Section: Forest & Wood Sciences
Topic: Plant biology, Ecology, Physiology

Variability in seeds’ physicochemical characteristics, germination and seedling growth within and between two French Populus nigra L. populations

10.24072/pcjournal.86 - Peer Community Journal, Volume 2 (2022), article no. e10.

Get full text PDF Peer reviewed and recommended by PCI
article image

To improve understanding of the physiology, ecology, and regeneration requirements of black poplar (Populus nigra), a severely endangered tree species in Europe, we analysed the biochemical composition of seeds from 20 families derived from open pollination of 20 trees in two contrasting environments in France, along the Drôme and Loire rivers. Significant between-family differences were detected. Total lipid contents differed qualitatively between seed of the two populations and were higher in the Drôme population (214 more or less 29.8 versus 172.72 more or less 19.77 mg.g-1 dw). Soluble sugars were less abundant in seeds of the Drôme population (78.78 more or less 10.01 versus 104.10 more or less 25.32 mg.g-1 dw). The protein content (322 more or less 74.3 mg.g-1 dw) and quantity of reserve proteins did not differ between seeds of the two populations. Measurements in three consecutive years showed that seeds of the Loire population had significantly higher dry weight (0.69 more or less 0.10 versus 0.45 more or less 0.10 mg.g-1 dw), but this did not significantly affect the germination rate or root growth of the seedlings measured 5 days after sowing. However, one group of Loire seedlings had substantially longer juvenile roots than another group. Overall, the results suggest that intrinsic qualities of the seeds are not critical factors in the early stages and in selection pressure of the species life cycle and recruitment.

Published online:
DOI: 10.24072/pcjournal.86
Type: Research article

Lefebvre, Marlène 1; Villar, Marc 1; Boizot, Nathalie 1; Delile, Armelle 1; Dimouro, Benjamin 2; Lomenech, Anne-Marie 3; Teyssier, Caroline 1

1 INRAE, ONF, BioForA, Orléans, France
2 INRAE, GBFor, Orléans, France
3 University of Bordeaux, Centre de Génomique Fonctionnelle, Plateforme Protéome, Bordeaux, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Lefebvre, Marl\`ene and Villar, Marc and Boizot, Nathalie and Delile, Armelle and Dimouro, Benjamin and Lomenech, Anne-Marie and Teyssier, Caroline},
     title = {Variability in seeds{\textquoteright} physicochemical characteristics, germination and seedling growth within and between two {French} {\protect\emph{Populus} nigra} {L.} populations},
     journal = {Peer Community Journal},
     eid = {e10},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.86},
     url = {}
AU  - Lefebvre, Marlène
AU  - Villar, Marc
AU  - Boizot, Nathalie
AU  - Delile, Armelle
AU  - Dimouro, Benjamin
AU  - Lomenech, Anne-Marie
AU  - Teyssier, Caroline
TI  - Variability in seeds’ physicochemical characteristics, germination and seedling growth within and between two French Populus nigra L. populations
JO  - Peer Community Journal
PY  - 2022
VL  - 2
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.86
ID  - 10_24072_pcjournal_86
ER  - 
%0 Journal Article
%A Lefebvre, Marlène
%A Villar, Marc
%A Boizot, Nathalie
%A Delile, Armelle
%A Dimouro, Benjamin
%A Lomenech, Anne-Marie
%A Teyssier, Caroline
%T Variability in seeds’ physicochemical characteristics, germination and seedling growth within and between two French Populus nigra L. populations
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%R 10.24072/pcjournal.86
%F 10_24072_pcjournal_86
Lefebvre, Marlène; Villar, Marc; Boizot, Nathalie; Delile, Armelle; Dimouro, Benjamin; Lomenech, Anne-Marie; Teyssier, Caroline. Variability in seeds’ physicochemical characteristics, germination and seedling growth within and between two French Populus nigra L. populations. Peer Community Journal, Volume 2 (2022), article  no. e10. doi : 10.24072/pcjournal.86.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.forestwoodsci.100004

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Akbulut, M.; Bozhuyuk, M. R.; Ercisli, S.; Skender, A.; Sorkheh, K. Chemical Composition of Seed Propagated Chestnut Genotypes from Northeastern Turkey, Notulae Botanicae Horti Agrobotanici Cluj-Napoca, Volume 45 (2017) no. 2, pp. 425-430 | DOI

[2] Azarkovich, M. I. Protein Complex as Indicator of Seed Recalcitrance, American Journal of Biomedical Science & Research, Volume 6 (2019) no. 2, pp. 131-132 | DOI

[3] Barsoum, N.; Muller, E.; Skot, L. Variations in levels of clonality among Populus nigra L. stands of different ages, Evolutionary Ecology, Volume 18 (2004) no. 5-6, pp. 601-624 | DOI

[4] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Usinglme4, Journal of Statistical Software, Volume 67 (2015) no. 1 | DOI

[5] Bishi, S.; Kumar, L.; Dagla, M.; Mahatma, M.; Rathnakumar, A.; Lalwani, H.; Misra, J. Characterization of Spanish peanut germplasm (Arachis hypogaea L.) for sugar profiling and oil quality, Industrial Crops and Products, Volume 51 (2013), pp. 46-50 | DOI

[6] Bonner F Storage of seed In: In Bonner F and Karrfalt R (Ed.) The woody plant seed manual Vol. 727. United States Department of Agriculture, Forest Service ((2008)), pp. 85-96

[7] Bourgeois, B.; González, E. Pulses of seed release in riparian Salicaceae coincide with high atmospheric temperature, River Research and Applications, Volume 35 (2019) no. 9, pp. 1590-1596 | DOI

[8] Castro, J.; Hodar, J.; Gomez, J. Seed size In: In Basra AS (Ed.) Handbook of Seed Science and Technology. New York. Food Products Press ((2006)), pp. 397-427

[9] Chenault, N.; Arnaud-Haond, S.; Juteau, M.; Valade, R.; Almeida, J.-L.; Villar, M.; Bastien, C.; Dowkiw, A. SSR-based analysis of clonality, spatial genetic structure and introgression from the Lombardy poplar into a natural population of Populus nigra L. along the Loire River, Tree Genetics & Genomes, Volume 7 (2011) no. 6, pp. 1249-1262 | DOI

[10] Cheng, Y.-S.; Zheng, Y.; VanderGheynst, J. S. Rapid Quantitative Analysis of Lipids Using a Colorimetric Method in a Microplate Format, Lipids, Volume 46 (2011) no. 1, pp. 95-103 | DOI

[11] Collective work The world of food grains, Academic Press, United Kingdom, (2015), 1976 pages

[12] Corbineau, F. Markers of seed quality: from present to future, Seed Science Research, Volume 22 (2012) no. S1 | DOI

[13] Corenblit, D.; Steiger, J.; González, E.; Gurnell, A. M.; Charrier, G.; Darrozes, J.; Dousseau, J.; Julien, F.; Lambs, L.; Larrue, S.; Roussel, E.; Vautier, F.; Voldoire, O. The biogeomorphological life cycle of poplars during the fluvial biogeomorphological succession: a special focus onPopulus nigraL., Earth Surface Processes and Landforms, Volume 39 (2014) no. 4, pp. 546-563 | DOI

[14] Dewan, S.; Vander Mijnsbrugge, K.; De Frenne, P.; Steenackers, M.; Michiels, B.; Verheyen, K. Maternal temperature during seed maturation affects seed germination and timing of bud set in seedlings of European black poplar, Forest Ecology and Management, Volume 410 (2018), pp. 126-135 | DOI

[15] Dronne, S.; Label, P.; Lelu, M.-A. Desiccation decreases abscisic acid content in hybrid larch (Larix X leptoeuropaea) somatic embryos, Physiologia Plantarum, Volume 99 (1997) no. 3, pp. 433-438 | DOI

[16] Egea, G.; González-Real, M. M.; Baille, A.; Nortes, P. A.; Sánchez-Bel, P.; Domingo, R. The effects of contrasted deficit irrigation strategies on the fruit growth and kernel quality of mature almond trees, Agricultural Water Management, Volume 96 (2009) no. 11, pp. 1605-1614 | DOI

[17] Fady, B.; Cottrell, J.; Ackzell, L.; Alía, R.; Muys, B.; Prada, A.; González-Martínez, S. C. Forests and global change: what can genetics contribute to the major forest management and policy challenges of the twenty-first century?, Regional Environmental Change, Volume 16 (2015) no. 4, pp. 927-939 | DOI

[18] 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, M. C.; Berard, A.; Allwright, M. R.; Villar, M.; Taylor, G.; Bastien, C.; Morgante, M. New resources for genetic studies inPopulus nigra: genome-wide SNP discovery and development of a 12k Infinium array, Molecular Ecology Resources, Volume 16 (2016) no. 4, pp. 1023-1036 | DOI

[19] Fenner, M. Environmental Influences on Seed Size and Composition, Horticultural Reviews, John Wiley & Sons, Inc., Oxford, UK, 2010, pp. 183-213 | DOI

[20] Folkes, B. F. The physiology of the synthesis of amino acids and their movement into the seed proteins of plants, Proceedings of the Nutrition Society, Volume 29 (1970) no. 1, pp. 12-20 | DOI

[21] Foussadier R Initiation des successions végétales dans les lits endigués des cours d’eau alpins. Inluence des paramètres abiotiques sur la régénération des salicacées. Université de Grenoble, France, (1998)

[22] Gautier, F.; Eliášová, K.; Leplé, J.-C.; Vondráková, Z.; Lomenech, A.-M.; Le Metté, C.; Label, P.; Costa, G.; Trontin, J.-F.; Teyssier, C.; Lelu-Walter, M.-A. Repetitive somatic embryogenesis induced cytological and proteomic changes in embryogenic lines of Pseudotsuga menziesii [Mirb.], BMC Plant Biology, Volume 18 (2018) no. 1 | DOI

[23] Gautier, F.; Label, P.; Eliášová, K.; Leplé, J.-C.; Motyka, V.; Boizot, N.; Vondráková, Z.; Malbeck, J.; Trávníčková, A.; Le Metté, C.; Lesage-Descauses, M.-C.; Lomenech, A.-M.; Trontin, J.-F.; Costa, G.; Lelu-Walter, M.-A.; Teyssier, C. Cytological, Biochemical and Molecular Events of the Embryogenic State in Douglas-fir (Pseudotsuga menziesii [Mirb.]), Frontiers in Plant Science, Volume 10 (2019) (10) | DOI

[24] Ghaffaripour, S.; Van den Bilcke, N.; Samson, R. The importance of seed reserve on performance and breeding of tamarind seedlings, Scientia Horticulturae, Volume 222 (2017), pp. 145-152 | DOI

[25] González-Rodríguez, V.; Barrio, I. C.; Villar, R. Within-population variability influences early seedling establishment in four Mediterranean oaks, Acta Oecologica, Volume 41 (2012), pp. 82-89 | DOI

[26] González, E.; Bourgeois, B.; Masip, A.; Sher, A. A. Trade-Offs in Seed Dispersal Strategies Across Riparian Trees: The How Matters as Much as the When, River Research and Applications, Volume 32 (2016) no. 4, pp. 786-794 | DOI

[27] Gosling, P. Raising trees and shrubs from seeds. Practice guide. Forest Research Publications, (2007)

[28] Gösslová, M.; Svobodová, H.; Lipavská, H.; Albrechtová, J.; Vreugdenhil, D. Comparing carbohydrate status during norway spruce seed development and somatic embryo formation, In Vitro Cellular & Developmental Biology - Plant, Volume 37 (2001) no. 1, pp. 24-28 | DOI

[29] Greulich, S.; Chevalier, R.; Villar, M. Soil seed banks in the floodplain of a large river: A test of hypotheses on seed bank composition in relation to flooding and established vegetation, Journal of Vegetation Science, Volume 30 (2019) no. 4, pp. 732-745 | DOI

[30] Guilloy-Froget, H.; Muller, E.; Barsoum, N.; Hughes, F. M. M. Dispersal, germination, and survival of Populus nigra L. (Salicaceae) in changing hydrologic conditions, Wetlands, Volume 22 (2002) no. 3, pp. 478-488 | DOI

[31] Gurnell, A.; Petts, G. Trees as riparian engineers: the Tagliamento river, Italy, Earth Surface Processes and Landforms, Volume 31 (2006) no. 12, pp. 1558-1574 | DOI

[32] Hampton, J. G.; Boelt, B.; Rolston, M. P.; Chastain, T. G. Effects of elevated CO2and temperature on seed quality, The Journal of Agricultural Science, Volume 151 (2013) no. 2, pp. 154-162 | DOI

[33] Imbert, E.; Lefevre, F. Dispersal and gene flow of Populus nigra (Salicaceae) along a dynamic river system, Journal of Ecology, Volume 91 (2003) no. 3, pp. 447-456 | DOI

[34] Kabeya, D.; Sakai, S. The Role of Roots and Cotyledons as Storage Organs in Early Stages of Establishment in Quercus crispula: a Quantitative Analysis of the Nonstructural Carbohydrate in Cotyledons and Roots, Annals of Botany, Volume 92 (2003) no. 4, pp. 537-545 | DOI

[35] Karrenberg, S.; Edwards, P. J.; Kollmann, J. The life history of Salicaceae living in the active zone of floodplains, Freshwater Biology, Volume 47 (2002) no. 4, pp. 733-748 | DOI

[36] Karrenberg, S.; Suter, M. Phenotypic trade-offs in the sexual reproduction of Salicaceae from flood plains, American Journal of Botany, Volume 90 (2003) no. 5, pp. 749-754 | DOI

[37] Kim, D. H. Extending Populus seed longevity by controlling seed moisture content and temperature, PLOS ONE, Volume 13 (2018) no. 8 | DOI

[38] Kitajima, K. Cotyledon functional morphology, patterns of seed reserve utilization and regeneration niches of tropical tree seedlings In: In Swaine and Md B (Ed.) The Ecology of Tropical Forest Tree Seedlings. Parthenon, Carnforth, UK. ((1996)), pp. 193-210

[39] Kondolf, G. M.; Piégay, H.; Landon, N. Changes in the riparian zone of the lower Eygues River, France, since 1830, Landscape Ecology, Volume 22 (2007) no. 3, pp. 367-384 | DOI

[40] Lamarca, E. V.; Prataviera, J. S.; Borges, I. F.; Delgado, L. F.; Teixeira, C. C.; Camargo, M. B. d.; Faria, J. M.; Barbedo, C. J. Maturation of Eugenia pyriformis seeds under different hydric and thermal conditions, Anais da Academia Brasileira de Ciências, Volume 85 (2013) no. 1, pp. 223-233 | DOI

[41] Lê, S.; Josse, J.; Husson, F. FactoMineR: AnRPackage for Multivariate Analysis, Journal of Statistical Software, Volume 25 (2008) no. 1, pp. 1-18 | DOI

[42] Lefèvre F,; Barsoum N,; Heinze B,; Kajba D,; Rotach P,; de Vries SMG; Turok J In situ conservation of Populus nigra, EUFORGEN technical bulletin, (2001), 58 pages

[43] Lipavská, H.; Konrádová, H. Somatic embryogenesis in conifers: The role of carbohydrate metabolism, In Vitro Cellular & Developmental Biology - Plant, Volume 40 (2004) no. 1, pp. 23-30 | DOI

[44] Mahoney, J. M.; Rood, S. B. Streamflow requirements for cottonwood seedling recruitment—An integrative model, Wetlands, Volume 18 (1998) no. 4, pp. 634-645 | DOI

[45] Michalak, M.; Plitta, B. P.; Tylkowski, T.; Chmielarz, P.; Suszka, J. Desiccation tolerance and cryopreservation of seeds of black poplar (Populus nigra L.), a disappearing tree species in Europe, European Journal of Forest Research, Volume 134 (2015) no. 1, pp. 53-60 | DOI

[46] Miernyk, J. A.; Hajduch, M. Seed proteomics, Journal of Proteomics, Volume 74 (2011) no. 4, pp. 389-400 | DOI

[47] Morel, A.; Trontin, J.-F.; Corbineau, F.; Lomenech, A.-M.; Beaufour, M.; Reymond, I.; Le Metté, C.; Ader, K.; Harvengt, L.; Cadene, M.; Label, P.; Teyssier, C.; Lelu-Walter, M.-A. Cotyledonary somatic embryos of Pinus pinaster Ait. most closely resemble fresh, maturing cotyledonary zygotic embryos: biological, carbohydrate and proteomic analyses, Planta, Volume 240 (2014) no. 5, pp. 1075-1095 | DOI

[48] Muller, C.; Teissier Du Cros, E.; Laroppe, E.; Duval, H. Conservation pendant 5 ans de graines de peupliers noirs (Populus nigra L.), Annales des Sciences Forestières, Volume 39 (1982) no. 2, pp. 179-185 | DOI

[49] Nilsson, C.; Reidy, C. A.; Dynesius, M.; Revenga, C. Fragmentation and Flow Regulation of the World's Large River Systems, Science, Volume 308 (2005) no. 5720, pp. 405-408 | DOI

[50] Parker, W. C.; Noland, T. L.; Morneault, A. E. The Effects of Seed Mass on Germination, Seedling Emergence, and Early Seedling Growth of Eastern White Pine (Pinus strobus L.), New Forests, Volume 32 (2006) no. 1, pp. 33-49 | DOI

[51] Pawłowski, T. A.; Klupczyńska, E. A.; Staszak, A. M.; Suszka, J. Proteomic analysis of black poplar (Populus nigra L.) seed storability, Annals of Forest Science, Volume 76 (2019) no. 4 | DOI

[52] Pritchard, H. W. Water Potential and Embryonic Axis Viability in Recalcitrant Seeds of Quercus rubra, Annals of Botany, Volume 67 (1991) no. 1, pp. 43-49 | DOI

[53] Rajjou, L.; Duval, M.; Gallardo, K.; Catusse, J.; Bally, J.; Job, C.; Job, D. Seed Germination and Vigor, Annual Review of Plant Biology, Volume 63 (2012) no. 1, pp. 507-533 | DOI

[54] Roberts, E. Predicting the storage life of seeds , Seed Science Technology, Volume 1 (1973), pp. 499-514

[55] Rodrigues, I. M.; Coelho, J. F.; Carvalho, M. G. V. Isolation and valorisation of vegetable proteins from oilseed plants: Methods, limitations and potential, Journal of Food Engineering, Volume 109 (2012) no. 3, pp. 337-346 | DOI

[56] Shi, J.; Zhen, Y.; Zheng, R.-H. Proteome profiling of early seed development in Cunninghamia lanceolata (Lamb.) Hook, Journal of Experimental Botany, Volume 61 (2010) no. 9, pp. 2367-2381 | DOI

[57] Soriano, D.; Huante, P.; Gamboa-de Buen, A.; Orozco-Segovia, A. Seed reserve translocation and early seedling growth of eight tree species in a tropical deciduous forest in Mexico, Plant Ecology, Volume 214 (2013) no. 11, pp. 1361-1375 | DOI

[58] Soriano, D.; Orozco-Segovia, A.; Márquez-Guzmán, J.; Kitajima, K.; Gamboa-de Buen, A.; Huante, P. Seed reserve composition in 19 tree species of a tropical deciduous forest in Mexico and its relationship to seed germination and seedling growth, Annals of Botany, Volume 107 (2011) no. 6, pp. 939-951 | DOI

[59] Stanton, B.; Villar, M. Controlled reproduction of Populus In: In Stettler RF, Bradshaw HD, Heilman PE, and Hinckley TM (Ed.) Biology of Populus and its implications for management and conservation, NRC Research Press, Ottawa, Ontario, Canada ((1996)), pp. 113-138

[60] Steadman, K. J.; Pritchard, H. W.; Dey, P. M. Tissue-specific Soluble Sugars in Seeds as Indicators of Storage Category, Annals of Botany, Volume 77 (1996) no. 6, pp. 667-674 | DOI

[61] Stella, J. C.; Battles, J. J.; Orr, B. K.; McBride, J. R. Synchrony of Seed Dispersal, Hydrology and Local Climate in a Semi-arid River Reach in California, Ecosystems, Volume 9 (2006) no. 7, pp. 1200-1214 | DOI

[62] Suszka, J.; Plitta, B. P.; Michalak, M.; Bujarska-Borkowska, B.; Tylkowski, T.; Chmielarz, P. Optimal seed water content and storage temperature for preservation of Populus nigra L. germplasm, Annals of Forest Science, Volume 71 (2014) no. 5, pp. 543-549 | DOI

[63] Teyssier, C.; Grondin, C.; Bonhomme, L.; Lomenech, A.-M.; Vallance, M.; Morabito, D.; Label, P.; Lelu-Walter, M.-A. Increased gelling agent concentration promotes somatic embryo maturation in hybrid larch (Larix×eurolepsis): a 2-DE proteomic analysis, Physiologia Plantarum, Volume 141 (2011) no. 2, pp. 152-165 | DOI

[64] Teyssier, C.; Maury, S.; Beaufour, M.; Grondin, C.; Delaunay, A.; Le Metté, C.; Ader, K.; Cadene, M.; Label, P.; Lelu-Walter, M.-A. In search of markers for somatic embryo maturation in hybrid larch (Larix×eurolepis): global DNA methylation and proteomic analyses, Physiologia Plantarum, Volume 150 (2014) no. 2, pp. 271-291 | DOI

[65] Van Splunder, I.; Coops, H.; Voesenek, L. A. C. J.; Blom, C. W. P. M. Establishment of alluvial forest species in floodplains: the role of dispersal timing, germination characteristics and water level fluctuations, Acta Botanica Neerlandica, Volume 44 (1995) no. 3, pp. 269-278 | DOI

[66] Vanden-Broeck, A.; Cox, K.; Villar, M. Natural hybridization and potential seed set of sympatric Populus nigra and Populus × canadensis along the river IJzer in Flanders (Belgium), Plant Ecology and Evolution, Volume 145 (2012) no. 3, pp. 341-349 | DOI

[67] Wang, L.; Patrick, J. W.; Ruan, Y.-L. Live Long and Prosper: Roles of Sugar and Sugar Polymers in Seed Vigor, Molecular Plant, Volume 11 (2018) no. 1, pp. 1-3 | DOI

[68] Wintenberger, C. L.; Rodrigues, S.; Greulich, S.; Bréhéret, J. G.; Jugé, P.; Tal, M.; Dubois, A.; Villar, M. Control of Non-migrating Bar Morphodynamics on Survival of Populus nigra Seedlings during Floods, Wetlands, Volume 39 (2019) no. 2, pp. 275-290 | DOI

[69] Yada, S.; Huang, G.; Lapsley, K. Natural variability in the nutrient composition of California-grown almonds, Journal of Food Composition and Analysis, Volume 30 (2013) no. 2, pp. 80-85 | DOI

[70] Young, L. W.; Wilen, R. W.; Bonham-Smith, P. C. High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production, Journal of Experimental Botany, Volume 55 (2004) no. 396, pp. 485-495 | DOI

[71] Zanne, A. E.; Chapman, C. A.; Kitajima, K. Evolutionary and ecological correlates of early seedling morphology in East African trees and shrubs, American Journal of Botany, Volume 92 (2005) no. 6, pp. 972-978 | DOI

[72] Zhang, H.; Wang, W.-Q.; Liu, S.-J.; Møller, I. M.; Song, S.-Q. Proteome Analysis of Poplar Seed Vigor, PLOS ONE, Volume 10 (2015) no. 7 | DOI

[73] Zhang, H.; Zhou, D.; Matthew, C.; Wang, P.; Zheng, W. Photosynthetic contribution of cotyledons to early seedling development inCynoglossum divaricatumandAmaranthus retroflexus, New Zealand Journal of Botany, Volume 46 (2008) no. 1, pp. 39-48 | DOI

[74] Zhu, B.; Coleman, G. D. Plant Molecular Biology, 46 (2001) no. 4, pp. 383-394 | DOI

[75] Zsuffa, L. The Genetics of Populus nigra L, Annales Forestales, Volume 6 (1974), pp. 29-53

Cited by Sources: