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New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View

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A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Molecular Biology".

Deadline for manuscript submissions: closed (15 June 2021) | Viewed by 43909

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Dr. Itziar A. Montalbán

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Guest Editor

Department of Forestry Science, NEIKER-BRTA, 01080 Arkaute, Spain
Interests: cryopreservation; in vitro culture; physiology; forestry
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Dr. Paloma Moncaleán

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Department of Forestry Science, NEIKER-BRTA, 01080 Arkaute, Spain
Interests: bioeconomy; in vitro culture; physiology; forestry
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Dear Colleagues,

Plant somatic embryogenesis has been proven to be a potent biotechnological tool with multiple applications: clonal propagation of genetically uniform plants, source of material for genetic transformation, supply of material for multivariate forestry, development of synthetic seeds, or regeneration of plants from protoplasts. In addition, it is an ideal model to try to understand the molecular mechanisms that control the developmental plasticity in plants.

Plant plasticity is affected by many factors that include genetic composition, explant type, and the physicochemical environment. The induction of plant somatic embryogenesis is accomplished via the transcriptomic reprogramming of the somatic cells in response to signals usually related to stress. The stress is produced through the application of hormones or high temperatures, among others. In this reprogramming, epigenetic changes such as DNA methylation or histone modifications, among others, play a key role.

Epigenetic changes, apart from modifying the developmental cell fate, can trigger adaptative responses at plant level; this, together with the abovementioned applications of somatic embryogenesis, has enormous potentialities for agriculture and forestry. In spite of the fair amount of information being gathered in recent years, there are still challenges and questions to be solved—for example, knowledge about the underlying molecular mechanisms in dedifferentiation and subsequent redifferentiation of somatic cells, and why it is only accomplished in some cells or genotypes, remains scarce. Consequently, this Special Issue will welcome research that focuses on new insights into plant somatic embryogenesis: genetic and epigenetic view.

Dr. Itziar A. Montalbán
Dr. Paloma Moncaleán
Guest Editors

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Keywords

DNA methylation
epigenetic changes
gene expression
histone modification
in vitro culture
plasticity
somatic embryo
tissue culture
totipotency

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Published Papers (10 papers)

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11 pages, 632 KiB

Open AccessArticle

Heat Stress in Pinus halepensis Somatic Embryogenesis Induction: Effect in DNA Methylation and Differential Expression of Stress-Related Genes

by Cátia Pereira, Ander Castander-Olarieta, Ester Sales, Itziar A. Montalbán, Jorge Canhoto and Paloma Moncaleán

Plants 2021, 10(11), 2333; https://doi.org/10.3390/plants10112333 - 29 Oct 2021

Cited by 13 | Viewed by 2748

Abstract

In the current context of climate change, plants need to develop different mechanisms of stress tolerance and adaptation to cope with changing environmental conditions. Temperature is one of the most important abiotic stresses that forest trees have to overcome. Recent research developed in our laboratory demonstrated that high temperatures during different stages of conifer somatic embryogenesis (SE) modify subsequent phases of the process and the behavior of the resulting ex vitro somatic plants. For this reason, Aleppo pine SE was induced under different heat stress treatments (40 °C for 4 h, 50 °C for 30 min, and 60 °C for 5 min) in order to analyze its effect on the global DNA methylation rates and the differential expression of four stress-related genes at different stages of the SE process. Results showed that a slight decrease of DNA methylation at proliferating embryonal masses (EMs) can correlate with the final efficiency of the process. Additionally, different expression patterns for stress-related genes were found in EMs and needles from the in vitro somatic plants obtained; the DEHYDRATION INDUCED PROTEIN 19 gene was up-regulated in response to heat at proliferating EMs, whereas HSP20 FAMILY PROTEIN and SUPEROXIDE DISMUTASE [Cu–Zn] were down-regulated in needles. Full article

(This article belongs to the Special Issue New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View)

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16 pages, 1840 KiB

Open AccessArticle

Comparative Transcriptomics of Non-Embryogenic and Embryogenic Callus in Semi-Recalcitrant and Non-Recalcitrant Upland Cotton Lines

by Sonika Kumar, Ashleigh Ruggles, Sam Logan, Alora Mazarakis, Thomas Tyson, Matthew Bates, Clayton Grosse, David Reed, Zhigang Li, Jane Grimwood, Jeremy Schmutz and Christopher Saski

Plants 2021, 10(9), 1775; https://doi.org/10.3390/plants10091775 - 26 Aug 2021

Cited by 11 | Viewed by 3252

Abstract

Somatic embryogenesis-mediated plant regeneration is essential for the genetic manipulation of agronomically important traits in upland cotton. Genotype specific recalcitrance to regeneration is a primary challenge in deploying genome editing and incorporating useful transgenes into elite cotton germplasm. In this study, transcriptomes of a semi-recalcitrant cotton (Gossypium hirsutum L.) genotype ‘Coker312’ were analyzed at two critical stages of somatic embryogenesis that include non-embryogenic callus (NEC) and embryogenic callus (EC) cells, and the results were compared to a non-recalcitrant genotype ‘Jin668’. We discovered 305 differentially expressed genes in Coker312, whereas, in Jin668, about 6-fold more genes (2155) were differentially expressed. A total of 154 differentially expressed genes were common between the two genotypes. Gene enrichment analysis of the upregulated genes identified functional categories, such as lipid transport, embryo development, regulation of transcription, sugar transport, and vitamin biosynthesis, among others. In Coker312 EC cells, five major transcription factors were highly upregulated: LEAFY COTYLEDON 1 (LEC1), WUS-related homeobox 5 (WOX5), ABSCISIC ACID INSENSITIVE3 (ABI3), FUSCA3 (FUS3), and WRKY2. In Jin668, LEC1, BABY BOOM (BBM), FUS3, and AGAMOUS-LIKE15 (AGL15) were highly expressed in EC cells. We also found that gene expression of these embryogenesis genes was typically higher in Jin668 when compared to Coker312. We conclude that significant differences in the expression of the above genes between Coker312 and Jin668 may be a critical factor affecting the regenerative ability of these genotypes. Full article

(This article belongs to the Special Issue New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View)

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19 pages, 2676 KiB

Open AccessArticle

Histone Deacetylase Inhibitors Increase the Embryogenic Potential and Alter the Expression of Embryogenesis-Related and HDAC-Encoding Genes in Grapevine (Vitis vinifera L., cv. Mencía)

by Óscar Martínez, Verónica Arjones, María Victoria González and Manuel Rey

Plants 2021, 10(6), 1164; https://doi.org/10.3390/plants10061164 - 8 Jun 2021

Cited by 11 | Viewed by 3448

Abstract

The low induction rates of somatic embryogenesis are one of the main limitations in its routine application in the grapevine (Vitis vinifera L.). The use of an induction medium containing histone deacetylase inhibitors (trichostatin A and, mainly, sodium butyrate) resulted in an improvement of the embryogenic responses in grapevine (cv. Mencía) cotyledonary and recently germinated somatic embryos. The relative expression of several grapevine genes related to embryogenic competence or encoding histone deacetylase enzymes was studied in cotyledonary somatic embryos that were cultured in the presence of 0.5 mM sodium butyrate. The results showed a significant overexpression of the BBM and VvSERK2 genes after 24 h of culture, whereas the VvWOX2 gene was underexpressed less in treated versus untreated explants. The results suggest that the inhibitor may trigger a molecular response related to an increase in embryogenic competence and changes in the expression of associated genes. The treatment with sodium butyrate also produced significant variations in the expression of several histone deacetylase enzyme-encoding genes. These results may enhance the possibility of obtaining somatic embryos, reducing the seasonal constraints associated with the use of floral explants in grapevines. Full article

(This article belongs to the Special Issue New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View)

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16 pages, 1274 KiB

Open AccessArticle

Factors Influencing Somatic Embryo Maturation in Sugi (Japanese Cedar, Cryptomeria japonica (Thunb. ex L.f.) D. Don)

by Tsuyoshi E. Maruyama, Saneyoshi Ueno, Hideki Mori, Takumi Kaneeda and Yoshinari Moriguchi

Plants 2021, 10(5), 874; https://doi.org/10.3390/plants10050874 - 26 Apr 2021

Cited by 14 | Viewed by 2818

Abstract

This paper presents the results of several experiments identifying basal salts (BS) contained in maturation medium, polyethylene glycol (PEG) concentration, abscisic acid (ABA) concentration, additional supplementation with potassium chloride (KCl), amino acid (AA) concentration, and proliferation culture medium (PCM) as the main culture factors affecting somatic embryo maturation in sugi (Japanese cedar, Cryptomeria japonica, Cupressaceae). Highly efficient embryo maturation was achieved when embryogenic cell lines (ECLs) were cultured on media supplemented with a combination of PEG, ABA, and AAs. More than 1000 embryos per gram of fresh weight (FW) can be produced on EM maturation medium supplemented with 175 g L⁻¹ PEG, 100 µM ABA, 2 g L⁻¹ glutamine, 1 g L⁻¹ asparagine, and 0.5 g L⁻¹ arginine. Full article

(This article belongs to the Special Issue New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View)

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24 pages, 3624 KiB

Open AccessArticle

Priming Maritime Pine Megagametophytes during Somatic Embryogenesis Improved Plant Adaptation to Heat Stress

by María Amparo Pérez-Oliver, Juan Gregorio Haro, Iva Pavlović, Ondřej Novák, Juan Segura, Ester Sales and Isabel Arrillaga

Plants 2021, 10(3), 446; https://doi.org/10.3390/plants10030446 - 26 Feb 2021

Cited by 11 | Viewed by 3392

Abstract

In the context of global climate change, forest tree research should be addressed to provide genotypes with increased resilience to high temperature events. These improved plants can be obtained by heat priming during somatic embryogenesis (SE), which would produce an epigenetic-mediated transgenerational memory. Thereby, we applied 37 °C or 50 °C to maritime pine (Pinus pinaster) megagametophytes and the obtained embryogenic masses went through the subsequent SE phases to produce plants that were further subjected to heat stress conditions. A putative transcription factor WRKY11 was upregulated in priming-derived embryonal masses, and also in the regenerated P37 and P50 plants, suggesting its role in establishing an epigenetic memory in this plant species. In vitro-grown P50 plants also showed higher cytokinin content and SOD upregulation, which points to a better responsiveness to heat stress. Heat exposure of two-year-old maritime pine plants induced upregulation of HSP70 in those derived from primed embryogenic masses, that also showed better osmotic adjustment and higher increases in chlorophyll, soluble sugars and starch contents. Moreover, ϕPSII of P50 plants was less affected by heat exposure. Thus, our results suggest that priming at 50 °C at the SE induction phase is a promising strategy to improve heat resilience in maritime pine. Full article

(This article belongs to the Special Issue New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View)

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15 pages, 2319 KiB

Open AccessArticle

Telomere Length in Norway Spruce during Somatic Embryogenesis and Cryopreservation

by Tuija Aronen, Susanna Virta and Saila Varis

Plants 2021, 10(2), 416; https://doi.org/10.3390/plants10020416 - 23 Feb 2021

Cited by 7 | Viewed by 2549

Abstract

Telomeres i.e., termini of the eukaryotic chromosomes protect chromosomes during DNA replication. Shortening of telomeres, either due to stress or ageing is related to replicative cellular senescence. There is little information on the effect of biotechnological methods, such as tissue culture via somatic embryogenesis (SE) or cryopreservation on plant telomeres, even if these techniques are widely applied. The aim of the present study was to examine telomeres of Norway spruce (Picea abies (L.) Karst.) during SE initiation, proliferation, embryo maturation, and cryopreservation to reveal potential ageing or stress-related effects that could explain variation observed at SE process. Altogether, 33 genotypes from 25 families were studied. SE initiation containing several stress factors cause telomere shortening in Norway spruce. Following initiation, the telomere length of the embryogenic tissues (ETs) and embryos produced remains unchanged up to one year of culture, with remarkable genotypic variation. Being prolonged in vitro culture can, however, shorten the telomeres and should be avoided. This is achieved by successful cryopreservation treatment preserving telomere length. Somatic embryo production capacity of the ETs was observed to vary a lot not only among the genotypes, but also from one timepoint to another. No connection between embryo production and telomere length was found, so this variation remains unexplained. Full article

(This article belongs to the Special Issue New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View)

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16 pages, 764 KiB

Open AccessArticle

Induction of Radiata Pine Somatic Embryogenesis at High Temperatures Provokes a Long-Term Decrease in DNA Methylation/Hydroxymethylation and Differential Expression of Stress-Related Genes

by Ander Castander-Olarieta, Cátia Pereira, Ester Sales, Mónica Meijón, Isabel Arrillaga, María Jesús Cañal, Tomás Goicoa, María Dolores Ugarte, Paloma Moncaleán and Itziar A. Montalbán

Plants 2020, 9(12), 1762; https://doi.org/10.3390/plants9121762 - 13 Dec 2020

Cited by 20 | Viewed by 3259

Abstract

Based on the hypothesis that embryo development is a crucial stage for the formation of stable epigenetic marks that could modulate the behaviour of the resulting plants, in this study, radiata pine somatic embryogenesis was induced at high temperatures (23 °C, eight weeks, control; 40 °C, 4 h; 60 °C, 5 min) and the global methylation and hydroxymethylation levels of emerging embryonal masses and somatic plants were analysed using LC-ESI-MS/ MS-MRM. In this context, the expression pattern of six genes previously described as stress-mediators was studied throughout the embryogenic process until plant level to assess whether the observed epigenetic changes could have provoked a sustained alteration of the transcriptome. Results indicated that the highest temperatures led to hypomethylation of both embryonal masses and somatic plants. Moreover, we detected for the first time in a pine species the presence of 5-hydroxymethylcytosine, and revealed its tissue specificity and potential involvement in heat-stress responses. Additionally, a heat shock protein-coding gene showed a down-regulation tendency along the process, with a special emphasis given to embryonal masses at first subculture and ex vitro somatic plants. Likewise, the transcripts of several proteins related with translation, oxidative stress response, and drought resilience were differentially expressed. Full article

(This article belongs to the Special Issue New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View)

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16 pages, 996 KiB

Open AccessEditor’s ChoiceReview

Genetic and Molecular Control of Somatic Embryogenesis

by Camille Salaün, Loïc Lepiniec and Bertrand Dubreucq

Plants 2021, 10(7), 1467; https://doi.org/10.3390/plants10071467 - 17 Jul 2021

Cited by 58 | Viewed by 9961

Abstract

Somatic embryogenesis is a method of asexual reproduction that can occur naturally in various plant species and is widely used for clonal propagation, transformation and regeneration of different crops. Somatic embryogenesis shares some developmental and physiological similarities with zygotic embryogenesis as it involves common actors of hormonal, transcriptional, developmental and epigenetic controls. Here, we provide an overview of the main signaling pathways involved in the induction and regulation of somatic embryogenesis with a focus on the master regulators of seed development, LEAFY COTYLEDON 1 and 2, ABSCISIC ACID INSENSITIVE 3 and FUSCA 3 transcription factors whose precise role during both zygotic and somatic embryogenesis remains to be fully elucidated. Full article

(This article belongs to the Special Issue New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View)

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30 pages, 1105 KiB

Open AccessReview

Modulation of Organogenesis and Somatic Embryogenesis by Ethylene: An Overview

by Mariana Neves, Sandra Correia, Carlos Cavaleiro and Jorge Canhoto

Plants 2021, 10(6), 1208; https://doi.org/10.3390/plants10061208 - 14 Jun 2021

Cited by 18 | Viewed by 6202

Abstract

Ethylene is a plant hormone controlling physiological and developmental processes such as fruit maturation, hairy root formation, and leaf abscission. Its effect on regeneration systems, such as organogenesis and somatic embryogenesis (SE), has been studied, and progress in molecular biology techniques have contributed to unveiling the mechanisms behind its effects. The influence of ethylene on regeneration should not be overlooked. This compound affects regeneration differently, depending on the species, genotype, and explant. In some species, ethylene seems to revert recalcitrance in genotypes with low regeneration capacity. However, its effect is not additive, since in genotypes with high regeneration capacity this ability decreases in the presence of ethylene precursors, suggesting that regeneration is modulated by ethylene. Several lines of evidence have shown that the role of ethylene in regeneration is markedly connected to biotic and abiotic stresses as well as to hormonal-crosstalk, in particular with key regeneration hormones and growth regulators of the auxin and cytokinin families. Transcriptional factors of the ethylene response factor (ERF) family are regulated by ethylene and strongly connected to SE induction. Thus, an evident connection between ethylene, stress responses, and regeneration capacity is markedly established. In this review the effect of ethylene and the way it interacts with other players during organogenesis and somatic embryogenesis is discussed. Further studies on the regulation of ERF gene expression induced by ethylene during regeneration can contribute to new insights on the exact role of ethylene in these processes. A possible role in epigenetic modifications should be considered, since some ethylene signaling components are directly related to histone acetylation. Full article

(This article belongs to the Special Issue New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View)

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17 pages, 721 KiB

Open AccessReview

Small Non-Coding RNAs at the Crossroads of Regulatory Pathways Controlling Somatic Embryogenesis in Seed Plants

by Ana Alves, Daniela Cordeiro, Sandra Correia and Célia Miguel

Plants 2021, 10(3), 504; https://doi.org/10.3390/plants10030504 - 9 Mar 2021

Cited by 6 | Viewed by 3190

Abstract

Small non-coding RNAs (sncRNAs) are molecules with important regulatory functions during development and environmental responses across all groups of terrestrial plants. In seed plants, the development of a mature embryo from the zygote follows a synchronized cell division sequence, and growth and differentiation events regulated by highly regulated gene expression. However, given the distinct features of the initial stages of embryogenesis in gymnosperms and angiosperms, it is relevant to investigate to what extent such differences emerge from differential regulation mediated by sncRNAs. Within these, the microRNAs (miRNAs) are the best characterized class, and while many miRNAs are conserved and significantly represented across angiosperms and other seed plants during embryogenesis, some miRNA families are specific to some plant lineages. Being a model to study zygotic embryogenesis and a relevant biotechnological tool, we systematized the current knowledge on the presence and characterization of miRNAs in somatic embryogenesis (SE) of seed plants, pinpointing the miRNAs that have been reported to be associated with SE in angiosperm and gymnosperm species. We start by conducting an overview of sncRNA expression profiles in the embryonic tissues of seed plants. We then highlight the miRNAs described as being involved in the different stages of the SE process, from its induction to the full maturation of the somatic embryos, adding references to zygotic embryogenesis when relevant, as a contribution towards a better understanding of miRNA-mediated regulation of SE. Full article

(This article belongs to the Special Issue New Insights into Plant Somatic Embryogenesis: Genetic and Epigenetic View)

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