Protein post-translational modifications in auxin signaling

Xiankui Cui; Junxia Wang; Ke Li; Bingsheng Lv; Bingkai Hou; Zhaojun Ding

doi:10.1016/j.jgg.2023.07.002

Protein post-translational modifications in auxin signaling

doi: 10.1016/j.jgg.2023.07.002

1 The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, China;
2 Shandong Academy of Grape, Jinan, Shandong 250100, China;
3 College of Horticulture, Qingdao Agricultural University, Qingdao, Shandong 266109, China

基金项目:

This work was supported by the National Natural Science Foundation of China (Projects 32061143005, 32170313, and 32100266) and Shandong Provincial Natural Science Foundation (ZR2021QC022 and ZR2022QC059).

详细信息

通讯作者:
Bingsheng Lv,Email:lvbingsheng@qau.edu.cn

Bingkai Hou,Email:bkhou@sdu.edu.cn

Zhaojun Ding,Email:dingzhaojun@sdu.edu.cn

计量
- 文章访问数: 159
- HTML全文浏览量: 75
- PDF下载量: 33
- 被引次数: 0
出版历程
- 收稿日期: 2023-05-08
- 录用日期: 2023-07-05
- 修回日期: 2023-07-05
- 网络出版日期: 2023-07-12

Protein post-translational modifications in auxin signaling

Xiankui Cui¹,
Junxia Wang¹,
Ke Li²,
Bingsheng Lv^{3
, ,},
Bingkai Hou^{1
, ,},
Zhaojun Ding^{1
, ,}

1 The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, China;
2 Shandong Academy of Grape, Jinan, Shandong 250100, China;
3 College of Horticulture, Qingdao Agricultural University, Qingdao, Shandong 266109, China

Funds:

摘要

摘要: Protein post-translational modifications (PTMs), such as ubiquitination, phosphorylation, and SUMOylation, are crucial for regulating protein stability, activity, subcellular localization, and binding with cofactors. Such modifications remarkably increase the variety and complexity of proteomes, which are essential for regulating numerous cellular and physiological processes. The regulation of auxin signaling is finely tuned in time and space to guide various plant growth and development. Accumulating evidence indicates that PTMs play critical roles in auxin signaling regulations. Thus, a thorough and systematic review of the functions of PTMs in auxin signal transduction will improve our profound comprehension of the regulation mechanism of auxin signaling and auxin-mediated various processes. This review discusses the progress of protein ubiquitination, phosphorylation, histone acetylation and methylation, SUMOylation, and S-nitrosylation in the regulation of auxin signaling.
- Arabidopsis /
- auxin /
- auxin signaling /
- post-translational modifications (PTMs) /
- protein regulation
Abstract: Protein post-translational modifications (PTMs), such as ubiquitination, phosphorylation, and SUMOylation, are crucial for regulating protein stability, activity, subcellular localization, and binding with cofactors. Such modifications remarkably increase the variety and complexity of proteomes, which are essential for regulating numerous cellular and physiological processes. The regulation of auxin signaling is finely tuned in time and space to guide various plant growth and development. Accumulating evidence indicates that PTMs play critical roles in auxin signaling regulations. Thus, a thorough and systematic review of the functions of PTMs in auxin signal transduction will improve our profound comprehension of the regulation mechanism of auxin signaling and auxin-mediated various processes. This review discusses the progress of protein ubiquitination, phosphorylation, histone acetylation and methylation, SUMOylation, and S-nitrosylation in the regulation of auxin signaling.
- Arabidopsis /
- auxin /
- auxin signaling /
- post-translational modifications (PTMs) /
- protein regulation

HTML全文

参考文献(145)

Alvarez-Venegas, R., 2010. Regulation by polycomb and trithorax group proteins in Arabidopsis. Arabidopsis Book 8, e0128.

An, C., Deng, L., Zhai, H., You, Y., Wu, F., Zhai, Q., Goossens, A., Li, C., 2022.Regulation of jasmonate signaling by reversible acetylation of TOPLESS in Arabidopsis. Mol. Plant 15, 1329-1346.

Bao, Y., Aggarwal, P., Robbins, N.E., Sturrock, C.J., Thompson, M.C., Tan, H.Q., Tham, C., Duan, L., Rodriguez, P.L., Vernoux, T., et al., 2014. Plant roots use a patterning mechanism to position lateral root branches toward available water.Proc. Natl. Acad. Sci. U. S. A. 111, 9319-9324.

Barbez, E., Dünser, K., Gaidora, A., Lendl, T., Busch, W., 2017. Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana. Proc. Natl.Acad. Sci. U. S. A. 114, E4884-E4893.

Bashandy, T., Guilleminot, J., Vernoux, T., Caparros-Ruiz, D., Ljung, K., Meyer, Y., Reichheld, J.P., 2010. Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22, 376-391.

Benhamed, M., Bertrand, C., Servet, C., Zhou, D.X., 2006. Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell 18, 2893-2903.

Benlloch, R., Lois, L.M., 2018. Sumoylation in plants: Mechanistic insights and its role in drought stress. J. Exp. Bot. 69, 4539-4554.

Bhaumik, S.R., Smith, E., Shilatifard, A., 2007. Covalent modifications of histones during development and disease pathogenesis. Nat. Struct. Mol. Biol. 14, 1008- 1016.

Calderon-Villalobos, L.I., Lee, S., De Oliveira, C., Ivetac, A., Brandt, W., Armitage, L., Sheard, L.B., Tan, X., Parry, G., Mao, H., et al., 2012. A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat.Chem. Biol. 8, 477-485.

Callis, J., 2014. The ubiquitination machinery of the ubiquitin system. Arabidopsis Book 12, e0174.

Cao, M., Chen, R., Li, P., Yu, Y., Zheng, R., Ge, D., Zheng, W., Wang, X., Gu, Y., Gelova, Z., et al., 2019. TMK1-mediated auxin signalling regulates differential growth of the apical hook. Nature 568, 240-243.

Cho, H., Ryu, H., Rho, S., Hill, K., Smith, S., Audenaert, D., Park, J., Han, S., Beeckman, T., Bennett, M.J., et al., 2014. A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nat. Cell Biol. 16, 66-76.

Clark, N.M., Elmore, J.M., Walley, J.W., 2022. To the proteome and beyond: Advances in single-cell omics profiling for plant systems. Plant Physiol. 188, 726-737.

Colón-Carmona, A., Chen, D.L., Yeh, K.C., Abel, S., 2000. Aux/IAA proteins are phosphorylated by phytochrome in vitro. Plant Physiol. 124, 1728-1738.

Corpas, F.J., 2017. Reactive nitrogen species (RNS) in plants under physiological and adverse environmental conditions: Current view. Prog. Bot. 78, 97-119.

Correa-Aragunde, N., Foresi, N., Delledonne, M., Lamattina, L., 2013. Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in Arabidopsis. J. Exp. Bot. 64, 3339-3349.

Correa-Aragunde, N., Graziano, M., Lamattina, L., 2004. Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218, 900-905.

del Pozo, J.C., Boniotti, M.B., Gutierrez, C., 2002. Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCFAtSKP2 pathway in response to light.Plant Cell 14, 3057-3071.

del Pozo, J.C., Diaz-Trivino, S., Cisneros, N., Gutierrez, C., 2006. The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 18, 2224-2235.

Dezfulian, M.H., Jalili, E., Roberto, D.K., Moss, B.L., Khoo, K., Nemhauser, J.L., Crosby, W.L., 2016. Oligomerization of SCFTIR1 is essential for Aux/IAA degradation and auxin signaling in Arabidopsis. PLoS Genet. 12, e1006301.

Dreher, K.A., Brown, J., Saw, R.E., Callis, J., 2006. The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell 18, 699-714.

Du, M., Spalding, E.P., Gray, W.M., 2020. Rapid auxin-mediated cell expansion. Annu.Rev. Plant Biol. 71, 379-402.

Duan, Q., Kita, D., Li, C., Cheung, A.Y., Wu, H.-M., 2010. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc. Natl.Acad. Sci. U. S. A. 107, 17821-17826.

Efroni, I., Han, S.-K., Kim, H.J., Wu, M.-F., Steiner, E., Birnbaum, K.D., Hong, J.C., Eshed, Y., Wagner, D., 2013. Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev. Cell 24, 438-445.

Exner, V., Aichinger, E., Shu, H., Wildhaber, T., Alfarano, P., Caflisch, A., Gruissem, W., Kohler, C., Hennig, L., 2009. The chromodomain of LIKE HETEROCHROMATIN PROTEIN 1 is essential for H3K27me3 binding and function during Arabidopsis development. PLoS One 4, e5335.

Feng, J., Chen, L., Zuo, J., 2019. Protein S-nitrosylation in plants: Current progresses and challenges. J. Integr. Plant Biol. 61, 1206-1223.

Fernández-Marcos, M., Sanz, L., Lewis, D.R., Muday, G.K., Lorenzo, O., 2011. Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc. Natl. Acad.Sci. U. S. A. 108, 18506-18511.

Friml, J., Gallei, M., Gelová, Z., Johnson, A., Mazur, E., Monzer, A., Rodriguez, L., Roosjen, M., Verstraeten, I., Živanović, B.D., et al., 2022. ABP1-TMK auxin perception for global phosphorylation and auxin canalization. Nature 609, 575- 581.

Guilfoyle, T.J., 2015. The PB1 domain in auxin response factor and Aux/IAA proteins:A versatile protein interaction module in the auxin response. Plant Cell 27, 33- 43.

Guilfoyle, T.J., Hagen, G., 2007. Auxin response factors. Curr. Opin. Plant Biol. 10, 453-460.

Guo, L., Yu, Y., Law, J.A., Zhang, X., 2010. SET DOMAIN GROUP2 is the major histone H3 lysine 4 trimethyltransferase in Arabidopsis. Proc. Natl. Acad. Sci.U. S. A. 107, 18557-18562.

He, C., Chen, X., Huang, H., Xu, L., 2012. Reprogramming of H3K27me3 is critical for acquisition of pluripotency from cultured Arabidopsis tissues. PLoS Genet. 8, e1002911.

He, W., Brumos, J., Li, H., Ji, Y., Ke, M., Gong, X., Zeng, Q., Li, W., Zhang, X., An, F., et al., 2011. A small-molecule screen identifies L-kynurenine as a competitive inhibitor of TAA1/TAR activity in ethylene-directed auxin biosynthesis and root growth in Arabidopsis. Plant Cell 23, 3944-3960.

Henderson, J., Bauly, J.M., Ashford, D.A., Oliver, S.C., Hawes, C.R., Lazarus, C.M., Venis, M.A., Napier, R.M., 1997. Retention of maize auxin-binding protein in the endoplasmic reticulum: Quantifying escape and the role of auxin. Planta 202,313-323.

Hendriks, I.A., Vertegaal, A.C., 2016. A comprehensive compilation of sumo proteomics. Nat. Rev. Mol. Cell Biol. 17, 581-595.

Huang, L., Yang, S., Zhang, S., Liu, M., Lai, J., Qi, Y., Shi, S., Wang, J., Wang, Y., Xie, Q., et al., 2009. The Arabidopsis SUMO E3 ligase AtMMS21, a homologue of NSE2/MMS21, regulates cell proliferation in the root. Plant J. 60, 666-678.

Huang, R., Zheng, R., He, J., Zhou, Z., Wang, J., Xiong, Y., Xu, T., 2019. Noncanonical auxin signaling regulates cell division pattern during lateral root development.Proc. Natl. Acad. Sci. U. S. A. 116, 21285-21290.

Iglesias, M.J., Terrile, M.C., Correa-Aragunde, N., Colman, S.L., Izquierdo-Alvarez, A., Fiol, D.F., Paris, R., Sanchez-Lopez, N., Marina, A., Calderon Villalobos, L.I.A., et al., 2018. Regulation of SCFTIR1/AFBs E3 ligase assembly by S-nitrosylation of Arabidopsis SKP1-like1 impacts on auxin signaling. Redox Biol. 18, 200-210.

Ishida, T., Yoshimura, M., Miura, K.,Sugimoto, K., 2012. MMS21/HPY2 and SIZ1, two Arabidopsis SUMO E3 ligases, have distinct functions in development.PLoS One 7, e46897.

Jenuwein, T., Allis, C.D., 2001. Translating the histone code. Science 293, 1074-1080.

Jiang, J., Xie, Y., Du, J., Yang, C., Lai, J., 2021. A SUMO ligase OsMMS21 regulates rice development and auxin response. J. Plant Physiol. 263, 153447.

Jing, H., Korasick, D.A., Emenecker, R.J., Morffy, N., Wilkinson, E.G., Powers, S.K., Strader, L.C., 2022. Regulation of auxin response factor condensation and nucleo-cytoplasmic partitioning. Nat. Commun. 13, 4015.

Jing, H., Yang, X., Emenecker, R.J., Feng, J., Zhang, J., Figueiredo, M.R.A.D., Chaisupa, P., Wright, R.C., Holehouse, A.S., Strader, L.C., et al., 2023. Nitric oxide-mediated S-nitrosylation of IAA17 protein in intrinsically disordered region represses auxin signaling. J. Genet. Genomics https://doi.org/10.1016/j.jgg.2023.05.001

Jurado, S., Abraham, Z., Manzano, C., López-Torrejón, G., Pacios, L.F., del Pozo, J.C., 2010. The Arabidopsis cell cycle F-box protein SKP2a binds to auxin. Plant Cell 22, 3891-3904.

Jurado, S., Díaz-Triviño, S., Abraham, Z., Manzano, C., Gutierrez, C., del Pozo, C., 2008. SKP2a, an F-box protein that regulates cell division, is degraded via the ubiquitin pathway. Plant J. 53, 828-841.

Kanaoka, M.M., Torii, K.U., 2010. FERONIA as an upstream receptor kinase for polar cell growth in plants. Proc. Natl. Acad. Sci. U. S. A. 107, 17461-17462.

Kelley, D.R., Estelle, M., 2012. Ubiquitin-mediated control of plant hormone signaling.Plant Physiol. 160, 47-55.

Keyzor, C., Mermaz, B., Trigazis, E., Jo, S., Song, J., 2021. Histone demethylases ELF6and JMJ13 antagonistically regulate self-fertility in Arabidopsis. Front. Plant Sci. 12, 640135.

Kim, B.C., Soh, M.S., Hong, S.H., Furuya, M., Nam, H.G., 1998. Photomorphogenic development of the Arabidopsis shy2-1D mutation and its interaction with phytochromes in darkness. Plant J. 15, 61-68.

Kim, S.H., Bahk, S., Nguyen, N.T., Pham, M.L.A., Kadam, U.S., Hong, J.C., Chung, W.S., 2022. Phosphorylation of the auxin signaling transcriptional repressor IAA15 by MPKs is required for the suppression of root development under drought stress in Arabidopsis. Nucleic Acids Res. 50, 10544-10561.

Korasick, D.A., Westfall, C.S., Lee, S.G., Nanao, M.H., Dumas, R., Hagen, G., Guilfoyle, T.J., Jez, J.M., Strader, L.C., 2014. Molecular basis for auxin response factor protein interaction and the control of auxin response repression.Proc. Natl. Acad. Sci. U. S. A. 111, 5427-5432.

Kornet, N., Scheres, B., 2009. Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis. Plant Cell 21, 1070-1079.

Kovtun, Y., Chiu, W.-L., Zeng, W., Sheen, J., 1998. Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 395, 716-720.

Kubeš, M., Napier, R., 2019. Non-canonical auxin signalling: Fast and curious. J. Exp.Bot. 70, 2609-2614.

Kuhn, A., Harborough, S.R., McLaughlin, H.M., Natarajan, B., Verstraeten, I., Friml, J., Kepinski, S., Østergaard, L., 2020. Direct ETTIN-auxin interaction controls chromatin states in gynoecium development. eLife 9, e51787.

Kumar, V., Thakur, J.K., Prasad, M., 2021. Histone acetylation dynamics regulating plant development and stress responses. Cell Mol. Life Sci. 78, 4467-4486.

Lafos, M., Kroll, P., Hohenstatt, M.L., Thorpe, F.L., Clarenz, O., Schubert, D., 2011.Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation.PLoS Genet. 7, e1002040.

Lakehal, A., Chaabouni, S., Cavel, E., Le Hir, R., Ranjan, A., Raneshan, Z., Novak, O., Pacurar, D.I., Perrone, I., Jobert, F., et al., 2019. A molecular framework for the control of adventitious rooting by TIR1/AFB2-Aux/IAA-dependent auxin signaling in Arabidopsis. Mol. Plant 12, 1499-1514.

Lamotte, O., Bertoldo, J.B., Besson-Bard, A., Rosnoblet, C., Aime, S., Hichami, S., Terenzi, H., Wendehenne, D., 2014. Protein S-nitrosylation: Specificity and identification strategies in plants. Front. Chem. 2, 114.

Langston, S.P., Grossman, S., England, D., Afroze, R., Bence, N., Bowman, D., Bump, N., Chau, R., Chuang, B.-C., Claiborne, C., et al., 2021. Discovery of TAK-981, a first-in-class inhibitor of SUMO-activating enzyme for the treatment of cancer.J. Med. Chem. 64, 2501-2520.

Lanteri, M.A.L., Laxalt, A.M.A., Lamattina, L., 2008. Nitric oxide triggers phosphatidic acid accumulation via phospholipase d during auxin-induced adventitious root formation in cucumber. Plant Physiol. 147, 188-198.

Lee, J.S., Wang, S., Sritubtim, S., Chen, J.-G., Ellis, B.E., 2009. Arabidopsis mitogen-activated protein kinase MPK12 interacts with the MAPK phosphatase IBR5 and regulates auxin signaling. Plant J. 57, 975-985.

Lee, K., Park, O.S., Seo, P.J., 2017. Arabidopsis ATXR2 deposits H3K36me3 at the promoters of LBD genes to facilitate cellular dedifferentiation. Sci. Signal. 10, eaan0316.

Lee, K., Park, O.S., Seo, P.J., 2018. JMJ30-mediated demethylation of H3K9me3 drives tissue identity changes to promote callus formation in Arabidopsis. Plant J. 95, 961-975.

Li, H., Johnson, P., Stepanova, A., Alonso, J.M., Ecker, J.R., 2004. Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev.Cell 7, 193-204.

Li, K., Wang, S., Wu, H.,Wang, H., 2020. Protein levels of several Arabidopsis auxin response factors are regulated by multiple factors and ABA promotes ARF6 protein ubiquitination. Int. J. Mol. Sci. 21, 9437.

Li, L., Verstraeten, I., Roosjen, M., Takahashi, K., Rodriguez, L., Merrin, J., Chen, J., Shabala, L., Smet, W., Ren, H., et al., 2021. Cell surface and intracellular auxin signalling for H+ fluxes in root growth. Nature 599, 273-277.

Lin, W., Zhou, X., Tang, W., Takahashi, K., Pan, X., Dai, J., Ren, H., Zhu, X., Pan, S., Zheng, H., et al., 2021. TMK-based cell-surface auxin signalling activates cell-wall acidification. Nature 599, 278-282.

Liu, C., Lu, F., Cui, X., Cao, X., 2010. Histone methylation in higher plants. Annu. Rev.Plant Biol. 61, 395-420.

Liu, C., Yu, H., Li, L., 2019. SUMO modification of LBD30 by SIZ1 regulates secondary cell wall formation in Arabidopsis thaliana. PLoS Genet. 15, e1007928.

Liu, L., Chai, M., Huang, Y., Qi, J., Zhu, W., Xi, X., Chen, F., Qin, Y.,Cai, H., 2021.SDG2 regulates Arabidopsis inflorescence architecture through SWR1-ERECTA signaling pathway. iScience 24, 103236.

Liu, Y., Lai, J., Yu, M., Wang, F., Zhang, J., Jiang, J., Hu, H., Wu, Q., Lu, G., Xu, P., et al., 2016. The Arabidopsis SUMO E3 ligase AtMMS21 dissociates the E2Fa/DPa complex in cell cycle regulation. Plant Cell 28, 2225-2237.

Lombardo, M.C., Graziano, M., Polacco, J.C., Lamattina, L., 2006. Nitric oxide functions as a positive regulator of root hair development. Plant Signal. Behav. 1, 28-33.

Lu, F., Cui, X., Zhang, S., Jenuwein, T., Cao, X., 2011. Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nat Genet. 43, 715-719.

Lv, B., Wei, K., Hu, K., Tian, T., Zhang, F., Yu, Z., Zhang, D., Su, Y., Sang, Y., Zhang, X., et al., 2021. MPK14-mediated auxin signaling controls lateral root development via ERF13-regulated very-long-chain fatty acid biosynthesis. Mol.Plant 14, 285-297.

Lv, B., Yu, Q., Liu, J., Wen, X., Yan, Z., Hu, K., Li, H., Kong, X., Li, C., Tian, H., et al., 2020. Non-canonical Aux/IAA protein IAA33 competes with canonical Aux/IAA repressor IAA5 to negatively regulate auxin signaling. EMBO J. 39, e101515.

Ma, J., Li, Q., Zhang, L., Cai, S., Liu, Y., Lin, J., Huang, R., Yu, Y., Wen, M.,Xu, T., 2022. High auxin stimulates callus through SDG8-mediated histone H3K36 methylation in Arabidopsis. J. Integr. Plant Biol. 64, 2425-2437.

Magyar, Z.N., De Veylder, L., Atanassova, A., Bakó, L.S., Inzé, D., Bögre, L.S., 2005. The role of the Arabidopsis E2Fb transcription factor in regulating auxin-dependent cell division. Plant Cell 17, 2527-2541.

Matunis, M.J., Coutavas, E., Blobel, G., 1996. A novel ubiquitin-like modification modulates the partitioning of the RAN-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 135, 1457-1470.

McLaughlin, H.M., Ang, A.C.H., Østergaard, L., 2021. Noncanonical auxin signaling.Cold Spring Harb. Perspect. Biol. 13, a039917.

Miao, R., Russinova, E., Rodriguez, P.L., 2022. Tripartite hormonal regulation of plasma membrane H+-ATPase activity. Trends Plant Sci. 27, 588-600.

Miura, K., Lee, J., Gong, Q., Ma, S., Jin, J.B., Yoo, C.Y., Miura, T., Sato, A., Bohnert,H.J., Hasegawa, P.M., 2011. SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol. 155, 1000-1012.

Miura, K., Rus, A., Sharkhuu, A., Yokoi, S., Karthikeyan, A.S., Raghothama, K.G., Baek, D., Koo, Y.D., Jin, J.B., Bressan, R.A., et al., 2005. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc. Natl.Acad. Sci. U. S. A. 102, 7760-7765.

Mockaitis, K.,Howell, S.H., 2000. Auxin induces mitogenic activated protein kinase(MAPK) activation in roots of Arabidopsis seedlings. Plant J. 24, 785-796.

Müller, J., Verrijzer, P., 2009. Biochemical mechanisms of gene regulation by polycomb group protein complexes. Curr. Opin. Genet. Dev. 19, 150-158.

Nakagami, H., Soukupová, H., Schikora, A., Zárský, V., Hirt, H., 2006. A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J. Biol. Chem. 281, 38697-38704.

Nanao, M.H., Vinos-Poyo, T., Brunoud, G., Thevenon, E., Mazzoleni, M., Mast, D., Laine, S., Wang, S., Hagen, G., Li, H., et al., 2014. Structural basis for oligomerization of auxin transcriptional regulators. Nat. Commun. 5, 3617.

Nguyen, C.T., Tran, G.-B., Nguyen, N.H., 2020. Homeostasis of histone acetylation is critical for auxin signaling and root morphogenesis. Plant Mol. Biol. 103, 1-7.

Nguyen, H.N., Kim, J.H., Jeong, C.Y., Hong, S.W., Lee, H., 2013. Inhibition of histone deacetylation alters Arabidopsis root growth in response to auxin via PIN1 degradation. Plant Cell Rep. 32, 1625-1636.

Ni, M., Zhang, L., Shi, Y.-F., Wang, C., Lu, Y., Pan, J., Liu, J.-Z., 2017. Excessive cellular S-nitrosothiol impairs endocytosis of auxin efflux transporter PIN2.Front. Plant Sci. 8, 1988.

Nishimura, T., Hayashi, K.-I., Suzuki, H., Gyohda, A., Takaoka, C., Sakaguchi, Y., Matsumoto, S., Kasahara, H., Sakai, T., Kato, J.-I., et al., 2014. Yucasin is a potent inhibitor of YUCCA, a key enzyme in auxin biosynthesis. Plant J. 77,352-366.

Orosa-Puente, B., Leftley, N., von Wangenheim, D., Banda, J., Srivastava, A.K., Hill, K., Truskina, J., Bhosale, R., Morris, E., Srivastava, M., et al., 2018. Root branching toward water involves posttranslational modification of transcription factor ARF7. Science 362, 1407-1410.

Ötvös, K., Pasternak, T.P., Miskolczi, P., Domoki, M., Dorjgotov, D., Szűcs, A., Bottka, S., Dudits, D., Fehér, A., 2005. Nitric oxide is required for, and promotes auxin-mediated activation of, cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures. Plant J. 43, 849-860.

Pagnussat, G.C., Lanteri, M.a.L., Lombardo, M.A.C., Lamattina, L., 2004. Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol. 135, 279-286.

Pagnussat, G.C., Simontacchi, M., Puntarulo, S.,Lamattina, L., 2002. Nitric oxide is required for root organogenesis. Plant Physiol. 129, 954-956.

Peer, W.A., 2013. From perception to attenuation: Auxin signalling and responses. Curr.Opin. Plant Biol. 16, 561-568.

Piya, S., Shrestha, S.K., Binder, B., Stewart, C.N., Hewezi, T., 2014. Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis.Front. Plant Sci. 5, 744.

Plant, A.R., Larrieu, A., Causier, B., 2021. Repressor for hire! The vital roles of TOPLESS-mediated transcriptional repression in plants. New Phytol. 231, 963- 973.

Pontvianne, F., Blevins, T., Pikaard, C.S., 2010. Arabidopsis histone lysine methyltransferases. Adv. Bot. Res. 53, 1-22.

Popescu, S.C., Popescu, G.V., Bachan, S., Zhang, Z., Gerstein, M., Snyder, M., Dinesh-Kumar, S.P., 2009. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev. 23, 80-92.

Powers, S.K., Holehouse, A.S., Korasick, D.A., Schreiber, K.H., Clark, N.M., Jing, H., Emenecker, R., Han, S., Tycksen, E., Hwang, I., et al., 2019. Nucleo-cytoplasmic partitioning of arf proteins controls auxin responses in Arabidopsis thaliana. Mol. Cell 76, 177-190.

Prigge, M.J., Platre, M., Kadakia, N., Zhang, Y., Greenham, K., Szutu, W., Pandey, B.K., Bhosale, R.A., Bennett, M.J., Busch, W., et al., 2020. Genetic analysis of the Arabidopsis TIR1/AFB auxin receptors reveals both overlapping and specialized functions. Elife 9, e54740.

Ramos, J.A., Zenser, N., Leyser, O., Callis, J., 2001. Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain ii and is proteasome dependent. Plant Cell 13, 2349-2360.

Rizzardi, K., Landberg, K., Nilsson, L., Ljung, K., Sundas-Larsson, A., 2011.TFL2/LHP1 is involved in auxin biosynthesis through positive regulation of YUCCA genes. Plant J. 65, 897-906.

Salmon, J., Ramos, J., Callis, J., 2008. Degradation of the auxin response factor ARF1.Plant J. 54, 118-128.

Schuettengruber, B., Chourrout, D., Vervoort, M., Leblanc, B., Cavalli, G., 2007.Genome regulation by polycomb and trithorax proteins. Cell 128, 735-745.

Shen, Y., Lei, T., Cui, X., Liu, X., Zhou, S., Zheng, Y., Guerard, F., Issakidis-Bourguet, E., Zhou, D.X., 2019. Arabidopsis histone deacetylase HDA15 directly represses plant response to elevated ambient temperature. Plant J. 100, 991- 1006.

Shi, Y.-F., Wang, D.-L., Wang, C., Culler, A.H., Kreiser, M.A., Suresh, J., Cohen, J.D., Pan, J., Baker, B., Liu, J.-Z., 2015. Loss of GSNOR1 function leads to compromised auxin signaling and polar auxin transport. Mol. Plant 8, 1350- 1365.

Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J.R., Cole, P.A., Casero, R.A., Shi, Y., 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941-953.

Springer, N.M., Napoli, C.A., Selinger, D.A., Pandey, R., Cone, K.C., Chandler, V.L., Kaeppler, H.F., Kaeppler, S.M., 2003. Comparative analysis of SET domain proteins in maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots. Plant Physiol. 132, 907-925.

Tan, S., Luschnig, C., Friml, J., 2021. Pho-view of auxin: Reversible protein phosphorylation in auxin biosynthesis, transport and signaling. Mol. Plant 14, 151-165.

Teale, W., Palme, K., 2017. Naphthylphthalamic acid and the mechanism of polar auxin transport. J. Exp. Bot. 69, 303-312.

Terrile, M.C., Paris, R., Calderon-Villalobos, L.I., Iglesias, M.J., Lamattina, L., Estelle, M., Casalongue, C.A., 2012. Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J. 70, 492-500.

Tomanov, K., Zeschmann, A., Hermkes, R., Eifler, K., Ziba, I., Grieco, M., Novatchkova, M., Hofmann, K., Hesse, H., Bachmair, A., 2014. Arabidopsis PIAL1 and 2 promote SUMO chain formation as E4-type SUMO ligases and are involved in stress responses and sulfur metabolism. Plant Cell 26, 4547- 4560.

Tsukada, Y., Fang, J., Erdjument-Bromage, H., Warren, M.E., Borchers, C.H., Tempst, P.,Zhang, Y., 2006. Histone demethylation by a family of Jmjc domain-containing proteins. Nature 439, 811-816.

Vert, G., Walcher, C.L., Chory, J., Nemhauser, J.L., 2008. Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc. Natl. Acad. Sci. U.S. A. 105, 9829-9834.

Vierstra, R.D., 2009. The ubiquitin-26S proteasome system at the nexus of plant biology.Nat. Rev. Mol. Cell Biol. 10, 385-397.

Vierstra, R.D., 2012. The expanding universe of ubiquitin and ubiquitin-like modifiers.Plant Physiol. 160, 2-14.

Vlachonasios, K.E., Thomashow, M.F., Triezenberg, S.J., 2003. Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell 15, 626-638.

Wang, J., Li, X., Chen, X., Tang, W., Yu, Z., Xu, T., Tian, H., Ding, Z., 2023. Dual regulations of cell cycle regulator DPa by auxin in Arabidopsis root distal stem cell maintenance. Proc. Natl. Acad. Sci. U. S. A. 120, e2218503120.

Wang, Q., Qin, G., Cao, M., Chen, R., He, Y., Yang, L., Zeng, Z., Yu, Y., Gu, Y., Xing, W., et al., 2020a. A phosphorylation-based switch controls TAA1-mediated auxin biosynthesis in plants. Nat. Commun. 11, 679.

Wang, X., Gao, J., Gao, S., Li, Z., Kuai, B., Ren, G., 2019. REF6 promotes lateral root formation through de-repression of PIN1/3/7 genes. J. Integr. Plant Biol. 61, 383-387.

Wang, Y.S., Wu, K.P., Jiang, H.K., Kurkute, P., Chen, R.H., 2020b. Branched ubiquitination: Detection methods, biological functions and chemical synthesis.Molecules 25, 5200.

Weiste, C., Droge-Laser, W., 2014. The Arabidopsis transcription factor bZIP11activates auxin-mediated transcription by recruiting the histone acetylation machinery. Nat. Commun. 5, 3883.

Woo, E.-J., Marshall, J., Bauly, J., Chen, J.-G., Venis, M., Napier, R.M., Pickersgill, R.W., 2002. Crystal structure of auxin-binding protein 1 in complex with auxin.EMBO J. 21, 2877-2885.

Wu, M.F., Yamaguchi, N., Xiao, J., Bargmann, B., Estelle, M., Sang, Y., Wagner, D., 2015. Auxin-regulated chromatin switch directs acquisition of flower primordium founder fate. Elife 4, e09269.

Xia, J., Kong, M., Yang, Z., Sun, L., Peng, Y., Mao, Y., Wei, H., Ying, W., Gao, Y., Friml, J., et al., 2023. Chemical inhibition of Arabidopsis PIN-FORMED auxin transporters by the anti-inflammatory drug naproxen. Plant Commun.https://doi.org/10.1016/j.xplc.2023.100632.

Xu, F., He, S., Zhang, J., Mao, Z., Wang, W., Li, T., Hua, J., Du, S., Xu, P., Li, L., et al., 2018. Photoactivated CRY1 and phyB interact directly with Aux/IAA proteins to inhibit auxin signaling in Arabidopsis. Mol. Plant 11, 523-541.

Xu, J., Zhang, S., 2015. Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends Plant Sci. 20, 56-64.

Xu, P., Yuan, D., Liu, M., Li, C., Liu, Y., Zhang, S., Yao, N.,Yang, C., 2013. AtMMS21, an SMC5/6 complex subunit, is involved in stem cell niche maintenance and DNA damage responses in Arabidopsis roots. Plant Physiol. 161, 1755-1768.

Xu, T., Dai, N., Chen, J., Nagawa, S., Cao, M., Li, H., Zhou, Z., Chen, X., De Rycke, R., Rakusová, H., et al., 2014. Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343, 1025-1028.

Xue, H., Zhang, Q., Wang, P., Cao, B., Jia, C., Cheng, B., Shi, Y., Guo, W.F., Wang, Z., Liu, Z.X., et al., 2022. qPTMplants: An integrative database of quantitative post-translational modifications in plants. Nucleic Acids Res. 50, D1491-D1499.

Yan, W., Chen, D., Smaczniak, C., Engelhorn, J., Liu, H., Yang, W., Graf, A., Carles, C.C., Zhou, D.X., Kaufmann, K., 2018. Dynamic and spatial restriction of polycomb activity by plant histone demethylases. Nat. Plants 4, 681-689.

Yang, B.-J., Han, X.-X., Yin, L.-L., Xing, M.-Q., Xu, Z.-H., Xue, H.-W., 2016.Arabidopsis PROTEASOME REGULATOR1 is required for auxin-mediated suppression of proteasome activity and regulates auxin signalling. Nat.Commun. 7, 11388.

Yang, C., Xie, F., Jiang, Y., Li, Z., Huang, X., Li, L., 2018. Phytochrome A negatively regulates the shade avoidance response by increasing auxin/indole acidic acid protein stability. Dev. Cell 44, 29-41.

Yao, X., Feng, H., Yu, Y., Dong, A., Shen, W.H., 2013. SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development.PLoS One 8, e56537.

Yu, Z., Ma, J., Zhang, M., Li, X., Sun, Y., Zhang, M., Ding, Z., 2023. Auxin promotes hypocotyl elongation by enhancing BZR1 nuclear accumulation in Arabidopsis.Sci. Adv. 9, eade2493.

Yu, Z., Zhang, F., Friml, J., Ding, Z., 2022. Auxin signaling: Research advances over the past 30 years. J. Integr. Plant Biol. 64, 371-392.

Yuan, L., Chen, X., Chen, H., Wu, K., Huang, S., 2019. Histone deacetylases HDA6 and HDA9 coordinately regulate valve cell elongation through affecting auxin signaling in Arabidopsis. Biochem. Biophys. Res. Commun. 508, 695-700.

Zhang, C., Yang, Y., Yu, Z., Wang, J., Huang, R., Zhan, Q., Li, S., Lai, J., Zhang, S., Yang, C., 2023. SUMO E3 ligase AtMMS21-dependent SUMOylation of AUXIN/INDOLE-3-ACETIC ACID 17 regulates auxin signaling. Plant Physiol. 191, 1871-1883.

Zhang, C.L., Wang, G.L., Zhang, Y.L., Hu, X., Zhou, L.J., You, C.X., Li, Y.Y., Hao, Y.J., 2021. Apple SUMO E3 ligase MdSIZ1 facilitates sumoylation of MdARF8 to regulate lateral root formation. New Phytol. 229, 2206-2222.

Zhang, J., Huang, D., Wang, C., Wang, B., Fang, H., Huo, J., Liao, W., 2019. Recent progress in protein S-nitrosylation in phytohormone signaling. Plant Cell Physiol. 60, 494-502.

Zhao, F.Y., Hu, F., Zhang, S.Y., Wang, K., Zhang, C.R., Liu, T., 2013. MAPKs regulate root growth by influencing auxin signaling and cell cycle-related gene expression in cadmium-stressed rice. Environ. Sci. Pollut. Res. Int. 20, 5449- 5460.

Zhao, L., Peng, T., Chen, C.Y., Ji, R., Gu, D., Li, T., Zhang, D., Tu, Y.T., Wu, K., Liu, X., 2019. HY5 interacts with the histone deacetylase HDA15 to repress hypocotyl cell elongation in photomorphogenesis. Plant Physiol. 180, 1450- 1466.

Zhu, Q., Shao, Y., Ge, S., Zhang, M., Zhang, T., Hu, X., Liu, Y., Walker, J., Zhang, S.,Xu, J., 2019. A MAPK cascade downstream of IDA-HAE/HSL2 ligand-receptor pair in lateral root emergence. Nat. Plants 5, 414-423.

施引文献

资源附件(0)

访问统计