Fruit trees have a long juvenile phase. For example, the juvenile phase of apple lasts for 6–12 years and is a serious constraint for creating new varieties by breeding based on crossing and selection. In this chapter, we report a novel technology using the apple latent spherical virus (ALSV) vector to accelerate flowering time and life cycle in apple and pear seedlings. Inoculation of apple and pear cotyledons immediately after germination with ALSV-AtFT/MdTFL1 concurrently expressing Arabidopsis FLOWERING LOCUS T (AtFT) gene and suppressing apple TERMINAL FLOWER 1-1 (MdTFL1-1) gene can shorten the period from seeding to flowering to 1.5–3 months after germination and generation times in order to obtain next-generation seeds in 1 year or less. Most next-generation seedlings obtained from ALSV vector–infected plants were free of the virus. We also developed a method for eliminating ALSV vectors from infected apple and pear plants by only high-temperature treatment. A method combining the promotion of flowering in apple and pear by ALSV vector with an ALSV elimination technique is expected to see future application as a new plant breeding technique that can significantly shorten the breeding periods of apple and pear.
- apple latent spherical virus (ALSV) vector
- promotion of flowering
- elimination of ALSV
Woody fruit trees have a long juvenile phase—the period between germination and flowering of plants. In apple and pear, the vegetative growth (juvenile phase) generally lasts for 6–12 years with no flowering and fruiting. After transition from the juvenile phase to the adult phase, the trees flower/fruit every year [1–3].
Several apple varieties have been bred to in order to impart resistance to diseases and insect pests, as well as for quality improvement of the fruit. Breeding of fruit trees is conventionally conducted by crossing and selection [4, 5]. So, it is necessary to cultivate many hybrid seedlings to examine their characteristics for breeding new varieties. For example, “Fuji,” an apple variety that currently has the world’s highest production, was selected from 787 hybrid seedlings obtained by crossing “Kokkou (Ralls Janet)” with “Delicious” apples. This variety flowered and fruited approximately 12 years after seeding . Since apple fruits are produced continuously on the same tree over dozens of years, breeding of a high-quality variety is very important for apple production.
A long juvenile period of apple seedlings is a major barrier to the breeding of new varieties. Moreover, breeding of fruit trees requires large fields for cultivation of seedlings and considerable labor for their management. Technologies for shortening the juvenile phase, including grafting onto dwarfing rootstocks, have been developed; however, despite the use of these technologies, several years are required for flowering/fruition [1, 2].
In recent years, global warming is advancing owing to an increase of greenhouse gas concentrations in the atmosphere. Fruit trees are susceptible to global warming because their important physiological phenomena, such as flowering and dormancy, are dependent on environmental climates. In Japan, the influences of global warming on the production of apples have already begun to appear, with poor coloration of fruit, increased frost injury due to early flowering phase, and damage by harmful insects reported . It is presumed that a further shift of land suitable for cultivation of fruit trees and changes in the distribution of diseases and pests caused by global warming will be accelerated in the future; therefore, it is necessary to implement rapid fruit breeding technologies. The improvement in efficiency of fruit tree breeding, particularly shortening of the juvenile phase, is gaining a great deal of attention.
Many genes involved in plant flowering have been identified in the past 20 years in model plants such as
Proteins belonging to the PEBP family contain the
Viral vector technology is a tool to express or suppress the target gene in the virus-infected plant [24, 25]. Infection of a plant by a plant virus vector integrated with the target gene for expression results in the occurrence of expression of the gene in the infected plant. Conversely, when attempting to suppress the expression of a gene, infection of a plant by a viral vector with a part of the target gene leads to induction of suppression of the target gene in the infected plant by virus-induced gene silencing (VIGS). Viral vectors have the advantage of allowing us to evaluate phenotypes rapidly. Recently, we constructed apple latent spherical virus (ALSV) vectors by adding cloning sites to the ALSV genome. The ALSV vector system can be used for the expression of a foreign gene and VIGS in various plant species [26–38].
In this chapter, we introduce an ALSV vector-based technology for early flowering and shortening of a generation time in the apple and pear. Use of this technology allows apples and pear to complete a generation within 1 year, which reduces a breeding term of fruit trees substantially. Moreover, because the viral vectors can easily be removed from both next-generation seedlings and infected plants, this technology is considered not applicable to regulations of the Conservation and Sustainable Use of Biological Diversity through Regulations on the Use of Living Modified Organisms (Cartagena Protocol).
2. Apple latent spherical virus (ALSV) vectors
ALSV is a spherical virus with a diameter of approximately 25 nm originally isolated from an apple tree and is composed of two RNA genome segments (RNA1 and RNA2) and three types of coat proteins (Vp25, Vp20, and Vp24) [39–41]. The apple is the only natural host of ALSV; however, ALSV has a relatively wide range of hosts, and it can experimentally infect not only herbaceous plants such as
Previously, we used ALSV vectors constructed using pUC18 plasmid. These vectors had to be inoculated to
3. Efficient inoculation method of ALSV vector
Generally, it is difficult to directly inoculate cDNA clones of ALSV vector to apple and pear seedlings because cDNA clone results in a very low infection rate. Therefore, we first inoculated the clones to an experimental plant,
4. Induction of early flowering of apple and pear by ALSV vector infection
We first constructed an ALSV vector expressing
Finally, we constructed an ALSV vector (ALSV-AtFT/MdTFL1) that expresses
It was revealed that infection of apple seedlings by ALSV-AtFT1/MdTFL1 allowed us to shorten one generation (from seeds of the current generation to formation of the next-generation seeds) of apples that usually takes 5–12 years, to a year or less. This new technology is expected to be able to shorten substantially the period for breeding a new variety of apple via crossbreeding. In addition, as conventional breeding of fruit trees requires large fields, the use of this new technology enables completion of one generation in a growth chamber (Figure 3).
We also verified whether the technology of inducing early flowering using ALSV vector was applicable to pear . We inoculated cotyledons of pear seedlings immediately after germination with ALSV-AtFT/MdTFL1 and confirmed that approximately 33% of the infected individuals flowered and showed continuous flowering where they flowered continuously over several months as the apple seedlings did (Figure 4a, b). We also constructed an ALSV vector (ALSV-AtFT/PcTFL1) that simultaneously performs
5. Elimination of ALSV from infected apple and pear trees
We tested 487 seeds obtained using pollens of ALSV-infected apple trees as the pollen parent, as well as 450 seeds from fruits on ALSV-infected apple trees, by ELISA and RT-PCR to test seed transmission. The rates of seed transmission from pollens and ovules were 0.38 and 4.5%, respectively . We also investigated the rate of seed transmission from ovules using qRT-PCR, indicating that approximately 1% seedlings (two individuals out of 192 individuals) were infected with the virus . Examination of 47 next-generation apple seedlings obtained from early-flowered seedlings using ALSV technology (ALSV-AtFT1/MdTFL1) showed that none of them were infected with ALSV vector, indicating that virus-free individuals can be obtained successfully .
Elimination of ALSV vectors from infected plants may allow the use of early flowering plants as breeding materials without genetic modification. We sometimes observed a phenomenon in which ALSV multiplied in inoculated leaves but not move to upper un-inoculated leaves . We incubated ALSV-infected apple and pear seedlings for four weeks in a 37°C chamber, then returned them to a 25°C, and investigated the distribution of ALSV in infected plants. It was revealed that ALSV stopped movement to new tissues after the 37°C treatment, and no ALSV multiplication was observed in new tissues developed at 25°C . We attempted detection of ALSV from the shoot apical meristem tissue of ALSV-infected apple and pear seedlings after incubation at 37°C by
The results indicate that ALSV free tissues could be easily obtained from infected plants that flowered early by ALSV-AtFT1/MdTFL1 infection. Use of virus-free tissues as scions is likely to allow us to grow virus-free plants.
6. Discussion and perspective
The long juvenile phase of fruit trees is a significant barrier for efficient fruit tree breeding [3, 51]. The technology developed in the present study substantially shortens one generation of fruit trees via infection of the trees with an ALSV vector for promotion of flowering in fruit tree breeding. Conveniently, the majority of individuals of the obtained next-generation seedlings were free of ALSV because of low seed transmission rate of ALSV. Our ALSV vector technology, which is different from recombinant DNA technology, induces no mutation on the genome of the infected fruit tree. It is difficult to distinguish between normal plants and the plants after removal of ALSV vector. It is also possible to remove the virus easily by heat treatment from the infected materials, with these fruit trees not distinguishable from normal fruit trees. Therefore, these trees are likely to be used for breeding materials.
Velázquez et al. reported that they constructed a
In recent years, determination of the full genome sequence of fruit trees has advanced, leading to publication of these sequences [53, 54]. This information is expected to accelerate bioinformatics, identification of molecular markers, marker selection, and omics research in fruit trees even more [3, 51, 55–59]. The combination of virus-induced flowering technology described here with information obtained from these research is expected to lead to further optimization of fruit tree breeding in the future.
This study was supported in part by the Science and Technology Research Promotion Program for Agriculture, Forestry, Fisheries and Food Industry and by the Council for Science, Technology and Innovation (CSTI), Cross-Ministerial Strategic Innovation, Promotion Program (SIP), and “Technologies for Creating Next-Generation Agriculture, Forestry and Fisheries.”
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