Revista Mexicana de Ciencias Forestales Vol. 9 (47)

Mayo-Junio (2018)

Fecha de recepción/Reception date: 15 de diciembre de 2017

Fecha de aceptación/Acceptance date: 2 de abril de 2018

_______________________________

1Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco, A.C. Unidad Noreste. México. Correo-e: rafaelurrea80@yahoo.es

Resumen

Los bosques y selvas enfrentan el reto de satisfacer la demanda por recursos de una población en crecimiento, así como la amenaza del rápido cambio climático que exacerba la magnitud y frecuencia de estreses bióticos y abióticos. Para ello, es urgente acelerar el mejoramiento genético de especies forestales. Sin embargo, sus largas etapas juveniles y asincronía floral retrasan peligrosamente este proceso. El presente ensayo explora los adelantos biotecnológicos en inducción floral y su potencial aplicación en especies forestales. Entre los genes identificados y caracterizados que participan en la ruta de señalización de la floración, especial atención se destina al gen FLOWERING LOCUS T, considerado un integrador de rutas de señalización altamente conservado entre las angiospermas, que, al sobre-expresarse por ingeniería genética, es capaz de inducir la floración de forma eficiente. Esta novedosa estrategia biotecnológica se ha utilizado, recientemente, para segregar genes de resistencia a enfermedades, en un menor tiempo, en germoplasma comercial de manzana y ciruela. Permite soslayar barreras naturales que por mucho tiempo han restringido a las especies forestales al mejoramiento por selección, principalmente. Entre sus ventajas está la de poder restringirla al proceso y no al producto, para acelerar las cruzas sexuales sin modificar genéticamente la progenie; se aleja así de la controversia alrededor de la liberación y consumo de organismos genéticamente modificados, y de los costos y trámites obligatorios para los OGM para monitoreo de posibles riesgos. Se proyecta como una tecnología que puede acelerar, significativamente, el mejoramiento de especies forestales.

Palabras clave: Biotecnología forestal, FLOWERING LOCUS T, ingeniería genética vegetal, mejoramiento acelerado de perennes, mejoramiento de árboles, inducción de floración.

Abstract

Forests and tropical forests face the challenge of meeting the demand for resources from a growing population, as well as the threat of rapid climate change that exacerbates the magnitude and frequency of biotic and abiotic stresses. For this, it is urgent to accelerate the genetic improvement of forest species. However, its long juvenile stages and floral asynchrony dangerously delay this process. This essay explores biotechnological advances in floral induction and its potential application in forest species; among the identified and characterized genes involved in the flowering signaling path, special attention is given to the FLOWERING LOCUS T gene, considered an integrator of highly conserved signaling pathways among angiosperms, which, when over-expressed by genetic engineering, it is able to induce flowering efficiently. This innovative biotechnological strategy has recently been used to segregate disease resistance genes, in a shorter time, in commercial apple and plum germplasm. It allows to avoid natural barriers that have long restricted forest species to breeding by selection, mainly. Among the advantages of this strategy is to be able to restrict it to the process and not to the product, to accelerate the sexual crossings without genetically modifying the progeny; it moves away from the controversy surrounding the release and consumption of genetically modified organisms, and the costs and obligatory procedures in GMOs for monitoring possible risks. It is projected as a technology that can significantly accelerate the improvement of forest species.

Key words: Forest biotechnology, FLOWERING LOCUS T, plant genetic engineering, accelerated tree breeding, forest tree breeding, flowering induction.

Population growth and forest resources

The world population is experiencing continuous growth and by 2050 is projected to increase 30 % to add more than 9 000 million people, an increase that translates into a greater demand for natural resources to meet their needs (FAO, 2014). The Food and Agriculture Organization of the United Nations (FAO) estimates that the demand for timber and energy resources for industrial and domestic uses will increase by 40 % by the middle of 2030.

The growth of the demand for forest resources has driven the selective extraction of wood and the deforestation of forests and natural forests. In the first decade of the 21st century it is estimated that 40 million hectares of primary forests were lost worldwide (FAO, 2010).

Climate change and forest resources

Currently, at the same time as the demand for forest resources increases due to a growing population, environmental changes of great magnitude are experienced due to climate change, as a result of the accumulation in the atmosphere of anthropogenic emissions of greenhouse gases (carbon dioxide, nitrous oxide and methane, mainly) since the pre-industrial era. Rapid global warming causes alterations in the intensity and frequency of climatic phenomena such as droughts, torrential rains and floods; these conditions can cause biochemical, molecular, physiological and morphological changes in plants, which depending on the intensity and duration as well as the stage of development of the plant, have significant consequences in their growth, development and reproduction. This limits the expression of their genetic yield potential and affects the geographical distribution of the species by the desynchronization with the climate to which they adapted (Doroszuk et al., 2006; Srinivasa et al., 2016).

Additionally, climate change can exacerbate biotic threats, due to the effects on the biology, physiology and dynamics of populations, as well as the ecological relationships between pathogens with the other biota in their ecosystem (Garrett et al., 2006).

The direct effects (precipitation, temperature), and indirect effects (increase of pests, diseases and fires) of climate change can significantly impact the conservation of biodiversity and, therefore, the provision of goods and services to meet the needs of a population worldwide increase (UN-DESA, 2015), mainly of those plant species with longer biological cycles than the others, as is the case of perennial species.

Loss of biodiversity of forest resources

Climate change causes anomalies in the phenology of perennial species, such as a lower rate of germination of floral and vegetative shoots, a less vigorous growth of the shoots and a lower fixation and filling of the fruits (Ramírez and Kallarackal, 2015).

Illegal logging along with biotic and abiotic threats exacerbated by the effects of climate change pose a threat to the biodiversity of ecosystems by affecting the sizes and structures of populations and diminishing the diversity and genetic richness of their species, which induces to the extinction of the species.

Globally there are already significant impacts on the forest resources associated with this factor, such as the massive death of Pinus edulis Engelm. in 12 000 km2 at south-western United States (Breshears et al., 2005); a reduction of poplar (Populus tremuloides Michx.) in western United States (Rehfeldt et al., 2009), of cedar (Cedrus atlantica (Endl.) Manetti ex Carrière) in Morocco, and of common beech (Fagus sylvatica L.) in south-western Hungary (Mátyás, 2010).

The speed at which this problem reveals itself exceeds the ability of the trees to face it, which propitiates a reduction in their resistance and recovery from extreme weather events, and / or the attack of pests and diseases, which represents a serious risk for the preservation of the genetic diversity of many species (Jump and Peñuelas, 2005).

The different challenges and threats that climate change imposes on forest resources urgently demand accelerating the genetic improvement of forest species with greater yield and tolerance to biotic and abiotic stress conditions. However, perennial species face the same challenge in particular, the extensive period of the juvenile stage before flowering, which in angiosperms is usually between seven years or more (Häggman et al., 2013).

FT gene in the regulation of flowering in angiosperms

Recently, scientific and technological advances in genomics have helped to reveal the biological function of genes present in plants. Its functional characterization is carried out through the deliberate manipulation of the positive or negative expression of one or several of them, for which the sequencing of the genome and the use of model systems is indispensable.

The first sequenced plant genome was that of Arabidopsis thaliana (L.) Heynh. sequenced in the year 2000. This plant is currently the most widely used model system, due to its small size, short life cycle, high production and seed viability, ease of crossing by autogamy, and small genome (<200 megabases) (The Arabidopsis Genome Initiative, 2000).

At present, angiosperms constitute the most diverse group of terrestrial plants, since around 79 % of the 374 000 plant species described correspond to this phylum (Christenhusz and Byng, 2016). They are vascular plants with tissues and organs perfectly differentiated; its most outstanding characteristic and key factor of its evolutionary success is its complex reproductive structure (flower), which gives rise to the production of seeds covered by a fruit.

The model plant Arabidopsis has served enormously for the study of the flowering process, in which the differentiation of the apical meristem to floral meristem is regulated by genetic, epigenetic and environmental factors. Among the main stimuli that control the transition from vegetative to reproductive stage in Arabidopsis are the endogenous stimuli (autonomous pathways, gibberellin, circadian clock, age, sugar levels) and environmental (vernalization, room temperature and photoperiod), organized in complex and hierarchical signaling routes. Both the routes triggered by the internal state of the plant and in response to exogenous factors, converge in flowering integrating genes that activate meristem identity genes, among them the SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1); FLOWERING LOCUS T (FT) and AGAMOUS-LIKE24 (AGL24) (Blümel et al., 2015).

The transition through the different life cycles in plants is regulated transcriptionally and post-transcriptionally by short sequences of non-coding RNAs (miRNA) that affect the expression of key transcription factors. In the case of the transition from juvenile to adult stage, miR156 negatively controls the expression of 11 of the 17 transcription factors SQUAMOSA PROMOTER BINDING-LIKE (SPL), which affects, in turn, the expression of the integrative gene of the flowering FT route (Spanudakis and Jackson, 2014).

In Arabidopsis, the transcription of FT is promoted by the transcription factor CO (CONSTANS), which is governed by the biological clock of the plant when exposed to more than 12 hours of light, during long days (Calviño et al., 2005). The FT gene is highly conserved among angiosperms; it participates in the transition to flowering in neutral plants to the extension of the day as tomato (Lifschitz et al., 2006) and banana (Chaurasia et al.,2017), as well as in plants that require vernalization (Yan et al., 2006), for which it is considered as an integrator of signaling routes.

Once the conditions that activate the transition from the vegetative to the reproductive phase are perceived by the plant, the expression of the FT gene in the vascular tissues of the leaves is triggered. The resulting FT protein (~ 20 KDa), from the family of phosphatidylethanolamine binding proteins (Kardailsky et al., 1999), is transported through the phloem to the apical meristems. It stands out as one of the few examples of macro-molecules in plants that travel great distances to play a role in receptor tissues (Abe et al., 2015; McGarry and Kragler, 2013). Once at the apex of the outbreak, the FT protein interacts with the transcription factor FLOWERING LOCUS D (FD). The FT / FD heterodimer triggers a cascade of positive transcriptional signals that activate several transcription factors of genes such as APETALA1 (AP1), FRUITFULL (FUL), SOC1, and LEAFY (LFY) that lead to the reprogramming of the primordium to produce reproductive organs in instead of vegetative (Abe et al., 2005; Teper and Samach, 2005).

Additionally, FT type proteins have been related as regulatory factors in a large number of development processes including fruit formation, vegetative growth, stomatal control and tuberization (Wickland and Hanzawa, 2015). This diversity of functions has been the result of gene duplication events, followed by sub- or new-functionalization. The evolution of FT proteins has had consequences in the diversification of plants, adaptation and domestication, showing that the molecular plasticity of a single essential gene can direct the evolution of plants and provide key evidence of the mechanisms involved. The duplication of FT sometimes results in the presence of many copies of FT paralogs in a single species, which may have different spatio-temporal expression patterns, as well as different functions (Pin and Nilsson, 2012). Apparently, some FT homologs have acquired the function of suppression of flowering during evolution, antagonizing the function of the FT paralogs that induce it (Blackman et al., 2010).

At present, the FT gene is recognized as a fundamental integrator in the flowering path in angiosperms that responds to endogenous and environmental stimuli (Wigge, 2011). Different orthologs of FT induce flowering in a large number of plants from grasses, legumes, ornamentals to woody perennials.

FT function in perennial species

Perennial species have a life cycle similar to annual plants, such as Arabidopsis, with some modifications that allow them to live for multiple years, including a juvenile stage that is measured in years and not days, and several reproductive cycles as long of his life before dying (polyarctic reproduction); in the case of species from temperate zones, a period of dormancy that allows them to survive under unfavorable conditions (Callahan et al., 2016). Although the growth habits between perennial and annual plants are different, just as there is a great diversity of flowers between the species of one group and another, the similarity in the use of FT as an integrator in the flowering process evidences a very conserved among angiosperms (Klintenäs et al., 2012).

The function of the FT gene, as an integrator of the signaling of flowering routes capable of triggering the transition from the vegetative to the reproductive stage, has been evaluated through genetic engineering strategies in woody stem perennial species that naturally take several years (Table 1).

Table 1. Perennial woody stem species in which the FT gene has been described functionally, through over-expression by genetic engineering.

In these species, overexpression of FT orthologous genes, endogenous or exogenous in nature, have achieved significant reductions of up to less than one year in the juvenile stage. This suggests that the FT gene plays an indispensable role in the manipulation of flowering time, by shortening the juvenile phase, and can be used as a tool for research and improvement of woody perennial species (van Nocker and Gardiner, 2014).

Accelerated biotechnological improvement of trees

The knowledge of the molecular mechanisms that control the flowering and the technology to manipulate them by genetic engineering open the possibility of shortening the necessary time for the crosses in programs of improvement of perennial species. The potential of accelerated improvement via biotechnological induction of flowering has been demonstrated in the development of new varieties of apple (Malus domestica Borkh.) with greater resistance to diseases such as fire blight, or against fungi such as powdery mildew, and scabies, characteristics introduced in commercial germplasm.

The strategy used in M. domestica was to first generate a transgenic cultivar with induced flowering and then pollinate it with wild individuals which had quantitative trait locus, (QTL) specific disease resistance. The seeds obtained from the crosses were screened with molecular markers and crossed with commercial germplasm, always monitored by molecular diagnoses of the presence of the responsible locus for such resistance. In this way it was possible to combine this type of gene in a crop in only three years, when by the traditional method it would have required more than 10 and a much larger seedling population (Flachowsky et al., 2011; Le Roux et al., 2012).

However, the genetic engineering strategy used can have important repercussions on the morphology and physiology of the plant. The use of potent constitutive promoters such as the tobacco mosaic virus (35S) causes the continuous formation of flowers that cannot be supported by the seedling and, consequently, the fall of many of the fruits; the dominance of apical growth can also be affected in favor of a greater development of branches and shrub type growth habit (Flachowsky et al., 2011, Le Roux et al., 2012). In order to avoid these disadvantages, promoters have been incorporated that allow a temporal control in the expression of the gene, such as the heat inducible Gmhsp 17.5-E of soybean. By using this promoter to control the heterologous expression of poplar (Populus trichocarpa Torr. & A. Gray ex Hook.) PtFT1 and PtFT2 gene in apple seedlings, the induction of flowering was achieved in six of seven transgenic lines by submitting the seedlings for 60' at 42°C daily for 28 days (Wenzel et al., 2013).

Although the results clearly demonstrated the efficiency of both FT genes in inducing flowering, M. domestica seedlings subjected to heat treatment showed contrasts in them. The seedlings were in the same stage of development, but the percentage with flowering per line and the number of flowers per plant varied considerably between each transgenic line and between the different transgenic lines. This variation may be due to dissimilarities in the copy number of the transgene and the transgene integration site (position effect) (Wenzel et al., 2013).

Another perennial species of woody stem in which the induction of flowering has allowed to accelerate its genetic improvement has been the plum (Prunus domestica L.). The plum cultivar HoneySweet, highly resistant to Sharka disease caused by the plum pox virus (PPV) (Scorza et al., 2013) was crossed with California prune seedlings in order to segregate in the latter the gene of resistance. To accelerate sexual crosses, the FT1 gene of Populus trichocarpa (PtFT) was over-expressed in plum seedlings (Srinivasan et al., 2012); flowering was obtained in less than a year. The seedlings obtained from these crosses were analyzed using molecular markers for the PPV resistance transgene and the FT bloom induction gene, the positive ones were crossed with California-type prune to secrete the resistance to PPV from HoneySweet.

The use of the plum flowering induction strategy for PtFT over-expression allowed to significantly reduce the time required to segregate the PPV resistance genes (4 to 1 year in each cross) by sexual crossings. Another important advantage of the biotechnological induction of flowering, in addition to the significant reduction of the time necessary in the process of plant genetic improvement, is the possibility of using it in the process and not in the product; that is, to be able to segregate outside, through crossing, the transgene necessary to induce flowering and, thus, not to include it in the product (Callahan et al., 2016).

Examples of stable transformation in apple and plum to over-express the FT gene, could be difficult to replicate in other perennial species due to disadvantages such as low efficiencies of transformation and regeneration (recalcitrant plants), which hinder the functional characterization of genes and biotechnological applications. This is the case of the perennial Kiwi species (Actinidia eriantha Benth.) Where it was not possible to perform the functional characterization of the endogenous FT gene due to the low number of transgenic lines that were obtained (Varkonyi et al., 2013). To overcome the difficulties inherent in perennial species, modern techniques have been proposed, such as the editing of genes with CRISPR / Cas9 (Fan et al., 2015), as well as the use of viral vectors that allow transient transformations bypassing tissue culture (Gleba et al., 2004; Yamagishi et al., 2011).

Biosecurity of the induction of flowering

One of the main advantages in biosecurity issues of the flowering induction strategy via manipulation of FT genes consists in the possibility of the application of genetic engineering in the process, but not in the product. The reduction to less than a year of flowering in perennial species allows to work with seedlings in the greenhouse, crossing them and evaluating them in controlled and isolated environments to contain the possible flow of pollen.

Given the mobile capacity of the stimulus (FT) through the vascular conduits from the leaves to meristems, the strategy of induction of flowering can be applied through the use of grafts (Notaguchi et al., 2008), in which the rootstock is the over-expressor of the FT gene, which guarantees that the fruits and seeds have no modifications in their genome. When stable transformations are used to accelerate the process of sexual crossings, the gene can be segregated outside of plants (Hoenicka et al., 2014). It is also possible to use transient transformations in distant leaves in order to generate the stimulus that will travel to the meristems and produce flowers and seeds free of genetic modifications.

In relation to the induction of flowering by transient over-expression of the FT gene, the use of modified viral vectors has been reported that take advantage of the inherent abilities of the virus to transfer and replicate the genetic material, particularly in those species in which where it is difficult to use recombinant DNA techniques. One example was the use of the Apple Latent Spherical Virus vector (ALSV) to over-express the FT gene of Arabidopsis, in apple seedlings, inoculated by biobalistics in cotyledons after germination (Yamagishi et al., 2011).

The flexibility and biosecurity offered by this strategy promises to bypass natural barriers that for a long time restricted forest species from breeding by selection. In addition to significantly reducing the time needed to improve forest species by sexual crossings, the induction of flowering will make it possible to take advantage of the genetic diversity available among sexually compatible forest species; additionally, the possibility of using biotechnological strategies in the process and not in the product will avoid the costs and delays of the obligatory procedures in genetically modified organisms for the monitoring of possible risks, in which the total cost for the discovery, development and authorization of a new genetically modified crop may exceed USD $100 million (McDougall, 2011).

Perspectives for the forestry sector

At present, more than 30 000 species of plants are covered by the Convention on International Trade in Wildlife Species (CITES, 2017) against over-exploitation due to international trade, with which the producing countries commit themselves in a priority to guarantee its sustainable management. However, in the case of perennial species, the long juvenile stages hinder their reproduction and improvement. For forest species such as mahogany (Swietenia macrophylla King.) and cedar (Cedrela odorata L.), considered the basis of the tropical timber industry in Latin America and included in the appendixes of CITES, the biotechnological induction strategies of the flowering are a possibility to accelerate the improvement of varieties with commercial characteristics that promote commercial reforestation and reduce the pressure on natural forests; this contributes to the use of its diversity and at the same time to its conservation.

The export of roundwood worldwide for 2015 amounted to 121 billion m3 with a value close to $ 15 billion dollars; of this total, the non-coniferous species produced 34 % of the volume and 51 % of the total value (FAO-STAT, 2017). The ability to accelerate the genetic improvement of forest angiosperms through the biotechnological induction of flowering is a disruptive technology that will add value to the forestry sector in a different way, allowing to go beyond the selection improvement that was restricted to forest species due to its long juvenile stages, being able to segregate genes of resistance to biotic and abiotic stress in commercial germplasm.

The flowering induction strategy also has the potential to contribute to the exploitation of the biological diversity of the angiosperm perennial species at a speed never before experienced by the forest sector, with the potential to increase the current production volumes of forest species non-coniferous to meet the needs of timber and energy resources for industrial and domestic uses, increase the flow of foreign currency for export of forest resources, while boosting the economy of rural sectors associated with forest use.

Despite the advances achieved in the functional characterization of the FT gene in a wide range of perennial species, in order to take advantage of the biotechnological strategy of induction of flowering in genetic improvement programs of perennial species, it is necessary to advance in the obtaining of genomic information of these plants as well as in the development and validation of fast, economic and efficient techniques that allow us to avoid the difficulties of the perennial species, among them the low efficiencies of transformation and regeneration.

Acknowledgements

The author expresses his gratitude to Conacyt and Ciatej for the support provided to carry out this research.

Conflict of interest

The author declares no conflict of interest.

Contribution by author

Rafael Urrea López: responsible for the design and execution of the described study and for the preparation and correction of the manuscript.

Referencias

Abe, M., Y. Kobayashi, S. Yamamoto, Y. Daimon, A. Yamaguchi, Y. Ikeda, H Ichinoki, M. Notaguchi, K. Goto and T. Araki. 2005. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309(5737): 1052–1056.

Abe, M., H. Kaya, A. Watanabe T., M. Shibuta, A. Yamaguchi, T. Sakamoto, T. Kurata, I. Ausín, T. Araki and C. Alonso B. 2015. FE, a phloem-specific Myb-related protein, promotes flowering through transcriptional activation of FLOWERING LOCUS T and FLOWERING LOCUS T INTERACTING PROTEIN 1. Plant Journal 83(6): 1059–1068.

Blackman, B. K., J. L. Strasburg, A. R. Raduski, S. D. Michaels and L. H. Rieseberg. 2010. The role of recently derived FT paralogs in sunflower domestication. Current Biology 20(7): 629–635.

Blümel, M., N. Dally, and C. Jung. 2015. Flowering time regulation in crops-what did we learn from Arabidopsis? Current Opinion in Biotechnology 32: 121–129.

Böhlenius, H., T. Huang, L. Charbonnel C., A. M. Brunner, S. Jansson, S. H. Strauss and O. Nilsson. 2006. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312 (5776): 1040–1043.

Breshears, D. D., N. S. Cobb, P. M. Rich, K. P. Price, C. D. Allen, R. G. Balice, W. H. Romme, J. H. Kastens, M. L. Floyd, J. Belnap, J. J. Anderson, O. B. Myers and C. W. Meyer. 2005. Regional vegetation die-off in response to global-change-type drought. Proceedings of the National Academy of Sciences of the United States of America 102(42): 15144–15148.

Callahan, A. M., C. Srinivasan, C. Dardick and R.  Scorza. 2016. Rapid cycle breeding: application of transgenic early flowering for perennial trees. Plant Breeding Reviews 40: 299–334.

Calviño, M., H. Kamada and T. Mizoguchi. 2005. Is the role of the short-day solely to switch off the CONSTANS in Arabidopsis? Plant Biotechnology 22(3): 179–183.

Chaurasia, A. K., H. B. Patil, B. Krishna, V. R. Subramaniam, P. V. Sane and A. P. Sane. 2017. Flowering time in banana (Musa spp.), a day neutral plant, is controlled by at least three FLOWERING LOCUS T homologues. Scientific Reports 7(1): 1–14.

Christenhusz, M. and J. W. Byng. 2016. The number of known plants species in the world and its annual increase. Phytotaxa 261(3): 201–217.

Convención sobre Comercio Internacional de Especies de Flora y Fauna Silvestres (CITES). 2017. Especies CITES. https://cites.org/esp/disc/species.php (1 de octubre de 2017).

Doroszuk, A., M. W. Wojewodzic and J. E. Kammenga. 2006. Rapid adaptive divergence of life-history traits in response to abiotic stress within a natural population of a parthenogenetic nematode. Proceedings of the Royal Society B: Biological Sciences 273(1601): 2611–2618.

Endo, T., T. Shimada, H. Fujii, Y. Kobayashi, T. Araki and M. Omura. 2005. Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliata L. Raf.). Transgenic Research 14(5): 703–712.

Fan, D., T. Liu, C. Li, B. Jiao, S. Li, Y. Hou and K. Luo. 2015. Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Scientific Reports 5: 12217. doi: 10.1038/srep12217.

Food and Agriculture Organization of the United Nations (FAO). 2010. Global Forest Resources Assessment 2010. New York, NY, USA. 340 p.

Food and Agriculture Organization of the United Nations (FAO). 2014. The state of the world´s forest genetic resources. Rome, Italy. 276 p.

Flachowsky, H., P. M. Le Roux, A. Peil, A. Patocchi, K. Richter and M. V. Hanke. 2011. Application of a high-speed breeding technology to apple (Malus x domestica) based on transgenic early flowering plants and marker-assisted selection. New Phytologist. 192: 364–377.

Garrett, K. A., S. P. Dendy, E. E. Frank, M. N. Rouse and S. E. Travers. 2006. Climate change effects on plant disease: genomes to ecosystems. Annual Review of Phytopathology 44(1): 489–509.

Gleba, Y., S. Marillonnet and V. Klimyuk. 2004. Engineering viral expression vectors for plants: The “full virus” and the “deconstructed virus” strategies. Current Opinion in Plant Biology 7(2): 182–188.

Häggman, H., A. Raybould, A. Borem, T. Fox, L. Handley, M. Hertzberg, M. Z. Lu, P. Macdonald, T. Oguchi, G. Pasquali, L. Pearson, G. Peter, H. Quemada, A. Séguin, K. Tattersall, E. Ulian, C. Walter and M. McLean. 2013. Genetically engineered trees for plantation forests: Key considerations for environmental risk assessment. Plant Biotechnology Journal 11(7): 785–798.

Hoenicka, H., D. Lehnhardt, O. Nilsson, D. Hanelt and M. Fladung, 2014. Successful crossings with early flowering transgenic poplar: interspecific crossings, but not transgenesis, promoted aberrant phenotypes in offspring. Plant Biotechnology Journal 12(8): 1066-1074.

Hsu, C. Y., Y. Liu, D S. Luthe and C. Yuceer. 2006. Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. The Plant Cell 18: 1846-1861.

Jump, A. S. and J. Peñuelas. 2005. Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters 8(9): 1010-1020.

Kardailsky, I., V. K. Shukla, J. H. Ahn, N. Dagenais, S. K. Christensen, J. T. Nguyen, J. Chory, M. J. Harrison and D. Weigel. 1999. Activation tagging of the floral inducer FT. Science 286(5446): 1962–1965.

Klintenäs, M., P. a. Pin, R. Benlloch, P. K. Ingvarsson and O. Nilsson. 2012. Analysis of conifer FLOWERING LOCUS T/TERMINAL FLOWER1-like genes provides evidence for dramatic biochemical evolution in the angiosperm FT lineage. New Phytologist 196(4): 1260–1273.

Klocko, A., C. Ma, S. Robertson, E. Esfandiari, O. Nilsson and S. Strauss. 2016. FT overexpression induces precocious flowering and normal reproductive development in Eucalyptus. Plant Biotechnology Journal 14(2): 808–819.

Kotoda, N., H. Hayashi, M. Suzuki, M. Igarashi, Y. Hatsuyama, S. I. Kidou, T. Igasaki, M. Nishiguchi, K. Yano, T. Shimizu, S. Takahashi, H. Iwanami, S. Moriya and K. Abe. 2010. Molecular characterization of FLOWERING LOCUS T-like genes of apple (Malus x domestica Borkh.). Plant and Cell Physiology 51(4): 561–575.

Le Roux, P. M., H. Flachowsky, M. V. Hanke, C. Gesseler and A. Patocchi. 2012. Use of transgenic early flowering approach in apple (Malus x domestica Borkh.) to introgress fire blight resistance from ‘Evereste’. Molecular Breeding 30:857–874.

Lifschitz, E., T. Eviatar, A. Rozman, A. Shalit, A. Goldshmidt, Z. Amsellem, J. P. Álvarez and Y. Eshed. 2006. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proceedings of the National Academy of Sciences 103(16): 6398–6403.

Matsuda, N., K. Ikeda, M. Kurosaka, T. Takashina, K. Isuzugawa, T. Endo and M. Omura. 2009. Early flowering phenotype in transgenic pears (Pyrus communis L.) Expressing the CiFT Gene. Journal of the Japanese Society for Horticultural Science 78(4): 410–416.

Mátyás, C. 2010. Forecasts needed for retreating forests. Nature 464(7293): 1271. doi: 10.1038/4641271a.

McDougall, P. 2011. The cost and time involved in the discovery, development and authorization of a new plant biotechnology derived trait. Consultancy Study for Crop Life. International Midlothian. Midlothian, UK. 24 p.

McGarry, R. C. and F. Kragler. 2013. Phloem-mobile signals affecting flowers: Applications for crop breeding. Trends in Plant Science 18(4): 198–206.

Notaguchi, M., M. Abe, T. Kimura, Y. Daimon, T. Kobayashi, A. Yamaguchi, Y. Tomita, K. Dohi, M. Mori and T. Araki. 2008. Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering. Plant Cell Physiology 49(11): 1645-1658.

Organización de las Naciones Unidas para la Agricultura y la Alimentación – División de Estadística (FAO-STAT). 2017. Producción forestal y comercio. http://www.fao.org/faostat/en/#data/FO (1 de octubre de 2017).

Pin, P. A. and O. Nilsson. 2012. The multifaceted roles of FLOWERING LOCUS T in plant development. Plant, Cell and Environment 35(10): 1742–1755.

Ramírez F. and J. Kallarackal. 2015. Responses of fruit trees to global climate change. Springer Brief in Plant Science. New York, NY, USA. 47 p.

Rehfeldt, G. E., D. E. Ferguson and N. L. Crookston. 2009. Aspen, climate, and sudden decline in western USA. Forest Ecology and Management 258(11): 2353–2364.

Scorza, R., A. Callahan, C. Dardick, M. Ravelonandro, J. Polak, T. Malinowski, I. Zagrai, M. Cambra and I. Kamenova. 2013. Genetic engineering of plum pox virus resistance: HoneySweet plum-from concept to product. Plant Cell, Tissue and Organ Culture 115(1): 1–12.

Spanudakis, E. and S. Jackson. 2014. The role of microRNAs in the control of flowering time. Journal of Experimental Botany 65(2): 365–380.

Srinivasan, C., C. Dardick, A. Callahan and R. Scorza. 2012. Plum (Prunus domestica) trees transformed with poplar FT1 result in altered architecture, dormancy requirement, and continuous flowering. PLoS ONE 7(7): 1–11.

Srinivasa R., N. K., R. H. Laxman and K. S. Shivashankara. 2016. Physiological and Morphological Responses of Horticultural Crops to Abiotic Stresses. In: Srinivasa R., N. K., K. S. Shivashankara and R. H. Laxman (eds.). Abiotic Stress Physiology of Horticultural Crops. New York, NY, USA. pp. 3–18.

Teper B., P. and A. Samach. 2005. The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. The Plant Cell 17(10): 2661–2675.

The Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814): 796–815.

Tränkner, C., S. Lehmann, H. Hoenicka, M. V. Hanke, M. Fladung, D. Lenhardt, F. Dunemann, A. Gau, K. Schlangen, M. Malnoy and H. Flachowsky. 2010. Over-expression of an FT-homologous gene of apple induces early flowering in annual and perennial plants. Planta 232(6): 1309–1324.

United Nations, Department of Economic and Social Affairs, and Population division. (UN-DESA) 2015. World Population Prospects: The 2015 Revision, Key Findings and Advance Tables (No. No. ESA/P/WP.241.). New York, NY, USA. 59 p.

van Nocker, S. and S. E. Gardiner. 2014. Breeding better cultivars, faster: applications of new technologies for the rapid deployment of superior horticultural tree crops. Horticulture Research 1(14022):1-8.

Varkonyi G., E., S. M. A. Moss, C. Voogd, T. Wang, J. Putterill and R. P. Hellens. 2013). Homologs of FT, CEN and FD respond to developmental and environmental signals affecting growth and flowering in the perennial vine kiwifruit. New Phytologist 198(3): 732–746.

Wenzel, S., H. Flachowsky and M.-V. Hanke. 2013. The fast-track breeding approach can be improved by heat-induced expression of the FLOWERING LOCUS T genes from poplar (Populus trichocarpa) in apple (Malus X domestica Borkh.). Plant Cell, Tissue and Organ Culture (PCTOC) 115(2): 127–37.

Wickland, D. and Y. Hanzawa. 2015. The FLOWERING LOCUS T/TERMINAL FLOWER 1 Gene Family: Functional Evolution and Molecular Mechanisms. Molecular Plant 8(7): 983–997.

Wigge, P. A. 2011. FT, a mobile developmental signal in plants. Current Biology 21(9): R374–R378.

Yamagishi, N., S. Sasaki, K. Yamagata, S. Komori, M. Nagase, M. Wada, T. Yamamoto and N. Yoshikawa. 2011. Promotion of flowering and reduction of a generation time in apple seedlings by ectopical expression of the Arabidopsis thaliana FT gene using the Apple Latent Spherical Virus vector. Plant Molecular Biology 75: 193-204.

Yan, L., D. Fu, C. Li, A. Blechl, G. Tranquilli, M. Bonafede, A. Sanchez, M. Valarik, S. Yasuda and J. Dubcovsky. 2006. The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proceedings of the National Academy of Sciences 103(51): 19581–19586.

Zhang, H., D. E. Harry, C. Ma, C. Yuceer, C. Y. Hsu, V. Vikram, O. Shevchenko, E. Etherington and S. H. Strauss. 2010. Precocious flowering in trees: the FLOWERING LOCUS T gene as a research and breeding tool in Populus. Journal of Experimental Botany 61(10): 2549–2560.

All the texts published by Revista Mexicana de Ciencias Forestales–with no exception– are distributed under a Creative Commons License Attribution-NonCommercial 4.0 International (CC BY-NC 4.0), which allows third parties to use the publication as long as the work’s authorship and its first publication in this journal are mentioned.