SUMOylation of different targets fine-tunes phytochrome signaling.


Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
11 2021
Historique:
received: 25 05 2021
accepted: 12 07 2021
pubmed: 22 7 2021
medline: 21 10 2021
entrez: 21 7 2021
Statut: ppublish

Résumé

Plants monitor their surrounding ambient light environment by specialized photoreceptor proteins. Among them, phytochromes monitor red and far-red light. These molecules perceive photons, undergo a conformational change, and regulate diverse light signaling pathways, resulting in the mediation of key developmental and growth responses throughout the whole life of plants. Posttranslational modifications of the photoreceptors and their signaling partners may modify their function. For example, the regulatory role of phosphorylation has been investigated for decades by using different methodological approaches. In the past few years, a set of studies revealed that ubiquitin-like short protein molecules, called small ubiquitin-like modifiers (SUMOs) are attached reversibly to different members of phytochrome signaling pathways, including phytochrome B, the dominant receptor of red light signaling. Furthermore, SUMO attachment modifies the action of the target proteins, leading to altered light signaling and photomorphogenesis. This review summarizes recent results regarding SUMOylation of various target proteins, the regulation of their SUMOylation level, and the physiological consequences of SUMO attachment. Potential future research directions are also discussed.

Identifiants

pubmed: 34289130
doi: 10.1111/nph.17634
doi:

Substances chimiques

Arabidopsis Proteins 0
Phytochrome 11121-56-5
Phytochrome B 136250-22-1

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

1201-1211

Informations de copyright

© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.

Références

von Arnim AG, Osterlund MT, Kwok SF, Deng XW. 1997. Genetic and developmental control of nuclear accumulation of COP1, a repressor of photomorphogenesis in Arabidopsis. Plant Physiology 114: 779-788.
Augustine RC, Vierstra RD. 2018. SUMOylation: re-wiring the plant nucleus during stress and development. Current Opinion in Plant Biology 45: 143-154.
Bailey M, Srivastava A, Conti L, Nelis S, Zhang C, Florance H, Love A, Milner J, Napier R, Grant M et al. 2016. Stability of small ubiquitin-like modifier (SUMO) proteases OVERLY TOLERANT TO SALT1 and 2 modulates salicylic acid signalling and SUMO1/2 conjugation in Arabidopsis thaliana. Journal of Experimental Botany 67: 353-363.
Bauer D, Viczián A, Kircher S, Nobis T, Nitschke R, Kunkel T, Panigrahi KCS, Adám E, Fejes E, Schäfer E et al. 2004. Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 16: 1433-1445.
Bernula P, Pettkó-Szandtner A, Hajdu A, Kozma-Bognár L, Josse E-M, Ádám É, Nagy F, Viczián A. 2021. SUMOylation of PHYTOCHROME INTERACTING FACTOR 3 promotes photomorphogenesis in Arabidopsis thaliana. New Phytologist 229: 2050-2061.
Boccaccini A, Legris M, Krahmer J, Allenbach-Petrolati L, Goyal A, Galvan-Ampudia C, Vernoux T, Karayekov E, Casal JJ, Fankhauser C. 2020. Low blue light enhances phototropism by releasing cryptochrome1-mediated inhibition of PIF4 expression. Plant Physiology 183: 1780-1793.
Budhiraja R, Hermkes R, Müller S, Schmidt J, Colby T, Panigrahi K, Coupland G, Bachmair A. 2009. Substrates related to chromatin and to RNA-dependent processes are modified by Arabidopsis SUMO isoforms that differ in a conserved residue with influence on desumoylation. Plant Physiology 149: 1529-1540.
van den Burg HA, Kini RK, Schuurink RC, Takken FLW. 2010. Arabidopsis small ubiquitin-like modifier paralogs have distinct functions in development and defense. Plant Cell 22: 1998-2016.
Cai B, Kong X, Zhong C, Sun S, Zhou XF, Jin YH, Wang Y, Li X, Zhu Z, Jin JB. 2017. SUMO E3 ligases GmSIZ1a and GmSIZ1b regulate vegetative growth in soybean. Journal of Integrative Plant Biology 59: 2-14.
Castaño-Miquel L, Mas A, Teixeira I, Seguí J, Perearnau A, Thampi BN, Schapire AL, Rodrigo N, La Verde G, Manrique S et al. 2017. SUMOylation inhibition mediated by disruption of SUMO E1-E2 interactions confers plant susceptibility to necrotrophic fungal pathogens. Molecular Plant 10: 709-720.
Castaño-Miquel L, Seguí J, Manrique S, Teixeira I, Carretero-Paulet L, Atencio F, Lois LM. 2013. Diversification of SUMO-activating enzyme in Arabidopsis: implications in SUMO conjugation. Molecular Plant 6: 1646-1660.
Castro PH, Tavares RM, Bejarano ER, Azevedo H. 2012. SUMO, a heavyweight player in plant abiotic stress responses. Cellular and Molecular Life Sciences 69: 3269-3283.
Chen F, Li B, Demone J, Charron J-B, Shi X, Deng XW. 2014. Photoreceptor partner FHY1 has an independent role in gene modulation and plant development under far-red light. Proceedings of the National Academy of Sciences, USA 111: 11888-11893.
Chen F, Shi X, Chen L, Dai M, Zhou Z, Shen Y, Li J, Li G, Wei N, Deng XW. 2012. Phosphorylation of FAR-RED ELONGATED HYPOCOTYL1 is a key mechanism defining signaling dynamics of phytochrome A under red and far-red light in Arabidopsis. Plant Cell 24: 1907-1920.
Chico J-M, Fernández-Barbero G, Chini A, Fernández-Calvo P, Díez-Díaz M, Solano R. 2014. Repression of jasmonate-dependent defenses by shade involves differential regulation of protein stability of MYC transcription factors and their JAZ repressors in Arabidopsis. Plant Cell 26: 1967-1980.
Cho SK, Ben Chaabane S, Shah P, Poulsen CP, Yang SW. 2014. COP1 E3 ligase protects HYL1 to retain microRNA biogenesis. Nature Communications 5: e5867.
Conti L, Price G, O’Donnell E, Schwessinger B, Dominy P, Sadanandom A. 2008. Small ubiquitin-like modifier proteases OVERLY TOLERANT TO SALT1 and 2 regulate salt stress responses in Arabidopsis. Plant Cell 20: 2894-2908.
Elrouby N. 2015. Analysis of small ubiquitin-like modifier (SUMO) targets reflects the essential nature of protein SUMOylation and provides insight to elucidate the role of SUMO in plant development. Plant Physiology 169: 1006-1017.
Elrouby N, Coupland G. 2010. Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes. Proceedings of the National Academy of Sciences, USA 107: 17415-17420.
Franks RG, Wang C, Levin JZ, Liu Z. 2002. SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129: 253-263.
Galvão VC, Fankhauser C. 2015. Sensing the light environment in plants: photoreceptors and early signaling steps. Current Opinion in Neurobiology 34: 46-53.
Genoud T, Schweizer F, Tscheuschler A, Debrieux D, Casal JJ, Schäfer E, Hiltbrunner A, Fankhauser C. 2008. FHY1 mediates nuclear import of the light-activated phytochrome A photoreceptor. PLoS Genetics 4: e1000143.
Gong X, Flores-Vergara MA, Hong JH, Chu H, Lim J, Franks RG, Liu Z, Xu J. 2016. SEUSS integrates gibberellin signaling with transcriptional inputs from the SHR-SCR-SCL3 module to regulate middle cortex formation in the Arabidopsis root. Plant Physiology 170: 1675-1683.
Grigorova B, Mara C, Hollender C, Sijacic P, Chen X, Liu Z. 2011. LEUNIG and SEUSS co-repressors regulate miR172 expression in Arabidopsis flowers. Development 138: 2451-2456.
Hammoudi V, Vlachakis G, Schranz ME, van den Burg HA. 2016. Whole-genome duplications followed by tandem duplications drive diversification of the protein modifier SUMO in angiosperms. New Phytologist 211: 172-185.
Han X, Huang X, Deng XW. 2020. The photomorphogenic central repressor COP1: conservation and functional diversification during evolution. Plant Communications 1: e100044.
Hayes S, Velanis CN, Jenkins GI, Franklin KA. 2014. UV-B detected by the UVR8 photoreceptor antagonizes auxin signaling and plant shade avoidance. Proceedings of the National Academy of Sciences, USA 111: 11894-11899.
Hermkes R, Fu Y-F, Nürrenberg K, Budhiraja R, Schmelzer E, Elrouby N, Dohmen RJ, Bachmair A, Coupland G. 2011. Distinct roles for Arabidopsis SUMO protease ESD4 and its closest homolog ELS1. Planta 233: 63-73.
Hiltbrunner A, Tscheuschler A, Viczián A, Kunkel T, Kircher S, Schäfer E. 2006. FHY1 and FHL act together to mediate nuclear accumulation of the phytochrome A photoreceptor. Plant & Cell Physiology 47: 1023-1034.
Hiltbrunner A, Viczián A, Bury E, Tscheuschler A, Kircher S, Tóth R, Honsberger A, Nagy F, Fankhauser C, Schäfer E. 2005. Nuclear accumulation of the phytochrome A photoreceptor requires FHY1. Current Biology 15: 2125-2130.
Hoecker U. 2017. The activities of the E3 ubiquitin ligase COP1/SPA, a key repressor in light signaling. Current Opinion in Plant Biology 37: 63-69.
Huai J, Zhang X, Li J, Ma T, Zha P, Jing Y, Lin R. 2018. SEUSS and PIF4 coordinately regulate light and temperature signaling pathways to control plant growth. Molecular Plant 11: 928-942.
Huq E, Quail PH. 2002. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO Journal 21: 2441-2450.
Jang I-C, Henriques R, Seo HS, Nagatani A, Chua N-H. 2010. Arabidopsis PHYTOCHROME INTERACTING FACTOR proteins promote phytochrome B polyubiquitination by COP1 E3 ligase in the nucleus. Plant Cell 22: 2370-2383.
Jang I-C, Henriques R, Chua N-H. 2013. Three transcription factors, HFR1, LAF1 and HY5, regulate largely independent signaling pathways downstream of phytochrome A. Plant & Cell Physiology 54: 907-916.
Jeong R-D, Chandra-Shekara AC, Barman SR, Navarre D, Klessig DF, Kachroo A, Kachroo P. 2010. Cryptochrome 2 and phototropin 2 regulate resistance protein-mediated viral defense by negatively regulating an E3 ubiquitin ligase. Proceedings of the National Academy of Sciences, USA 107: 13538-13543.
Jin JB, Jin YH, Lee J, Miura K, Yoo CY, Kim W-Y, Van Oosten M, Hyun Y, Somers DE, Lee I et al. 2008. The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. The Plant Journal: for Cell and Molecular Biology 53: 530-540.
Kerscher O. 2007. SUMO junction - what’s your function? New insights through SUMO-interacting motifs. EMBO Reports 8: 550-555.
Khanna R, Huq E, Kikis EA, Al-Sady B, Lanzatella C, Quail PH. 2004. A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. Plant Cell 16: 3033-3044.
Kim JY, Jang I-C, Seo HS. 2016. COP1 controls abiotic stress responses by modulating AtSIZ1 function through its E3 ubiquitin ligase activity. Frontiers in Plant Science 7: e1182.
Klose C, Nagy F, Schäfer E. 2020. Thermal reversion of plant phytochromes. Molecular Plant 13: 386-397.
Kong X, Luo X, Qu G-P, Liu P, Jin JB. 2017. Arabidopsis SUMO protease ASP1 positively regulates flowering time partially through regulating FLC stability. Journal of Integrative Plant Biology 59: 15-29.
Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung D-Y, Vierstra RD. 2003. The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and 2 conjugates is increased by stress. The Journal of Biological Chemistry 278: 6862-6872.
Łabuz J, Sztatelman O, Jagiełło-Flasińska D, Hermanowicz P, Bażant A, Banaś AK, Bartnicki F, Giza A, Kozłowska A, Lasok H et al. 2021. Phototropin interactions with SUMO proteins. Plant and Cell Physiology 62: 693-707.
Lamoliatte F, McManus FP, Maarifi G, Chelbi-Alix MK, Thibault P. 2017. Uncovering the SUMOylation and ubiquitylation crosstalk in human cells using sequential peptide immunopurification. Nature Communications 8: e14109.
Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC et al. 2007. Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. The Plant Journal 49: 79-90.
Legris M, Ince YÇ, Fankhauser C. 2019. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nature Communications 10: e5219.
Leivar P, Monte E, Oka Y, Liu T, Carle C, Castillon A, Huq E, Quail PH. 2008. Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Current Biology 18: 1815-1823.
Leivar P, Monte E. 2014. PIFs: systems integrators in plant development. Plant Cell 26: 56-78.
Leivar P, Quail PH. 2011. PIFs: pivotal components in a cellular signaling hub. Trends in Plant Science 16: 19-28.
Lin F, Xu D, Jiang Y, Chen H, Fan L, Holm M, Deng XW. 2017. Phosphorylation and negative regulation of CONSTITUTIVELY PHOTOMORPHOGENIC 1 by PINOID in Arabidopsis. Proceedings of the National Academy of Sciences, USA 114: 6617-6622.
Lin X-L, Niu D, Hu Z-L, Kim DH, Jin YH, Cai B, Liu P, Miura K, Yun D-J, Kim W-Y et al. 2016. An Arabidopsis SUMO E3 ligase, SIZ1, negatively regulates photomorphogenesis by promoting COP1 activity. PLoS Genetics 12: e1006016.
López-Torrejón G, Guerra D, Catalá R, Salinas J, del Pozo JC. 2013. Identification of SUMO targets by a novel proteomic approach in plants. Journal of Integrative Plant Biology 55: 96-107.
Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C. 2008. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. The Plant Journal 53: 312-323.
Luo X-M, Lin W-H, Zhu S, Zhu J-Y, Sun Yu, Fan X-Y, Cheng M, Hao Y, Oh E, Tian M et al. 2010. Integration of light and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Developmental Cell 19: 872-883.
Ma D, Li X, Guo Y, Chu J, Fang S, Yan C, Noel JP, Liu H. 2016. Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light. Proceedings of the National Academy of Sciences, USA 113: 224-229.
Mazur MJ, Kwaaitaal M, Arroyo Mateos M, Maio F, Kini RK, Prins M, van den Burg HA. 2019. The SUMO conjugation complex self-assembles into nuclear bodies independent of SIZ1 and COP1. Plant Physiology 179: 168-183.
Menon C, Klose C, Hiltbrunner A. 2020. Arabidopsis FHY1 and FHY1-LIKE are not required for phytochrome A signal transduction in the nucleus. Plant Communications 1: e100007.
Miller MJ, Barrett-Wilt GA, Hua Z, Vierstra RD. 2010. Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis. Proceedings of the National Academy of Sciences, USA 107: 16512-16517.
Miller MJ, Scalf M, Rytz TC, Hubler SL, Smith LM, Vierstra RD. 2013. Quantitative proteomics reveals factors regulating RNA biology as dynamic targets of stress-induced SUMOylation in Arabidopsis. Molecular & Cellular Proteomics 12: 449-463.
Miura K, Hasegawa PM. 2010. Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends in Cell Biology 20: 223-232.
Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA et al. 2005. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proceedings of the National Academy of Sciences, USA 102: 7760-7765.
Mukhopadhyay D, Dasso M. 2007. Modification in reverse: the SUMO proteases. Trends in Biochemical Sciences 32: 286-295.
Murtas G, Reeves PH, Fu Y-F, Bancroft I, Dean C, Coupland G. 2003. A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of SMALL UBIQUITIN-RELATED MODIFIER conjugates. Plant Cell 15: 2308-2319.
Ni W, Xu S-L, Chalkley RJ, Pham TND, Guan S, Maltby DA, Burlingame AL, Wang Z-Y, Quail PH. 2013. Multisite light-induced phosphorylation of the transcription factor PIF3 is necessary for both its rapid degradation and concomitant negative feedback modulation of photoreceptor phyB levels in Arabidopsis. Plant Cell 25: 2679-2698.
Ni W, Xu S-L, Tepperman JM, Stanley DJ, Maltby DA, Gross JD, Burlingame AL, Wang Z-Y, Quail PH. 2014. A mutually assured destruction mechanism attenuates light signaling in Arabidopsis. Science 344: 1160-1164.
Ni W, Xu S-L, González-Grandío E, Chalkley RJ, Huhmer AFR, Burlingame AL, Wang Z-Y, Quail PH. 2017. PPKs mediate direct signal transfer from phytochrome photoreceptors to transcription factor PIF3. Nature Communications 8: e15236.
Novatchkova M, Budhiraja R, Coupland G, Eisenhaber F, Bachmair A. 2004. SUMO conjugation in plants. Planta 220: 1-8.
Novatchkova M, Tomanov K, Hofmann K, Stuible H-P, Bachmair A. 2012. Update on sumoylation: defining core components of the plant SUMO conjugation system by phylogenetic comparison. New Phytologist 195: 23-31.
Pacín M, Legris M, Casal JJ. 2014. Rapid decline in nuclear COSTITUTIVE PHOTOMORPHOGENESIS1 abundance anticipates the stabilization of its target ELONGATED HYPOCOTYL5 in the light. Plant Physiology 164: 1134-1138.
Park HC, Choi W, Park HJ, Cheong MS, Koo YD, Shin G, Chung WS, Kim W-Y, Kim MG, Bressan RA et al. 2011. Identification and molecular properties of SUMO-binding proteins in Arabidopsis. Molecules and Cells 32: 143-151.
Pfluger J, Zambryski P. 2004. The role of SEUSS in auxin response and floral organ patterning. Development 131: 4697-4707.
Qiu Y, Pasoreck EK, Reddy AK, Nagatani A, Ma W, Chory J, Chen M. 2017. Mechanism of early light signaling by the carboxy-terminal output module of Arabidopsis phytochrome B. Nature Communications 8: e1905.
Qu G-P, Li H, Lin X-L, Kong X, Hu Z-L, Jin YH, Liu Yu, Song H-L, Kim DH, Lin R et al. 2020. Reversible SUMOylation of FHY1 regulates phytochrome A signaling in Arabidopsis. Molecular Plant 13: 879-893.
Quint M, Delker C, Franklin KA, Wigge PA, Halliday KJ, van Zanten M. 2016. Molecular and genetic control of plant thermomorphogenesis. Nature Plants 2: e15190.
Rausenberger J, Tscheuschler A, Nordmeier W, Wüst F, Timmer J, Schäfer E, Fleck C, Hiltbrunner A. 2011. Photoconversion and nuclear trafficking cycles determine phytochrome A’s response profile to far-red light. Cell 146: 813-825.
Rockwell NC, Su Y-S, Lagarias JC. 2006. Phytochrome structure and signaling mechanisms. Annual Review of Plant Biology 57: 837-858.
Rösler J, Klein I, Zeidler M. 2007. Arabidopsis fhl/fhy1 double mutant reveals a distinct cytoplasmic action of phytochrome A. Proceedings of the National Academy of Sciences, USA 104: 10737-10742.
Rott R, Szargel R, Shani V, Hamza H, Savyon M, Abd Elghani F, Bandopadhyay R, Engelender S. 2017. SUMOylation and ubiquitination reciprocally regulate α-synuclein degradation and pathological aggregation. Proceedings of the National Academy of Sciences, USA 114: 13176-13181.
Rytz TC, Miller MJ, McLoughlin F, Augustine RC, Marshall RS, Juan Y-T, Charng Y-Y, Scalf M, Smith LM, Vierstra RD. 2018. SUMOylome profiling reveals a diverse array of nuclear targets modified by the SUMO ligase SIZ1 during heat stress. Plant Cell 30: 1077-1099.
Sadanandom A, Ádám É, Orosa B, Viczián A, Klose C, Zhang C, Josse E-M, Kozma-Bognár L, Nagy F. 2015. SUMOylation of phytochrome-B negatively regulates light-induced signaling in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 112: 11108-11113.
Saracco SA, Miller MJ, Kurepa J, Vierstra RD. 2007. Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential. Plant Physiology 145: 119-134.
Seo HS, Watanabe E, Tokutomi S, Nagatani A, Chua N-H. 2004. Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes & Development 18: 617-622.
Sharrock RA, Clack T. 2002. Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiology 130: 442-456.
Sheerin DJ, Menon C, zur Oven-Krockhaus S, Enderle B, Zhu L, Johnen P, Schleifenbaum F, Stierhof Y-D, Huq E, Hiltbrunner A. 2015. Light-activated phytochrome A and B interact with members of the SPA family to promote photomorphogenesis in Arabidopsis by reorganizing the COP1/SPA complex. Plant Cell 27: 189-201.
Shen Y, Zhou Z, Feng S, Li J, Tan-Wilson A, Qu L-J, Wang H, Deng XW. 2009. Phytochrome A mediates rapid red light-induced phosphorylation of Arabidopsis FAR-RED ELONGATED HYPOCOTYL1 in a low fluence response. Plant Cell 21: 494-506.
Shin J, Kim K, Kang H, Zulfugarov IS, Bae G, Lee C-H, Lee D, Choi G. 2009. Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochrome-interacting factors. Proceedings of the National Academy of Sciences, USA 106: 7660-7665.
Sridhar VV, Surendrarao A, Gonzalez D, Conlan RS, Liu Z. 2004. Transcriptional repression of target genes by LEUNIG and SEUSS, two interacting regulatory proteins for Arabidopsis flower development. Proceedings of the National Academy of Sciences, USA 101: 11494-11499.
Sridhar VV, Surendrarao A, Liu Z. 2006. APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133: 3159-3166.
Stacey MG, Hicks SN, von Arnim AG. 1999. Discrete domains mediate the light-responsive nuclear and cytoplasmic localization of Arabidopsis COP1. Plant Cell 11: 349-364.
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.
Verma V, Croley F, Sadanandom A. 2018. Fifty shades of SUMO: its role in immunity and at the fulcrum of the growth-defence balance. Molecular Plant Pathology 19: 1537-1544.
Verma V, Srivastava AK, Gough C, Campanaro A, Srivastava M, Morrell R, Joyce J, Bailey M, Zhang C, Krysan PJ et al. 2021. SUMO enables substrate selectivity by mitogen-activated protein kinases to regulate immunity in plants. Proceedings of the National Academy of Sciences 118: e2021351118.
Viczián A, Ádám É, Wolf I, Bindics J, Kircher S, Heijde M, Ulm R, Schäfer E, Nagy F. 2012. A short amino-terminal part of Arabidopsis phytochrome A induces constitutive photomorphogenic response. Molecular Plant 5: 629-641.
Viczián A, Ádám É, Staudt A-M, Lambert D, Klement E, Romero Montepaone S, Hiltbrunner A, Casal J, Schäfer E, Nagy F et al. 2020. Differential phosphorylation of the N-terminal extension regulates phytochrome B signaling. New Phytologist 225: 1635-1650.
Vierstra RD. 2009. The ubiquitin-26S proteasome system at the nexus of plant biology. Nature Reviews. Molecular Cell Biology 10: 385-397.
Vierstra RD. 2012. The expanding universe of ubiquitin and ubiquitin-like modifiers. Plant Physiology 160: 2-14.
Yang SW, Jang I-C, Henriques R, Chua N-H. 2009. FAR-RED ELONGATED HYPOCOTYL1 and FHY1-LIKE associate with the Arabidopsis transcription factors LAF1 and HFR1 to transmit phytochrome A signals for inhibition of hypocotyl elongation. Plant Cell 21: 1341-1359.
Yates G, Srivastava AK, Sadanandom A. 2016. SUMO proteases: uncovering the roles of deSUMOylation in plants. Journal of Experimental Botany 67: 2541-2548.
Yu Y, Wang J, Zhang Z, Quan R, Zhang H, Deng XW, Ma L, Huang R. 2013. Ethylene promotes hypocotyl growth and HY5 degradation by enhancing the movement of COP1 to the nucleus in the light. PLoS Genetics 9: e1004025.
Zeidler M, Zhou Q, Sarda X, Yau C-P, Chua N-H. 2004. The nuclear localization signal and the C-terminal region of FHY1 are required for transmission of phytochrome A signals. The Plant Journal 40: 355-365.
Zhang B, Holmlund M, Lorrain S, Norberg M, Bakó L, Fankhauser C, Nilsson O. 2017. BLADE-ON-PETIOLE proteins act in an E3 ubiquitin ligase complex to regulate PHYTOCHROME INTERACTING FACTOR 4 abundance. eLife 6: e26759.
Zhang X, Huai J, Liu S, Jin JB, Lin R. 2020. SIZ1-mediated SUMO modification of SEUSS regulates photomorphogenesis in Arabidopsis. Plant Communications 1: e100080.
Zhang Y, Mayba O, Pfeiffer A, Shi H, Tepperman JM, Speed TP, Quail PH. 2013. A quartet of PIF bHLH factors provides a transcriptionally centered signaling hub that regulates seedling morphogenesis through differential expression-patterning of shared target genes in Arabidopsis. PLoS Genetics 9: e1003244.
Zhao Q, Xie Y, Zheng Y, Jiang S, Liu W, Mu W, Liu Z, Zhao Y, Xue Y, Ren J. 2014. Gps-sumo: a tool for the prediction of sumoylation sites and SUMO-interaction motifs. Nucleic Acids Research 42: W325-330.
Zhou Q, Hare PD, Yang SW, Zeidler M, Huang L-F, Chua N-H. 2005. FHL is required for full phytochrome A signaling and shares overlapping functions with FHY1. The Plant Journal 43: 356-370.
Zhu D, Maier A, Lee J-H, Laubinger S, Saijo Y, Wang H, Qu L-J, Hoecker U, Deng XW. 2008. Biochemical characterization of Arabidopsis complexes containing CONSTITUTIVELY PHOTOMORPHOGENIC1 and SUPPRESSOR OF PHYA proteins in light control of plant development. Plant Cell 20: 2307-2323.

Auteurs

Csaba Péter (C)

Laboratory of Photo and Chronobiology, Institute of Plant Biology, Biological Research Centre, Eötvös Loránd Research Network (ELKH), Szeged, H-6726, Hungary.
Doctoral School in Biology, Faculty of Science and Informatics, University of Szeged, Szeged, H-6726, Hungary.

Ferenc Nagy (F)

Laboratory of Photo and Chronobiology, Institute of Plant Biology, Biological Research Centre, Eötvös Loránd Research Network (ELKH), Szeged, H-6726, Hungary.

András Viczián (A)

Laboratory of Photo and Chronobiology, Institute of Plant Biology, Biological Research Centre, Eötvös Loránd Research Network (ELKH), Szeged, H-6726, Hungary.

Articles similaires

Arabidopsis Arabidopsis Proteins Osmotic Pressure Cytoplasm RNA, Messenger
Fragaria Light Plant Leaves Osmosis Stress, Physiological

The FGF/FGFR/c-Myc axis as a promising therapeutic target in multiple myeloma.

Arianna Giacomini, Sara Taranto, Giorgia Gazzaroli et al.
1.00
Humans Multiple Myeloma Receptors, Fibroblast Growth Factor Fibroblast Growth Factors Proto-Oncogene Proteins c-myc
Animals Lung India Sheep Transcriptome

Classifications MeSH