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Article: Defence‐related priming and responses to recurring drought: Two manifestations of plant transcriptional memory mediated by the ABA and JA signalling pathways

Avramova, Zoya

Plant, cell and environment. 2019 Mar., v. 42, no. 3

2019

Abstract: Collective evidence from agricultural practices and from scientific research has demonstrated that plants can alter their phenotypic responses to repeated biotic and abiotic stresses or their elicitors. A coordinated reaction at the organismal, cellular, ...

Abstract	Collective evidence from agricultural practices and from scientific research has demonstrated that plants can alter their phenotypic responses to repeated biotic and abiotic stresses or their elicitors. A coordinated reaction at the organismal, cellular, and genome levels has suggested that plants can “remember” an earlier stress and modify their future responses, accordingly. Stress memory may increase a plant's survival chances by improving its tolerance/avoidance abilities and may provide a mechanism for acclimation and adaptation. Understanding the mechanisms that regulate plant stress memory is not only an intellectually challenging topic but has important implications for agricultural practices as well. Here, I focus exclusively on specific aspects of the transcription memory in response to recurring dehydration stresses and the memory‐type responses to insect damage in a process known as “priming.” The questions discussed are (a) whether/how the two memory phenomena are connected at the level of transcriptional regulation; (b) how differential transcription is achieved mechanistically under a repeated stress; and (c) whether similar molecular and/or epigenetic mechanisms are involved. Possible biological relevance of transcriptional stress memory and its preservation in plant evolution are also discussed.
Keywords	abiotic stress ; abscisic acid ; acclimation ; biotic stress ; drought ; elicitors ; epigenetics ; evolution ; genome ; insects ; jasmonic acid ; phenotype ; plant stress ; signal transduction ; transcription (genetics)
Language	English
Dates of publication	2019-03
Size	p. 983-997.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	REVIEW
ZDB-ID	391893-2
ISSN	1365-3040 ; 0140-7791
ISSN (online)	1365-3040
ISSN	0140-7791
DOI	10.1111/pce.13458
Database	NAL-Catalogue (AGRICOLA)

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Article: Heterochromatin in animals and plants. Similarities and differences.

Avramova, Zoya V

Plant physiology

2002 Volume 129, Issue 1, Page(s) 40–49

MeSH term(s)	Animals ; Drosophila melanogaster/genetics ; Evolution, Molecular ; Gene Silencing/physiology ; Heterochromatin/genetics ; Heterochromatin/physiology ; Plant Proteins/genetics ; Plants/genetics ; Saccharomyces cerevisiae/genetics
Chemical Substances	Heterochromatin ; Plant Proteins
Language	English
Publishing date	2002-05
Publishing country	United States
Document type	Comparative Study ; Journal Article ; Review
ZDB-ID	208914-2
ISSN	1532-2548 ; 0032-0889
ISSN (online)	1532-2548
ISSN	0032-0889
DOI	10.1104/pp.010981
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: The jasmonic acidâsignalling and abscisic acidâsignalling pathways cross talk during one, but not repeated, dehydration stress: a nonâspecific âpanickyâ or a meaningful response?

Avramova, Zoya

Plant, cell and environment. 2017 Sept., v. 40, no. 9

2017

Abstract: Experiencing diverse and recurring biotic and abiotic stresses throughout life, plants have evolved mechanisms to respond, survive and, eventually, adapt to changing habitats. The initial response to drought involves a large number of genes that are ... ...

Abstract	Experiencing diverse and recurring biotic and abiotic stresses throughout life, plants have evolved mechanisms to respond, survive and, eventually, adapt to changing habitats. The initial response to drought involves a large number of genes that are involved also in response to other stresses. According to current models, this initial response is nonâspecific, becoming stressâspecific only at later time points. The question, then, is whether nonâspecific activation of various stressâsignalling systems leading to the expression of numerous stressâregulated genes is a falseâalarm (panicky) response or whether it has biologically relevant consequences for the plant. Here, it is argued that the initial activation of genes associated other stresses reflects an important event during which stressâspecific mechanisms are generated to prevent subsequent activation of nonâdrought signalling pathways. How plants discriminate between a first and a repeated dehydration stress and how repression of nonâdrought specific genes is achieved will be discussed on the example of jasmonic acidâassociated Arabidopsis genes activated by a first, but not subsequent, dehydration stresses. Revealing how expression of various biotic/abiotic stress responding genes is prevented under recurring drought spells may be critical for our understanding of how plants respond to dynamically changing environments.
Keywords	Arabidopsis ; abiotic stress ; drought ; genes ; habitats ; models ; signal transduction
Language	English
Dates of publication	2017-09
Size	p. 1704-1710.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	391893-2
ISSN	1365-3040 ; 0140-7791
ISSN (online)	1365-3040
ISSN	0140-7791
DOI	10.1111/pce.12967
Database	NAL-Catalogue (AGRICOLA)

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Article: Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress‐response genes

Avramova, Zoya

plant journal. 2015 July, v. 83, no. 1

2015

Abstract: Drought, salinity, extreme temperature variations, pathogen and herbivory attacks are recurring environmental stresses experienced by plants throughout their life. To survive repeated stresses, plants provide responses that may be different from their ... ...

Abstract	Drought, salinity, extreme temperature variations, pathogen and herbivory attacks are recurring environmental stresses experienced by plants throughout their life. To survive repeated stresses, plants provide responses that may be different from their response during the first encounter with the stress. A different response to a similar stress represents the concept of ‘stress memory’. A coordinated reaction at the organismal, cellular and gene/genome levels is thought to increase survival chances by improving the plant's tolerance/avoidance abilities. Ultimately, stress memory may provide a mechanism for acclimation and adaptation. At the molecular level, the concept of stress memory indicates that the mechanisms responsible for memory‐type transcription during repeated stresses are not based on repetitive activation of the same response pathways activated by the first stress. Some recent advances in the search for transcription ‘memory factors’ are discussed with an emphasis on super‐induced dehydration stress memory response genes in Arabidopsis.
Keywords	Arabidopsis ; acclimation ; chromatin ; drought ; epigenetics ; genes ; herbivores ; pathogens ; salinity ; stress response ; temperature ; transcription (genetics)
Language	English
Dates of publication	2015-07
Size	p. 149-159.
Publishing place	Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology
Document type	Article
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.12832
Database	NAL-Catalogue (AGRICOLA)

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Article: ATX1/AtCOMPASS and the H3K4me3 marks: how do they activate Arabidopsis genes?

Fromm, Michael / Zoya Avramova

Current opinion in plant biology. 2014 Oct., v. 21

2014

Abstract: Despite the proven correlation between gene transcriptional activity and the levels of tri-methyl marks on histone 3 lysine4 (H3K4me3) of their nucleosomes, whether H3K4me3 contributes to, or âregistersâ, activated transcription is still ... ...

Abstract	Despite the proven correlation between gene transcriptional activity and the levels of tri-methyl marks on histone 3 lysine4 (H3K4me3) of their nucleosomes, whether H3K4me3 contributes to, or âregistersâ, activated transcription is still controversial. Other questions of broad relevance are whether histone-modifying proteins are involved in the recruitment of Pol II and the general transcription machinery and whether they have roles other than their enzyme activities. We address these questions as well as the roles of the ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1), of the COMPASS-related (AtCOMPASS) protein complex, and of their product, H3K4me3, at ATX1-dependent genes. We suggest that the ambiguity about the role of H3K4me3 as an activating mark is due to the unknown duality of the ATX1/AtCOMPASS to facilitate PIC assembly and to generate H3K4me3, which is essential for activating transcriptional elongation.
Keywords	Arabidopsis ; enzyme activity ; genes ; histones ; nucleosomes ; transcription (genetics)
Language	English
Dates of publication	2014-10
Size	p. 75-82.
Publishing place	Elsevier Ltd
Document type	Article
ZDB-ID	1418472-2
ISSN	1879-0356 ; 1369-5266
ISSN (online)	1879-0356
ISSN	1369-5266
DOI	10.1016/j.pbi.2014.07.004
Database	NAL-Catalogue (AGRICOLA)

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Article: Memory responses of jasmonic acidâassociated Arabidopsis genes to a repeated dehydration stress

Liu, Ning / Paul E. Staswick / Zoya Avramova

Plant, cell and environment. 2016 Nov., v. 39, no. 11

2016

Abstract: Dehydration stress activates numerous genes coâregulated by diverse signaling pathways. Upon repeated exposures, however, a subset of these genes does not respond maintaining instead transcription at their initial preâstressed levels (ârevisedâ ... ...

Abstract	Dehydration stress activates numerous genes coâregulated by diverse signaling pathways. Upon repeated exposures, however, a subset of these genes does not respond maintaining instead transcription at their initial preâstressed levels (ârevisedâresponseâ genes). Most of these genes are involved in jasmonic acid (JA) biosynthesis, JAâsignaling and JAâmediated stress responses. How these JAâassociated genes are regulated to provide different responses to similar dehydration stresses is an enigma. Here, we investigate molecular mechanisms that contribute to this transcriptional behavior. The memoryâmechanism is stressâspecific: one exposure to dehydration stress or to abscisic acid (ABA) is required to prevent transcription in the second. Both ABAâmediated and JAâmediated pathways are critical for the activation of these genes, but the two signaling pathways interact differently during a single or multiple encounters with dehydration stress. Synthesis of JA during the first (S1) but not the second dehydration stress (S2) accounts for the altered transcriptional responses. We propose a model for these memory responses, wherein lack of MYC2 and of JA synthesis in S2 is responsible for the lack of expression of downstream genes. The similar length of the memory displayed by different memoryâtype genes suggests biological relevance for transcriptional memory as a geneâregulating mechanism during recurring bouts of drought.
Keywords	abscisic acid ; Arabidopsis ; biosynthesis ; drought ; genes ; jasmonic acid ; models ; signal transduction ; stress response ; transcription (genetics)
Language	English
Dates of publication	2016-11
Size	p. 2515-2529.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	391893-2
ISSN	1365-3040 ; 0140-7791
ISSN (online)	1365-3040
ISSN	0140-7791
DOI	10.1111/pce.12806
Database	NAL-Catalogue (AGRICOLA)

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Article: H3K27me3 and H3K4me3 Chromatin Environment at Super-Induced Dehydration Stress Memory Genes of Arabidopsis thaliana

Liu, Ning / Michael Fromm / Zoya Avramova

Molecular plant. 2014 Mar., v. 7

2014

Abstract: Pre-exposure to a stress may alter the plantâs cellular, biochemical, and/or transcriptional responses during future encounters as a âmemoryâ from the previous stress. Genes increasing transcription in response to a first dehydration stress, but ... ...

Abstract	Pre-exposure to a stress may alter the plantâs cellular, biochemical, and/or transcriptional responses during future encounters as a âmemoryâ from the previous stress. Genes increasing transcription in response to a first dehydration stress, but producing much higher transcript levels in a subsequent stress, represent the super-induced âtranscription memoryâ genes in Arabidopsis thaliana. The chromatin environment (histone H3 tri-methylations of Lys 4 and Lys 27, H3K4me3, and H3K27me3) studied at five dehydration stress memory genes revealed existence of distinct memory-response subclasses that responded differently to CLF deficiency and displayed different transcriptional activities during the watered recovery periods. Among the most important findings is the novel aspect of the H3K27me3 function observed at specific dehydration stress memory genes. In contrast to its well-known role as a chromatin repressive mechanism at developmentally regulated genes, H3K27me3 did not prevent transcription from the dehydration stress-responding genes. The high H3K27me3 levels present during transcriptionally inactive states did not interfere with the transition to active transcription and with H3K4me3 accumulation. H3K4me3 and H3K27me3 marks function independently and are not mutually exclusive at the dehydration stress-responding memory genes.Genes increasing transcription in response to a first dehydration stress, but producing much higher transcript levels in a subsequent stress, represent the super-induced âtranscription memoryâ genes in Arabidopsis thaliana. Despite providing similar memory-type responses to a repeated stress, the genes respond differently to CLF deficiency outlining distinct memory-response subclasses. High H3K27me3 levels present during transcriptionally inactive states did not interfere with the transition to active transcription and with H3K4me3 accumulation indicating the H3K4me3 and H3K27me3 marks function independently and are not mutually exclusive at the dehydration stress-responding memory genes.
Keywords	Arabidopsis thaliana ; chromatin ; genes ; histones ; transcription (genetics)
Language	English
Dates of publication	2014-03
Size	p. 502-513.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	2393618-6
ISSN	1752-9867 ; 1674-2052
ISSN (online)	1752-9867
ISSN	1674-2052
DOI	10.1093/mp/ssu001
Database	NAL-Catalogue (AGRICOLA)

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Article: Subcellular localizations of Arabidopsis myotubularins MTM1 and MTM2 suggest possible functions in vesicular trafficking between ER and cis-Golgi

Nagpal, Akanksha / Ammar Hassan / František Baluška / Ivan Ndamukong / Zoya Avramova

Journal of plant physiology. 2016 Aug. 01, v. 200

2016

Abstract: The two Arabidopsis genes AtMTM1 and AtMTM2 encode highly similar phosphoinositide 3-phosphatases from the myotubularin family. Despite the high-level conservation of structure and biochemical activities, their physiological roles have significantly ... ...

Abstract	The two Arabidopsis genes AtMTM1 and AtMTM2 encode highly similar phosphoinositide 3-phosphatases from the myotubularin family. Despite the high-level conservation of structure and biochemical activities, their physiological roles have significantly diverged. The nature of a membrane and the concentrations of their membrane-anchored substrates (PtdIns3P or PtdIns3,5P2) and/or products (PtdIns5P and PtdIns) are considered critical for determining the functional specificity of myotubularins. We have performed comprehensive analyses of the subcellular localization of AtMTM1 and AtMTM2 using a variety of specific constructs transiently expressed in Nicotiana benthamiana leaf epidermal cells under the control of 35S promoter. AtMTM1 co-localized preferentially with cis-Golgi membranes, while AtMTM2 associated predominantly with ER membranes. In a stark contrast with animal/human MTMs, neither AtMTM1 nor AtMTM2 co-localizes with early or late endosomes or with TGN/EE compartments, making them unlikely participants in the endosomal trafficking system. Localization of the AtMTM2 is sensitive to cold and osmotic stress challenges. In contrast to animal myotubularins, Arabidopsis myotubularins do not associate with endosomes. Our results suggest that Arabidopsis myotubularins play a role in the vesicular trafficking between ER exit sites and cis-Golgi elements. The significance of these results is discussed also in the context of stress biology and plant autophagy.
Keywords	Arabidopsis ; autophagy ; cold ; endosomes ; genes ; humans ; leaves ; Nicotiana benthamiana ; osmotic stress ; promoter regions
Language	English
Dates of publication	2016-0801
Size	p. 45-52.
Publishing place	Elsevier GmbH
Document type	Article
ZDB-ID	283647-6
ISSN	1618-1328 ; 0176-1617
ISSN (online)	1618-1328
ISSN	0176-1617
DOI	10.1016/j.jplph.2016.06.001
Database	NAL-Catalogue (AGRICOLA)

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Article: The Arabidopsis trithorax-like factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways

Ding, Yong / Avramova, Zoya / Fromm, Michael

Plant journal. 2011 June, v. 66, no. 5

2011

Abstract: Emerging evidence suggests that the molecular mechanisms driving the responses of plants to environmental stresses are associated with specific chromatin modifications. Here, we demonstrate that the Arabidopsis trithorax-like factor ATX1, which ... ...

Abstract	Emerging evidence suggests that the molecular mechanisms driving the responses of plants to environmental stresses are associated with specific chromatin modifications. Here, we demonstrate that the Arabidopsis trithorax-like factor ATX1, which trimethylates histone H3 at lysine 4 (H3K4me3), is involved in dehydration stress signaling in both abscisic acid (ABA)-dependent and ABA-independent pathways. The loss of function of ATX1 results in decreased germination rates, larger stomatal apertures, more rapid transpiration and decreased tolerance to dehydration stress in atx1 plants. This deficiency is caused in part by reduced ABA biosynthesis in atx1 plants resulting from decreased transcript levels from NCED3, which encodes a key enzyme controlling ABA production. Dehydration stress increased ATX1 binding to NCED3, and ATX1 was required for the increased levels of NCED3 transcripts and nucleosomal H3K4me3 that occurred during dehydration stress. Mechanistically, ATX1 affected the quantity of RNA polymerase II bound to NCED3. By upregulating NCED3 transcription and ABA production, ATX1 influenced ABA-regulated pathways and genes. ATX1 also affected the expression of ABA-independent genes, implicating ATX1 in diverse dehydration stress-response mechanisms in Arabidopsis.
Keywords	Arabidopsis ; DNA-directed RNA polymerase ; abscisic acid ; biosynthesis ; chromatin ; genes ; germination ; histones ; lysine ; stomatal movement ; stress response ; transpiration
Language	English
Dates of publication	2011-06
Size	p. 735-744.
Publishing place	Blackwell Publishing Ltd
Document type	Article
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/j.1365-313X.2011.04534.x
Database	NAL-Catalogue (AGRICOLA)

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Article: Two Distinct Roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) at Promoters and within Transcribed Regions of ATX1-Regulated Genes

Ding, Yong / Avramova, Zoya / Fromm, Michael

Plant cell. 2011 Jan., v. 23, no. 1

2011

Abstract: The Arabidopsis thaliana trithorax-like protein, ATX1, shares common structural domains, has similar histone methyltransferase (HMT) activity, and belongs in the same phylogenetic subgroup as its animal counterparts. Most of our knowledge of the role of ... ...

Abstract	The Arabidopsis thaliana trithorax-like protein, ATX1, shares common structural domains, has similar histone methyltransferase (HMT) activity, and belongs in the same phylogenetic subgroup as its animal counterparts. Most of our knowledge of the role of HMTs in trimethylating lysine 4 of histone H3 (H3K4me3) in transcriptional regulation comes from studies of yeast and mammalian homologs. Little is known about the mechanism by which ATX1, or any other HMT of plant origin, affects transcription. Here, we provide insights into how ATX1 influences transcription at regulated genes, playing two distinct roles. At promoters, ATX1 is required for TATA binding protein (TBP) and RNA Polymerase II (Pol II) recruitment. In a subsequent event, ATX1 is recruited by a phosphorylated form of Pol II to the +300-bp region of transcribed sequences, where it trimethylates nucleosomes. In support of this model, inhibition of phosphorylation of the C-terminal domain of Pol II reduced the amounts of H3K4me3 and ATX1 bound at the +300-nucleotide region. Importantly, these changes did not reduce the occupancy of ATX1, TBP, or Pol II at promoters. Our results indicate that ATX1 affects transcription at target genes by a mechanism distinct from its ability to trimethylate H3K4 within genes.
Keywords	Arabidopsis thaliana ; DNA-directed RNA polymerase ; binding proteins ; gene expression regulation ; gene targeting ; genes ; lysine ; mammals ; models ; nucleosomes ; phosphorylation ; plants ; yeasts
Language	English
Dates of publication	2011-01
Size	p. 350-363.
Publishing place	American Society of Plant Biologists
Document type	Article
ZDB-ID	623171-8
ISSN	1532-298X ; 1040-4651
ISSN (online)	1532-298X
ISSN	1040-4651
Database	NAL-Catalogue (AGRICOLA)

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