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Marin-Montes, I.M.;  Rodríguez-Pérez, J.E.;  Robledo-Paz, A.;  Cruz-Torres, E.D.L.;  Peña-Lomelí, A.;  Sahagún-Castellanos, J. Doubled Haploids in Tomato. Encyclopedia. Available online: https://encyclopedia.pub/entry/24307 (accessed on 18 May 2024).
Marin-Montes IM,  Rodríguez-Pérez JE,  Robledo-Paz A,  Cruz-Torres EDL,  Peña-Lomelí A,  Sahagún-Castellanos J. Doubled Haploids in Tomato. Encyclopedia. Available at: https://encyclopedia.pub/entry/24307. Accessed May 18, 2024.
Marin-Montes, Ivan Maryn, Juan Enrique Rodríguez-Pérez, Alejandrina Robledo-Paz, Eulogio De La Cruz-Torres, Aureliano Peña-Lomelí, Jaime Sahagún-Castellanos. "Doubled Haploids in Tomato" Encyclopedia, https://encyclopedia.pub/entry/24307 (accessed May 18, 2024).
Marin-Montes, I.M.,  Rodríguez-Pérez, J.E.,  Robledo-Paz, A.,  Cruz-Torres, E.D.L.,  Peña-Lomelí, A., & Sahagún-Castellanos, J. (2022, June 21). Doubled Haploids in Tomato. In Encyclopedia. https://encyclopedia.pub/entry/24307
Marin-Montes, Ivan Maryn, et al. "Doubled Haploids in Tomato." Encyclopedia. Web. 21 June, 2022.
Doubled Haploids in Tomato
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This entry is adapted from the peer-reviewed paper 10.3390/plants11121595

The generation of new hybrid varieties of tomato (Solanum lycopersicum L.) is the most widely used breeding method for this species and requires at least seven self-fertilization cycles to generate stable parent lines. The development of doubled haploids aims at obtaining completely homozygous lines in a single generation.

doubled haploids anther culture Solanum lycopersicum L.

1. Introduction

Tomato (Solanum lycopersicum L.) is one of the most consumed vegetable species worldwide, which is reflected in its production in 2019 when just over five million hectares were planted, yielding 180,166,329 tons of fruits [1]. This wide diffusion in production areas with the presence of various adverse factors continuously demands improved varieties that provide the possibility of increasing the production and quality of the fruit, with the necessary characteristics to carry out the appropriate agronomic management. This is a constant task within the world seed market in which the plant breeder is obliged to design strategies to reduce the time required to obtain new commercial varieties.
The vegetable seed market is increasingly offering hybrid varieties that allow obtaining better yields and fruit quality by taking advantage of the phenomenon of heterosis and by immediately combining characteristics of both parents. This methodology, in its classic version, requires obtaining pure lines, or populations with high inbreeding, to ensure the stability of the generated genotype [2][3]. The classical breeding of autogamous species, such as tomato, requires the execution of several stages: an initial cross to generate genetic variability, the selection of segregating genotypes to obtain homozygous lines with traits of agronomic interest, the identification of combinations between parent lines with a high expression of heterosis, the evaluation of yield and quality and stability of the hybrids under production conditions and the final release of the improved hybrid variety.
In this process, obtaining lines alone requires at least seven self-fertilization cycles [3][4], which means that the time invested to release a new variety occurs in a period of 11 to 13 years [3]. This makes it necessary to develop alternatives to reduce the time to obtain homozygous genotypes. Currently, two main techniques are used: (a) doubled haploids (DHs) and (b) the fast generation cycle system (FGCS) [3]. Of these options, doubled haploids are the most widely used in different agricultural crops due to their efficiency in obtaining pure lines in crops such as Oryza sativa L. [5][6], Zea mays L. [7][8][9] and Triticum aestivum L. [10][11].
The generation of doubled haploids through androgenesis has not had the expected results in some vegetables of high economic value such as chili pepper (Capsicum spp.) [12], eggplant (Solanum melongena L.) [13], tomato [2][4] and cucurbits [14]. In tomatoes, studies have been carried out to induce haploidy by another culture, although satisfactory results have not been obtained to allow its routine application in breeding programs [4][15]. However, given the possibility of substantially reducing the time to obtain lines by using this technique, it is attractive to continue the search for alternatives that allow for efficiently obtaining DHs in this crop.
Gynogenesis is a viable methodology with promising results in recalcitrant species for the generation of doubled haploids, which uses unpollinated female gametophytes [14][16]. This technique has been successful in loquat (Eriobotrya japonica (Thumb) Lindl.) [17], citrus (Citrus grandis (L.) Osbeck) [18], spinach (Spinacia oleracea L.) [19], cucurbits [14][20], red beet (Beta vulgaris L.) [21] and Gentiana ssp. [22] crops, where it is feasible to apply this technique in breeding.

2. Importance of Doubled Haploids

Doubled haploid (DH) produces homozygous genotypes in a single generation. The idea is to generate a haploid genotype with a single set of n chromosomes; subsequently, through chromosomal duplication, genotypes with 2n chromosomes are generated. These plants have two identical chromosome sets and, consequently, are homozygous at each of their loci [23][24]. To achieve the above, the protocols reported worldwide coincide in the following procedure: (a) induction of haploidy by in vitro culture of anthers [5], ovules [12][13] or in vivo induction [9][25]; (b) duplication of chromosomal material by colchicine [26]; and (c) determination of haploidy level by squash root apices and/or flow cytometry [5][7][17].
The generation of homozygous individuals by haploid doubling has become a useful and efficient tool in the breeding of plants such as maize [27][28], wheat [29][30] and rice [31][32]. The main reasons for using DHs in breeding programs are: (1) obtaining pure lines in a single generation, (2) fixing desirable genotypic combinations, (3) increasing selection efficiency, and (4) reducing sample size for selection. These advantages help reduce the time and cost of breeding, which can represent savings in the order of millions of dollars, even in the case of small breeding programs, by substantially increasing the achievement of outstanding results [23].
Several in vitro tissue culture techniques have been developed in different species of agricultural interest for the generation of doubled haploids for commercial purposes. Of these, androgenesis is the most reported worldwide [23][24]. However, the results of this methodology are varied due to the little or no response of anthers to in vitro culture conditions (recalcitrance). A recalcitrant species is one in which morphogenetic processes such as somatic embryogenesis or organogenesis are not successful, and therefore, it is not possible to regenerate plants even when provided with favorable culture conditions [33]. For this reason, recalcitrance is the main problem for haploidy induction by in vitro anther culture. Among the species of agricultural interest with this problem are some Solanaceae [2] and Cucurbitaceae [14]; therefore, the search for alternatives to induce haploids continues to reduce breeding processes for the development of new commercial varieties.

3. Doubled Haploids in Tomato

Obtaining DHs in tomato has been the subject of research for more than 30 years due to the economic importance of the crop; however, no standardized, efficient and reproducible protocols for generating doubled haploids in this vegetable have been reported in the literature reviewed. Among the factors identified that prevent the achievement of this objective are recalcitrance to in vitro culture [4][15] and polyploidy generated by the fusion of nuclei [34][35]. It is still necessary to define the incubation conditions, the physical and chemical conditions of the medium, the genotype dependency of the in vitro culture, the physiological state of the mother plant, and anther development, which affect the repeatability of protocols to achieve the induction of haploid plants [2][15]. The first published studies on androgenesis in tomato reported that it is possible to obtain haploid callus and maintain it for 7 months, although with the subsequent morphogenetic induction of roots only [36]. Subsequently, it was reported that it is feasible to obtain haploid plants by in vitro culture of anthers of S. pimpinelilfolium L. and S. peruvianum L. [37]. Their success was in choosing the correct developmental stage of the anthers, which is between metaphase I and telophase II of microspore development [38].
Different evaluations of the in vitro culture of tomato anthers led to the conclusion that it is possible to obtain plants by organogenesis (adventitious shoots) and that this would allow accelerating their breeding, although it is still not an efficient way for haploid induction due to the few replicable results [39][40]. The generation of haploids in tomato is not efficient because anthers generate three types of callus (an irregular mass of parenchyma tissue that, despite lacking structure, allows cell differentiation), which was induced by 4.4 g·L−1 of Murashige and Skoog medium, 20 g L−1 sucrose, 1 mg·L−1 2-isopenteniladenina and 2 mg·L−1 indoleacetic acid, where the calli that presented polygonal cells with a large vacuole and faster growth became amorphous and friable macroscopic masses with a rough and granular surface where only 7% of cells were haploid [41]. Similarly, it was shown that from gametophytes and sporophytes it is possible to obtain calli; however, in these the nuclei fuse, leading to polyploidy [42]. Likewise, Corral-Martínez et al. [34] obtained calli by culturing 4- to 5-mm-long anthers of the ms1035 mutant in an induction medium composed of 4.4 g·L−1 of Murashige and Skoog medium, 2.5 g·L−1 phytagel, 20 g·L−1 sucrose, 1 mg·L−1 2-isopentenyladenine and 2 mg·L−1 indoleacetic acid; however, they did not obtain a favorable response, and only one plant was haploid out of the 83 regenerated, which was attributed to the fact that the growth rate of callus of somatic origin is higher compared to those generated from meiocytes.
Based on these advances, further research has been carried out to improve protocols for generating doubled haploids. For example, Moreno et al. [43] determined that in tomato it is possible to culture anthers in vitro with microspores from the tetrad stage to the uninucleate stage by using the regulators 2-isopentenyladenine (1 mg·L−1) and indoleacetic acid (4 mg·L−1); with this, the 2n androgenic plants generated was 97%, although the fusion of the meiocyte nuclei generated the loss of complete homozygosity of the plants obtained. Thus, Niazian et al. [15], using the artificial neural network model for image processing, found that the main factors determining androgenesis and callus induction and regeneration are the genotype and the concentration of 2,4-dichlorophenoxyacetic.
Due to the recalcitrance of tomato, the results achieved in androgenesis so far have not been favorable or replicable; therefore, there is still no reliable and efficient methodology for haploid induction. However, due to the great advantages that DHs represent in breeding, it is necessary to continue searching for successful alternatives for this purpose (Table 1).
Table 1. Reports of androgenesis methodology in Solanum lycopersicum L.
Species Common Name Pathway Ploidy Level Determination Haploid Plants Reference
S. lycopersicum L. Tomato Anther culture Flow cytometry 3 Corral-Martínez et al. [34]
Anther culture Flow cytometry 0 Julião et al. [35]
Anther culture Burn’s technique 0 Sharp et al. [36]
Anther culture Flow cytometry 0 Seguí–Simarro et al. [38]
Anther culture Flow cytometry 0 Seguí–Simarro et al. [41]
Anther culture Flow cytometry 0 Seguí–Simarro et al. [42]
Anther culture Flow cytometry 0 Moreno et al. [43]

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Subjects: Horticulture
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Ivan Maryn Marin-Montes
,
Juan Enrique Rodríguez-Pérez
,
Alejandrina Robledo-Paz
,
Eulogio de la Cruz-Torres
,
Aureliano Peña-Lomelí
,
Jaime Sahagún-Castellanos
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Entry Collection: Environmental Sciences
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Update Date: 23 Jun 2022
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