Somatic embryogenesis - Stress-induced remodeling of plant cell fate.

Histone acetylation and deacetylation play essential roles in eukaryotic gene regulation. Reversible modifications of core histones are catalyzed by two intrinsic enzymes, histone acetyltransferase and histone deacetylase (HD). In general, histone deacetylation is related to transcriptional gene silencing, whereas acetylation correlates with gene activation. We produced transgenic plants expressing the antisense Arabidopsis HD (AtHD1) gene. AtHD1 is a homolog of human HD1 and RPD3 global transcriptional regulator in yeast. Expression of the antisense AtHD1 caused dramatic reduction in endogenous AtHD1 transcription, resulting in accumulation of acetylated histones, notably tetraacetylated H4. Reduction in AtHD1 expression and AtHD1 production and changes in acetylation profiles were associated with various developmental abnormalities, including early senescence, ectopic expression of silenced genes, suppression of apical dominance, homeotic changes, heterochronic shift toward juvenility, flower defects, and male and female sterility. Some of the phenotypes could be attributed to ectopic expression of tissue-specific genes (e.g., SUPERMAN) in vegetative tissues. No changes in genomic DNA methylation were detected in the transgenic plants. These results suggest that AtHD1 is a global regulator, which controls gene expression during development through DNA-sequence independent or epigenetic mechanisms in plants. In addition to DNA methylation, histone modifications may be involved in a general regulatory mechanism responsible for plant plasticity and variation in nature.

Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. [Erratum: June 19, 2001, v. 98 (13), p. 7647.]

Stress-induced structural changes in plant chromatin

The study of senescence in plants is complicated by diverse levels of temporal and spatial dynamics as well as the impact of external biotic and abiotic factors and crop plant management. Whereas the molecular mechanisms involved in developmentally regulated leaf senescence are very well understood, in particular in the annual model plant species Arabidopsis, senescence of other organs such as the flower, fruit, and root is much less studied as well as senescence in perennials such as trees. This review addresses the need for the integration of multi-omics techniques and physiological phenotyping into holistic phenomics approaches to dissect the complex phenomenon of senescence. That became feasible through major advances in the establishment of various, complementary 'omics' technologies. Such an interdisciplinary approach will also need to consider knowledge from the animal field, in particular in relation to novel regulators such as small, non-coding RNAs, epigenetic control and telomere length. Such a characterization of phenotypes via the acquisition of high-dimensional datasets within a systems biology approach will allow us to systematically characterize the various programmes governing senescence beyond leaf senescence in Arabidopsis and to elucidate the underlying molecular processes. Such a multi-omics approach is expected to also spur the application of results from model plants to agriculture and their verification for sustainable and environmentally friendly improvement of crop plant stress resilience and productivity and contribute to improvements based on postharvest physiology for the food industry and the benefit of its customers.

Integration of multi-omics techniques and physiological phenotyping within a holistic phenomics approach to study senescence in model and crop plants.

To better adapt transiently or lastingly to stimuli from the surrounding environment, the chromatin states in plant cells vary to allow the cells to fine-tune their transcriptional profiles. Modifications of chromatin states involve a wide range of post-transcriptional histone modifications, histone variants, DNA methylation, and activity of non-coding RNAs, which can epigenetically determine specific transcriptional outputs. Recent advances in the area of '-omics' of major crops have facilitated identification of epigenetic marks and their effect on plant response to environmental stresses. As most epigenetic mechanisms are known from studies in model plants, we summarize in this review recent epigenetic studies that may be important for improvement of crop adaptation and resilience to environmental changes, ultimately leading to the generation of stable climate-smart crops. This has paved the way for exploitation of epigenetic variation in crop breeding.

/pdf/epigenetics-possible-applications-in-climate-smart-crop-2jdt4jg8bv.pdf

Epigenetics: possible applications in climate-smart crop breeding.

Senescence processes are part of the plant developmental programme. They involve reprogramming of gene expression and are under the control of a complex regulatory network closely linked to other developmental and stressresponsive pathways. Recent evidence indicates that leaf senescence is regulated via epigenetic mechanisms. In the present review, the epigenetic control of plant senescence is discussed in the broader context of environmentsensitive plant development. The review outlines the concept of epigenetic control of interconnected regulatory pathways steering stress responses and plant development. Besides giving an overview of techniques used in the field, it summarizes recent findings on global alterations in chromatin structure, histone and DNA modifications, and ATPdependent chromatin remodelling during plant senescence and linked processes.

/pdf/epigenetic-control-of-plant-senescence-and-linked-processes-ipumowptdb.pdf

Epigenetic control of plant senescence and linked processes

The plastid-nucleus located protein WHIRLY1 has been described as an upstream regulator of leaf senescence, binding to the promoter of senescence-associated genes like HvS40. To investigate the impact of WHIRLY1 on drought stress-induced, premature senescence, transgenic barley plants with an RNAi-mediated knockdown of the HvWHIRLY1 gene were grown under normal and drought stress conditions. The course of leaf senescence in these lines was monitored by physiological parameters and studies on the expression of senescence- and drought stress-related genes. Drought treatment accelerated leaf senescence in WT plants, whereas WHIRLY 1 knockdown lines (RNAi-W1) showed a stay-green phenotype. Expression of both senescence-associated and drought stress-responsive genes, was delayed in the transgenic plants. Notably, expression of transcription factors of the WRKY and NAC families, which are known to function in senescence- and stress-related signaling pathways, was affected in plants with impaired accumulation of WHIRLY1, indicating that WHIRLY1 acts as an upstream regulator of drought stress-induced senescence. To reveal the epigenetic indexing of HvS40 at the onset of drought-induced senescence in WT and RNAi-W1 lines, stress-responsive loading with histone modifications of promoter and coding sequences of HvS40 was analyzed by chromatin immunoprecipitation and quantified by qRT-PCR. In the wildtype, the euchromatic mark H3K9ac of the HvS40 gene was low under control conditions and was established in response to drought treatment, indicating the action of epigenetic mechanisms in response to drought stress. However, drought stress caused no significant increase in H3K9ac in plants impaired in accumulation of WHIRLY1. The results show that WHIRLY1 knockdown sets in motion a delay in senescence that involves all aspects of gene expression, including changes in chromatin structure.

/pdf/knockdown-of-whirly1-affects-drought-stress-induced-leaf-2lauzvdd76.pdf

Knockdown of WHIRLY1 Affects Drought Stress-Induced Leaf Senescence and Histone Modifications of the Senescence-Associated Gene HvS40.

Stress-inducible genes undergo epigenetic modifications under stress conditions. To investigate if HSP17, of which transcripts accumulate in plant cells under stress, is regulated through epigenetic mechanisms under drought stress, 5-day-old barley (Hordeum vulgare cv. Carina) plants were subjected to progressive drought through water withholding for 22 days. Changes in physiological status and expression of HSP17 gene were monitored in primary leaves of control and drought-treated plants every two days. Twelve days after drought started, control and drought-treated plants were analyzed by chromatin-immunoprecipitation using antibodies against three histone modifications (H3K4me3, H3K9ac, and H3K9me2) and H3 itself. Already after four days of drought treatment, stomatal conductance was severely decreased. Thereafter, maximum and quantum yield of photosystem II (PSII), regulated and non-regulated energy dissipation in PSII, and later also chlorophyll content, were affected by drought, indicating the stress-induced onset of senescence. At the 12th day of drought, before leaf water content declined, expression of HSP17 gene was increased two-fold in drought-treated plants compared to the controls. Twelve days of drought caused an increase in H3 and a loss in H3K9me2 not only at HSP17, but also at constitutively transcribed reference genes ACTIN, PROTEIN PHOSPHATASE 2A (pp2A), and at silent regions BM9, CEREBA. In contrast, H3K4me3 showed a specific increase at HSP17 gene at the beginning and the middle part of the coding region, indicating that this mark is critical for the drought-responsive transcription status of a gene.

https://www.mdpi.com/2073-4395/7/2/43/pdf

Drought Stress-Related Physiological Changes and Histone Modifications in Barley Primary Leaves at HSP17 Gene

The barley gene HvS40, encoding a putative regulator of leaf senescence, is strongly induced during leaf senescence. As shown by chromatin immunoprecipitation, euchromatic histone modification H3K9ac is added at promoter close to ATG and coding sequence of HvS40 after onset of senescence. In parallel, level of heterochromatic H3K9me2 decreases at this gene. Bisulfite sequencing revealed no DNA-methylation in this region, but a heavily methylated DNA-island, starting 664 bp upstream from translational start site in both, mature and senescent leaves. A decrease in DNA methylation in senescing leaves could be shown at one specific CpG motif at the end of this methylation island. In addition, global changes in chromatin structure during senescence were analyzed via immunocytology, revealing senescence-associated changes in spatial distribution of heterochromatic H3K9me2 patterns in the nuclei. Our results prove a senescence-specific mechanism, altering histone modification marks at distinct sequences of the senescence-associated gene HvS40 and altering distribution of heterochromatic areas in the nuclei.

Alterations of histone modifications at the senescence-associated gene HvS40 in barley during senescence.

Environment-sensitive plant development follows a program inscribed in the DNA, and differential expression of the genes is the prerequisite of this program. In the last decades, it was possible to unravel how genes are correctly transcribed in time and space by interaction of trans-acting factors with cis elements often located in the promoter of a gene. However recently, we learned that, in addition, another level of control, called epigenetic regulation, acting via alterations in chromatin structure is involved.



In this review, we will first summarise the basic mechanisms underlying epigenetic control of gene expression in plants. In the following article, we will focus on some selected recent results showing epigenetic control of major steps in plant development. This review cannot cover all new results in the field and we want to apologise to all who are not mentioned.



Key Concepts 

Plant development involves coordinated expression of genes.
Recent findings show that this is also under epigenetic control.
Epigenetic control is exerted by different mechanisms, including DNA methylation, histone modifications and chromatin remodelling.
These modifications alter chromatin state, and by this, it can induce or repress expression of genes.
Major developmental steps, including seed development, flowering, sexual reproduction and leaf senescence are controlled by epigenetic mechanisms.
Stress responses of plants are also regulated by epigenetic mechanisms.




Keywords:

chromatin;
DNA methylation;
epigenetic control;
histone modifications

Bianka Janack

Papers

Epigenetic control of plant senescence and linked processes

Knockdown of WHIRLY1 Affects Drought Stress-Induced Leaf Senescence and Histone Modifications of the Senescence-Associated Gene HvS40.

Drought Stress-Related Physiological Changes and Histone Modifications in Barley Primary Leaves at HSP17 Gene

Alterations of histone modifications at the senescence-associated gene HvS40 in barley during senescence.

Epigenetic Regulation in Plants