the transcription factor STOP1. Plant Cell 36: 688-708.
2023
38. Luo ZL, Liu CL, Yang XF, Zhu JK, and Huang CF* (2023) Mitigating cadmium accumulation in rice without compromising growth via modifying the regulatory region of OsNRAMP5. Stress Biology 3: 34.
37. Xie WX, Liu S, Gao HL, Wu J, Liu DL, Kinoshita T, and Huang CF* (2023) PP2C.D phosphatase SAL1 positively regulates aluminum resistance via restriction of aluminum uptake in rice. Plant Physiology 192: 1498-1516.
36. Zhou FL, Somesh S, Zhang J, Fang Q, Li CY, Wang JW, Zhao CZ, Wang PC, and Huang CF* (2023) The MEKK1-MKK1/2-MPK4 cascade phosphorylates and stabilizes STOP1 to confer aluminum resistance in Arabidopsis. Molecular Plant 16: 337-353.
2022
35. Huang CF* (2022) Ca2+ signaling in plant manganese uptake: CPK21/23 kinases phosphorylate and activate manganese transporter NRAMP1. Stress Biology 2: 43.
34. Li L#, Zhu ZZ#, Liao YH #, Yang CH, Fan N, Zhang J, Yamaji N, Dirick L, Jian Feng Ma, Curie C, and Huang CF* (2022) NRAMP6 and NRAMP1 cooperatively regulate root growth and manganese translocation under manganese deficiency in Arabidopsis. Plant Journal 110: 1564-1577.
33. Zhu X#, Wang P#, Bai ZM, Herde M, Ma YQ, Li N, Liu S, Huang CF, Cui RX, Ma HY, Zhang M, Wang H, Wei TD, Quan TY, Zhang W, Liu CG, Zhang T, and Yang ZB* (2022) Calmodulin-like protein CML24 interacts with CAMTA2 and WRKY46 to regulate ALMT1-dependent Al resistance in Arabidopsis thaliana. New Phytologist 233: 2471-2487.
2021
32. Yang CH#, Wang C#, Singh S#, Fan N, Liu S, Zhao L, Cao HL, Xie WX, Yang CW* and Huang CF* (2021) Golgi‐localised manganese transporter PML3 regulates Arabidopsis growth through modulating Golgi glycosylation and cell wall biosynthesis. New Phytologist 231: 2200-2214.
31. Zhu YF#, Guo J#, Zhang Y, and Huang CF* (2021) The THO/TREX complex component RAE2/TEX1 is involved in the regulation of aluminum resistance and low phosphate response in Arabidopsis. Frontiers in Plant Science 12:698443.
30. Huang CF* (2021) Activation and activity of STOP1 in aluminum resistance. Journal of Experimental Botany 72: 2269-2272.
29. Fang Q, Zhang J, Yang DL, and Huang CF* (2021) The SUMO E3 ligase SIZ1 partially regulates STOP1 SUMOylation and stability in Arabidopsis thaliana. Plant Signaling & Behavior 16 (5): 1899487.
28. Fang Q#, Zhou FL#, Zhang Y, Singh S, and Huang CF* (2021) Degradation of STOP1 mediated by the F‐box proteins RAH1 and RAE1 balances aluminum resistance and plant growth in Arabidopsis thaliana. Plant Journal 106:493-506.
2020
27. Fang Q#, Zhang J#, Zhang Y, Fan N, van den Burg HA, and Huang CF* (2020) Regulation of aluminum-resistance in Arabidopsis involves the SUMOylation of the zinc finger transcription factor STOP1. Plant Cell 32: 3921-3938.
26. Liu S, Zhao L, Liao YH, Luo ZL, Wang H, Wang P, Zhao H, Xia JX, and Huang CF* (2020) Dysfunction of the 4-Coumarate:Coenzyme A Ligase 4CL4 impacts aluminum resistance and lignin accumulation in rice. Plant Journal 104:1233-1250.
25. Guo JL, Zhang Y, Gao HL, Li SB, Wang ZY, and Huang CF* (2020) Mutation of HPR1 encoding a component of the THO/TREX complex reduces STOP1 accumulation and aluminum resistance in Arabidopsis thaliana. New Phytologist 228: 179-193
24. Liu CL#, Gao ZY#, Shang LG#, Yang CH, Ruan BP, Zeng DL, Guo LB, Zhao FJ, Huang CF*, and Qian Q* (2020) Natural variation in the promoter of OsHMA3 contributes to differential grain cadmium accumulation between Indica and Japonica rice. Journal of Integrative Plant Biology 62: 314-329
2019
23. Zhang Y#, Zhang J#, Guo JL#, Zhou FL, Singh S, Xu X, Xie Q, Yang ZB, and Huang CF* (2019) F-box protein RAE1 regulates the stability of the aluminum-resistance transcription factor STOP1 in Arabidopsis. PNAS 116: 319-327
22. Yang CH#, Zhang Y# and Huang CF*(2019) Reduction in cadmium accumulation in japonica rice grains by CRISPR/Cas9-mediated editing of OsNRAMP5. Journal of Integrative Agriculture 18:688-697.
2018
21. Zhu HF#, Xie WX#, Xu DC#, Miki D, Tang K, Huang CF*, and Zhu JK* (2018) DNA demethylase ROS1 negatively regulates the imprinting of DOGL4 and seed dormancy in Arabidopsis thaliana. PNAS 115: E9962-E9970.
20. Zhang Y#, Guo JL#, Chen M, Li L, Wang LH, and Huang CF* (2018) The cell cycle checkpoint regulator ATR is required for internal aluminum toxicity-mediated root growth inhibition in Arabidopsis. Frontiers in Plant Science 9:118.
19. Gao HL, Xie WX, Yang CH, Xu JY, Li JJ, Wang H, Chen X, and Huang CF* (2018) NRAMP2, a trans-Golgi network localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. New Phytologist 217:179-193.
2014-2016
18. Liu S, Gao HL, Wu XY, Fang Q, Chen L, Zhao FJ, and Huang CF* (2016) Isolation and characterization of an aluminum-resistant mutant in rice. Rice 9:60.
17. Yan JL, Wang PT, Wang P, Yang M, Lian XM, Tang Z, Huang CF, Salt DE, and Zhao FJ (2016) A loss-of-function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars. Plant Cell & Environment 39:1941–1954.
16. Yang Y, Liu Y, Huang CF, Silva J, and Zhao FJ (2016) Aluminium alleviates fluoride toxicity in tea (Camellia sinensis). Plant Soil 402:179-190.
15. Zhu HF, Wang H, Zhu YF, Zou JW, Zhao FJ, and Huang CF* (2015) Genome-wide transcriptomic and phylogenetic analyses reveal distinct aluminum-tolerance mechanisms in the aluminum-accumulating species buckwheat (Fagopyrum tataricum). BMC Plant Biology 15:16.
14. Yang M, Zhang YY, Zhang LJ, Hu JT, Zhang X, Lu K, Dong HX, Wang DJ, Zhao FJ, Huang CF, and Lian XM (2014) OsNRAMP5 contributes to manganese translocation and distribution in rice shoots. Journal of Experimental Botany 65: 4849–4861.
13. Huang CF* and Zhu JK* (2014) RNA splicing factors and RNA-directed DNA methylation. Biology 3:243-254.
Before 2014
12. Huang CF, Miki D, Tang K, Zhou HR, Zheng Z, Chen W, Ma ZY, Yang L, Zhang H, Liu R, He XJ, Zhu JK (2013) A pre-mRNA-splicing factor is required for RNA-directed DNA methylation in Arabidopsis. PLOS Genetics 9: e1003779.
11. Dou K#, Huang CF#, Ma ZY, Zhang CJ, Zhou JX, Huang HW, Cai T, Tang K, Zhu JK, and He XJ (2013) The PRP6-like splicing factor STA1 is involved in RNA-directed DNA methylation by facilitating the production of Pol V-dependent scaffold RNAs. Nucleic Acids Research 41: 8489-8502.
10. Tsutsui T, Yamaji N, Huang CF, Motoyama R, Nagamura Y, Ma JF (2012) Comparative genome-wide transcriptional analysis of Al-responsive genes reveals novel Al tolerance mechanisms in rice. PLOS ONE 7: e48197.
9. Huang CF, Yamaji N, Chen ZC, and Ma JF (2012) A tonoplast-localized half-size ABC transporter is required for internal detoxification of Al in rice. Plant Journal 69: 857-867.
8. Huang CF, Yamaji N, Ono K, and Ma JF (2012) A leucine-rich repeat receptor-like kinase gene is involved in the specification of outer cell layers in rice roots. Plant Journal 69: 565–576 (Cover story).
7. Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, and Ma JF (2010) Gene limiting cadmium accumulation in rice. PNAS 107: 16500-16505.
6. Huang CF, Yamaji N, and Ma JF (2010) Knockout of a bacterial-type ATP-binding cassette transporter gene, AtSTAR1, results in increased aluminum sensitivity in Arabidopsis. Plant Physiology 153: 1669-1677.
5. Yamaji N#, Huang CF#, Nagao S, Yano M, Sato Y, Nagamura Y, and Ma JF (2009) A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21: 3339-3349.
4. Huang CF, Yamaji N, Nishimura M, Tajima S, and Ma JF (2009) A rice mutant sensitive to Al toxicity is defective in the specification of root outer cell layers. Plant and Cell Physiology 50: 976 -985.
3. Wang LP, Yin HF, Qian Q, Yang J, Huang CF, Hu XH, and Luo D (2009) NECK LEAF 1, a GATA type transcription factor, modulates organogenesis by regulating the expression of multiple regulatory genes during reproductive development in rice. Cell Research 19: 598-611.
2. Huang CF#, Yamaji N#, Mitani N, Yano M, Nagamura Y, and Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21: 655-667.
1. Ma JF, Nagao S, Huang CF, and Nishimura M (2005) Isolation and characterization of a rice mutant hypersensitive to Al. Plant and Cell Physiology 46: 1054-1061.