ISSN e:2007-4034 / ISSN print: 2007-4034

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Vol. 25, issue 3 Septiembre - Diciembre 2019

ISSN: ppub: 1027-152X epub: 2007-4034

Review article

Mutagenesis in the improvement of ornamental plants

http://dx.doi.org/10.5154/r.rchsh.2018.12.022

Hernández-Muñoz, Selene 1 ; Pedraza-Santos, Martha Elena 1 * ; López, Pedro Antonio 2 ; Gómez-Sanabria, Juan Manuel 1 ; Morales-García, José Luciano 1

  • 1Universidad Michoacana de San Nicolás de Hidalgo, Facultad de Agrobiología. Paseo de la Revolución esquina con Berlín, col. Emiliano Zapata, Uruapan, Michoacán, C. P. 60180, MÉXICO.
  • 2Colegio de Postgraduados, Campus Puebla. Carretera Federal México-Puebla km 125.5, Santiago Momoxpan, San Pedro Cholula, Puebla, C. P. 72760, MÉXICO.

*Corresponding author: mpedraza@umich.mx

Received: December 07, 2018; Accepted: June 12, 2019

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Abstract

Mutagenesis is an important tool in the generation of ornamental plant varieties. By 2017, more than 700 varieties had been registered in the mutant variety database jointly administered by the Food and Agriculture Organization of the United Nations and the International Atomic Energy Agency. Among the main genera reported are Chrysanthemum, Rosa, Dahlia and Alstroemeria, with 283, 67, 35 and 35 registered varieties, respectively. Germplasm native to Mexico has been used to generate several varieties of mutant plants abroad. From Dahlia, 18 varieties have been registered and a large number of mutant forms have been generated in Asia and Europe, while from Polianthes mutant forms have been developed in Iran and India, and from Helianthus 569 mutant forms have been developed in Bulgaria. Although mutation induction has proven to be an efficient method for generating ornamental plant varieties, Mexico has failed to register ornamental varieties, and there are few reported studies, among which are reports of mutation induction in species such as Tigridia pavonia, P. tuberosa, Euphorbia pulcherrima, Dendranthema grandiflora, H. annuus and Laelia autumnalis. These works have established the foundations for implementing genetic improvement programs by mutation induction and developing varieties adapted to the different conditions of the country, which also have ornamental attributes that meet the quality standards demanded by the international market.

Keywordsgamma rays; ionizing radiation; mutation induction; radiosensitivity; ornamental varieties

Introduction

The discovery of x-rays by Röentgen in 1895, radioactivity by Becquerel in 1896 and radioactive elements by Marie and Pierre Curie in 1898 (Mba, 2013) led to the deliberate induction of mutations in plants. The first investigations were done with X-rays and caused alterations in the genetic structure of corn (Zea mays) and barley (Hordeum vulgare) crops (Stadler, 1928a; Stadler, 1928b). Beginning with these studies, mutagenesis has been an important method in the successful generation of a large number of promising varieties in different crops (Datta, 2009), such as maize, barley, wheat (Triticum sp.), cotton (Gossypium sp.) and beans (Phaseolus vulgaris) (Chopra, 2005). In ornamental plants, many new varieties have been successfully produced, so it is considered a successful tool (Datta, 2009).

In Mexico, three varieties of soybean (Glycine max) and two of wheat (Triticum aestivum) have been generate with this biotechnology tool has generated (Food and Agriculture Organization of the United Nations / International Atomic Energy Agency [FAO/IAEA], 2017). In ornamentals, efforts have focused on species such as tuberose (Polianthes tuberosa) (Estrada-Basaldua et al., 2011), wild poinsettia (Euphorbia pulcherrima) (Canul-Ku et al., 2012), chrysanthemum (Dendranthema grandiflora) (Castillo-Martínez, de la Cruz-Torrez, Carrillo-Castañeda, & Avendaño-Arrazate, 2015) and sunflower (Helianthus annuus) (Díaz-López et al., 2017).

This review focuses on the use and efficiency of mutation induction with 60Co gamma rays in ornamental plants, with emphasis on plants native to Mexico, for which two objectives were set: to provide a review on mutation induction with 60Co gamma rays in ornamental plants and to carry out a review on variability induction by mutagenesis in plants native to Mexico.

Methodology and criteria used in the search for information

The search for articles was carried out in the Dialnet, Google Scholar, Redalyc, Science Research and Springer Link databases, for which the following keywords were considered in English: ionizing radiation in plants, effect of gamma irradiation, induced mutation ornamental plants, induced mutation by gamma irradiation, mutations in flowers, physical and chemical mutagenesis in ornamental plants, effect of ionizing radiation on plant DNA, cellular changes by gamma irradiation, mutagenesis in crop improvement, plant mutation breeding, in vitro mutagenesis and somaclonal variation, and the following keywords in Spanish: efecto de la radiación gamma, inducción de mutagénesis en ornamentales, irradiación gamma en plantas nativas de México and energía nuclear en el mejoramiento de plantas. The selected articles were those directly related to improvement by mutagenesis with 60Co gamma rays in ornamental plants. In addition, the mutant variety database administered by the joint FAO/IAEA agency was reviewed in detail.

Importance of ornamental plants and their improvement

Floriculture is one of the most important sectors within agriculture, with its growth estimated at approximately $500 million annually. Countries with developed economies, such as the United States, Australia and European countries, have generated a well-established floriculture industry where cut flowers are the most prominent sector (Singh, 2017). By 2010 there were 702,383 ha in production worldwide and exports amounted to $9,784,525,000.00 USD, where Holland was the world leader with 47.7 % of total exports, followed by Colombia, Ecuador, Kenya, Ethiopia and Belgium (Malhotra, 2017). In the same year, the main consumer countries were concentrated in Western Europe and North America, where about 80 % of total production was consumed.

Due to the development of new production areas, where traditional varieties are not adapted, the need to produce new ornamental varieties with improved attributes has increased to provide growth to the floriculture industry (Aida, Ohmiya, & Onozaki, 2018). In addition, European producers maintain novel products as a marketing strategy to remain in the market; therefore, the international demand for new varieties is very high (Gupta & Agnihotri, 2017). However, at the international level, Mexico's participation in this economic chain does not correspond with the advantages that the country has: great floristic wealth, ideal geographic location to facilitate commercialization and solid infrastructure in biotechnological plant research; this is mainly because the floriculture sector depends on foreign varieties, which increases production costs. In 2018, the import value of Dutch Lilium sp. bulbs amounted to $28,778.00 USD, and imports of Rododendrum and Rosa cuttings from the United States and Ecuador amounted to $68,199.00 and $144,545.00 USD, respectively (International Trade Center [ITC], 2019).

Mutations as a source of variation

The growing demand for novel varieties of ornamental plants implies a challenge for plant breeders (Urrea & Ceballos, 2005). Many of the objectives of genetic improvement programs consist of achieving morphological changes and inducing resistance to diseases, pests and adverse abiotic factors, among other outstanding agronomic traits, which can be achieved through mutation induction.

In mutagenesis, deletions or insertions of DNA fragments are induced, which eventually lead to changes in amino acids and modifications in the pigmentation of leaves and stems, as happens with Arabidopsis thaliana (Shikazono et al., 2003). On the other hand, a mutation in the biosynthetic pathway of structural or regulatory genes may cause a change in the color of the gentian (Gentiana triflora) flower (Nakatsuka, Nishihara, Mishiba, & Yamamura, 2005), while changes in coconut palm (Cocos nucifera) leaves may be due to phytochrome alterations, chromosomal aberrations and mitotic inhibition (Abraham & Ninan, 1968). The change in flower color in ornamental plants may be due to a mutation in the L1 layer of the apical meristem, because the epidermis is responsible for flower color (Yamaguchi, 2018). On the other hand, polyploid organisms are more tolerant to irradiation than diploids (Chopra, 2005), so the latter have higher mutation frequencies (Mac, 1954); however, changes do not always occur immediately (Canul-Ku et al., 2012).

In higher plants, mutations may occur with the use of T-DNA (or transposons) or through the exposure of propagules to chemical and physical mutagenic agents. The insertion of T-DNA destroys the structure of the gene, while physical and chemical agents break the DNA strand and during the DNA repair mechanism process, new mutations may occur randomly that are inheritable (Kayalvizhi, Kannan, & Ganga, 2017).

Mutagenic agents and their mode of action

Chemical mutagens

This type of mutagenic agent generates stable and inheritable changes because it induces alterations in simple nucleotides, which can form a new allelic series. Over 80 % of the mutagens applied in plants are alkylating agents, such as ethylmethanesulfonate (EMS), methylnitrosourea (MNU) and ethylnitrosourea (ENU) (Pacher & Puchta, 2017). EMS causes point mutations due to the addition of an alkyl group in the guanine that results in the transition from G:C to A:T, creating allelic versions of genes that give rise to phenotypes with agronomically relevant traits (Dhaliwal, Mohan, Sidhu, Maqbool, & Gill, 2015). Other mutagens, such as hydroxylamine, react with cytosine in the NH group and form hydroxyl cytosine which pairs with adenine instead of guanine. On the other hand, the 5-amino-acridine mutagen is a flat molecule like the base of purine and at low concentrations can be inserted or intercalated between bases of DNA helix and stretches the distance between adjacent base pairs, which distorts the DNA strand (Bhat, Pandit, Sheikh, & Hassan, 2016).

Physical mutagens

In physical mutagens, atoms are the main source material. Unstable atoms of the same element with different weights provide energy particles called radioisotopes and the electromagnetic waves associated with nuclear disintegration are called radiation (Kayalvizhi et al., 2017). These mutagenic agents produce oxygen-reactive species that interact with DNA and cause oxidative damage, such as altered bases (Roldán-Arjona & Ariza, 2009), which induce multiple single or double breaks in the DNA strand (Pacher & Puchta, 2017). Physical mutagens are divided into ionizing and non-ionizing radiation. Neutrons and alpha (α), beta (β), gamma (γ) and X- rays belong to the group of ionizing radiations, while non-ionizing radiation includes only UV rays (Kayalvizhi et al., 2017).

Ionizing radiation

Ionizing radiation is the most commonly used due to the high energy levels employed, making it able to dislodge electrons from the nuclear orbits of the atoms, and the affected atoms become ions, hence the term ionizing radiation (Mba, Afza, & Shu, 2012). This type of radiation causes biological lesions in higher plants through interactions with the genetic material (Lagoda, 2012), which can generate from DNA-level aberrations to chromosomal ruptures and rearrangements (Mba, 2013); that is, it can cause changes in the bases and single or double breaks of the DNA strand (Morita et al., 2009).

Gamma rays. This type of ray is one of the most important mutagenic agents within ionizing radiation because they have been shown to be highly penetrating and potent in inducing variability in plants (Deshpande, Mehetre, & Pingle, 2010). The success of gamma rays has been demonstrated in the generation of new varieties, as more than 55 % of the mutant varieties released have been generated with this technique (Kulkarni, Ganapathi, Suprasanna, & Bapat, 2007). Gamma rays are emitted in the disintegration process of the radioisotopes of carbon-14 (14C), cobalt-60 (60Co), caesium-137 (137Cs) and to a lesser extent plutonium-239 (239Pu). Irradiation may be acute (short periods) or chronic (long periods) (Mba, 2013). The high efficiency of this radiation is because it has an energy level ranging from 10 keV to several hundred keV (Table 1), which gives it greater penetration power than alpha and beta rays (Kovacs & Keresztes, 2002). Its biological effect is based on the interaction with atoms or molecules in the cell, particularly with water, to produce free radicals, which can damage or modify important cellular components. It has been reported that these radicals affect the morphology, anatomy, biochemistry and physiology of plants, according to the level of irradiation (Wi et al., 2005).

Table 1. Electromagnetic wave properties of commonly used physical mutagens.

Mutagenic agent Typical frequency (s-1) Typical energy (kJ·mol-1) Typical photonic energy (eV)
Particles
Alfa 4.1 x 108
Beta 1.5 x 107
Electromagnetic radiation
Gamma rays 3 x 102 1.2 x 108 1 MeV
X-rays 3 x 1017 1.2 x 105 100 KeV
Ultraviolet 3 x 1015 1,200 4 eV

Effect of radiation on plant cells

The response of plants to radiation is more or less linear with the dose used (Yamaguchi, Shimizu, Degi, & Morishita, 2008), which can cause changes in cell structure, such as physical-chemical lesions, small lesions on chromosomes or the combination of both effects (Ramesh, Murthy, & Munirajappa, 2013). Primary lesions delay or inhibit cell division, affect mitotic activity, growth rate or habit, metabolism (such as dilation of thylakoid membranes), photosynthesis, modulation of the antioxidant system and accumulation of phenolic compounds (Wi et al., 2005), cause modifications in lipids, enzymes and other cellular constituents (Kodym & Afza, 2003) and induce cell death (Wi et al., 2005).

Radiation modifies the DNA strand, and the repair mechanism can be produced through two pathways: homologous recombination and nonhomologous-end joining (Kimura & Sakaguchi, 2006). The first is an error-free repair pathway, while the second is an error-prone repair pathway and often causes mutations such as deletions, insertions and inversions in repair sites (Kirik, Salomon, & Puchta, 2000).

Radiosensitivity and median lethal dose

Radiosensitivity depends on the type of radiation and the dose used, as well as on the explant’s traits: type of tissue, size, degree of development and moisture content (Datta & Teixeira-da Silva, 2006), as these traits alter the cells' response to radiation. Soft materials such as in vivo and in vitro cuts and embryogenic calluses require lower doses compared to seeds. Sensitivity also depends on the genetic constitution of the plant material, such as the number and chromosomal size, the nucleotide, the heterochromatin, centromere number and position, degree of polyploidy, nuclear DNA content and replication time at initial stages, as well as cytoplasmic, biological, chemical and environmental factors (Deshpande et al., 2010). Therefore, each genotype should be evaluated for optimal treatment within a range of conditions (Urrea & Ceballos, 2005).

The main purpose of the radiosensitivity study is to determine the most effective radiation dose to increase the frequency of mutations (Barakat & El-Sammak, 2011). Median lethal dose, prolonged level of damage, lethal radiation exposure rate (Abdullah, Endan, & Mohd-Nazir, 2009), reductions in germination rate, seedling height, survival rate and chlorophyll mutations are the main parameters evaluated in sensitivity tests to determine optimal doses (Mba, 2013).

Median lethal dose or mean reductive dose

This dose is the one that reduces survival and growth to 50 % in relation to the control treatment, and is where most mutations are obtained. Some authors recommend an interval of 20 % higher and lower (FAO/IAEA, 1977); other authors state that the optimal dose should lead to the survival of 40 to 60 % of the treated material with respect to the untreated material (Urrea & Ceballos, 2005).

Radioinhibition

Radioinhibition is the negative effect of radiation, and usually occurs at very high doses, where most plants die because mutagens have a direct negative effect on plant tissue, multiplication and regeneration, as well as on their height and development. High doses of radiation cause loss of regenerative capacity and malformation of plants (Chakravarty & Sen, 2001), and many mutations become lethal (Abdullah et al., 2009), since at the cellular level diverse reactions occur that affect vital macromolecules and result in physiological imbalances. High doses of ionizing radiation have been shown to damage DNA and macromolecular components, such as cell walls, membranes (Wi et al., 2005) and organic molecules that are essential for the cell division process, stopping cell division (Tangpong, Taychasinpitak, Jompuk, & Jompuk, 2009).

The death of plants is attributed to the interaction of radiation with molecules in cells, in particular with the water with which they produce free radicals (H and OH). These radicals can combine to form toxic substances, such as hydrogen peroxide (H2O2), which contribute to cell destruction. This indirect effect influences plant cells, as about 80 % of the cytoplasm content is water (Kovacs & Keresztes, 2002).

Radiostimulation

Radio-stimulation occurs with the use of low radiation doses, which stimulate physical and biochemical changes that are reflected in physiological processes such as accelerated plant regeneration (Chakravarty & Sen, 2001) and increased formation of reserve substances (Al-Safadi, Ayyoubi, & Jawdat, 2000).

In vitro culture in mutagenesis

Mutagenesis is more efficient when using cellular totipotency; that is, by using single cells and in vitro cultured plant tissues as starting materials for mutation induction (Mba, 2013). The combination of both techniques has been widely used in the improvement of vegetatively propagated varieties (Maluszynski, Nichterlein, Van-Zanten, & Ahloowalia, 2000); in addition, it has opened up new possibilities to induce a greater number of mutants with outstanding agronomic traits in crops of economic importance. In vitro mutagenesis, as well as increasing genetic variants, makes it possible to supply seedlings for field cultivation on a large scale (Barakat & El-Sammak, 2011). Any explant or callus can be treated with a mutagenic agent and regenerate large populations of plants through in vitro methods under controlled conditions, in limited spaces and at any time of the year. In addition, plants can be observed in the second generation of treated plants (M1V2) and later generations, which is where the possibility of obtaining a greater number of mutants is presented, since the mutated cells of the lower axillary buds remain in latent phase and express their mutant character when they develop during the vegetative propagation of M1V2 (Datta & Teixeira-da Silva, 2006). In vitro mutagenesis has the particular advantage of possibly increasing the frequencies of gene and point mutations, which are the most important in crop improvement (Estrada-Basaldua et al., 2011).

Somaclonal mutation

This type of mutation is the variation that arises in the culture of cells and regenerated plants in vitro, as well as in their progeny. Among the most important factors for the appearance of somaclonal variation are the regeneration system, the type of tissue, the source of the explant, the components of the medium and the duration of the culture cycle (Sarmah et al., 2017). Changes occur when a cell undergoes a mutation and continues to divide; the single cell generate tissue with a genotype different from the rest of the plant cells (Brar & Jain, 1998). These mutations include karyotypic changes, point mutations, somatic crossing-over, somatic gene arrangement, changes in DNA amplification and segregation of pre-existing chimeric tissues (Kearsey & Pooni, 1998).

Ornamental plant varieties generated by mutagenesis

Mutagenesis in ornamental plants represents a powerful tool, not only to clarify physiological mechanisms in plant functioning (Honda et al., 2006), but also to obtain new varieties useful for the floriculture industry (Canul-Ku et al., 2012). Changes in phenotypic traits, such as the color, shape or size of the flower and chlorophyll variegation in leaves, can be easily detected; in addition, due to the heterozygous nature of many cultivars, a high frequency of mutation can occur (Datta & Teixeira-da Silva, 2006), which makes ornamental plants ideal for mutation induction (Urrea & Ceballos, 2005).

By the year 2000, more than 2,200 varieties of mutant plants had been released into the world market; by 2005, this value had increased to 2,335 varieties, of which 552 were ornamental crops (Mba, Afza, Lagoda, & Darwig, 2005), and by 2017 it had increased to 3,249 varieties, of which 720 are ornamental crops (FAO/IAEA, 2017). Mutagenesis has been used in cut flowers and potted plants (Taheri, Abdullah, Ahmad, & Abdullah, 2014). The largest number of varieties have been obtained in the genera Chrysanthemum, Rosa, Dahlia, Alstroemeria, Streptocarpus, Dianthus and Begonia (Table 2) (FAO/IAEA, 2017).

Table 2. Genera with mutant ornamental varieties registered in the joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency database (FAO/IAEA, 2017).

Genus Varieties obtained Varieties obtained with gamma rays
Chrysanthemum 283 150
Rosa 67 52
Dahlia 35 18
Alstroemeria 35 11
Streptocarpus 30 0
Dianthus 28 8
Begonia 25 17
Portulaca 17 17
Bougainvillea 16 14
Rhododendron 15 9
Hibiscus 10 10
Cytisus 9 9
Tulipa 9 0
Achimenes 8 0
Canna 8 8
Lilium 6 4
Limonium 6 6
Antirrhinum 5 0
Iris 5 5
Tibouchina 5 0
Albelmoschus 4 4
Gladiolus 4 2
Hoya 4 4
Juncus 4 3
Kalanchoe 4 1

Chrysanthemum (synonym Dendranthema): Between 1962 and 2015, 283 varieties of this genus were registered with FAO/IAEA. Flower color stands out as the main modified trait (Table 3).

Table 3. Origin, method, material used and number of Chrysanthemum varieties registered in the joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency database (FAO/IAEA, 2017).

Country Varieties Method used Year Material used Improved traits
Germany 34 X-rays (221) and gamma rays (12) 1962 (3), 1964 (1), 1966 (4), 1977 (1),
1979 (1), 1981 (1), 1983 (3), 1984 (2),
1985 (3), 1987 (3), 1988 (8), 1989 (4)
Shoots (4), cuttings (10), not reported (20) Flower color (34)
Belgium 7 X-rays (7) 1985 (7) Cuttings (7) Flower color (7)
Brazil 4 Gamma rays (4) 1995 (2), 1996 (2) Cuttings (1), pedicel (1), not reported (2) Flower color (4)
China 21 Gamma rays (18), not reported (3) 1986 (1), 1987 (1), 1989 (10),
1990 (2) 1991 (1), 1996 (6),
Leaf callus (4), not reported (17) Agronomic and botanical traits (17), growth habit (1), not reported (3)
United States 1 X-rays (1) 1960 (1) Rooted cuttings (1) Flower color (1)
Russia 17 Gamma rays (17) 1976 (17) Rooted cuttings (17) Flower color (17)
Hungary 1 Gamma rays (1) 1969 (1) Not reported (1) Not reported (1)
India 48 Gamma rays (44), X-rays (1),,
irradiation (1), colchicine (1),,
not reported (1)
1969 (1), 1974 (11), 1975 (9), 1978
(3), 1979 (4), 1982 (3), 1984 (1),
1985 (3), 1987 (3), 1990 (1), 1991
(1), 1992 (2), 1993 (1), 1994 (1),
1996 (1), 2003 (1), 2015 (1)
Cuttings (19), vegetative reproduction (21), not reported (8) Flower color (30), flower shape and color (18)
Japan 56 Gamma rays (36), gamma ,
rays and X-rays (1), irradiation,
(1), X-rays (4), ion beams (7),,
somaclonal variation (3), not reported (2)
1985 (4), 1986 (1), 1990 (1), 1991 (6),
1994 (1), 1995 (6), 1997 (7), 1998 (6),
2000 (3), 2001 (3), 2002 (1)
In vitro petal explants (7), in vitro explants (13), leaves (3), not reported (33) Flower color (51), flower size (2), short stems (1), not reported (2)
Malaysia 2 Gamma rays (2) 1976 (2) Callus (2) Flower color and shape (2)
Netherlands 80 Gamma rays (11), X-rays (67), not ,
reported (2)
1969 (1), 1970 (1), 1973 (4), 1975 (5),
1976 (10), 1977 (5), 1978 (10), 1979 (6),
1983 (2), 1984 (9), 1985 (20), 1986 (7)
Rooted cuttings (52), not reported (28) Flower color (79), flower color and size (1)
Poland 6 Gamma rays (2) and X-rays (4) 1993 (6) Not reported (6) Flower color (6)
Republic of Korea 2 Gamma rays (2) 2011 (2) In vitro explants (2) Flower color (2)
Thailand 1 Gamma rays (1) 1987 (1) In vitro explants (1) Flower color (1)
Vietnam 3 Not reported (3) 2010 (1), 2011 (2) Not reported (3) Not reported (3)
1The quantity in brackets indicates the number of varieties registered.

Rosa: The improvement programs of this genus focus on traits linked to the color and size of the flower to increase its economic and ornamental value (Qadeer, Hafiz, Abbasi, & Ahmad, 2015). By 2017, 67 varieties had been released and registered in the FAO/IAEA database. The highest number of varieties was recorded in Asia (86.56 %), Europe (7.46 %) and North America (5.97 %) (Table 4).

Table 4. Origin, method, material used and number of Rosa varieties registered in the joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency database (FAO/IAEA, 2017).

Country Varieties Method used Year Material used Improved traits
Germany 4 X-rays (21), not reported (2) 1965 (1), 1976 (1),
1987 (1), 1988 (1)
Shoots (1), in vitro explants (1), not reported (2) Flower color (4)
Canada 2 Irradiation (1), X-rays (1) 1964 (1), 1976 (1) Not reported (2) Flower color (2)
China 35 Gamma rays (30), not reported (5) 1984 (6), 1985 (2),
1986 (10), 1987 (1),
1989 (5), 1990 (11)
Buds (14), buds and seeds (2), seeds (2), graft (2), branch (4), not reported (1) Leaves and flowers (4), agronomic and botanical traits (24), resistance to pests and diseases (3), not reported (4)
Slovakia 1 Gamma rays (1) 1964 (1) Seeds (1) Flower color (1)
United States 2 Gamma rays (2) 1960 (2) Shoots (2) Flower color (2)
India 15 Gamma rays (14), EMS,
chemical mutagen (1)
1975 (5), 1983 (6),
1986 (3), 1989 (1)
Shoots (14), not reported (1) Flower color (15)
Japan 8 Gamma rays (5), chemical mutagen (3) 1985 (1), 1990 (3),
1995 (1), 2000 (2),
2001 (1)
Not reported (8) Flower color (5), flower color and shape (2), leaf size (1)
1The quantity in brackets indicates the number of varieties released.

Dahlia: The improvement of Dahlia by mutagenesis has been carried out in Europe and Asia. The former generated 65.71 % of the varieties between 1966 and 1971, while the remaining 34.28 % was generated in China and India from 1978 to 1989 (Table 5).

Table 5. Origin, method, material used and number of Dahlia varieties registered in the joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency database (FAO/IAEA, 2017).

Country Varieties Method used Year Material used Improved traits
China 2 Gamma rays (21) 1989 (2) Not reported (2) Agronomic and botanical traits (2)
France 5 Gamma rays (5) 1970 (5) Tubers (5) Flower color (5)
India 10 Gamma rays (10) 1978 (10) Tubers (5) Plant architecture and flower color (5)
Netherlands 18 X-rays (18) 1966 (4), 1967 (5),
1968 (3), 1969 (1),
1970 (1), 1971
(1), 1972 (3)
Tubers (13), not reported (5) Flower color (16), plant architecture and flower color (1), flower size (1)
1The quantity in brackets indicates the number of varieties released.

Alstroemeria: By 2017, the International Atomic Energy Agency database had registered 35 varieties. All varieties were generated in Europe; the Netherlands released 68.57 % and Germany the remaining 31.43 % (Table 6).

Table 6. Origin, method, material used and number of Alstroemeria varieties registered in the joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency database (FAO/IAEA, 2017).

Country Varieties Method used Year Material used Improved traits
Germany 11 Gamma rays (111) 1979 (1), 1981 (5), 1989 (5) Not reported (11) Flower color, early,
flowering and longer post-,
harvest life (11)
Netherlands 24 X-rays (23) and gamma rays (1) 1970 (2), 1971 (1),,
1972 (2), 1973 (1),,
1975 (2), 1977 (6),,
1978 (1), 1979 (4),,
1980 (1), 1983 (2),,
1984 (2)
Rhizomes (7), stolons (1), not reported (16) Flower color (22), plant ,
architecture and flower size (1), early flowering (1)
1The quantity in brackets indicates the number of varieties released.

Ornamental plants native to Mexico improved by mutagenesis in other countries

Mexico is a country with a wide diversity of ornamental plants. The native germplasm of genera such as Dahlia, Eustoma, Helianthus, and Polianthes, among others, has been used abroad to generate diverse varieties of mutant plants. In sunflower (Helianthus annuus), Bulgarian researchers developed 569 mutant forms by treating seeds with 60Co and 137Cs gamma rays (Encheva et al., 2014), and in the FAO/IAEA they registered the Rada variety in 2006, generated with 8 Gy of 137Cs gamma rays, and the Madan variety in 2008, generated with 120 Gy of 60Co gamma rays (FAO/IAEA, 2017). In tuberose (Polianthes tuberosa), genetic improvement techniques developed in Iran generated mutant forms for flower length and weight from irradiating mature bulbs with 10 Gy of 60Co gamma rays (Navabi, Norouzi, Arab, & Daylami, 2016). In India, flower mutants were generated with four, five, seven, eight and eleven tepals per flower (Kayalvizhi et al., 2017), as well as two varieties with leaf variegation (Datta, 2009).

In dahlia (Dahlia), the use of mutagenesis began in the 1960s, and from then until the early 1970s, 18 varieties were registered with FAO/IAEA in the Netherlands and numerous mutant forms were developed for flower color and shape (Broertjes & Ballego, 1967). In India, Dube, Das, Dey, and Bid (1980) selected 19 mutants with changes in the color of the dahlia flower, and by 2017, 12 mutant varieties had been reported in this country (De, 2017). The great aesthetic and economic importance of this genus has encouraged plant breeders to continue with the development of new cultivars to this day. In Egypt, Abou et al. (2017) found that with doses of 100 or 120 KR of 60Co gamma rays in Eustoma gradiflorum the senescence of the flowers is delayed six days and the number of petals per flower is increased, in addition to generating a wide range of colors in the flowers.

These studies, carried out in other countries, have demonstrated that mutation induction is an efficient method in the generation of ornamental and commercial plant varieties from germplasm native to Mexico. However, there are few reported studies on genetic improvement by mutagenesis in Mexico.

Use of mutagenesis in Mexico

The induction of variability by mutagenesis in ornamental plants in Mexico began in the last century. In orchids, roses and daisies, it was possible to increase the number of flowers, vase life and production of marbled petals, respectively. Additionally, researchers from the National Institute of Nuclear Research increased the genetic variability of two Mexican species: Mammillaria sanangelensis, a plant considered in danger of extinction, and Sprekelia formosissima, where they increased the vigor of their root system (González-Jiménez, 2004), while in Tigridia pavonia, with 60Co gamma radiation at doses between 15 and 25 Gy, three mutants were induced in the color hue of the flowers (Díaz-López et al., 2003).

In tuberose (P. tuberosa) tubers, grown in vitro with doses of 5 and 10 Gy, seedlings increased their height and the LD50 was determined at 9 Gy. On the other hand, tubers established in vivo showed differences in leaf length and width, and the LD50 was determined at 25 Gy (Estrada-Basaldua et al., 2011).

Canul-Ku et al. (2012) irradiated wild poinsettia (E. pulcherrima) seeds with 60Co gamma rays and observed a reduction in plant size, an important trait for generating varieties in this species, as well as an increase in seed size. Castillo-Martínez et al. (2015) used 200 Gy of 60Co gamma rays in chrysanthemum (Dendranthema grandiflora) and obtained a dwarf mutant. Díaz-López et al. (2017) evaluated the effect of 60Co gamma radiation on the germination of sunflower (H. annuus) seeds; with 35 Gy they obtained a lower germination percentage (72 %), and as this was the highest dose they did not determine the LD50 and concluded that it is necessary to increase the irradiation dose to 1 KGy.

Hernández-Muñoz et al. (2017a) assessed the effect of 60Co gamma radiation on asymptotic germination of orchid (Laelia autumnalis) seeds and found that 3 Gy stimulated germination and formed complete promeristems, leaves and seedlings, 20, 20 and 10 days earlier than in the control treatment, respectively. In this same species, when irradiating protocorms, it was found that 60Co gamma radiation at doses between 20 and 30 Gy stimulated chlorophyll formation in the protocorms; in addition, seedling length increased 32 % with the 5 Gy dose. The LD50 for protocorm survival and the mean reductive dose for leaf formation were determined with 53 and 28 Gy, respectively (Hernández-Muñoz et al., 2017b).

Conclusions

The use of 60Co gamma radiation in the generation of new ornamental plant varieties is an important and widely used tool in various ornamental crops of economic importance. This technique is an effective option to meet the growing demand for promising new varieties for the floriculture industry in Mexico.

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Tables:

Table 1. Electromagnetic wave properties of commonly used physical mutagens.
Mutagenic agent Typical frequency (s-1) Typical energy (kJ·mol-1) Typical photonic energy (eV)
Particles
Alfa 4.1 x 108
Beta 1.5 x 107
Electromagnetic radiation
Gamma rays 3 x 102 1.2 x 108 1 MeV
X-rays 3 x 1017 1.2 x 105 100 KeV
Ultraviolet 3 x 1015 1,200 4 eV
Table 2. Genera with mutant ornamental varieties registered in the joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency database (FAO/IAEA, 2017).
Genus Varieties obtained Varieties obtained with gamma rays
Chrysanthemum 283 150
Rosa 67 52
Dahlia 35 18
Alstroemeria 35 11
Streptocarpus 30 0
Dianthus 28 8
Begonia 25 17
Portulaca 17 17
Bougainvillea 16 14
Rhododendron 15 9
Hibiscus 10 10
Cytisus 9 9
Tulipa 9 0
Achimenes 8 0
Canna 8 8
Lilium 6 4
Limonium 6 6
Antirrhinum 5 0
Iris 5 5
Tibouchina 5 0
Albelmoschus 4 4
Gladiolus 4 2
Hoya 4 4
Juncus 4 3
Kalanchoe 4 1
Table 3. Origin, method, material used and number of Chrysanthemum varieties registered in the joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency database (FAO/IAEA, 2017).
Country Varieties Method used Year Material used Improved traits
Germany 34 X-rays (221) and gamma rays (12) 1962 (3), 1964 (1), 1966 (4), 1977 (1),
1979 (1), 1981 (1), 1983 (3), 1984 (2),
1985 (3), 1987 (3), 1988 (8), 1989 (4)
Shoots (4), cuttings (10), not reported (20) Flower color (34)
Belgium 7 X-rays (7) 1985 (7) Cuttings (7) Flower color (7)
Brazil 4 Gamma rays (4) 1995 (2), 1996 (2) Cuttings (1), pedicel (1), not reported (2) Flower color (4)
China 21 Gamma rays (18), not reported (3) 1986 (1), 1987 (1), 1989 (10),
1990 (2) 1991 (1), 1996 (6),
Leaf callus (4), not reported (17) Agronomic and botanical traits (17), growth habit (1), not reported (3)
United States 1 X-rays (1) 1960 (1) Rooted cuttings (1) Flower color (1)
Russia 17 Gamma rays (17) 1976 (17) Rooted cuttings (17) Flower color (17)
Hungary 1 Gamma rays (1) 1969 (1) Not reported (1) Not reported (1)
India 48 Gamma rays (44), X-rays (1),,
irradiation (1), colchicine (1),,
not reported (1)
1969 (1), 1974 (11), 1975 (9), 1978
(3), 1979 (4), 1982 (3), 1984 (1),
1985 (3), 1987 (3), 1990 (1), 1991
(1), 1992 (2), 1993 (1), 1994 (1),
1996 (1), 2003 (1), 2015 (1)
Cuttings (19), vegetative reproduction (21), not reported (8) Flower color (30), flower shape and color (18)
Japan 56 Gamma rays (36), gamma ,
rays and X-rays (1), irradiation,
(1), X-rays (4), ion beams (7),,
somaclonal variation (3), not reported (2)
1985 (4), 1986 (1), 1990 (1), 1991 (6),
1994 (1), 1995 (6), 1997 (7), 1998 (6),
2000 (3), 2001 (3), 2002 (1)
In vitro petal explants (7), in vitro explants (13), leaves (3), not reported (33) Flower color (51), flower size (2), short stems (1), not reported (2)
Malaysia 2 Gamma rays (2) 1976 (2) Callus (2) Flower color and shape (2)
Netherlands 80 Gamma rays (11), X-rays (67), not ,
reported (2)
1969 (1), 1970 (1), 1973 (4), 1975 (5),
1976 (10), 1977 (5), 1978 (10), 1979 (6),
1983 (2), 1984 (9), 1985 (20), 1986 (7)
Rooted cuttings (52), not reported (28) Flower color (79), flower color and size (1)
Poland 6 Gamma rays (2) and X-rays (4) 1993 (6) Not reported (6) Flower color (6)
Republic of Korea 2 Gamma rays (2) 2011 (2) In vitro explants (2) Flower color (2)
Thailand 1 Gamma rays (1) 1987 (1) In vitro explants (1) Flower color (1)
Vietnam 3 Not reported (3) 2010 (1), 2011 (2) Not reported (3) Not reported (3)
1The quantity in brackets indicates the number of varieties registered.
Table 4. Origin, method, material used and number of Rosa varieties registered in the joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency database (FAO/IAEA, 2017).
Country Varieties Method used Year Material used Improved traits
Germany 4 X-rays (21), not reported (2) 1965 (1), 1976 (1),
1987 (1), 1988 (1)
Shoots (1), in vitro explants (1), not reported (2) Flower color (4)
Canada 2 Irradiation (1), X-rays (1) 1964 (1), 1976 (1) Not reported (2) Flower color (2)
China 35 Gamma rays (30), not reported (5) 1984 (6), 1985 (2),
1986 (10), 1987 (1),
1989 (5), 1990 (11)
Buds (14), buds and seeds (2), seeds (2), graft (2), branch (4), not reported (1) Leaves and flowers (4), agronomic and botanical traits (24), resistance to pests and diseases (3), not reported (4)
Slovakia 1 Gamma rays (1) 1964 (1) Seeds (1) Flower color (1)
United States 2 Gamma rays (2) 1960 (2) Shoots (2) Flower color (2)
India 15 Gamma rays (14), EMS,
chemical mutagen (1)
1975 (5), 1983 (6),
1986 (3), 1989 (1)
Shoots (14), not reported (1) Flower color (15)
Japan 8 Gamma rays (5), chemical mutagen (3) 1985 (1), 1990 (3),
1995 (1), 2000 (2),
2001 (1)
Not reported (8) Flower color (5), flower color and shape (2), leaf size (1)
1The quantity in brackets indicates the number of varieties released.
Table 5. Origin, method, material used and number of Dahlia varieties registered in the joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency database (FAO/IAEA, 2017).
Country Varieties Method used Year Material used Improved traits
China 2 Gamma rays (21) 1989 (2) Not reported (2) Agronomic and botanical traits (2)
France 5 Gamma rays (5) 1970 (5) Tubers (5) Flower color (5)
India 10 Gamma rays (10) 1978 (10) Tubers (5) Plant architecture and flower color (5)
Netherlands 18 X-rays (18) 1966 (4), 1967 (5),
1968 (3), 1969 (1),
1970 (1), 1971
(1), 1972 (3)
Tubers (13), not reported (5) Flower color (16), plant architecture and flower color (1), flower size (1)
1The quantity in brackets indicates the number of varieties released.
Table 6. Origin, method, material used and number of Alstroemeria varieties registered in the joint Food and Agriculture Organization of the United Nations/International Atomic Energy Agency database (FAO/IAEA, 2017).
Country Varieties Method used Year Material used Improved traits
Germany 11 Gamma rays (111) 1979 (1), 1981 (5), 1989 (5) Not reported (11) Flower color, early,
flowering and longer post-,
harvest life (11)
Netherlands 24 X-rays (23) and gamma rays (1) 1970 (2), 1971 (1),,
1972 (2), 1973 (1),,
1975 (2), 1977 (6),,
1978 (1), 1979 (4),,
1980 (1), 1983 (2),,
1984 (2)
Rhizomes (7), stolons (1), not reported (16) Flower color (22), plant ,
architecture and flower size (1), early flowering (1)
1The quantity in brackets indicates the number of varieties released.