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Application of Tissue Culture in Plant Reproduction

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A special issue of Forests (ISSN 1999-4907). This special issue belongs to the section "Forest Ecophysiology and Biology".

Deadline for manuscript submissions: closed (20 October 2020) | Viewed by 36905

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Dr. Elena Corredoira

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Instituto de Investigaciones Agrobiológicas de Galicia (IIAG), Avd Vigo s/n, 15705 Santiago de Compostela, Spain
Interests: cell culture; plant biotechnology; tissue culture; biotechnology; plant biology; genetics plant genetics; plant physiology; plant breeding; PCR
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Dr. Rita Lourenço Costa

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Co-Guest Editor

Instituto Nacional de Investigação Agrária e Veterinária, I.P. Av. da República, Quinta do Marquês, 2780-157 Oeiras, Portugal
Interests: gene expression; transcriptome analysis; RNA-sequencing; pine wilt disease; Pinus pinaster; Bursaphelenchus xylophilus; Castanea spp.; molecular breeding; biotic stresses
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Trees have an environmental, social, and economic impact. The increasing degradation of forests, together with a higher demand for wood and fruits, has led to the need for more efficient trees, adapted to the current climatic conditions and thus to the need for genetic improvement programs. Traditional methods of genetic improvement are limited by the long reproductive cycle of woody species, as well as by the genetic complexity of many characteristics of interest, including tolerance to abiotic stresses, diseases, and pests and the quality of forest products. Micropropagation techniques are valuable biotechnological tools that show significant benefits when applied to tree regeneration and clonal propagation. Cryostorage of valuable germoplasm and genetic transformation are regarded as some of the most promising applications. Biotechnology and in particular vegetative propagation techniques, via somatic embryogenesis, may shorten the time required for genetic improvements if the desirable characters are maintained in clonal descendants. However, problems related to tree age or maturity must be overcome. Thus, while seedlings or juvenile tree explants are relatively easy to regenerate and transform, explants from mature trees tend to lose regeneration potential.

In genetic transformation programs for forest trees, several traits could be potentially targeted in a molecular breeding approach, with the aim of, e.g., reducing the generation time, producing sterile trees, increasing pest or disease resistance, improving wood formation, developing phytoremediation procedures, and producing new chemicals and pharmaceuticals. However, efficient in vitro regeneration systems are required in order to enable new characteristics to be incorporated and to produce large populations of transformants. The same applies to cryopreservation procedures.

The aim of this issue is to report progress on the development of methods for improving woody plant regeneration, especially from adult trees, and on the use of genetic transformation approaches for tree improvement and tree conservation. Original research articles, reviews, mini reviews, methods, and opinion articles are welcome.

Dr. Elena Corredoira
Dr. Rita Lourenço Costa
Guest Editors

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Keywords

adult trees
adventitious buds
axillary shoot proliferation
germplasm conservation
genetic transformation
organogenesis
phase change
somatic embryogenesis
tree biotechnology
tree improvement

Published Papers (12 papers)

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Editorial

Jump to: Research, Review, Other

3 pages, 661 KiB

Open AccessEditorial

Application of Tissue Culture in Plant Reproduction

by Elena Corredoira and Rita L. Costa

Forests 2021, 12(3), 342; https://doi.org/10.3390/f12030342 - 15 Mar 2021

Cited by 3 | Viewed by 2306

Abstract

The increasing degradation of forests, together with a higher demand for wood and fruit, has led to the need for more efficient trees adapted to the current climatic conditions and, thus, to the need for genetic improvement programs [...] Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

Research

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10 pages, 1544 KiB

Open AccessArticle

Root Rot Resistance Locus PaLAR3 Is Delivered by Somatic Embryogenesis (SE) Pipeline in Norway Spruce (Picea abies (L.) Karst.)

by Jaanika Edesi, Mikko Tikkinen, Malin Elfstrand, Åke Olson, Saila Varis, Ulrika Egertsdotter and Tuija Aronen

Forests 2021, 12(2), 193; https://doi.org/10.3390/f12020193 - 08 Feb 2021

Cited by 6 | Viewed by 2173

Abstract

Research Highlights: The Norway spruce somatic embryogenesis (SE) pipeline is suitable for multiplication of material with root rot resistance traits. Background and Objectives: Heterobasidion root rot is the economically most severe forest pathogen in Europe, reducing the benefit of planting elite forest material. In this study, the SE-propagation ability of elite Norway spruce material carrying root rot resistance traits was studied. Materials and Methods: We analyzed the presence of the root rot resistance locus PaLAR3B among 80 Finnish progeny-tested Norway spruce plus-trees used for SE-plant production as well as in 241 SE lines (genotypes) derived from them. Seven full-sib families with lines having either AA, AB, or BB genotype for PaLAR3 locus were further studied for their SE-plant propagation ability. Results: The results indicate that 47.5% of the studied elite trees carry the PaLAR3B allele (45% are heterozygous and 2.5% homozygous). The resistance allele was present among the SE lines as expected based on Mendelian segregation and did not interfere with somatic embryo production capacity. All embryos from PaLAR3 genotypes germinated well and emblings were viable in the end of first growing season. However, in three families, PaLAR3B homo- or heterozygotes had 23.2% to 32.1% lower viability compared to their respective hetero- or PaLAR3A homozygotes. Conclusions: There is no trade-off between root rot resistance locus PaLAR3B and somatic embryo production ability, but the allele may interfere with Norway spruce embling establishment. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

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10 pages, 3250 KiB

Open AccessArticle

Putrescine Promotes Betulin Accumulation in Suspension Cell Cultures of Betula platyphylla by Regulating NO and NH₄⁺ Production

by Guizhi Fan, Tingting Zhang, Yingtian Liu, Yaguang Zhan and Baojiang Zheng

Forests 2020, 11(12), 1336; https://doi.org/10.3390/f11121336 - 16 Dec 2020

Cited by 2 | Viewed by 1450

Abstract

Putrescine (Put) can enhance secondary metabolite production, but its intrinsic regulatory mechanism remains unclear. In this study, Put treatment promoted betulin production and gene expression of lupeol synthase (LUS), one of betulin synthetic enzymes. The maximum betulin content and gene expression level of LUS was 4.25 mg·g⁻¹ DW and 8.25 at 12 h after 1 mmol·L⁻¹ Put treatment, approximately two- and four-times that in the control, respectively. Put treatment increased the content of nitric oxide (NO) and its biosynthetic enzyme activity of nitrate reductase (NR) and NO synthase (NOS). Pretreatment of the birch suspension cells with NO-specific scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline- 1-oxyl-3-oxide (cPTIO), NR inhibitor sodium azide (NaN₃), and NOS inhibitor N^G-nitro-L-Arg methyl ester (L-NAME) decreased Put-triggered NO generation and blocked Put-induced betulin production. Put treatment improved the content of NH₄⁺ and its assimilation enzyme activity of glutamate synthase and glutamate dehydrogenase. NH₄⁺ supplementation also promoted NO and betulin production. Thus, the above data indicated that Put-induced NO was essential for betulin production. NO derived from NR, NOS, and NH₄⁺ mediated betulin production in birch suspension cell cultures under Put treatment. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

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15 pages, 2235 KiB

Open AccessArticle

Physiological and Structural Aspects of In Vitro Somatic Embryogenesis in Abies alba Mill

by Terezia Salaj, Katarina Klubicová, Bart Panis, Rony Swennen and Jan Salaj

Forests 2020, 11(11), 1210; https://doi.org/10.3390/f11111210 - 17 Nov 2020

Cited by 10 | Viewed by 2747

Abstract

Initiation of somatic embryogenesis from immature zygotic embryos, long-term maintenance of embryogenic tissue in vitro or by cryopreservation, as well as maturation, of somatic embryos of Abies alba Mill. are reported in this study. For the initiation of embryogenic tissues, a DCR medium containing different types of cytokinins (1 mg.L⁻¹) were tested. During three consecutive years, 61 cell lines were initiated out of 1308 explants, with initiation frequencies ranging between 0.83 and 13.33%. The type of cytokinin had no profound effect on the initiation frequency within one given year. Microscopic observations revealed presence of bipolar somatic embryos in all initiated embryogenic tissues. Besides the typical bipolar somatic embryos, huge polyembryonal complexes, as well as “twin” embryos, were observed. Maturation of somatic embryos occurred on a DCR medium supplemented by abscisic acid (10 mg.L⁻¹), polyethylene glycol (PEG-4000, 7.5%) and 3% maltose. The maturation capacity was cell-line dependent. All of the four tested cell lines produced cotyledonary somatic embryos, though at different quantities, of 16 to 252 per g of fresh weight. After germination, seedlings developed, but their further growth soon stopped after the formation of a resting bud. Altogether, seven cell lines were cryopreserved, using the slow-freezing technique. After rewarming, all tested cell lines showed regrowth rates between 81.8 and 100%. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

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15 pages, 4932 KiB

Open AccessArticle

Transformation of American Chestnut (Castanea dentata (Marsh.) Borkh) Using RITA^® Temporary Immersion Bioreactors and We Vitro Containers

by Linda McGuigan, Patrícia Fernandes, Allison Oakes, Kristen Stewart and William Powell

Forests 2020, 11(11), 1196; https://doi.org/10.3390/f11111196 - 13 Nov 2020

Cited by 8 | Viewed by 3461

Abstract

American chestnut (Castanea dentata (Marsh.) Borkh) was almost completely wiped out by the fungal pathogen, Cryphonectria parasitica (Murrill) M.E. Barr. Another invasive pathogen, Phytophthora cinnamomi Rands, is devastating American chestnuts in the southern region of the United States. An alternative approach for controlling these pathogens is to use genetic engineering or gene editing. We successfully transformed American chestnut with a detoxifying enzyme, oxalate oxidase, to enhance blight tolerance and more recently with the Cast_Gnk2-like gene, which encodes for an antifungal protein, to be tested for P. cinnamomi putative tolerance. Eight somatic embryo lines were transformed using three methods of selection: semisolid medium in Petri plates, liquid medium in RITA^® temporary immersion bioreactors, or liquid medium in We Vitro containers. No significant differences were found between the treatments. These methods will allow for further testing of transgenes and the development of enhanced pathogen resistance in chestnut. It can serve as a model for other tree species threatened by invasive pests and pathogens. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

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14 pages, 3791 KiB

Open AccessArticle

Pinus spp. Somatic Embryo Conversion under High Temperature: Effect on the Morphological and Physiological Characteristics of Plantlets

by Antonia Maiara Marques do Nascimento, Priscila Alves Barroso, Naysa Flavia Ferreira do Nascimento, Tomás Goicoa, María Dolores Ugarte, Itziar Aurora Montalbán and Paloma Moncaleán

Forests 2020, 11(11), 1181; https://doi.org/10.3390/f11111181 - 08 Nov 2020

Cited by 8 | Viewed by 2415

Abstract

Climatic variations in the current environmental scenario require plants with tolerance to sudden changes in temperature and a decrease in water availability. Accordingly, this tolerance will enable successful plantations and the maintenance of natural and planted forests. Consequently, in the last two decades, drought tolerance and high temperatures in conifers have been an important target for morphological, physiological, and epigenetic studies. Based on this, our research team has optimized different stages of somatic embryogenesis (SE) in Pinus spp. improving the success of the process. Through this method, we can obtain a large amount of clonal material and then analyze the somatic plants under different conditions ex vitro. The analysis of the morphological and physiological parameters in somatic embryos (ses) and plants with different tolerances to abiotic stress can provide us with valuable information about the mechanisms used by plants to survive under adverse environmental conditions. Thus, the objective of this work was to evaluate the influence of high temperatures (23, 40, 50, and 60 °C, after 12 weeks, 90, 30, 5 min, respectively) on the morphology of somatic embryos obtained from Pinus radiata D.Don (Radiata pine) and Pinus halepensis Mill. (Aleppo pine). In addition, we carried out a physiological evaluation of the somatic plants of P. radiata submitted to heat and water stress in a greenhouse. We observed that the number of somatic embryos was not affected by maturation temperatures in both species. Likewise, P. radiata plants obtained from these somatic embryos survived drought and heat stress in the greenhouse. In addition, plants originating from embryonal masses (EMs) subjected to high maturation temperature (40 and 60 °C) had a significant increase in g_s and E. Therefore, it is possible to modulate the characteristics of somatic plants produced by the manipulation of environmental conditions during the process of SE. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

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22 pages, 2957 KiB

Open AccessArticle

Vegetative Propagation of Phytophthora cinnamomi-Tolerant Holm Oak Genotypes by Axillary Budding and Somatic Embryogenesis

by Maria Teresa Martínez, Francisco Javier Vieitez, Alejandro Solla, Raúl Tapias, Noelia Ramírez-Martín and Elena Corredoira

Forests 2020, 11(8), 841; https://doi.org/10.3390/f11080841 - 02 Aug 2020

Cited by 12 | Viewed by 2886

Abstract

Holm oak (Quercus ilex) is one of the most widely distributed tree species in the Mediterranean basin. High mortality rates have been observed in holm oak populations in the southwest of the Iberian Peninsula as a result of oak decline syndrome. Selection and propagation of genotypes tolerant to this syndrome could aid the restoration of affected areas. In this article, we report micropropagation and conservation procedures based on axillary budding and somatic embryogenesis (SE) of holm oak plants, selected for their tolerance to Phytophthora cinnamomi—the main biotic factor responsible for oak decline. Forced shoots were obtained from potted plants of eight different genotypes, and used as stock material to establish in vitro shoot proliferation cultures. Reliable shoot proliferation was obtained in seven out the eight genotypes established in vitro, whereas multiplication rates were genotype-dependent. The highest rooting rates were obtained by culturing shoots for 24 h or 48 h on rooting induction medium containing 25 mg L⁻¹ indole-3-butyric acid, followed by transfer to medium supplemented with 20 µM silver thiosulphate. Axillary shoot cultures can be successful conserved by cold storage for 12 months at 4 °C under dim lighting. Shoot tips, excised from axillary shoot cultures established from tolerant plants, were used as initial explants to induce SE. Somatic embryos and/or nodular embryogenic structures were obtained on induction medium with or without indole-acetic acid 4 mg L⁻¹, in two out the three genotypes evaluated, and induction rates ranged between 2 and 4%. Plantlet recovery was 45% after two months cold stratification of somatic embryos and eight weeks of culture on germination medium. Vegetative propagation of P. cinnamomi-tolerant Q. ilex trees is a valuable milestone towards the restoration of disease-affected areas. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

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26 pages, 4612 KiB

Open AccessArticle

Embryonal Masses Induced at High Temperatures in Aleppo Pine: Cytokinin Profile and Cytological Characterization

by Cátia Pereira, Ander Castander-Olarieta, Itziar A. Montalbán, Aleš Pěnčík, Ivan Petřík, Iva Pavlović, Eliana De Medeiros Oliveira, Hugo Pacheco de Freitas Fraga, Miguel Pedro Guerra, Ondrej Novák, Miroslav Strnad, Jorge Canhoto and Paloma Moncaleán

Forests 2020, 11(8), 807; https://doi.org/10.3390/f11080807 - 26 Jul 2020

Cited by 15 | Viewed by 2564

Abstract

Aleppo pine (Pinus halepensis Mill.), a native species of the Mediterranean region, has been suggested as a species that when introduced in degraded areas could facilitate the long-term colonization and expansion of late-successional species. Due to climate changes, plants need to withstand extreme environmental conditions through adaptation and changings in developmental pathways. Among other paths, plants undergo changes in developmental pathways controlled by phytohormones. At the same time, somatic embryogenesis has been widely used as a model to understand the mechanisms involved in plant response to different stresses. In this study, in order to induce a strong effect of temperature stress on plants regenerated from somatic embryos, higher temperatures (40 °C for 4 h, 50 °C for 30 min, and 60 °C for 5 min) than the control (23 °C) were applied during the induction stage of somatic embryogenesis in Pinus halepensis. A morphological characterization of the embryogenic cultures showed small differences in the number of starch grains, lipid bodies, and phenolic compounds between treatments. Results showed that high temperatures (60 °C) led to higher rates at the maturation stage of somatic embryogenesis when compared to the control (23 °C), strengthening the productivity through the increase in the number of somatic embryos obtained. Finally, analysis of endogenous concentration of cytokinins showed that different conditions applied during the initiation phase of somatic embryogenesis led to different hormonal profiles; isoprenoid cytokinins showed a clear defined pattern with the higher total hormone concentration being found in embryonal masses induced at 50 °C for 30 min, while different aromatic cytokinins presented different individual responses to the treatments applied. These differences corroborate the idea that cytokinins could be potential regulators of stress–response processes during initial steps of somatic embryogenesis. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

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18 pages, 4607 KiB

Open AccessArticle

Effects of Hormones and Epigenetic Regulation on the Callus and Adventitious Bud Induction of Fraxinus mandshurica Rupr.

by Lei Yu, Xinyu Li, Hongmei Tian, Hualing Liu, Ying Xiao, Nansong Liang, Xingtang Zhao and Yaguang Zhan

Forests 2020, 11(5), 590; https://doi.org/10.3390/f11050590 - 24 May 2020

Cited by 15 | Viewed by 3757

Abstract

Fraxinus mandshurica Rupr. (hereafter “F. mandshurica”) is known as one of northeast China′s important, valuable hardwood timber species. However, tissue culture and micropropagation of the species are difficult and have low efficiency, limiting asexual propagation. In this manuscript, stem explants were utilized to establish an effective regeneration system through adventitious bud organogenesis. The factors influencing callus regeneration in vitro were determined, and callus regeneration technology was established. The mechanism of adventitious bud formation was analyzed. Thidiazuron (TDZ) played a crucial role in the formation of adventitious buds. Elevated concentrations of TDZ were beneficial to callus induction and low concentrations of 6-benzyladenine (BA) led to loose state callus formation. The order of callus induction rates for different explants was stem cotyledon (100%) > segment (98.54%) > hypocotyl (92.56%) > root (50.71%). The effects of exogenous addition of 6-BA and TDZ on the endogenous hormone content of plants during the regeneration of adventitious buds were also assessed, as well as the expression characteristics of genes related to the regeneration pathway. The comprehensive analysis results showed that the suitable medium for callus induction and adventitious bud differentiation was c12 medium (MSB5 + 30 g/L sucrose + 7 g/L Agar + 5 mg/L 6-BA + 8 mg/L TDZ + 2 mg/L glycine + 0.1 mg/L IBA + 5% coconut water). The induction rates of callus and adventitious buds were 99.15% and 33.33%. The addition of 2.4 mg/L of the DNA demethylation reagent 5-azacytidine (5-aza) and 0.15 mg/L of the histone deacetylase inhibitor trichostatin A (TSA) increased the rates of adventitious bud induction by 17.78% over the control. This further laid the foundation for large-scale cultivation of excellent varieties and genetic transformation techniques. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

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Review

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23 pages, 867 KiB

Open AccessReview

The Cryobiotechnology of Oaks: An Integration of Approaches for the Long-Term Ex Situ Conservation of Quercus Species

by Daniel Ballesteros and Hugh W. Pritchard

Forests 2020, 11(12), 1281; https://doi.org/10.3390/f11121281 - 29 Nov 2020

Cited by 13 | Viewed by 4228

Abstract

Conventional dry seed storage is unlikely for about one third of all tree species (and nearly half of evergreen rain forest trees) as they probably produce desiccation sensitive (recalcitrant) seeds. Consequently, international ex situ conservation targets for threatened trees will be difficult to achieve without innovation, especially in cryobiotechnology. We assessed progress in the development of various cryobiotechnology approaches for the preservation of oaks (Quercus), which are keystone species of functioning landscapes, important to the bioeconomy and under increasing threats from the spread of pests and diseases under a changing climate. Various tissues of oaks can be used for banking, from pollen grains to embryo axes. Pollen from five oak species have been shown to be highly desiccation tolerant, making dry pollen storage at low temperatures (including in liquid nitrogen) a valuable technology to support conservation and breeding programs. Somatic embryo (SE) technology and/or shoot tip in vitro technology is available for 39 species, and SE cryopreservation is routinely performed on three commercial species and shoot tips cryopreservation successful in two more species. Seed embryonic axes are the preferred explants for oak ex situ conservation, with tissue survival and regeneration of plants after cryopreservation recorded for 14 and seven species respectively; although differential responses between the shoot and root meristems in the axes are known. Dormant bud preservation seems promising, but is under-researched. Overall, these results indicate the possibility of establishing an integrated platform for the ex situ conservation of oak species based on cryobiotechnology. Challenges of explant choice, optimization of methodologies and large-scale application do remain. However, multiple approaches for the cryopreservation of oak genetic resources are available and implementation programmes should not be delayed, particularly in the centres of species diversity. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

29 pages, 3013 KiB

Open AccessReview

The Prospect of Physiological Events Associated with the Micropropagation of Eucalyptus sp.

by Rambod Abiri, Narges Atabaki, Hazandy Abdul-Hamid, Ruzana Sanusi, Nor Aini Ab Shukor, Noor Azmi Shaharuddin, Siti Aqlima Ahmad and Sonia Malik

Forests 2020, 11(11), 1211; https://doi.org/10.3390/f11111211 - 18 Nov 2020

Cited by 17 | Viewed by 4046

Abstract

Micropropagation is a reliable technique in biotechnology and genetic engineering domain, which has been widely applied for rapid mass propagation of plants in vitro condition. Through micropropagation techniques, reproduction of plants can be attained from different explants using organogenesis and somatic embryogenesis. Over the decades, micropropagation techniques have offered tremendous potential for forest tree improvement. Eucalyptus is a woody plant species recalcitrant to in vitro culture. In general, the micropropagation of Eucalyptus culture processes and the genotype, environment surroundings, and age of explants in culture media is frequently linked with the occurrence of micropropagation variation. In the current review paper, an update of the most important physiological and molecular phenomena aspects of Eucalyptus micropropagation was linked to the most profound information. To achieve the mentioned target, the effect of plant growth regulators (PGRs), nutrients, other adjuvant and environmental features, as well as genetic interaction with morpho- and physiological mechanisms was studied from the induction to plant acclimatisation. On the other hand, important mechanisms behind the organogenesis and somatic embryogenesis of Eucalyptus are discussed. The information of current review paper will help researchers in choosing the optimum condition based on the scenario behind the tissue culture technique of Eucalyptus. However, more studies are required to identify and overcome some of the crucial bottlenecks in this economically important forest species to establish efficient micropropagation protocol at the industrial level. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

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Other

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10 pages, 3056 KiB

Open AccessTechnical Note

A New Clonal Propagation Protocol Develops Quality Root Systems in Chestnut

by Patrícia Fernandes, Sara Tedesco, Inês Vieira da Silva, Carmen Santos, Helena Machado and Rita Lourenço Costa

Forests 2020, 11(8), 826; https://doi.org/10.3390/f11080826 - 29 Jul 2020

Cited by 10 | Viewed by 3165

Abstract

There is, at the present time, a great demand for chestnut rootstocks with improved resistance to Phytophthora cinnamomi Rands in the nurseries. New genotypes are emerging from European chestnut breeding programs and the production of thriving plants to restore old orchards with low yields due to a high incidence of diseases, namely root rot, is necessary. Micropropagation is a useful technique for clonal propagation. Nevertheless, in vitro culture propagation is genotype-dependent. Consequently, the existing protocols may demonstrate poor reproducibility and low efficacy. Thus, the need to contribute to the development of new micropropagation protocols suitable for large production of emerging genotypes. As a contribution to fill this gap, a three-step protocol was developed by using new combinations of Murashige & Skoog, Woody Plant, and adapted modified Melin-Norkrans media in different stages of the propagation process. About 90% of shoots were rooted, and after three months of acclimatization, 85% of these plants survived and were capable of continuous growth in the field. Currently, this protocol is being used in the production of several hybrid genotypes (with improved resistance to P. cinnamomi), selected from our ongoing breeding program and also in Castanea sativa Mill. and Castanea crenata Siebold and Zucc. species. Full article

(This article belongs to the Special Issue Application of Tissue Culture in Plant Reproduction)

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