SUMO mediated regulation of transcription factors as a mechanism for transducing environmental cues into cellular signaling in plants

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Abstract

Across all species, transcription factors (TFs) are the most frequent targets of SUMOylation. The effect of SUMO conjugation on the functions of transcription factors has been extensively studied in animal systems, with over 200 transcription factors being documented to be modulated by SUMOylation. This has resulted in the establishment of a number of paradigms that seek to explain the mechanisms by which SUMO regulates transcription factor functions. For instance, SUMO has been shown to modulate TF DNA binding activity; regulate both localization as well as the abundance of TFs and also influence the association of TFs with chromatin. With transcription factors being implicated as master regulators of the cellular signalling pathways that maintain phenotypic plasticity in all organisms, in this review, we will discuss how SUMO mediated regulation of transcription factor activity facilitates molecular pathways to mount an appropriate and coherent biological response to environmental cues.

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ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis.

Viswanathan Chinnusamy, Masaru Ohta, Siddhartha Kanrar … (2003)

Cold temperatures trigger the expression of the CBF family of transcription factors, which in turn activate many downstream genes that confer chilling and freezing tolerance to plants. We report here the identification of ICE1 (inducer of CBF expression 1), an upstream transcription factor that regulates the transcription of CBF genes in the cold. An Arabidopsis ice1 mutant was isolated in a screen for mutations that impair cold-induced transcription of a CBF3 promoter-luciferase reporter gene. The ice1 mutation blocks the expression of CBF3 and decreases the expression of many genes downstream of CBFs, which leads to a significant reduction in plant chilling and freezing tolerance. ICE1 encodes a MYC-like bHLH transcriptional activator. ICE1 binds specifically to the MYC recognition sequences in the CBF3 promoter. ICE1 is expressed constitutively, and its overexpression in wild-type plants enhances the expression of the CBF regulon in the cold and improves freezing tolerance of the transgenic plants.

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Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis.

Qiang Liu, Mie Kasuga, Yoh Sakuma … (1998)

Plant growth is greatly affected by drought and low temperature. Expression of a number of genes is induced by both drought and low temperature, although these stresses are quite different. Previous experiments have established that a cis-acting element named DRE (for dehydration-responsive element) plays an important role in both dehydration- and low-temperature-induced gene expression in Arabidopsis. Two cDNA clones that encode DRE binding proteins, DREB1A and DREB2A, were isolated by using the yeast one-hybrid screening technique. The two cDNA libraries were prepared from dehydrated and cold-treated rosette plants, respectively. The deduced amino acid sequences of DREB1A and DREB2A showed no significant sequence similarity, except in the conserved DNA binding domains found in the EREBP and APETALA2 proteins that function in ethylene-responsive expression and floral morphogenesis, respectively. Both the DREB1A and DREB2A proteins specifically bound to the DRE sequence in vitro and activated the transcription of the b-glucuronidase reporter gene driven by the DRE sequence in Arabidopsis leaf protoplasts. Expression of the DREB1A gene and its two homologs was induced by low-temperature stress, whereas expression of the DREB2A gene and its single homolog was induced by dehydration. Overexpression of the DREB1A cDNA in transgenic Arabidopsis plants not only induced strong expression of the target genes under unstressed conditions but also caused dwarfed phenotypes in the transgenic plants. These transgenic plants also revealed freezing and dehydration tolerance. In contrast, overexpression of the DREB2A cDNA induced weak expression of the target genes under unstressed conditions and caused growth retardation of the transgenic plants. These results indicate that two independent families of DREB proteins, DREB1 and DREB2, function as trans-acting factors in two separate signal transduction pathways under low-temperature and dehydration conditions, respectively.

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Histone demethylation mediated by the nuclear amine oxidase homolog LSD1.

Yujiang Shi, Fei Lan, Caitlin Matson … (2004)

Posttranslational modifications of histone N-terminal tails impact chromatin structure and gene transcription. While the extent of histone acetylation is determined by both acetyltransferases and deacetylases, it has been unclear whether histone methylation is also regulated by enzymes with opposing activities. Here, we provide evidence that LSD1 (KIAA0601), a nuclear homolog of amine oxidases, functions as a histone demethylase and transcriptional corepressor. LSD1 specifically demethylates histone H3 lysine 4, which is linked to active transcription. Lysine demethylation occurs via an oxidation reaction that generates formaldehyde. Importantly, RNAi inhibition of LSD1 causes an increase in H3 lysine 4 methylation and concomitant derepression of target genes, suggesting that LSD1 represses transcription via histone demethylation. The results thus identify a histone demethylase conserved from S. pombe to human and reveal dynamic regulation of histone methylation by both histone methylases and demethylases.

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Contributors

Ari Sadanandom:

ORCID: http://orcid.org/0000-0003-0058-9479

ari.sadanandom@durham.ac.uk

Journal

Journal ID (nlm-ta): Cell Mol Life Sci

Journal ID (iso-abbrev): Cell Mol Life Sci

Title: Cellular and Molecular Life Sciences

Publisher: Springer International Publishing (Cham )

ISSN (Print): 1420-682X

ISSN (Electronic): 1420-9071

Publication date (Electronic): 16 January 2021

Publication date PMC-release: 16 January 2021

Publication date (Print): 2021

Volume: 78

Issue: 6

Pages: 2641-2664

Affiliations

GRID grid.8250.f, ISNI 0000 0000 8700 0572, Department of Biosciences, , Durham University, ; Stockton Road, Durham, DH1 3LE UK

Author information

Ari Sadanandom http://orcid.org/0000-0003-0058-9479

Article

Publisher ID: 3723

DOI: 10.1007/s00018-020-03723-4

PMC ID: 8004507

PubMed ID: 33452901

SO-VID: d7147026-1a2b-44be-b008-68018db5fbba

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 22 July 2020

Date revision received : 25 October 2020

Date accepted : 25 November 2020

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;

Award ID: BB/M002136/1

Award Recipient : Ari Sadanandom

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ScienceOpen disciplines: Molecular biology

Keywords: sumo,transcription factors,cell signalling,post-translational modifications,gene expression

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ScienceOpen disciplines: Molecular biology

Keywords: sumo, transcription factors, cell signalling, post-translational modifications, gene expression

SUMO mediated regulation of transcription factors as a mechanism for transducing environmental cues into cellular signaling in plants

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Abstract

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Higher order chromatin architecture

Most cited references 209

ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis.

Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis.

Histone demethylation mediated by the nuclear amine oxidase homolog LSD1.

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