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Melatonin facilitates lateral root development by coordinating PAO-derived hydrogen peroxide and Rboh-derived superoxide radical.
Free Radic Biol Med 2019; 143:534-544FR

Abstract

Melatonin, a phytochemical, can regulate lateral root (LR) formation, but the downstream signaling of melatonin remains elusive. Here we investigated the roles of hydrogen peroxide (H2O2) and superoxide radical (O2•‾) in melatonin-promoted LR formation in tomato (Solanum lycopersicum) roots by using physiological, histochemical, bioinformatic, and biochemical approaches. The increase in endogenous melatonin level stimulated reactive oxygen species (ROS)-dependent development of lateral root primordia (LRP) and LR. Melatonin promoted LRP/LR formation and modulated the expression of cell cycle genes (SlCDKA1, SlCYCD3;1, and SlKRP2) by stimulating polyamine oxidase (PAO)-dependent H2O2 production and respiratory burst oxidase homologue (Rboh)-dependent O2•‾ production, respectively. Screening of SlPAOs and SlRbohs gene family combined with gene expression analysis suggested that melatonin-promoted LR formation was correlated to the upregulation of SlPAO1, SlRboh3, and SlRboh4 in LR-emerging zone. Transient expression analysis confirmed that SlPAO1 was able to produce H2O2 while SlRboh3 and SlRboh4 were capable of producing O2•‾. Melatonin-ROS signaling cassette was also found in the regulation of LR formation in rice root and lateral hyphal branching in fungi. These results suggested that SlPAO1-H2O2 and SlRboh3/4-O2•‾ acted as downstream of melatonin to regulate the expression of cell cycle genes, resulting in LRP initiation and LR development. Such findings uncover one of the regulatory pathways for melatonin-regulated LR formation, which extends our knowledge for melatonin-regulated plant intrinsic physiology.

Authors+Show Affiliations

Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China. Electronic address: chenjian@jaas.ac.cn.Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China.Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China.Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China.College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China.Department of Food Science, Henan Institute of Science and Technology, Xinxiang, 453003, China.Institute of Industrial Crops, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China.Institute of Food Safety and Nutrition, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China. Electronic address: shizhiqi@jaas.ac.cn.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31520769

Citation

Chen, Jian, et al. "Melatonin Facilitates Lateral Root Development By Coordinating PAO-derived Hydrogen Peroxide and Rboh-derived Superoxide Radical." Free Radical Biology & Medicine, vol. 143, 2019, pp. 534-544.
Chen J, Li H, Yang K, et al. Melatonin facilitates lateral root development by coordinating PAO-derived hydrogen peroxide and Rboh-derived superoxide radical. Free Radic Biol Med. 2019;143:534-544.
Chen, J., Li, H., Yang, K., Wang, Y., Yang, L., Hu, L., ... Shi, Z. (2019). Melatonin facilitates lateral root development by coordinating PAO-derived hydrogen peroxide and Rboh-derived superoxide radical. Free Radical Biology & Medicine, 143, pp. 534-544. doi:10.1016/j.freeradbiomed.2019.09.011.
Chen J, et al. Melatonin Facilitates Lateral Root Development By Coordinating PAO-derived Hydrogen Peroxide and Rboh-derived Superoxide Radical. Free Radic Biol Med. 2019 Sep 11;143:534-544. PubMed PMID: 31520769.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Melatonin facilitates lateral root development by coordinating PAO-derived hydrogen peroxide and Rboh-derived superoxide radical. AU - Chen,Jian, AU - Li,Hui, AU - Yang,Kang, AU - Wang,Yongzhu, AU - Yang,Lifei, AU - Hu,Liangbin, AU - Liu,Ruixian, AU - Shi,Zhiqi, Y1 - 2019/09/11/ PY - 2019/08/19/received PY - 2019/09/10/revised PY - 2019/09/10/accepted PY - 2019/9/15/pubmed PY - 2019/9/15/medline PY - 2019/9/15/entrez KW - Hydrogen peroxide KW - Lateral root KW - Melatonin KW - Polyamine oxidase KW - RBOH KW - Reactive oxygen species KW - Superoxide radical SP - 534 EP - 544 JF - Free radical biology & medicine JO - Free Radic. Biol. Med. VL - 143 N2 - Melatonin, a phytochemical, can regulate lateral root (LR) formation, but the downstream signaling of melatonin remains elusive. Here we investigated the roles of hydrogen peroxide (H2O2) and superoxide radical (O2•‾) in melatonin-promoted LR formation in tomato (Solanum lycopersicum) roots by using physiological, histochemical, bioinformatic, and biochemical approaches. The increase in endogenous melatonin level stimulated reactive oxygen species (ROS)-dependent development of lateral root primordia (LRP) and LR. Melatonin promoted LRP/LR formation and modulated the expression of cell cycle genes (SlCDKA1, SlCYCD3;1, and SlKRP2) by stimulating polyamine oxidase (PAO)-dependent H2O2 production and respiratory burst oxidase homologue (Rboh)-dependent O2•‾ production, respectively. Screening of SlPAOs and SlRbohs gene family combined with gene expression analysis suggested that melatonin-promoted LR formation was correlated to the upregulation of SlPAO1, SlRboh3, and SlRboh4 in LR-emerging zone. Transient expression analysis confirmed that SlPAO1 was able to produce H2O2 while SlRboh3 and SlRboh4 were capable of producing O2•‾. Melatonin-ROS signaling cassette was also found in the regulation of LR formation in rice root and lateral hyphal branching in fungi. These results suggested that SlPAO1-H2O2 and SlRboh3/4-O2•‾ acted as downstream of melatonin to regulate the expression of cell cycle genes, resulting in LRP initiation and LR development. Such findings uncover one of the regulatory pathways for melatonin-regulated LR formation, which extends our knowledge for melatonin-regulated plant intrinsic physiology. SN - 1873-4596 UR - https://www.unboundmedicine.com/medline/citation/31520769/Melatonin_facilitates_lateral_root_development_by_coordinating_PAO-derived_hydrogen_peroxide_and_Rboh-derived_superoxide_radical L2 - https://linkinghub.elsevier.com/retrieve/pii/S0891-5849(19)31344-9 DB - PRIME DP - Unbound Medicine ER -