Histone ubiquitination controls organ size in cotton (Gossypium hirsutum).
cotton
histone
organ size
ubiquitin ligase
ubiquitin-conjugating enzyme
ubiquitination
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
revised:
21
01
2022
received:
22
10
2020
accepted:
22
02
2022
pubmed:
27
2
2022
medline:
31
5
2022
entrez:
26
2
2022
Statut:
ppublish
Résumé
Ubiquitination plays a vital role in modifying protein activity and destiny. Ub-conjugating enzyme E2 is one of the enzymes that participates in this precise process. There are at least 169 E2 proteins in the allotetraploid cotton (Gossypium hirsutum), but their function remains unknown. Here we identify an E2 gene GhUBC2L and show its positive role in cell proliferation and expansion. Complete knock-down of GhUBC2L in cotton resulted in retarded growth and reduced organ size. Conversely, overexpression of GhUBC2L promoted cotton growth, generating enlarged organs in size. Monoubiquitination of H2A and H2B was strongly impaired in GhUBC2L-suppressed cotton but slightly enhanced in GhUBC2L-overexpressed plant. GhUbox8, a U-box type E3 ligase protein, was found to interact with GhUBC2L both in vivo and in vitro, indicating their synergistical function in protein ubiquitination. Furthermore, GhUbox8 was shown to interact with a series of histone proteins, including histone H2A and H2B, indicating its potential monoubiquitination on H2A and H2B. Expression of genes relating to cell cycle and organ development were altered when the expression of GhUBC2L was changed. Our results show that GhUBC2L modulates histone monoubiquitination synergistically with GhUbox8 to regulate the expression of genes involved in organ development and cell cycle, thus controlling organ size in cotton. This research provides new insights into the role of protein ubiquitination in organ size control. Histone monoubiquitination plays an important role in plant development. Here, we identified an E2 enzyme GhUBC2L that modulates histone monoubiquitination synergistically with an E3 ligase GhUbox8 to mediate organ size control in cotton.
Substances chimiques
Histones
0
Ubiquitin-Protein Ligases
EC 2.3.2.27
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1005-1020Informations de copyright
© 2022 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Aravind, L. & Koonin, E.V. (2000) The U box is a modified RING finger -a common domain in ubiquitination. Current Biology, 10, R132-R134.
Aung, K., Lin, S.I., Wu, C.C., Huang, Y.T., Su, C.L. & Chiou, T.J. (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiology, 141, 1000-1011.
Bourbousse, C., Ahmed, I., Roudier, F., Zabulon, G., Blondet, E., Balzergue, S. et al. (2012) Histone H2B monoubiquitination facilitates the rapid modulation of gene expression during Arabidopsis photomorphogenesis. PLoS Genetics, 8, e1002825.
Bratzel, F., López-Torrejón, G., Koch, M., Del Pozo, J.C. & Calonje, M. (2010) Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A Monoubiquitination. Current Biology, 20, 1853-1859.
Cao, H., Li, X., Wang, Z., Ding, M., Sun, Y., Dong, F. et al. (2015) Histone H2B Monoubiquitination mediated by HISTONE MONOUBIQUITINATION1 and HISTONE MONOUBIQUITINATION2 is involved in anther development by regulating Tapetum degradation-related genes in Rice. Plant Physiology, 168, 1389-1405.
Cao, Y., Dai, Y., Cui, S. & Ma, L. (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell, 20, 2586-2602.
Chen, H., Zou, Y., Shang, Y., Lin, H., Wang, Y., Cai, R. et al. (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiology, 146, 368-376.
Cheng, M.-C., Kuo, W.-C., Wang, Y.-M., Chen, H.-Y. & Lin, T.-P. (2017) UBC18 mediates ERF1 degradation under light-dark cycles. The New Phytologist, 213, 1156-1167.
Cui, F., Liu, L., Zhao, Q., Zhang, Z., Li, Q., Lin, B. et al. (2012) Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance. Plant Cell, 24, 233-244.
Deng, F., Tu, L., Tan, J., Li, Y., Nie, Y. & Zhang, X. (2012) GbPDF1 is involved in cotton fiber initiation via the core cis-element HDZIP2ATATHB2. Plant Physiology, 158, 890-904.
Endoh, M., Endo, T.A., Endoh, T., Isono, K., Sharif, J., Ohara, O. et al. (2012) Histone H2A mono-ubiquitination is a crucial step to mediate PRC1-dependent repression of developmental genes to maintain ES cell identity. PLoS Genetics, 8, e1002774.
Feng, H., Li, X., Chen, H., Deng, J., Zhang, C., Liu, J. et al. (2018) GhHUB2, a ubiquitin ligase, is involved in cotton fiber development via the ubiquitin-26S proteasome pathway. Journal of Experimental Botany, 69, 5059-5075.
Fuchs, G., Hollander, D., Voichek, Y., Ast, G. & Oren, M. (2014) Cotranscriptional histone H2B monoubiquitylation is tightly coupled with RNA polymerase II elongation rate. Genome Research, 24, 1572-1583.
Gonzalez, N., Vanhaeren, H. & Inzé, D. (2012) Leaf size control: complex coordination of cell division and expansion. Trends in Plant Science, 17, 332-340.
Grefen, C. & Blatt, M.R. (2012) A 2in1 cloning system enables ratiometric bimolecular fluorescence complementation (rBiFC). BioTechniques, 53, 311-314.
He, L., Yang, X., Wang, L., Zhu, L., Zhou, T., Deng, J. et al. (2013) Molecular cloning and functional characterization of a novel cotton CBL-interacting protein kinase gene (GhCIPK6) reveals its involvement in multiple abiotic stress tolerance in transgenic plants. Biochemical and Biophysical Research Communications, 435, 209-215.
Himanen, K., Woloszynska, M., Boccardi, T.M., De Groeve, S., Nelissen, H., Bruno, L. et al. (2012) Histone H2B monoubiquitination is required to reach maximal transcript levels of circadian clock genes in Arabidopsis. The Plant Journal, 72, 249-260.
Huang, T.K., Han, C.L., Lin, S.I., Chen, Y.J., Tsai, Y.C., Chen, Y.R. et al. (2013) Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots. Plant Cell, 25, 4044-4060.
Jin, S.X., Zhang, X., Nie, Y., Guo, X., Liang, S. & Zhu, H. (2006) Identification of a novel elite genotype for in vitro culture and genetic transformation of cotton. Biologia Plantarum, 50, 519-524.
Kouzarides, T. (2007) Chromatin modifications and their function. Cell, 128, 693-705.
Kraft, E., Stone, S.L., Ma, L., Su, N., Gao, Y., Lau, O.S. et al. (2005) Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiology, 139, 1597-1611.
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25-R25.
Lau, O.S. & Deng, X.W. (2009) Effect of Arabidopsis COP10 ubiquitin E2 enhancement activity across E2 families and functional conservation among its canonical homologues. The Biochemical Journal, 418, 683-690.
Li, J., Wang, Z., Hu, Y., Cao, Y. & Ma, L. (2017a) Polycomb group proteins RING1A and RING1B regulate the vegetative phase transition in Arabidopsis. Frontiers in Plant Science, 8, 867.
Li, S., Ying, Y., Secco, D., Wang, C., Narsai, R., Whelan, J. et al. (2017b) Molecular interaction between PHO2 and GIGANTEA reveals a new crosstalk between flowering time and phosphate homeostasis in Oryza sativa. Plant, Cell & Environment, 40, 1487-1499.
Li, W. & Schmidt, W. (2010) A lysine-63-linked ubiquitin chain-forming conjugase, UBC13, promotes the developmental responses to iron deficiency in Arabidopsis roots. The Plant Journal, 62, 330-343.
Li, Y., Liu, D., Tu, L., Zhang, X., Wang, L., Zhu, L. et al. (2010) Suppression of GhAGP4 gene expression repressed the initiation and elongation of cotton fiber. Plant Cell Reports, 29, 193-202.
Li, Y., Tu, L., Pettolino, F.A., Ji, S., Hao, J., Yuan, D. et al. (2016) GbEXPATR, a species-specific expansin, enhances cotton fibre elongation through cell wall restructuring. Plant Biotechnology Journal, 14, 951-963.
Lingard, M.J., Monroe-Augustus, M. & Bartel, B. (2009) Peroxisome-associated matrix protein degradation in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 106, 4561-4566.
Liu, C., Wang, D., Wu, J., Keller, J., Ma, T. & Yu, X. (2013) RNF168 forms a functional complex with RAD6 during the DNA damage response. Journal of Cell Science, 126, 2042-2051.
Liu, T.Y., Huang, T.K., Tseng, C.Y., Lai, Y.S., Lin, S.I., Lin, W.Y. et al. (2012) PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell, 24, 2168-2183.
Ma, S., Tang, N., Li, X., Xie, Y., Xiang, D., Fu, J. et al. (2019) Reversible histone H2B monoubiquitination fine-tunes abscisic acid signaling and drought response in rice. Molecular Plant, 12, 263-277.
Menard, R., Verdier, G., Ors, M., Erhardt, M., Beisson, F. & Shen, W.H. (2014) Histone H2B monoubiquitination is involved in the regulation of cutin and wax composition in Arabidopsis thaliana. Plant & Cell Physiology, 55, 455-466.
Middleton, A.J., Wright, J.D. & Day, C.L. (2017) Regulation of E2s: a role for additional ubiquitin binding sites? Journal of Molecular Biology, 429, 3430-3440.
Minsky, N., Shema, E., Field, Y., Schuster, M., Segal, E. & Oren, M. (2008) Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nature Cell Biology, 10, 483-488.
Mural, R.V., Liu, Y., Rosebrock, T.R., Brady, J.J., Hamera, S., Connor, R.A. et al. (2013) The tomato Fni3 lysine-63-specific ubiquitin-conjugating enzyme and suv ubiquitin E2 variant positively regulate plant immunity. Plant Cell, 25, 3615-3631.
Pengelly, A.R., Kalb, R., Finkl, K. & Muller, J. (2015) Transcriptional repression by PRC1 in the absence of H2A monoubiquitylation. Genes & Development, 29, 1487-1492.
Ren, Z., Yu, D., Yang, Z., Li, C., Qanmber, G., Li, Y. et al. (2017) Genome-wide identification of the MIKC-type MADS-box gene family in Gossypium hirsutum L. unravels their roles in flowering. Frontiers in Plant Science, 8, 384.
Sadeghi, L., Siggens, L., Svensson, J.P. & Ekwall, K. (2014) Centromeric histone H2B monoubiquitination promotes noncoding transcription and chromatin integrity. Nature Structural & Molecular Biology, 21, 236-243.
Sridhar, V.V., Kapoor, A., Zhang, K., Zhu, J., Zhou, T., Hasegawa, P.M. et al. (2007) Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature, 447, 735-738.
Trujillo, M. (2018) News from the PUB: plant U-box type E3 ubiquitin ligases. Journal of Experimental Botany, 69, 371-384.
Turek, I., Tischer, N., Lassig, R. & Trujillo, M. (2018) Multi-tiered pairing selectivity between E2 ubiquitin-conjugating enzymes and E3 ligases. The Journal of Biological Chemistry, 293, 16324-16336.
Vierstra, R.D. (2003) The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends in Plant Science, 8, 135-142.
Wang, H., Lu, Y., Jiang, T., Berg, H., Li, C. & Xia, Y. (2013) The Arabidopsis U-box/ARM repeat E3 ligase AtPUB4 influences growth and degeneration of tapetal cells, and its mutation leads to conditional male sterility. The Plant Journal, 74, 511-523.
Wang, H., Wang, L., Erdjument-Bromage, H., Vidal, M., Tempst, P., Jones, R.S. et al. (2004) Role of histone H2A ubiquitination in Polycomb silencing. Nature, 431, 873-878.
Wang, L., Wen, R., Wang, J., Xiang, D., Wang, Q., Zang, Y. et al. (2019) Arabidopsis UBC13 differentially regulates two programmed cell death pathways in responses to pathogen and low-temperature stress. The New Phytologist, 221, 919-934.
Wang, S., Cao, L. & Wang, H. (2016) Arabidopsis ubiquitin-conjugating enzyme UBC22 is required for female gametophyte development and likely involved in Lys11-linked ubiquitination. Journal of Experimental Botany, 67, 3277-3288.
Weake, V.M. & Workman, J.L. (2008) Histone Ubiquitination: triggering gene activity. Molecular Cell, 29, 653-663.
Wen, R., Wang, S., Xiang, D., Venglat, P., Shi, X., Zang, Y. et al. (2014) UBC13, an E2 enzyme for Lys63-linked ubiquitination, functions in root development by affecting auxin signaling and aux/IAA protein stability. The Plant Journal, 80, 424-436.
Wheaton, K., Sarkari, F., Stanly Johns, B., Davarinejad, H., Egorova, O., Kaustov, L. et al. (2017) UbE2E1/UBCH6 is a critical in vivo E2 for the PRC1-catalyzed Ubiquitination of H2A at Lys-119. The Journal of Biological Chemistry, 292, 2893-2902.
Wojcik, F., Dann, G.P., Beh, L.Y., Debelouchina, G.T., Hofmann, R. & Muir, T.W. (2018) Functional crosstalk between histone H2B ubiquitylation and H2A modifications and variants. Nature Communications, 9, 1394.
Woloszynska, M., Le Gall, S., Neyt, P., Boccardi, T.M., Grasser, M., Längst, G. et al. (2019) Histone 2B monoubiquitination complex integrates transcript elongation with RNA processing at circadian clock and flowering regulators. Proceedings of the National Academy of Sciences, 116, 8060-8069.
Xu, L., Menard, R., Berr, A., Fuchs, J., Cognat, V., Meyer, D. et al. (2009) The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana. The Plant Journal, 57, 279-288.
Ye, Y. & Rape, M. (2009) Building ubiquitin chains: E2 enzymes at work. Nature Reviews. Molecular Cell Biology, 10, 755-764.
Yin, X., Romero-Campero, F.J., de Los Reyes, P., Yan, P., Yang, J., Tian, G. et al. (2021) H2AK121ub in Arabidopsis associates with a less accessible chromatin state at transcriptional regulation hotspots. Nature Communications, 12, 315.
Ying, Y., Yue, W., Wang, S., Li, S., Wang, M., Zhao, Y. et al. (2017) Two h-type Thioredoxins interact with the E2 ubiquitin Conjugase PHO2 to fine-tune phosphate homeostasis in Rice. Plant Physiology, 173, 812-824.
Yu, F., Lou, L., Tian, M., Li, Q., Ding, Y., Cao, X. et al. (2016) ESCRT-I component VPS23A affects ABA signaling by recognizing ABA receptors for Endosomal degradation. Molecular Plant, 9, 1570-1582.
Zhang, T., Hu, Y., Jiang, W., Fang, L., Guan, X., Chen, J. et al. (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nature Biotechnology, 33, 531-537.
Zhao, W., Neyt, P., Van Lijsebettens, M., Shen, W.H. & Berr, A. (2019) Interactive and noninteractive roles of histone H2B monoubiquitination and H3K36 methylation in the regulation of active gene transcription and control of plant growth and development. The New Phytologist, 221, 1101-1116.
Zhou, B., Mural, R.V., Chen, X., Oates, M.E., Connor, R.A., Martin, G.B. et al. (2017) A subset of ubiquitin-conjugating enzymes is essential for plant immunity. Plant Physiology, 173, 1371-1390.
Zhu, B., Zheng, Y., Pham, A.D., Mandal, S.S., Erdjument-Bromage, H., Tempst, P. et al. (2005) Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Molecular Cell, 20, 601-611.
Zou, B., Yang, D.L., Shi, Z., Dong, H. & Hua, J. (2014) Monoubiquitination of histone 2B at the disease resistance gene locus regulates its expression and impacts immune responses in Arabidopsis. Plant Physiology, 165, 309-318.