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Author(s): Aline Fugeray-Scarbel, Laurent Bouffier, Stéphane Lemarié, Leopoldo Sánchez, Ricardo Alia, Chiara Biselli, Joukje Buiteveld, Andrea Carra, Luigi Cattivelli, Arnaud Dowkiw, Luis Fontes, Agostino Fricano, Jean-Marc Gion, Jacqueline Grima-Pettenati, Andreas Helmersson, Francisco Lario, Luis Leal, Sven Mutke, Giuseppe Nervo, Torgny Persson, Laura Rosso, Marinus JM Smulders, Arne Steffenrem, Lorenzo Vietto, Matti Haapanen Title: Prospects for evolution in European tree breeding Year: 2024 Version: Published version Copyright: The Author(s) 2024 Rights: CC BY-NC 4.0 Rights url: http://creativecommons.org/licenses/by-nc/4.0/ Please cite the original version: Fugeray-Scarbel A, Bouffier L, Lemarié S, Sánchez L, Alia R, Biselli C, Buiteveld J, Carra A, Cattivelli L, Dowkiw A, Fontes L, Fricano A, Gion J-M, Grima-Pettenati J, Helmersson A, Lario F, Leal L, Mutke S, Nervo G, Persson T, Rosso L, Smulders MJM, Steffenrem A, Vietto L, Haapanen M (2024). Prospects for evolution in European tree breeding. iForest 17: 45-58. - doi: 10.3832/ifor4544-017 ii F o r e s tF o r e s t Biogeosciences and ForestryBiogeosciences and Forestry Prospects for evolution in European tree breeding Aline Fugeray-Scarbel (1), Laurent Bouffier (2), Stéphane Lemarié (1), Leopoldo Sánchez (3), Ricardo Alia (4), Chiara Biselli (5), Joukje Buiteveld (6), Andrea Carra (7), Luigi Cattivelli (8), Arnaud Dowkiw (9), Luis Fontes (10), Agostino Fricano (8), Jean-Marc Gion (11), Jacqueline Grima-Pettenati (12), Andreas Helmersson (13), Francisco Lario (14), Luis Leal (10), Sven Mutke (4), Giuseppe Nervo (7), Torgny Persson (15), Laura Rosso (7), Marinus JM Smulders (6), Arne Steffenrem (16), Lorenzo Vietto (7), Matti Haapanen (17) Genetically improved forest reproductive materials are now widely accessible in many European countries due to decades of continuous breeding efforts. Tree breeding does not only contribute to higher-value end products but al- lows an increase in the rate of carbon capture and sequestration, helping to mitigate the effects of climate change. The usefulness of breeding programmes depends on (i) the relevance of the set of selected traits and their relative weights (growth, drought tolerance, phenology, etc.); (ii) the explicit manage- ment of targeted and “neutral” diversity; (iii) the genetic gain achieved; and (iv) the efficiency of transferring diversity and gain to the plantation. Several biological factors limit both operational breeding and mass reproduction. To fully realise the potential of tree breeding, the introduction of new technolo- gies and concepts is pivotal for overcoming these constraints. We reviewed several European breeding programmes, examining their current status and factors that are likely to influence tree breeding in the coming decades. The synthesis was based on case studies developed for the European Union-funded B4EST project, which focused on eight economically important tree species with breeding histories and intensities ranging from low-input breeding (stone pine, Douglas-fir and ash) to more complex programmes (eucalyptus, maritime pine, Norway spruce, poplar, and Scots pine). Tree breeding for these species is managed in a variety of ways due to differences in species’ biology, breeding objectives, and economic value. Most programmes are managed by govern- mental institutes with full or partial public support because of the relatively late return on investment. Eucalyptus is the only tree species whose breeding is entirely sponsored and managed by a private company. Several new tech- nologies have emerged for both phenotyping and genotyping. They have the potential to speed up breeding processes and make genetic evaluations more accurate, thereby reducing costs and increasing genetic gains per unit of time. In addition, genotyping has allowed the explicit control of genetic diversity in selected populations with great precision. The continuing advances in tree ge- nomics are expected to revolutionise tree breeding by moving it towards ge- nomic-based selection, a perspective that requires new types of skills that are not always available in the institutions hosting the programmes. We therefore recognise the importance of promoting coordination and collaboration be- tween the many groups involved in breeding. Climate change is expected to bring in new pests and diseases and increase the frequency of extreme weather events such as late frosts and prolonged droughts. Such stresses will © SISEF https://iforest.sisef.org/ 45 iForest 17: 45-58 (1) Univ. Grenoble Alpes, INRAE, CNRS, Grenoble INP, GAEL, 38000 Grenoble (France); (2) INRAE, Univ. Bordeaux, BIOGECO, F-33610 Ces- tas (France); (3) UMR BioForA, INRA, 45160, Ardon (France); (4) Institute of Forest Science - ICIFOR-INIA, CSIC, carretera de La Coruña km 7.5, 28040, Madrid (Spain); (5) Research Centre for Forestry and Wood, Council for Agricultural Research and Economics - CREA-FL, v.le Santa Margherita 80, I-52100 Arezzo (Italy); (6) Wageningen University and Research, Wageningen (The Netherlands); (7) Council for Agricultural Re- search and Economics, Research Centre for Forestry and Wood, str. Frassineto 35, 15033 Casale Monferrato (Italy); (8) Council for Agricultural Research and Economics, Research Centre for Genomics and Bioinformatics, v. San Protaso 302, 29017 Fiorenzuola d’Arda (Italy); (9) INRAE, UMR 0588 BioForA, 2163 avenue de la Pomme de Pin, CS 40001 Ardon, 45075 Orléans Cedex 2 (France); (10) Altri Florestal, 2510-582 Olho Marinho (Portugal); (11) CIRAD UMR AGAP, F-33612 CESTAS Cedex (France); (12) Laboratoire de Recherche en Sciences Végétales, Université Toulouse, CNRS, INP, Castanet-Tolosan (France); (13) The Forestry Research Institute of Sweden - Skogforsk, Ekebo 2250, 26890 Svalöv (Swe- den); (14) TRAGSA, Vivero Maceda, Carretera Maceda - Baldrei, km 2, 32708 Maceda, Galicia (Spain); (15) The Forestry Research Institute of Sweden - Skogforsk, Sävar SE-918 21 (Sweden); (16) Norwegian Institute of Bioeconomy Research - NIBIO, Skolegata 22, 7713 Steinkjer (Nor- way); (17) Natural Resources Institute Finland - Luke, Helsinki (Finland) @@ Matti Haapanen (matti.haapanen@luke.fi) Received: Dec 16, 2023 - Accepted: Feb 27, 2024 Citation: Fugeray-Scarbel A, Bouffier L, Lemarié S, Sánchez L, Alia R, Biselli C, Buiteveld J, Carra A, Cattivelli L, Dowkiw A, Fontes L, Fricano A, Gion J-M, Grima-Pettenati J, Helmersson A, Lario F, Leal L, Mutke S, Nervo G, Persson T, Rosso L, Smulders MJM, Steffenrem A, Vietto L, Haapanen M (2024). Prospects for evolution in European tree breeding. iForest 17: 45-58. – doi: 10.3832/ifor4544-017 [online 2024-03-06] Communicated by: Marco Borghetti Review ArticleReview Article doi: doi: 10.3832/ifor4544-01710.3832/ifor4544-017 vol. 17, pp. 45-58vol. 17, pp. 45-58 http://www.sisef.it/iforest/contents/?id=ifor4544-017 mailto:matti.haapanen@luke.fi Fugeray-Scarbel A et al. - iForest 17: 45-58 cause slow growth and mortality, reducing forest productivity and resilience. Most of these threats are difficult to predict, and the time-consuming nature of conventional breeding does not allow for an adequate and timely reaction. We anticipate that most breeding programmes will need to revise their selec- tion criteria and objectives to place greater emphasis on adaptive perfor- mance, tolerance to multiple environmental stresses, stability in different en- vironments, and conservation of genetic diversity. Testing breeding materials in a variety of environments, including potentially contrasting climates, will become increasingly important. Climate change may also force the incorpora- tion of new genetic resources that provide new useful adaptations, which may involve the use of new, previously unexplored gene pools or hybridisation, with the enormous challenge of incorporating useful alleles without adding along an unfavourable genetic background. Decision-support tools to help landowners and foresters select the best-performing forest reproductive mate- rial in each specific environment could also help reduce the impact of climate change. Keywords: Tree Breeding, Breeding Programmes, Breeding Strategies, Climate Change, Seed Orchards, Genomic Selection Introduction Forests provide a range of ecosystem ser- vices to society, most importantly ensuring the renewable raw materials for a wide range of manufactured products, including pulp, paper, cork, resins, fuel, and con- struction timber, which replace fossil- based carbon products. In addition, forests are efficient carbon sinks that mitigate the effects of climate change (Pan et al. 2011). Between 1990 and 2020, the global forest area decreased by 420 million hectares (FAO 2022). Despite a slight increase in Eu- ropean forest area, the global conversion of forests to agriculture and infrastructure is increasing pressure on production in cul- tivated forests and on the conservation of wild forests. It is expected that plantation forests, which can incorporate the benefits of genetic improvement and conservation, can play an important role in minimising the demand for wild resources. Both Euro- pean forest owners and forest managers agree that one of the strategies to be favoured in the face of climate change is the use of improved Forest Reproductive Material (FRM) in plantations and for the enrichment of natural regeneration zones (Roitsch et al. 2023). Forest tree breeding aims to improve the genetic qualities of FRM to increase the quantity and quality of harvested forest products and make for- ests more resilient to global change. In Eu- rope, breeding programmes have been car- ried out for decades in several economi- cally important tree species, resulting in significant genetic gains (Jansson et al. 2017), even maintaining the genetic vari- ability of improved FRM close to the level of the original natural stands (Muona & Harju 1989, Olsson et al. 2023). Many forest trees have biological charac- teristics such as a long lifespan, late fertil- ity, and difficult sexual or vegetative propa- gation that are not conducive to smooth breeding progress. As a result, tree breed- ing is a slow process compared to crop and livestock breeding, but the gain in each generation can still be relatively high. Tree breeders have already experimented with various tools and technologies to alleviate the major biological constraints in the hope of reducing the cost of breeding activities, increasing the pace of breeding, and in- creasing genetic gains. Some of these, such as flowering promotion by plant hormones or vegetative propagation by top-grafting (De Oliveira Castro et al. 2021), rooted cut- tings, or somatic embryogenesis (Lelu-Wal- ter et al. 2013), have proved to be opera- tionally feasible, while others, such as ge- netic engineering leading to genetically modified plants, have all but disappeared from the discussion. It has now become clear that most technologies require a long period of development before they are ready for large-scale breeding and that their application also depends on the con- text of the breeding programme. For ex- ample, the first DNA markers appeared in the 1980s, but it took decades for them to find their way into mainstream breeding programmes. More recently, advance- ments in high-throughput DNA sequencing and the introduction of Single Nucleotide Polymorphisms (SNPs) have greatly ex- panded the range of potential applications in tree breeding (Isik 2014). This article first presents the current sta- tus of forest tree breeding programmes in Europe through their organisation, the breeding objectives and the strategies con- sidered for selection and deployment of improved FRM. Then a transversal analysis of potential developments that could soon influence the way tree breeding is prac- tised in Europe and worldwide is detailed. The technological innovations examined cover those that reduce breeding costs by facilitating the collection and analysis of large amounts of phenotypic data; and those that take advantage of genomic knowledge and can be used to replace or supplement phenotyping data with infor- mation from SNP markers to improve the accuracy of genetic evaluation and speed up the breeding process. We also examine new challenges for tree breeding in the context of climate change, the potential barriers to the production of different FRM types, the breeding objectives and their fu- ture evolution, and the key players in the current tree breeding efforts taking place in Europe. Our synthesis owes a great deal to the species-specific case studies acquired as part of the “B4EST” H2020 research proj- ect (B4EST 2024), funded by the European Union and involving 21 partners from uni- versities, research organizations, and com- panies. These provide a more in-depth analysis for the breeding of eucalyptus (Leal et al. 2022), maritime pine (Alia et al. 2022, Bouffier 2022), Mediterranean stone pine (Mutke et al. 2022), Norway spruce (Steffenrem & Helmersson 2022), poplar (Biselli et al. 2022a), and Scots pine (Haapa- nen & Persson 2022). Current status of European tree breeding Breeding programmes and their organisation The breeding programmes included in the current analysis are listed in Tab. 1. Most of them were initiated in the second half of the twentieth century. They represent dif- ferent levels of complexity and progress, from basic breeding programmes with a limited number of trials (stone pine and ash) to more advanced ones (eucalyptus, maritime pine, Douglas-fir, Norway spruce, poplar, and Scots pine). The organisation of the tree breeding programmes considered here varies; some are run entirely by for-profit companies, while others are fully linked to the public sector. However, the general trend is that tree breeding in Europe is largely sup- ported by public funds. Maritime pine breeding activities in Spain are publicly funded and run by regional in- stitutions in the regions where maritime pine grows. The French maritime pine breeding programme also relies mainly on public funding. It is managed by two insti- tutions (INRAE, the National Research In- stitute for Agriculture, Food, and Environ- ment, and FCBA, the technological institute 46 iForest 17: 45-58 iF or es t – B io ge os ci en ce s an d Fo re st ry Prospects for evolution in European tree breeding for wood and forest sector) and coordi- nated by a common structure (GIS “Groupe Pin Maritime du Futur”). A similar scheme exists for Douglas-fir in France, involving three main players: INRAE, FCBA, ONF, and also coordinated through a GIS-like board, which is regularly funded by the Ministry. In the Netherlands, Wageningen Research, a non-profit research organisation, is the main actor engaged in ash tree improve- ment, with the Ministry of Agriculture, Na- ture, and Food Quality providing the major- ity of financing. Same in France with IN- RAE, and the Ministry of Agriculture. The Scots pine and Norway spruce breeding programmes in Finland are funded by the government and managed by a public re- search institute (Luke). The Norwegian breeding programmes of these two spe- cies are managed by the non-profit founda- tion Skogfrøverket (Norwegian Forest Seed Center), which is supported by 60 percent public money and 40 percent seed sales revenue. Stone pine breeding in Spain has been the result of isolated initiatives by forest administrations in different autono- mous regions of the country and by the Ministry for Ecological Transition, sup- ported by collaborations with several uni- versities and the national research institute ICIFOR-INIA (CSIC). The two eucalyptus breeding program- mes in Portugal, run by pulp and paper companies Altri and The Navigator Com- pany, are the only examples of private-sec- tor breeding, among the examples cited here. Cases of Norway spruce in Sweden, stone pine in Portugal, and poplar in Italy fall into the middle ground. In Sweden, Skogforsk, which is a private foundation with a mix of public and private support, runs the breeding programmes of Norway spruce and Scots pine and provides im- proved breeding material for private enter- prises that manage seed orchards of these species. In Portugal, the national research institute INIAV oversees stone pine breed- ing and receives funding from associations of large private landowners, whereas re- gional private forest owners’ associations own and manage mother-tree orchards (clonal gardens used to collect scions for grafting). In Italy, poplar breeding projects are independently run by the public organi- sation CREA and private enterprises, with no stable collaboration between the public and private research communities. The profitability of breeding activities heavily influences the mode of organisa- tion (Fugeray-Scarbel et al. 2023). There are many factors that contribute to a gen- erally low rate of return on investment, such as the long time between the start of breeding and the first releases of improved FRM and the resources required (time, money, land, and personnel). The market size (annual regeneration area) for some tree species may be modest. Finally, landowners’ reluctance to pay more for better materials may further discourage private investments in breeding. A larger investment in upstream activities includes the sizable investments made by the forest industry for conifer breeding in Sweden and eucalyptus in Portugal. Mills are sub- stantial investments that require a steady supply of wood in sufficient quantities. Breeding, as well as seed and seedling pro- duction, will increase the supply of raw ma- terials for this purpose, encouraging supe- rior varieties to be planted in both com- pany-owned and privately held forest ar- eas. The operative deployment and produc- tion of improved FRM consist of the estab- lishment, maintenance, and harvesting of seed orchards, as well as the production of seedlings and clonal plants in nurseries. Even in situations where breeding opera- tions receive only public funding, private businesses typically manage these com- mercial activities. More details on the type of FRM deployed for each tree species are reported below. Breeding objectives and selected traits As most forest trees have long commer- cial rotations, breeding objectives are usu- ally rather general to ensure that they are valid in a range of future scenarios, includ- ing those involving changing climate and evolving industrial processes and demands. Most breeding programmes aim to in- crease the quantity and quality of harvest- ed wood, but for a few species, there are other objectives such as resin supply (mar- itime pine in Spain) and cone production (Mediterranean stone pine). The main goal of breeding Scots pine and Norway spruce is to increase wood produc- tion and the economic value of end-prod- ucts (Rosvall 2011, Ruotsalainen & Persson 2013, Jansson et al. 2017, Skogfrøverket 2017). As these species are commonly used for sawn timber, it is important to achieve good stem quality (few knots, straight stems and no defects). For Norway spruce in particular, the economic value of wood is strongly linked to structural uses. In addi- tion to eliminating trees with stem defects, more attention is being paid to eliminating early flushing families that are susceptible to spring frost, as well as to increasing stiff- ness, reducing grain angle, and maintaining wood density (Steffenrem & Helmersson 2022). Eucalyptus breeding goals have been aligned with the demands of pulp and pa- per companies, with trees selected for growth, wood density, and wood cellulose content (Leal et al. 2022). In case of poplar, breeding mainly aims at improving vegeta- tive propagation capacity, growth vigour, stem form, and wood quality (Biselli et al. 2022a). Stone pine, traditionally used for land reclamation and forest restoration, has gained attention for producing highly prized edible pine nut kernels, and there- fore the main objective of breeding is now improved cone and kernel production (Ols- son et al. 2023). With respect to ash, breed- ing was primarily aimed at improving the growth and wood quality features, such as stem straightness, lack of forks, and fine branching (Pâques 2013), but recently the focus has shifted to tolerance to the devas- tating ash dieback disease (Vasaitis & En- derle 2017). Douglas-fir is appreciated mostly for structural timber. First selec- tions across European breeding programs were made with growth and general tree architecture being the most important traits, to obtain important volumes with as little defaults as possible in order to keep its good baseline mechanical properties iForest 17: 45-58 47 Tab. 1 - Main features of the European forest tree breeding programmes reviewed. SYEAR: starting year; GEN: the most advanced generation with selected trees; TOTHA: total accumulated trial area (ha); AVGHA: Average trial area established per year (ha). Tree species Country SYEAR GEN TOTHA AVGHA Maritime pine France 1960 3 400-600 6-10 Spain-Galicia 1998 1 10 1.5 Spain-Central 1990 1 100 3 Stone pine Spain 1989 1 20 <1 Scots pine Finland 1947 2 2250 3 Sweden 1940-1950 3 900 10-12 Norway 1947, 2020 1 10 5 Poplar Italy 1980 2 280-330 8-10 Norway spruce Finland 1947 2 420 8 Sweden 1940-1950 2 800 10 Norway 1947 2 225 8 Eucalyptus Portugal 1964 3 250 2 Ash Netherlands 1960-1970 1 9 0 France 1985 1 45 1 Douglas-fir France 1985 2 200 4 iF or es t – B io ge os ci en ce s an d Fo re st ry Fugeray-Scarbel A et al. - iForest 17: 45-58 (Bastien et al. 2013). Breeding goals have frequently evolved over time. Early in the breeding program- me of maritime pine, plus trees were se- lected for growth and stem straightness. While these traits remain essential selec- tion criteria, wood density, branch quality, and twisting-rust resistance were later added to the list of selection criteria. A sim- ilar trend has occurred in Douglas-fir breed- ing in France, which currently prioritises phenology, architecture, branching pat- terns, and wood density over growth (Bas- tien et al. 2021). In Nordic breeding pro- grammes of Norway spruce and Scots pine, increased adaptive performance and phe- notypic plasticity across environments (Da- nell 1993, Skrøppa & Steffenrem 2021) are now given more attention. Resistance and tolerance to biotic and abiotic stresses are frequently associated with potential breeding goals related to wood production. Resistance to pathogens and pests includes root rot (Heterobasidion spp.) in Norway spruce (Swedjemark & Karlsson 2004, Steffenrem et al. 2016, Chen et al. 2018), Fusarium circinatum and nema- tode in maritime pine (Alia et al. 2022), Phoracantha semipunctata, Gonipterus plat- ensis and fungi from genus Mycosphaerella in eucalyptus (Leal et al. 2022), ash dieback in ash (Muñoz et al. 2016), Phloeomyzus passerinni, Melampsora spp., and Marson- nina brunnea in poplar (Duplessis et al. 2011, Carletti et al. 2016, Gennaro & Giorcelli 2019, Chen et al. 2020). Drought tolerance is a major breeding target in eucalyptus to increase its resil- ience (Leal et al. 2022), but there is grow- ing interest in breeding for this trait in other species such as maritime pine (Papin et al. 2024), poplar (Rosso et al. 2023) and Norway spruce (Hayatgheibi et al. 2021). The lack of practical and effective methods for phenotyping is currently considered as a major bottleneck for the integration of abiotic stress resilience traits in breeding programmes. Breeding strategies Tree breeding customarily starts with the selection of phenotypically superior trees in natural stands as candidates. Following that, breeding advances to (i) the genetic evaluation by means of progeny testing; (ii) the selection of superior candidates for their breeding value; and (iii) the produc- tion of the next-generation recruitment population using the selected candidates as parents. At this stage, the top candi- dates are also deployed as seed orchard parents or in vegetative mass propagation. Beyond these general features, the precise format in which any breeding programme is carried out varies greatly (Pâques 2013). The structuring of breeding materials, for instance, may vary from a single to multiple populations. Such population division could be motivated by the need to cover diversifying breeding goals, for conserva- tion purposes, or the ability to provide un- related parents to production populations (Hallingback et al. 2014). In regions such as northern Europe, where there is a wide range of climatic conditions, breeding ma- terials are organised into smaller subpopu- lations, each of which is bred for a specific climate. Sometimes these subpopulations may have different testing and selection strategies, as in the case of Scots pine breeding in Sweden (Haapanen & Persson 2022). Phenotypic data gathered from progeny tests and pedigree information forms the basis of selection among candidates. Mix- ed-model methodology is now commonly used to produce robust BLUP (Best Linear Unbiased Prediction) calculations that take into account the information from a large number of trials connected through tree relatedness (Bouffier et al. 2016) or accom- modate spatial adjustments of environ- mental heterogeneity (Cappa et al. 2019) for the general improvement of selection accuracy. Sometimes, selection happens at subsequent steps for operational reasons. This is the case of Norway spruce, where preliminary selection for the most promis- ing candidates in the field may come at an age of around 7 years before the genetic testing in the field is finalised at ages higher than 12 (Steffenrem & Helmersson 2022). Considering poplar, selection is also done in multiple stages, with distinct em- phasis placed on different sets of traits at each stage. The candidates selected at each stage are cloned and evaluated more precisely based on data from many geneti- cally identical copies in the subsequent steps (Stanton et al. 2010, Pegard et al. 2020). Vegetative propagation (rooted cut- tings) is also employed for field testing of Norway spruce on multiple sites in Swe- den, Norway, and Finland to improve the accuracy of genetic evaluation (Karlsson & Rosvall 1993, Stejskal et al. 2022) and to get more information about the phenotypic plasticity of candidates (Karlsson et al. 2001, Steffenrem & Helmersson 2022). Breeding programmes use different methods to develop new recruitment pop- ulations depending on their biological and financial constraints. Most programmes rely on bi-parental crosses, but polycrosses (Bouffier et al. 2019) and open pollination, followed by paternity recovery or relation- ship analysis from genomic data can also be used. The time required for trees to reach reproductive maturity as well as un- even cone setting are considered major im- pediments to making fast breeding prog- ress in species like Norway spruce and Scots pine (Haapanen & Persson 2022, Stef- fenrem & Helmersson 2022). In the breeding programmes under con- sideration, the use of DNA markers has been confined to quality control (recogni- tion of the real genotypic identity of trees – Archambeau et al. 2023). Several pilot studies are underway, however, to use DNA markers to enhance selection within a marker assisted selection or genomic selec- tion scheme for some of the species con- sidered here. These are pilot studies be- cause the schemes are implemented on a reduced scale, involving a relatively small part of the whole breeding population and testing networks. Some of the most ad- vanced cases are those in Norway spruce (Chen et al. 2019, 2023), maritime pine (Isik et al. 2016), poplar (Pegard et al. 2020, Bi- selli et al. 2022a) and eucalyptus (Haristoy et al. 2023). In other species, like in ash, on- going research aims at developing DNA markers for species and genotype recogni- tion (Dowkiw A., pers. comm.) and ash die- back resistance (Stocks et al. 2019, Chaud- hary et al. 2020), or in Pinus pinea to test the application of genomic prediction (Ols- son et al. 2023). Deployment of improved FRM The impact of tree breeding is deter- mined by the scale at which improved FRM is used in forest regeneration. Tab. 2 sum- marises the types of FRM used as well as the magnitude of the current deployment by species and countries, showing that ge- netically improved FRM represents a sig- nificant portion of the materials accessible in Europe today. Improved FRM is produced by means of vegetative and sexual propagation. Seed- lings produced from open-pollinated seed orchards are the dominant type of FRM since they are cheaper to produce than vegetatively propagated plants. Nurseries use seed from seed orchards to grow seed- lings, but in some countries, orchard-repro- duced seeds are also directly used for re- generation (for the direct seeding of Scots pine, see Haapanen & Persson 2022). Seed orchards fall into two categories: clonal seed orchards, which consist of grafted propagules of multiple (often more than 20) selected trees, and seedling seed or- chards, which consist of offspring (families) of selected parents. Seedling seed or- chards have been established in Norway spruce, Scots pine, maritime pine, and eu- calyptus. Clonal plants are currently produced by means of rooted shoot cuttings (eucalyp- tus and poplar), rooted cuttings (Norway spruce), grafting (stone pine, Douglas-fir), or somatic tissues multiplied and manipu- lated in vitro (eucalyptus). In eucalyptus, the main limitation of vegetative propaga- tion is the rooting ability, which greatly varies among eucalyptus species and geno- types, with reproduction by means of seed orchards being the only option for propa- gating rooting recalcitrant genotypes (Leal et al. 2022). Production facilities for so- matic embryogenesis plants of Norway spruce are under implementation in Swe- den and Finland. Being generally based on more inten- sively selected material, clonal plants have the potential to be more productive than orchard-reproduced seedlings. The vegeta- tively propagated materials are usually progenies from intra-specific crosses or, as 48 iForest 17: 45-58 iF or es t – B io ge os ci en ce s an d Fo re st ry Prospects for evolution in European tree breeding is the case for poplar (P. deltoides × P. ni- gra), interspecific crosses (Biselli et al. 2022b). Controlled-crossed materials are free of the high quantities of pollen con- tamination that can cause significant ge- netic losses in open-pollinated seed or- chards (Heuchel et al. 2022). As a further advantage, vegetative propagation avoids the delay in the onset of seed production after selection that we experience with seed orchards. The constraints in FRM production are of- ten related to production capacity, and ad- justing them takes some time, especially in the case of conifer seed orchards, which show at least an 8- to 10-year lag from the establishment to the first harvest. Al- though occasional seed shortages could be avoided by increasing production capacity with regular turnover, this involves sub- stantial investment that is rarely compen- sated by moderately priced seed sales. Drivers of evolution in tree breeding Technological progress Phenotyping tools The collection of large quantities of phe- notypic data on an increasing range of traits and environments for genetic evalua- tion is both expensive and time-consum- ing. In addition, the reality and prospects of climate change have also given rise to the need to set up assessments in contrast- ing environments or complete gradients, in order to measure the plasticity and re- silience of FRM, which in turn generates new phenotyping needs. Given the finan- cial constraints of breeding, there is a need for more effective phenotyping methods that can increase the number of trees as- sessed, enabling more intense selection and higher genetic gain. It is difficult to summarise the diverse technological ad- vancements impacting phenotyping, but most of them fall into two categories: (i) robotic vehicles, which are the platforms for automated sensing assessments; (ii) technologies providing faster proxies for traditional assessments. Unmanned aerial vehicles (UAVs) are the most prominent examples of the first cate- gory and are among the most promising pieces of equipment for phenotyping since they may be used for high-resolution aerial photography (3D photogrammetry) or light detection and ranging scanning (Li- DAR). These techniques may be used to as- sess cone and pollen production in seed or- chards or clonal archives. In field trials, they are now replacing telescopic poles or Vertex for measuring tree heights in many situations, particularly after canopy closure in stands taller than 10-12 metres. This ap- proach is now being evaluated in maritime pine and is being evaluated and imple- mented in Norway spruce (Solvin et al. 2020) and Scots pine (Skogfrøverket 2021). In poplar, UAV-based thermal imaging was used to assess genotype variability under drought stress conditions, with promising results (Ludovisi et al. 2017). Currently, an UAV has been used, in conjunction with a UAV-born sawing system, to gather twigs (for grafting), needles (for DNA extrac- tion), and cone samples from Norway spruce and Scots pine trees in Norway (Skogfrøverket 2021). LIDAR has rapidly be- come a way to gather information on tree attributes that are challenging to assess us- ing conventional methods, like stem form, tree crown volume, and leaf area index, al- though the efforts needed for data pro- cessing are still limiting its application in breeding. The use of image-based pheno- typing could have been even more disrup- tive, as reviewed by Bian et al. (2022): it provides a means to precisely quantify complex traits that were only scored rudi- mentarily or even not considered until now. The technological advancements provid- ing faster proxies can be illustrated by two examples revealing the many technical rev- olutions to come: the resistograph tool and the use of Near-InfraRed Spectroscopy (NIRS). The resistograph is a device initially designed for structural assessments on wooden constructions, which can easily re- place in the field the X-ray measurements based on increment cores in most species. It evaluates wood density precisely and quickly, while simultaneously providing in- formation on annual radial growth (Isik & Li 2003, Bouffier et al. 2008, Fundova et al. 2018, Jacquin et al. 2019). Although many other non-destructive evaluation method- ologies for wood properties have been re- viewed by Schimleck et al. (2019), the use of resistograph appears to be the most ap- propriate for quickly evaluating a large number of trees and is now largely used by forest tree breeders. The second example is based on the use of NIRS which is widely used for phenotyping in plants and animals (Alamu et al. 2021, Bresolin & Dórea 2020). NIRS has been applied in forest trees for evaluation of wood lignin properties, wood density, as well as other wood properties such as extractives (Alves et al. 2020, Schimleck et al. 1999, Simões et al. 2022) or even for forecasting the susceptibility of ash to biotic stressors like chalara (Villari et al. 2018). The term “phenomic selection” was coined by Rincent et al. (2018) to de- scribe the use of NIRS as a high-through- put, inexpensive, and non-destructive tech- iForest 17: 45-58 49 Tab. 2 - FRM and their current deployment European countries. Tree species Country Type of FRM Seedling/clonal plants produced per year Share of improved FRM Maritime pine France Seedlings 37M >95% Spain - Galicia Seedlings 20K <5% Spain - Central Seedlings 0.5M <15% Stone pine Spain Clonal plants <1K <1% Portugal Clonal plants >10K <5% Scots pine Finland Seedlings / seeds 40M (seedlings) 96% Sweden Seedlings 236M 98% Norway Seedlings 2M 99% Poplar Italy Clonal plants 140K-180K 10-15% France Clonal plants 900K 40-50% Norway spruce Finland Seedlings 75M 70% Sweden Seedlings 197M 71% Norway Seedlings 50M 95% Ash Netherlands Seedlings < 4K 73% Eucalyptus Portugal Clonal plants / seedlings 16 M 58% Douglas-fir France Seedlings/seeds 12M (seedlings) 100% iF or es t – B io ge os ci en ce s an d Fo re st ry Fugeray-Scarbel A et al. - iForest 17: 45-58 nology to indirectly record endopheno- typic variations and calculate relationship matrices in Populus nigra. This method pro- vides intriguing new insights into charac- terising trees in various environments, en- hancing selection and exploiting greater genetic diversity. Phenomic selection proof-of-concepts must be developed to better assess its potential for breeding in other forest tree species besides poplar. Genotyping tools SNP arrays are generally preferred over genotyping-by-sequencing techniques for high-throughput genotyping in breeding because of their excellent repeatability and simpler raw data processing, but the in- vestments required for their design limit their development. Furthermore, they can be biased towards the specific germplasm used in the SNP discovery step (Barabaschi et al. 2016). However, they have been widely used in plant genetic applications, even for forest trees (Tab. 3). In particular, as a result of the B4EST ini- tiative, a commercial multi-species 4TREE array was designed with 50K SNPs for Pop- ulus sp., Fraxinus sp., Pinus pinaster, and Pi- nus pinea (Archambeau et al. 2023, Guil- baud et al. 2020). Two other arrays were also generated within the same project: one for Scots pine (Kastally et al. 2021) and one for Norway spruce (Bernhardsson et al. 2020). All these genotyping tools must be associated with genotyping platforms that ensure an efficient and robust proto- col for sample collection, DNA extraction, genotyping, and biobank storage, as devel- oped in Nordic countries for Scots pine, for example. Molecular markers are particularly useful for genotypic identification and pedigree correction. This means eliminating labelling and grafting errors, and guaranteeing that the correct genotypes are utilised for con- trolled crossings, clonal archives, and seed orchards. In France, for instance, a low- density SNP array (62 markers – Vidal et al. 2017) was optimised for identity and par- entage analyses in maritime pine. The re- sults showed that about 10% of the grafted plants in clonal archives were affected by pedigree errors. Each new selected tree is now genotyped for identity control before grafting to clonal archives. Furthermore, pedigree corrections enable a more precise BLUP evaluation and higher genetic gains, although the widespread adoption of mol- ecular markers for this purpose is still in its early stages (Vidal et al. 2017, Klápšte et al. 2022). The use of DNA markers to reconstruct pedigrees allows for less costly breeding strategies. One such potential strategy is to replace bi-parental controlled crosses with polymix breeding followed by pedi- gree reconstruction (Isik 2014, Lambeth et al. 2001). The main advantage of this strat- egy is its ability to generate a high number of families with a low number of pollina- tion operations, making it particularly at- tractive for breeding programmes with lim- ited resources to implement conventional breeding schemes. It has been evaluated in the context of the French maritime pine breeding programme (Bouffier et al. 2019) and more recently with attention to the cost of different breeding operations (B4EST deliverable D5.2). Two analogous strategies, known as “Breeding without Breeding” (BwB – El-Kassaby & Lstiburek 2009) and “quasi-field trial” have been suc- cessfully tested in the breeding of Euro- pean larch (Larix decidua – Lstiburek et al. 2020) and Nordmann fir (Abies Nordmanni- ana – Hansen & MacKinney 2010), respec- tively. In these cases, the concept was proven when planted stands were treated as ad-hoc progeny trials using DNA markers to fingerprint and reconstruct the pedigree of a population and candidates for pheno- typic forward selection. The basic concept is to skip the initial steps of plus-tree selec- tion in wild stands and establishment of progeny trials, and instead conduct the ini- tial selections in commercial stands that have been created using bulked seedlots from breeding arboretums, plus-tree selec- tions, or seed orchards. BwB is now being considered in breeding of Scots pine and Norway spruce in Norway, where stands are phenotyped using LiDAR scanning from drones, and a sample of top candidates and randomly selected trees is genotyped to ascertain their pedigree. A genomic rela- tionship matrix is estimated from genetic markers and then used for breeding value prediction (El-Kassaby et al. 2012, Lstiburek et al. 2015, 2017a, 2017b, Steffenrem & Hel- mersson 2022). High-throughput genotyping enables the quantification of genomic relatedness be- tween trees in a continuous and quantita- tive manner. This advancement allows for the substitution of pedigree-based related- ness matrices with their genomic counter- parts in solving mixed model equations used for genetic evaluation, leading to su- perior accuracy of BLUP for breeding val- ues (Hayes et al. 2009), a method referred to as G-BLUP. Considering that many breeding programmes have generations or cohorts of individuals in the pedigree that cannot be genotyped, a hybrid matrix called H-BLUP has been developed (Legar- ra et al. 2014). H-BLUP combines genomic and pedigree relatedness information, of- fering significant benefits in evaluation ac- curacy by integrating maximum genetic in- formation without incurring additional ge- notyping costs. In the near future, both G- BLUP and H-BLUP versions are expected to be widely adopted across various species as straightforward and effective ap- proaches to implementing genomic selec- tion (Scots pine, maritime pine, and Nor- way spruce). Genomic selection stands out as one of the most revolutionary applications of mol- ecular markers in breeding, particularly in perennial species faced with the significant expenses and time delays associated with traditional evaluation methods (Grattapa- glia 2022). Although its routine implemen- tation is not widespread across most spe- cies at present, it is highly plausible that it will emerge as a viable and valuable option 50 iForest 17: 45-58 Tab. 3 - High-throughput genotyping tools available per tree species. Tree species Genotyping tool Markers Reference Scots pine Thermo Fisher Axiom PiSy50k array 50K SNPs Kastally et al. 2021 Norway spruce Thermo Fisher Axiom Pcab50K array 50K SNPs Bernhardsson et al. 2020 Poplar Illumina ISelect Infinium 34K SNPs Geraldes et al. 2013 Infinium 12K SNPs Faivre-Rampant et al. 2016 Thermo Fisher Axiom 4TREE array 12K SNP Guilbaud et al. 2020 Maritime pine Illumina Infinium 12K SNPs Chancerel et al. 2013 Illumina Infinium 9K SNPs Plomion et al. 2016 Thermo Fisher Axiom 4TREE array 12.5K SNPs Guilbaud et al. 2020 Stone pine Thermo Fisher Axiom 4TREE array 5.7K SNPs Olsson et al. 2023 Eucalyptus Thermo Fisher Axiom Euc72K 14.7K SNPs Haristoy et al. 2023 Ash Thermo Fisher Axiom 4TREE array 13.4K SNPs Guilbaud et al. 2020 Douglas-fir Thermo Fisher Axiom PN550607 50K SNPs Howe et al. 2020 iF or es t – B io ge os ci en ce s an d Fo re st ry Prospects for evolution in European tree breeding for numerous forest breeding programmes in the near future. The most promising ap- plications of genomic selection lie in its po- tential for evaluation of costly traits, such as those concerning wood quality or drought tolerance, and for traits that are challenging to assess directly, such as resis- tance to emerging diseases in the context of climate change. Genomic selection has the potential to increase selection inten- sity, minimise phenotyping costs, and in- clude novel traits in breeding. It may also be used for early selection to speed up the breeding cycle, although this appears diffi- cult in many conifers, which reach sexual maturity rather late (Meuwissen et al. 2001, Wong & Bernardo 2008). Data analytics An important issue in long-term tree breeding is the need to maintain high lev- els of genetic variability for future breeding while maximising the short-term response to selection (Archambeau et al. 2023). Such levels of genetic variability over the long term may prove essential in the current context of substantial environmental change to ensure a minimum evolutionary potential in the face of unplanned pres- sures other than those generated by ge- netic gain. Finding the optimal balance of gain and diversity becomes difficult when the pool of selection candidates consists of related individuals from two or more gen- erations, as is usual in all advanced-genera- tion breeding programmes. Effective new tools, for example, based on the theory of genetic contributions and their optimiza- tion over one generation, such as OPSEL (Mullin 2017a) and XDESIGN (Mullin 2017b), have been developed and made available to breeders to carry out what is known as optimum contribution selection (OCS) or to optimise mating regimes. Other recent developments have gone further by pro- posing derivations of OCS with improved long-term performance (Tiret et al. 2021). High-throughput phenotyping, dense ge- notyping, and characterising the diverse experimental environments generate an immense volume of sometimes highly het- erogeneous data. Dealing with such vol- umes and heterogeneity requires novel an- alytical approaches that prioritise integrat- ing different layers of information to ex- tract meaningful signals from noise. Plat- forms like R (R Core Team 2024) have played a crucial role in enabling the devel- opment and accessibility of numerous in- novative and continuously evolving tools, which have undergone testing and im- provement by a rapidly growing user com- munity. Numerous examples exist, al- though not all can be cited here. One note- worthy tool tailored to the needs of for- estry field experiments is breedR (Muñoz 2024) which leverages mixed models and incorporates modules for spatial statistics, interaction between trees, and genomic se- lection (Cappa et al. 2017, Trebissou et al. 2021, Yasuda et al. 2021). The characterization of the environment in field experiments is becoming increas- ingly important in forestry studies. We have moved from a situation where envi- ronmental heterogeneity was absorbed an- alytically in order to work with average yields, to placing the environmental gradi- ent at the centre of genetic evaluation, which is undoubtedly necessary in the con- text of climate change (De la Mata & Zas 2023). The aforementioned spatial statisti- cal analyses, included in breedR, are widely used now in genetic trials to account for stand-level environmental variation (Bela- ber et al. 2019, Cappa & Cantet 2007). The environment is a major explanatory factor when constructing and explaining the plas- tic reaction functions to the changes that the tree undergoes, in what is known as re- action norm. Random regression has been widely used in animal genetics, for exam- ple, in dairy cattle to model the evolution of lactation with age. However, this now classical but promising methodology has been less used in perennial plants, even though these are the organisms that pres- ent the greatest advantages in terms of characterization of the environment given their immobility. Random regression mod- elling has been recently investigated for predicting tree growth norms of reaction over environmental gradients in a pedi- greed population (Marchal et al. 2019). It is now being used in maritime pine breeding to assess genomic norms of reaction over a water balance index gradient using annual growth data obtained from annual rings (Papin et al. 2024). However, despite the promise of these norms of reaction con- struction techniques, there are still many aspects to be clarified regarding their rou- tine use in breeding programs, given that their use represents a real paradigm shift between classical traits and the newer plasticity functions. Tools for vegetative propagation and seed production Mass vegetative propagation techniques greatly facilitate the dissemination of im- proved material through the use of large- scale clonal varieties and the setting up of clonal experiments that can greatly im- prove the accuracy of genetic evaluation. Somatic embryogenesis (SE) has emerged as a viable option in some species (stone pine, Norway spruce, eucalyptus, and Scots pine – see review Lelu-Walter et al. 2013, Egertsdotter 2019). However, to make em- bryogenic plants competitive with seed- lings, the SE operations must be further au- tomated in order to reduce costs. An alter- native is the development of vegetative propagation through cuttings, as it is being considered for maritime pine in Spain for deployment in the most productive areas or for Eucalyptus globulus in Portugal, but the fundamental issue is to develop a proc- ess that overcomes the limitations of poor rooting and high costs. Seed production can be optimised through the development of techniques to accelerate flowering. It is under considera- tion in Scots pine and Norway spruce, as performing controlled crosses on selected individuals is typically the most time-con- suming step of the breeding cycle. Various methods have been tested to promote flowering in these species, but the most promising ones include top-grafting onto sexually mature inter-stocks, gibberellin, heat and light treatments in greenhouses, and various damage-causing treatments applied to grafts (Eriksson et al. 1998, Johnsen et al. 1994). Optimal seed production in orchards faces several difficulties for most forest tree species. The first is the heterogeneous parental contribution and pollen contami- nation from unimproved surrounding stands when seed orchards are managed through open pollination. It can induce heavy losses in the genetic value of the crop (Bouffier et al. 2023). The second is the increasing damage due to biotic and abiotic factors, which contribute to a dras- tically lower seed yield. For example, mar- itime pine seed orchard productivity has plummeted since 2009-2010 (Boivin & Davi 2016), probably due to a combination of seed bug attacks (Leptoglossus occiden- talis) and climatic factors (spring frost, summer drought). Similarly, in Norway spruce seed orchards, cones and seed in- fections cause significant losses in cone harvests (Rosenberg et al. 2012). Various solutions are being examined, including chemical treatments and more intense management for seed production in a con- trolled greenhouse environment with mass pollination. In Norway spruce, the treat- ments proposed include the removal of Prunus species (known to be the primary hosts of cherry-spruce rust) in the proxim- ity of orchards (Kaitera et al. 2021), and the removal of redundant cones (Almqvist & Wennström 2020). In Eucalyptus globulus, evolution of controlled pollination tech- niques has enabled the development of cost-efficient mass controlled pollination programmes to produce improved eucalyp- tus full-sibs (Harbard et al. 1999). In Portu- gal, at Altri Florestal, controlled pollination has been carried out since 1984-1985. Ini- tially, ten thousand flowers were polli- nated, but since 2012, more than half a mil- lion flowers are pollinated every year through a simplified pollination technique where only two visits are needed (one for the controlled pollination and the other to collect the fruits that have been hand polli- nated). Transgenesis and new genomic techniques Transgenic technologies in forest trees have been studied for decades (Van Frank- enhuyzen & Beardmore 2004, Yin et al. 2021), but they have not entered opera- tional breeding. The primary concerns re- volve around the environmental and con- servation risks linked to the spread of the transgene into natural gene pools (Strauss iForest 17: 45-58 51 iF or es t – B io ge os ci en ce s an d Fo re st ry Fugeray-Scarbel A et al. - iForest 17: 45-58 et al. 2015). This dissemination might be more likely to occur within forest tree spe- cies, given the typically minimal genetic dis- tinction between improved tree varieties and wild populations. Transgenic trees are specifically banned in PEFC and FSC certifi- cations. On the other hand, applications of bio- technology to non-food crops such as for- est trees may be seen as more acceptable by the public than applications to food crops. The risk of transgene introduction into wild gene pools can be limited by con- tainment strategies based on modified ex- pression of floral regulatory genes leading to sterility or to the development of flow- ers impaired for the production of pollen or viable seeds (Klocko et al. 2018, Lu et al. 2019). In addition, in particular cultivation practises such as, for instance, poplar short-rotation coppices for energy use, the risk of gene flow is reduced as plants are harvested before reaching the flowering stage. In the last ten years, the introduction of the New Genomic Techniques (NGT), com- prising genome editing and cisgenesis, has opened new possibilities for the genetic improvement of forest trees. These tech- niques allow targeted mutagenesis, or the introduction of genes from sexually com- patible donors to selected genotypes with minimal unwanted (off-target) modifica- tions of the receiving genetic background. Although, NGTs are currently classified as GMOs following a ruling by the European Court of Justice in 2018, the European Com- mission (2023) has come up with a propos- al to treat plants obtained by targeted mu- tagenesis or cisgenesis that could also oc- cur naturally or be produced by conven- tional breeding, similarly to conventional plants. Genome editing has been success- fully applied in poplar for the modification of traits related to wood quality and resis- tance to biotic and abiotic stresses (Min et al. 2022). However, the realisation of “clean” genome editing in trees is still chal- lenging because the molecular compo- nents necessary for mutagenesis cannot be eliminated by crossing as easily as from an- nual crops. Several strategies have been proposed to overcome the problem, but since all of them have drawbacks or display low efficiency, further research on this topic is needed (Goralogia et al. 2021). The pattern of inheritance of traits of economic importance is another explanation for the low interest in these technologies. Most of these traits have a quantitative genetic ba- sis, which means they are regulated by nu- merous genes, each having a minor impact on the trait, whereas genetic engineering methods are mostly suited to traits with relatively simple inheritance (Van Tassel et al. 2021). However, genome editing tech- nologies targeting multiple genes are un- der development (Wang et al. 2018). Fur- thermore, functional genomics studies have led to the characterization of several genes that have a profound impact on use- ful traits, such as drought tolerance (Rosso et al. 2023). A limitation of these studies is that, in most cases, they were confined to the lab and greenhouse, which was par- tially due to legislative constraints in Eu- rope. These constraints, however, may be removed in the near future with the evolu- tion of European legislation. A step in this direction was taken in Italy in summer 2023, when the national Parliament pro- nounced favourably on the possibility of field trials for plants obtained by NGTs. Climate change Climate change is expected to reduce for- est production for most tree species due to drought and the expansion of insects and disease ranges. Trees will also be stressed by the increased occurrence of extreme weather events, such as cold and heat waves, windstorms, and floods (Jactel et al. 2019, Jandl et al. 2019, Subramanian et al. 2019, Albrich et al. 2020). However, in the boreal region, where tree species are mainly constrained by temperature, the ex- pected lengthening of the growing season may increase productivity (Bergh et al. 2010). The increase in growth could be en- hanced by FRM that is optimally adapted to the new conditions. A decision-support tool has been developed to help landown- ers in Sweden and Finland select the most productive FRMs for any site (Berlin et al. 2019). In the temperate and Mediterranean regions, drought stress reduces tree growth and increases mortality, reducing wood production (Rodriguez-Zaccaro & Groover 2019). Central Europe and the southern Nordic regions experienced ex- treme droughts in the early 2000s, when Norway spruce trees, especially those older than 40-50 years, showed poor drought tolerance (Rosner et al. 2014, 2016, Hentschel et al. 2014). More recently, the extremely hot and dry conditions in the summer of 2018 in Central Europe, fol- lowed by bark-beetle attacks, led to major forest diebacks, specifically in Norway spruce plantations in lowlands, a forest cri- sis that is considered a turning point for the forest sector in Germany (Schuldt et al. 2020, Roitsch et al. 2023). Even the growth of young trees was affected by drought, resulting in a significant genotype-by-en- vironment interaction (Hayatgheibi et al. 2021). Douglas-fir has often been cited as a re- placement alternative to other conifer spe- cies that are showing early symptoms of maladaptation in Europe, such as the fore- cited Norway spruce (Vitali et al. 2018, Roitsch et al. 2023). Nevertheless, some au- thors indicate that Douglas-fir is also show- ing symptoms of stress under extreme wa- ter scarcity conditions in some regions of Europe (Vejpustková & Cihák 2019). In eu- calyptus, drought and temperature in- creases are expected to be major causes of productivity decline in Portugal (Leal et al. 2022). In maritime pine and stone pine, drought stress also affects seed productiv- ity, decreasing the yield in seed orchards (Mutke et al. 2007). In southern environ- ments, drought is increasingly a problem for Scots and maritime pine (Navarro-Cer- rillo et al. 2019, Gea-Izquierdo et al. 2019). In poplar, unfavourable changes in wood composition following a drought stress treatment have been reported (Wildhagen et al. 2018). Furthermore, it has been de- monstrated recently that heat and drought stresses aggravate each other in poplar, leading to increased water loss by transpi- ration (Urban et al. 2017). Although the initial eucalyptus plantings in Portugal had essentially no pests, the number of harmful fungi and insects has risen exponentially over time. The pine wood nematode (Bursaphelenchus xylophil- us), now prevalent in Portugal, infects mar- itime pine forests and plantations, causing pine wilt disease and ultimately the mortal- ity of infected trees in a matter of weeks or months. Because there is no phytosanitary management for this pest, the nematode has become a major threat to maritime and radiata pine plantations in Spain and France. For ash, the ash dieback disease, caused by the invasive fungus Hymenoscy- phus fraxineus, is a relatively new disease, first observed in Poland in the 1990s. Since then, the fungus has spread rapidly over al- most the entire natural range of ash in Eu- rope, with a devastating impact on ash for- ests (Semizer-Cuming et al. 2019). New pests and diseases are likely to become new challenges for ash, such as the Emer- ald ash borer (Agrilus planipennis), which will require adapting the current breeding approaches to include more resistance traits. The difficulty of predicting the emer- gence and diffusion of pests is a major con- straint (Gougherty & Davies 2021, Prasanna et al. 2022, Singh et al. 2023). For example, in the case of poplar hybrids, there is a risk of releasing improved clones that might not perform as expected because of in- sufficient resistance. Climate change clearly mandates adjust- ments to conventional approaches to field- based tree breeding. The first is the re- quirement to evaluate breeding materials in a variety of conditions that can be warmer and drier than those prevailing in the current target climate. In maritime pine breeding, for example, some candidates selected in France are already being tested in genetic trials in Spain, and the number of Spanish trial locations is expected to in- crease. However, as maritime pine is pre- dicted to spread to Northern France, sev- eral experiments with genetic material se- lected in the current breeding zone are be- ing conducted in these potential future production areas. The Norway spruce breeding programmes in Sweden, Finland, and Norway use clonally propagated candi- dates, which are evaluated in field experi- ments established in multiple different en- vironments. Such field experiments facili- tate the evaluation of phenotypic plasticity and the stability of the candidates (Karls- 52 iForest 17: 45-58 iF or es t – B io ge os ci en ce s an d Fo re st ry Prospects for evolution in European tree breeding son & Högberg 1998). In poplar, some studies suggest that clones characterised by high productivity are generally less tol- erant to abiotic stresses (Monclus et al. 2006, Attia et al. 2015, Viger et al. 2016). These studies also highlight that the high degree of genetic variability among poplar clones should be further explored by re-as- sessing, in different environments, clones that are already established for their pro- ductivity and are grown in specific areas. In several studies of Norway spruce, it has been shown that adaptive perfor- mance is influenced by the reproductive environment (summarised in Johnsen et al. 2009). Higher temperatures during zygotic embryogenesis and seed maturation (John- sen et al. 2005) modify the phenology of future plants, resulting in progenies that are suited to a longer growth season (Sol- vin & Steffenrem 2019), without known ge- netic selection on the way (Kvaalen & Johnsen 2008). Similar regulation has been found in other conifers, e.g, Scots pine (Dormling & Johnsen 1992), lodgepole pine (Wei et al. 2001), and the Picea glauca × P. engelmannii complex (Webber et al. 2005), as well as in poplar for agamic (cuttings) propagation material (Raj et al. 2011). This plasticity, which is often linked to epige- netic regulation of gene expression, can be utilised to speed up adaptation by moving seed orchards closer to the future climate or changing the temperature during zygot- ic embryogenesis. The second predicted change in breeding activities of all the tree species is the intro- duction of new selection criteria connected to emerging biotic and abiotic stressors. Because breeding cannot respond quickly to environmental changes, it is vital to fore- see which new stresses will be most severe and estimate the new selection criterion thresholds, such as minimum tempera- tures. Breeding programmes must also consider their adaptability to various sce- narios. Some of the novel selection criteria may necessitate considerable investments, such as breeding for nematode tolerance in maritime pine, which has required the construction of a quarantine greenhouse in France. Investments in new traits may limit the resources available for work on exist- ing breeding goals. On the other hand, de- livering plant material with a sufficient level of tolerance to relevant pests, or abiotic stresses will ensure the long-term viability of profitable plantation forestry. For exam- ple, maritime pine silviculture in northwest- ern Iberia has ceased due to pine wood ne- matode predominance, and private spruce silviculture in the Central European low- lands has collapsed following large-scale diebacks. Breeding programmes must seek out new sources of genetic variation to better meet new breeding objectives (Isabel et al. 2019, Biselli et al. 2022b). This might include increasing the size of current breeding populations, establishing new ones, for in- stance, those required for calibrating ge- nomic evaluation. This variation must also be managed in an explicit and objective manner, using genomic information, to en- sure not only long-term genetic gain, but also the adaptive capacity of the system (Tiret et al. 2021). In maritime pine, the in- troduction of new genetic variation from non-local provenances is being examined, because, e.g., the Corsican provenance may be more tolerant to nematodes, but the Spanish, Portuguese, and Moroccan provenances appear to be more drought resilient. In eucalyptus, E. globulus can be crossed with other eucalyptus species that have a higher tolerance to drought and cold, or with a hybrid of E. rudis × E. saligna that is tolerant to the pest Gonipterus plat- ensis. Also, when Populus deltoides and P. nigra were hybridised, new clones (P. ×can- adensis) were produced that were more re- sistant to spring leaf and shoot blight (Gen- naro & Giorcelli 2019). Conclusions Tree breeding and related research initia- tives have demonstrated their ability to provide improvements in long-term wood production and associated services. How- ever, owing to the length of time required for tree development, the expense of ge- netic testing, and issues with FRM manu- facturing capacity, private investment in tree breeding has been limited. New tech- nological opportunities related to genom- ics, phenotyping, and mass propagation help to alleviate these issues by reducing breeding costs, speeding the breeding process, and increasing the accuracy of ge- netic evaluations. They also allow for more accurate monitoring of genetic diversity and conservation for advanced breeding, which can benefit long-term genetic gains. A disruptive effect on forest tree breed- ing cannot be achieved with a single tech- nology but rather requires a combination of technologies. In addition to the desire for new methods, it is crucial to stress the significance of conventional breeding (e.g., field testing, crossing) and associated ac- tivities (in situ and ex situ conservation). Additionally, the large-scale diffusion of im- proved varieties will always be limited by the mass production of FRM. Therefore, in- vestments in novel breeding techniques should be coordinated with those intended to enhance the efficiency of deployment. Evolution in social needs and expecta- tions is likely to influence tree breeding in various ways. Concerns have been ex- pressed that planted stands and intense sil- vicultural practises make forests more vul- nerable to diseases and extreme weather events. For instance, in Portugal, forest fires are commonly associated with the presence of large eucalyptus plantations. Although the issue is controversial (Fernan- des et al. 2019), eucalyptus plantations on new lands have been banned since 2018. Conversely, other factors, such as the in- creasing public awareness of forest trees as carbon sinks and the creation of a car- bon credit market (Van Kooten & Johnston 2016), are likely to raise the profile of man- aged forests and related activities, such as forest tree breeding. Finally, we may ex- pect a rising demand for bioeconomy raw materials, including, e.g., food additives, building materials, and various pulp-de- rived goods (Hurmekoski et al. 2018). The need to respond to both market and envi- ronmental changes will require a re-assess- ment of breeding strategies and, possibly, new tree species or hybrids that are more tolerant to predicted climate change and better suited to delivering new types of end-products. From an organisational point of view, tree breeding is becoming more complex, requiring new knowledge and advanced technologies, for which traditional breed- ers are not necessarily trained. This will de- mand new types of training and compe- tence, as well as changes that promote greater mutualism among breeding par- ties, which is likely to gradually eradicate the traditional paradigm of one tree spe- cies, one breeder. Strengthening collaboration among coun- tries could also be a useful tool for tackling breeding challenges in the context of cli- matic change and ensuring seed supply sta- bility. Special attention must be paid to mi- nor species with high ecological value but low economic importance, which rely on low-input breeding and limited funding. If new diseases and pests emerge due to cli- mate change, these species will be even more vulnerable. European-wide collabora- tion, particularly during the pre-breeding phase, can increase the effectiveness of ge- netic improvement work in minor species by screening a wide range of germplasm for resistance and exchanging the best-per- forming genotypes for further breeding or seed orchard establishment. Declarations This work was supported by the Euro- pean Union’s Horizon 2020 Research and Innovation Programme 813 Project under grant agreement no 773383 (B4EST). References Alamu EO, Nuwamanya E, Cornet D, Meghar K, Adesokan M, Tran T, Belalcazar J, Desfontaines L, Davrieux F (2021). Near-infrared spectrosco- py applications for high-throughput phenotyp- ing for cassava and yam: a review. International Journal of Food Science and Technology 56: 1491-1501. - doi: 10.1111/ijfs.14773 Albrich K, Rammer W, Seidl R (2020). Climate change causes critical transitions and irrevers- ible alterations of mountain forests. Global Change Biology 26: 4013-4027. - doi: 10.1111/gcb. 15118 Alia R, Mutke S, Lario F (2022). Maritime pine. Spain. In: “Breeding guidelines - transversal analysis”. B4EST Project, Deliverable D3.5, Ap- pendix, pp. 39-46. [online] URL: http://b4est. eu/wp-content/uploads/2022/11/D3.5-Breeding- guidelines-transversal-analysis.pdf Almqvist C, Wennström U (2020). Förädlat skog- iForest 17: 45-58 53 iF or es t – B io ge os ci en ce s an d Fo re st ry http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal-analysis.pdf http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal-analysis.pdf http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal-analysis.pdf https://doi.org/10.1111/gcb.15118 https://doi.org/10.1111/gcb.15118 https://doi.org/10.1111/ijfs.14773 Fugeray-Scarbel A et al. - iForest 17: 45-58 sodlingsmaterial 2020-2064 [Improved forest regeneration material 2020-2064]. Arbetsrap- port 1066, Skogforsk, Uppsala, Sweden. pp. 51. Alves A, Simões R, Lousada J, Lima-Brito J, Ro- drigues J (2020). Predicting the lignin H/G ratio of Pinus sylvestris L. wood samples by PLS-R models based on near-infrared spectroscopy. Holzforschung 74 (7): 655-662. - doi: 10.1515/hf- 2019-0186 Archambeau J, Bianchi S, Buiteveld J, Callejas- Díaz M, Cavers S, Hallingbäck H, Kastally C, De Miguel M, Mutke S, Sánchez L, Whittet R, González-Martínez SC, Bastien C (2023). Man- aging forest genetic resources for an uncertain future: findings and perspectives from an inter- national conference. Tree Genetics & Genomes 19 (3): 271. - doi: 10.1007/s11295-023-01603-z Attia Z, Domec JC, Oren R, Way D, Moshelion M (2015). Growth and physiological responses of isohydric and anisohydric poplars to drought. Journal of Experimental Botany 66: 4373-4381. - doi: 10.1093/jxb/erv195 Barabaschi D, Tondelli A, Desiderio F, Volante A, Vaccino P, Valè G, Cattivelli L (2016). Next gen- eration breeding. Plant Science 242: 3-13. - doi: 10.1016/j.plantsci.2015.07.010 Bastien JC, Philippe G, Rousselle Y, Sánchez L, Chaumet M, Girard S (2021). Les variétés améliorées de douglas en France [Improved va- rieties of Douglas-fir in France]. Schweizerische Zeitschrift fur Forstwesen 172 (2): 76-83. [in French] - doi: 10.3188/szf.2021.0076 Bastien JC, Sánchez L, Michaud D (2013). Dou- glas-fir (Pseudotsuga menziesii (Mirb.) Franco). In: “Forest tree breeding in Europe. Current state-of-the-art and perspectives” (Pâques LE ed). Springer, Dordrecht-Heidelberg-New York- London, pp. 325-372. Belaber EC, Gauchat ME, Rodríguez GH, Borralho NM, Cappa EP (2019). Estimation of genetic pa- rameters using spatial analysis of Pinus elliottii Engelm. var. elliottii second-generation prog- eny trials in Argentina. New Forests 50: 605- 627. - doi: 10.1007/s11056-018-9682-0 Bergh J, Nilsson U, Kjartansson B, Karlsson M (2010). Impact of climate change on the pro- ductivity of silver birch, Norway spruce and Scots pine stands in Sweden and economic im- plications for timber production. Ecological Bul- letins 53: 185-195. [online] URL: http://www. jstor.org/stable/41442030 Berlin M, Almqvist C, Haapanen M, Högberg K, Jansson G, Persson T, Ruotsalainen S (2019). Common Scots pine deployment recommenda- tions for Sweden and Finland. Skogforsk Arbet- srapport, Uppsala, Sweden, pp. 1-64. [online] URL: http://www.researchgate.net/publication/ 333079197 Bernhardsson C, Zan Y, Chen Z, Ingvarsson P, Wu H (2020). Development of a highly efficient 50K single nucleotide polymorphism genotyping ar- ray for the large and complex genome of Nor- way spruce (Picea abies L. Karst) by whole ge- nome resequencing and its transferability to other spruce species. Molecular Ecology Re- sources 21 (3): 880-896. - doi: 10.1111/1755-0998. 13292 B4EST (2024). Adaptive Breeding for Better For- ests. Web site. [online] URL: https://b4est.eu Bian L, Zhang H, Ge Y, Cepl J, Stejskal J, El-Kass- aby Y (2022). Closing the gap between pheno- typing and genotyping: review of advanced, im- age-based phenotyping technologies in for- estry. Annals of Forest Science 79: 22. - doi: 10.1186/s13595-022-01143-x Biselli C, Vietto L, Rosso L, Carra A, Cattivelli L, Nervo G, Fricano A (2022a). Poplar. In: “Breed- ing guidelines - transversal analysis”. B4EST Project, Deliverable D3.5, Appendix, pp. 90-107. [online] URL: http://b4est.eu/wp-content/uplo ads/2022/11/D3.5-Breeding-guidelines-transvers al-analysis.pdf Biselli C, Vietto L, Rosso L, Cattivelli L, Nervo G, Fricano A (2022b). Advanced breeding for biot- ic stress resistance in poplar. Plants 11: 2032. - doi: 10.3390/plants11152032 Boivin T, Davi H (2016). Mission d’expertise sur la rarefaction des fructifications du pin maritime dans les Landes de Gascogne [Evaluation of seed production decline in the maritime pine stands of the Landes de Gascogne forest]. Min- istère de l’Agriculture, de l’Agroalimentaire et de la Forêt - INRAE Science & Impacts, Avignon, France, pp. 25. [online] URL: http://hal.science/ hal-01604210 Bouffier L (2022). Maritime pine. In: “Breeding guidelines - transversal analysis”. B4EST Proj- ect, Deliverable D5.3, Appendix, pp. 47-57. [on- line] URL: http://b4est.eu/wp-content/uploads/ 2022/11/D3.5-Breeding-guidelines-transversal-an alysis.pdf Bouffier L, Charlot C, Raffin A, Rozenberg P, Kre- mer A (2008). Can wood density be efficiently selected at early stage in maritime pine (Pinus pinaster Ait.)? Annals of Forest Science 65 (1): 106. - doi: 10.1051/forest:2007078 Bouffier L, Debille S, Alazard P, Raffin A, Pas- tuszka P, Trontin JF (2023). Pollen contamina- tion and mating structure in maritime pine (Pi- nus pinaster Ait.) clonal seed orchards revealed by SNP markers. Peer Community Journal 3: e68. - doi: 10.1101/2022.09.27.509769 Bouffier L, Klápšte J, Suontama M, Dungey HS, Mullin TJ (2019). Evaluation of forest tree breeding strategies based on partial pedigree reconstruction through simulations: Pinus pin- aster and Eucalyptus nitens as case studies. Can- adian Journal of Forest Research 49 (12): 1504- 1515. - doi: 10.1139/cjfr-2019-0145 Bouffier L, Raffin A, Dutkowski G (2016). Using pedigree and trait relationships to increase gain in the French maritime pine breeding pro- gram. In: IUFRO Conference “Forest Genetics for Productivity”. Rotorua (New-Zealand) 14-18 March 2016, poster, p. 1. [online] URL: http:// hal.science/hal-02801580v1 Bresolin T, Dórea JRR (2020). Infrared spectrom- etry as a high-throughput phenotyping technol- ogy to predict complex traits in livestock sys- tems. Frontiers in Genetics 11: 700. - doi: 10.338 9/fgene.2020.00923 Cappa EP, Cantet RJC (2007). Bayesian estima- tion of a surface to account for a spatial trend using penalized splines in an individual-tree mixed model. Canadian Journal of Forest Re- search 37: 2677-2688. - doi: 10.1139/X07-116 Cappa EP, El-Kassaby YA, Muñoz F, Garcia MN, Villalba PV, Klápšte J, Marcucci Poltri SN (2017). Improving accuracy of breeding values by in- corporating genomic information in spatial- competition mixed models. Molecular Breeding 37 (10): 743. - doi: 10.1007/s11032-017-0725-6 Cappa EP, Muñoz F, Sánchez L (2019). Perfor- mance of alternative spatial models in empirical Douglas-fir and simulated datasets. Annals of Forest Science 76 (2): 716. - doi: 10.1007/s13595- 019-0836-9 Carletti G, Carra A, Allegro G, Vietto L, Desiderio F, Bagnaresi P, Gianinetti A, Cattivelli L, Valè G, Nervo G (2016). QTLs for woolly poplar aphid (Phloeomyzus passerinii L.) resistance detected in an inter-specific Populus deltoides x P. nigra mapping population. PLoS One 11: e0152569. - doi: 10.1371/journal.pone.0152569 Chancerel E, Lamy J-B, Lesur I, Noirot C, Klopp C, Ehrenmann F, Boury C, Le Provost G, Label P, Lalanne C, Léger V, Salin F, Gion J-M, Plomion C (2013). High-density linkage mapping in a pine tree reveals a genomic region associated with inbreeding depression and provides clues to the extent and distribution of meiotic recombi- nation. BMC Biology 11 (1): 40. - doi: 10.1186/17 41-7007-11-50 Chaudhary R, Rönneburg T, Aslund S, Lundén K, Durling MB, Ihrmark K, Menkis A, Stener L-G, Elfstrand M, Cleary M, Stenlid J (2020). Marker- trait associations for tolerance to ash dieback in common ash (Fraxinus excelsior L.). Forests 11: 1083. - doi: 10.3390/f11101083 Chen Z-Q, Baison J, Pan J, Westin J, Gil MRG, Wu HX (2019). Increased prediction ability in Nor- way spruce trials using a marker x environment interaction and non-additive genomic selection model. Journal of Heredity 110 (7): 830-843. - doi: 10.1093/jhered/esz061 Chen Z-Q, Lunden K, Karlsson B, Vos I, Olson A, Lundqvist SO, Stenlid J, Wu HX, Gil MRG, Elfs- trand M (2018). Early selection for resistance to Heterobasidion parviporum in Norway spruce is not likely to adversely affect growth and wood quality traits in late-age performance. Euro- pean Journal of Forest Research 137 (4): 517- 525. - doi: 10.1007/s10342-018-1120-5 Chen S, Zhang Y, Zhao Y, Xu W, Li Y, Xie J, Zhang D (2020). Key genes and genetic interactions of plant-pathogen functional modules in poplar in- fected by Marsonnina brunnea. IS-MPMI 33 (8): 1080-1090. - doi: 10.1094/MPMI-11-19-0325-R Chen Z-Q, Klingberg A, Hallingbäck HR, Wu HX (2023). Preselection of QTL markers enhances accuracy of genomic selection in Norway spruce. BMC Genomics 24: 147. - doi: 10.1186/ s12864-023-09250-3 Danell O (1993). Breeding programmes in Swe- den. In: Proceedings of the “Nordic Group of Tree Breeding” (Lee SJ ed), supplementary vol- ume. Forestry Commission, Edinburgh, Scot- land, UK, pp. 5. De la Mata R, Zas R (2023). Plasticity in growth is genetically variable and highly conserved across spatial scales in a Mediterranean pine. New Phytologist 240 (2): 542-554. - doi: 10.1111/ nph.19158 De Oliveira Castro CA, Dos Santos GA, Takahashi EK, Pires Nunes AC, Souza GA, De Resende MDV (2021). Accelerating Eucalyptus breeding strategies through top grafting applied to young seedlings. Industrial Crops and Products 171: 113906. - doi: 10.1016/j.indcrop.2021.113906 Dormling I, Johnsen O (1992). Effects of the par- ental environment on full-sib families of Pinus sylvestris. Canadian Journal of Forest Research 22 (1): 88-100. - doi: 10.1139/x92-01 54 iForest 17: 45-58 iF or es t – B io ge os ci en ce s an d Fo re st ry https://doi.org/10.1139/x92-01 https://doi.org/10.1016/j.indcrop.2021.113906 https://doi.org/10.1111/nph.19158 https://doi.org/10.1111/nph.19158 https://doi.org/10.1186/s12864-023-09250-3 https://doi.org/10.1186/s12864-023-09250-3 https://doi.org/10.1094/MPMI-11-19-0325-R https://doi.org/10.1007/s10342-018-1120-5 https://doi.org/10.1093/jhered/esz061 https://doi.org/10.3390/f11101083 https://doi.org/10.1186/1741-7007-11-50 https://doi.org/10.1186/1741-7007-11-50 https://doi.org/10.1371/journal.pone.0152569 https://doi.org/10.1007/s13595-019-0836-9 https://doi.org/10.1007/s13595-019-0836-9 https://doi.org/10.1007/s11032-017-0725-6 https://doi.org/10.1139/X07-116 https://doi.org/10.3389/fgene.2020.00923 https://doi.org/10.3389/fgene.2020.00923 http://hal.science/hal-02801580v1 http://hal.science/hal-02801580v1 https://doi.org/10.1139/cjfr-2019-0145 https://doi.org/10.1101/2022.09.27.509769 https://doi.org/10.1051/forest:2007078 http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal-analysis.pdf http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal-analysis.pdf http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal-analysis.pdf https://doi.org/10.3390/plants11152032 http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal-analysis.pdf http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal-analysis.pdf http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal-analysis.pdf https://doi.org/10.1186/s13595-022-01143-x https://b4est.eu/ https://doi.org/10.1111/1755-0998.13292 https://doi.org/10.1111/1755-0998.13292 http://www.researchgate.net/publication/333079197 http://www.researchgate.net/publication/333079197 http://www.jstor.org/stable/41442030 http://www.jstor.org/stable/41442030 https://doi.org/10.1007/s11056-018-9682-0 https://doi.org/10.3188/szf.2021.0076 https://doi.org/10.1016/j.plantsci.2015.07.010 https://doi.org/10.1093/jxb/erv195 https://doi.org/10.1007/s11295-023-01603-z https://doi.org/10.1515/hf-2019-0186 https://doi.org/10.1515/hf-2019-0186 http://hal.science/hal-01604210 http://hal.science/hal-01604210 Prospects for evolution in European tree breeding Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Am- selem J, Cantarel BL, Chiu R, Coutinho PM, Feau N, Field M, Frey P, Gelhaye E, Goldberg J, Grab- herr MG, Kodira CD, Kohler A, Kues U, Lindquist EA, Lucas SM, Mago R, Mauceli E, Morin E, Mu- rat C, Pangilinan JL, Park R, Pearson M, Ques- neville H, Rouhier N, Sakthikumar S, Salamov AA, Schmutz J, Selles B, Shapiro H, Tanguay P, Tuskan GA, Henrissat B, Van De Peer Y, Rouze P, Ellis JG, Dodds PN, Schein JE, Zhong S, Hamelin RC, Grigoriev IV, Szabo LJ, Martin F (2011). Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proceed- ings of the National Academy of Sciences USA 108 (22): 9166-9171. - doi: 10.1073/pnas.1019315 108 Egertsdotter U (2019). Plant physiological and genetical aspects of the somatic embryogene- sis process in conifers. Scandinavian Journal of Forest Research 34 (5): 360-369. - doi: 10.1080/ 02827581.2018.1441433 El-Kassaby YA, Klapste J, Guy RD (2012). Breed- ing without breeding: selection using the ge- nomic best linear unbiased predictor method (GBLUP). New Forests 43 (5-6): 631-637. - doi: 10.1007/s11056-012-9338-4 El-Kassaby YA, Lstiburek M (2009). Breeding without breeding. Genetics Research 91 (2): 111- 120. - doi: 10.1017/S001667230900007X Eriksson U, Jansson G, Almqvist C (1998). Seed and pollen production after stem injections of gibberellin A(4/7) in field-grown seed orchards of Pinus sylvestris. Canadian Journal of Forest Research 28 (3): 340-346. - doi: 10.1139/x97-219 European Commission (2023). Proposal for a reg- ulation of the European Parliament and of the Council on plants obtained by certain new ge- nomic techniques and their food and feed, and amending Regulation (EU) 2017/625. COM/ 2023/411 final. [online] URL: http://eur-lex.eu ropa.eu/legal-content/EN/TXT/?uri=CELEX:52023 PC0411 Faivre-Rampant P, Zaina G, Jorge V, Giacomello S, Segura V, Scalabrin S, Guérin V, De Paoli E, Aluome C, Viger M, Cattonaro F, Payne A, PaulStephenRaj P, Le Paslier MC, Berard A, All- wright MR, Villar M, Taylor G, Bastien C, Mor- gante M (2016). New resources for genetic studies in Populus nigra: genome-wide SNP dis- covery and development of a 12k Infinium ar- ray. Molecular Ecology Resources 16 (4): 1023- 1036. - doi: 10.1111/1755-0998.12513 FAO (2022). Global forest resources assessment 2020: main report. FAO, Rome, Italy, pp. 184. - doi: 10.4060/ca9825en Fernandes P, Guiomar N, Rossa C (2019). Analy- sing eucalypt expansion in Portugal as a fire- regime modifier. Science of The Total Environ- ment 666 (20): 79-88. - doi: 10.1016/j.scitotenv. 2019.02.237 Fugeray-Scarbel A, Irz X, Lemarié S (2023). Inno- vation in forest tree genetics: a comparative economic analysis in the European context. Forest Policy and Economics 155: 103030. - doi: 10.1016/j.forpol.2023.103030 Fundova I, Funda T, Wu H (2018). Non-destruc- tive wood density assessment of Scots pine (Pi- nus sylvestris L.) using Resistograph and Pilo- dyn. PLoS One 13 (9): e0204518. - doi: 10.1371/ journal.pone.0204518 Gea-Izquierdo G, Férriz M, García-Garrido S, Aguín O, Elvira-Recuenco M, Hernandez-Escrib- ano L, Martin-Benito D, Raposo T (2019). Syner- gistic abiotic and biotic stressors explain wide- spread decline of Pinus pinaster in a mixed for- est. Science of the Total Environment 685: 963- 975. - doi: 10.1016/j.scitotenv.2019.05.378 Gennaro M, Giorcelli A (2019). The biotic adversi- ties of poplar in Italy: a reasoned analysis of factors determining the current state and fu- ture perspectives. Annals of Silvicultural Re- search 43: 41-51. - doi: 10.12899/asr-1817 Geraldes A, DiFazio SP, Slavov GT, Ranjan P, Mu- chero W, Hannemann J, Gunter LE, Wymore AM, Grassa C, Farzaneh N, Porth I, McKown AD, Skyba O, Li E, Fujita M, Klápšte J, Martin J, Schackwitz W, Pennacchio C, Rokhsar D, Fried- mann MC, Wasteneys GO, Guy RD, El-Kassaby YA, Mansfield SD, Cronk QCB, Ehlting J, Dou- glas CJ, Tuskan GA (2013). A 34K SNP genotyp- ing array for Populus trichocarpa: design, appli- cation to the study of natural populations and transferability to other Populus species. Molec- ular Ecology Resources 13 (2): 306-323. - doi: 10.1111/1755-0998.12056 Goralogia GS, Redick TP, Strauss SH (2021). Gene editing in tree and clonal crops: progress and challenges. In Vitro Cellular and Developmental Biology-Plant 57: 683-699. - doi: 10.1007/s11627- 021-10197-x Gougherty AV, Davies TJ (2021). Towards a phylo- genetic ecology of plant pests and pathogens. Philosophical Transactions of the Royal Society B: Biological Sciences 376 (1837): 20200359. - doi: 10.1098/rstb.2020.0359 Grattapaglia D (2022). Twelve years into ge- nomic selection in forest trees: climbing the slope of enlightenment of marker assisted tree breeding. Forests 13 (10): 1554. - doi: 10.3390/f13 101554 Guilbaud R, Biselli C, Buiteveld J, Cattivelli L, Co- pini P, Dowkiw A, Esselink D, Fricano A, Guerin V, Jirge V, Kelly LJ, Kodde L, Metheringham CL, Pinosio S, Rogier O, Segura Spanu V I, Buggs RJA, González-Martínez SC, Nervo G, Smulders MJM, Sánchez Rodríguez L, Vendramin GG, Fauvre Rampant P (2020). Development of a new tool (4TREE) for adapted genome selec- tion in European tree species. In: Proceedings of the International Conference “Genetics to the Rescue: Managing Forests Sustainably in a Changing World”. Avignon (France) 27-31 Jan 2020. [online] URL: http://colloque.inrae.fr/conf gentree2020/content/download/4428/57324/ve rsion/1/file/PosterGuilbaud.pdf Haapanen M, Persson T (2022). Scots pine. In: “Breeding guidelines - transversal analysis”. B4EST Project, Deliverable D3.5, Appendix, pp. 108-119. [online] URL: http://b4est.eu/wp-cont ent/uploads/2022/11/D3.5-Breeding-guidelines- transversal Hallingback HR, Sánchez L, Wu HX (2014). Single versus subdivided population strategies in breeding against an adverse genetic correla- tion. Tree Genetics and Genomes 10: 605-617. - doi: 10.1007/s11295-014-0707-3 Hansen O, MacKinney L (2010). Establishment of a quasi-field trial in Abies nordmanniana - Test of a new approach to forest tree breeding. Tree Genetics and Genomes 6: 345-355. - doi: 10.1007/s11295-009-0253-6 Harbard JL, Griffin AR, Espejo J (1999). Mass con- trolled pollination of Eucalyptus globulus: a practical reality. Canadian Journal of Forest Re- search 29 (10): 1457-1463. - doi: 10.1139/x99-129 Haristoy G, Bouffier L, Fontes L, Leal L, Paiva J, Pina J-P, Gion J-M (2023). Genomic prediction in a multi-generation Eucalyptus globulus breed- ing population. Tree Genetics and Genomes 19, 8. - doi: 10.1007/s11295-022-01579-2 Hayatgheibi H, Haapanen M, Lundstromer J, Ber- lin M, Kärkkäinen K, Helmersson A (2021). The impact of drought stress on the height growth of young Norway spruce full-sib and half-sib clonal trials in Sweden and Finland. Forests 12 (4): 498. - doi: 10.3390/f12040498 Hayes BJ, Visscher M, Goddard E (2009). In- creased accuracy of artificial selection by using the realized relationship matrix. Genetics Re- search 91 (1): 47-60. - doi: 10.1017/S00166723080 09981 Hentschel R, Rosner S, Kayler ZE, Andreassen K, Borja I, Solberg S, Tveito OE, Priesack E, Gessler A (2014). Norway spruce physiological and anatomical predisposition to dieback. Forest Ecology and Management 322: 27-36. - doi: 10.1016/j.foreco.2014.03.007 Heuchel A, Hall D, Zhao W, Gao J, Wennström U, Wang X (2022). Genetic diversity and back- ground pollen contamination in Norway spruce and Scots pine seed orchard crops. Forestry Re- search 2: 8. - doi: 10.48130/FR-2022-0008 Howe GT, Jayawickrama K, Kolpak SE, Kling J, Trappe M, Hipkins V, Ye T, Guida S, Cronn R, Cushman S, McEvoy S (2020). An axiom SNP ge- notyping array for Douglas-fir. BMC Genomics 21: 9. - doi: 10.1186/s12864-019-6383-9 Hurmekoski E, Jonsson R, Korhonen J, Jänis J, Mäkinen M, Leskinen P, Hetemäki L (2018). Di- versification of the forest industries: role of new wood-based products. Canadian Journal of Forest Research 48 (12): 1417-1432. - doi: 10.1139/cjfr-2018-0116 Isabel N, Holliday JA, Aitken SN (2019). Forest genomics: advancing climate adaptation, forest health, productivity, and conservation. Evolu- tionary Applications 13: 3-10. - doi: 10.1111/eva.12 902 Isik F, Li B (2003). Rapid assessment of wood density of live trees using IML Resi for selection in tree improvement programs. Canadian Jour- nal of Forest Research 33: 2426-2435. - doi: 10.1139/X03-176 Isik F (2014). Genomic selection in forest tree breeding: the concept and an outlook to the fu- ture. New Forests 45 (3): 379-401. - doi: 10.1007/ s11056-014-9422-z Isik F, Bartholomé J, Farjat A, Chancerel E, Raffin A, Sanchez L, Plamion C, Bouffier L (2016). Ge- nomic selection in maritime pine. Plant Science 242: 108-119. - doi: 10.1016/j.plantsci.2015.08.006 Jacquin P, Mothe F, Longuetaud F, Billard A, Ker- friden B, Leban JM (2019). CarDen: a software for fast measurement of wood density on in- crement cores by CT scanning. Computers and Electronics in Agriculture 156 (5): 606-617. - doi: 10.1016/j.compag.2018.12.008 Jactel H, Koricheva J, Castagneyrol B (2019). Re- sponses of forest insect pests to climate change: not so simple. Current Opinion in In- sect Science 35: 103-108. - doi: 10.1016/j.cois.20 19.07.010 iForest 17: 45-58 55 iF or es t – B io ge os ci en ce s an d Fo re st ry https://doi.org/10.1016/j.cois.2019.07.010 https://doi.org/10.1016/j.cois.2019.07.010 https://doi.org/10.1016/j.compag.2018.12.008 https://doi.org/10.1016/j.plantsci.2015.08.006 https://doi.org/10.1007/s11056-014-9422-z https://doi.org/10.1007/s11056-014-9422-z https://doi.org/10.1139/X03-176 https://doi.org/10.1111/eva.12902 https://doi.org/10.1111/eva.12902 https://doi.org/10.1139/cjfr-2018-0116 https://doi.org/10.1186/s12864-019-6383-9 https://doi.org/10.48130/FR-2022-0008 https://doi.org/10.1016/j.foreco.2014.03.007 https://doi.org/10.1017/S0016672308009981 https://doi.org/10.1017/S0016672308009981 https://doi.org/10.3390/f12040498 https://doi.org/10.1007/s11295-022-01579-2 https://doi.org/10.1139/x99-129 https://doi.org/10.1007/s11295-009-0253-6 http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal http://b4est.eu/wp-content/uploads/2022/11/D3.5-Breeding-guidelines-transversal http://colloque.inrae.fr/confgentree2020/content/download/4428/57324/version/1/file/PosterGuilbaud.pdf http://colloque.inrae.fr/confgentree2020/content/download/4428/57324/version/1/file/PosterGuilbaud.pdf http://colloque.inrae.fr/confgentree2020/content/download/4428/57324/version/1/file/PosterGuilbaud.pdf https://doi.org/10.3390/f13101554 https://doi.org/10.3390/f13101554 https://doi.org/10.1098/rstb.2020.0359 https://doi.org/10.1007/s11627-021-10197-x https://doi.org/10.1007/s11627-021-10197-x https://doi.org/10.1111/1755-0998.12056 https://doi.org/10.12899/asr-1817 https://doi.org/10.1016/j.scitotenv.2019.05.378 https://doi.org/10.1371/journal.pone.0204518 https://doi.org/10.1371/journal.pone.0204518 https://doi.org/10.1016/j.forpol.2023.103030 https://doi.org/10.1016/j.scitotenv.2019.02.237 https://doi.org/10.1016/j.scitotenv.2019.02.237 https://doi.org/10.4060/ca9825en https://doi.org/10.1111/1755-0998.12513 https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:52023PC0411 https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:52023PC0411 https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:52023PC0411 https://doi.org/10.1139/x97-219 https://doi.org/10.1017/S001667230900007X https://doi.org/10.1007/s11056-012-9338-4 https://doi.org/10.1080/02827581.2018.1441433 https://doi.org/10.1080/02827581.2018.1441433 https://doi.org/10.1073/pnas.1019315108 https://doi.org/10.1073/pnas.1019315108 https://doi.org/10.1007/s11295-014-0707-3 Fugeray-Scarbel A et al. - iForest 17: 45-58 Jandl R, Spathelf P, Bolte A, Prescott C (2019). Forest adaptation to climate change is non- management an option? Annals of Forest Sci- ence 76: 48. - doi: 10.1007/s13595-019-0827-x Jansson G, Hansen J, Haapanen M, Kvaalen H, Steffenrem A (2017). The genetic and economic gains from forest tree breeding programmes in Scandinavia and Finland, Scandinavian Journal of Forest Research 32 (4): 273-286. - doi: 10.108 0/02827581.2016.1242770 Johnsen O, Haug G, Grönstad BS, Rognstad AT (1994). Effects of heat-treatment, timing of heat-treatment, and gibberellin a(4/7) on flow- ering in potted Picea abies grafts. Scandinavian Journal of Forest Research 9 (4): 333-340. - doi: 10.1080/02827589409382849 Johnsen O, Fossdal CG, Nagy N, Mølmann J, Daehlen OG, Skrøppa T (2005). Climatic adapta- tion in Picea abies progenies is affected by the temperature during zygotic embryogenes