Robinson, Kathryn - The genetic basis of ecological traits in aspen

@article{robinson_improved_2024,
	title = {An {Improved} {Chromosome}-scale {Genome} {Assembly} and {Population} {Genetics} resource for {Populus} tremula.},
	volume = {176},
	copyright = {© 2024 The Author(s). Physiologia Plantarum published by John Wiley \& Sons Ltd on behalf of Scandinavian Plant Physiology Society.},
	issn = {1399-3054},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/ppl.14511},
	doi = {10.1111/ppl.14511},
	abstract = {Aspen (Populus tremula L.) is a keystone species and a model system for forest tree genomics. We present an updated resource comprising a chromosome-scale assembly, population genetics and genomics data. Using the resource, we explore the genetic basis of natural variation in leaf size and shape, traits with complex genetic architecture. We generated the genome assembly using long-read sequencing, optical and high-density genetic maps. We conducted whole-genome resequencing of the Umeå Aspen (UmAsp) collection. Using the assembly and re-sequencing data from the UmAsp, Swedish Aspen (SwAsp) and Scottish Aspen (ScotAsp) collections we performed genome-wide association analyses (GWAS) using Single Nucleotide Polymorphisms (SNPs) for 26 leaf physiognomy phenotypes. We conducted Assay of Transposase Accessible Chromatin sequencing (ATAC-Seq), identified genomic regions of accessible chromatin, and subset SNPs to these regions, improving the GWAS detection rate. We identified candidate long non-coding RNAs in leaf samples, quantified their expression in an updated co-expression network, and used this to explore the functions of candidate genes identified from the GWAS. A GWAS found SNP associations for seven traits. The associated SNPs were in or near genes annotated with developmental functions, which represent candidates for further study. Of particular interest was a 177-kbp region harbouring associations with several leaf phenotypes in ScotAsp. We have incorporated the assembly, population genetics, genomics, and GWAS data into the PlantGenIE.org web resource, including updating existing genomics data to the new genome version, to enable easy exploration and visualisation. We provide all raw and processed data to facilitate reuse in future studies.},
	language = {en},
	number = {5},
	urldate = {2024-09-19},
	journal = {Physiologia Plantarum},
	author = {Robinson, Kathryn M. and Schiffthaler, Bastian and Liu, Hui and Rydman, Sara M. and Rendón-Anaya, Martha and Kalman, Teitur Ahlgren and Kumar, Vikash and Canovi, Camilla and Bernhardsson, Carolina and Delhomme, Nicolas and Jenkins, Jerry and Wang, Jing and Mähler, Niklas and Richau, Kerstin H. and Stokes, Victoria and A'Hara, Stuart and Cottrell, Joan and Coeck, Kizi and Diels, Tim and Vandepoele, Klaas and Mannapperuma, Chanaka and Park, Eung-Jun and Plaisance, Stephane and Jansson, Stefan and Ingvarsson, Pär K. and Street, Nathaniel R.},
	year = {2024},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/ppl.14511},
	keywords = {ATAC-Seq, GWAS, Populus, aspen, co-expression, genetic architecture, genome assembly, leaf physiognomy, leaf shape, leaf size, lncRNA, natural selection, population genetics},
	pages = {e14511},
}

Aspen (Populus tremula L.) is a keystone species and a model system for forest tree genomics. We present an updated resource comprising a chromosome-scale assembly, population genetics and genomics data. Using the resource, we explore the genetic basis of natural variation in leaf size and shape, traits with complex genetic architecture. We generated the genome assembly using long-read sequencing, optical and high-density genetic maps. We conducted whole-genome resequencing of the Umeå Aspen (UmAsp) collection. Using the assembly and re-sequencing data from the UmAsp, Swedish Aspen (SwAsp) and Scottish Aspen (ScotAsp) collections we performed genome-wide association analyses (GWAS) using Single Nucleotide Polymorphisms (SNPs) for 26 leaf physiognomy phenotypes. We conducted Assay of Transposase Accessible Chromatin sequencing (ATAC-Seq), identified genomic regions of accessible chromatin, and subset SNPs to these regions, improving the GWAS detection rate. We identified candidate long non-coding RNAs in leaf samples, quantified their expression in an updated co-expression network, and used this to explore the functions of candidate genes identified from the GWAS. A GWAS found SNP associations for seven traits. The associated SNPs were in or near genes annotated with developmental functions, which represent candidates for further study. Of particular interest was a 177-kbp region harbouring associations with several leaf phenotypes in ScotAsp. We have incorporated the assembly, population genetics, genomics, and GWAS data into the PlantGenIE.org web resource, including updating existing genomics data to the new genome version, to enable easy exploration and visualisation. We provide all raw and processed data to facilitate reuse in future studies.

@article{luomaranta_systems_2024,
	title = {Systems genetic analysis of lignin biosynthesis in \textit{{Populus} tremula}},
	volume = {243},
	issn = {0028-646X, 1469-8137},
	url = {https://nph.onlinelibrary.wiley.com/doi/10.1111/nph.19993},
	doi = {10.1111/nph.19993},
	abstract = {Summary
            
              
                
                  
                    The genetic control underlying natural variation in lignin content and composition in trees is not fully understood. We performed a systems genetic analysis to uncover the genetic regulation of lignin biosynthesis in a natural ‘SwAsp’ population of aspen (
                    Populus tremula
                    ) trees.
                  
                
                
                  We analyzed gene expression by RNA sequencing (RNA‐seq) in differentiating xylem tissues, and lignin content and composition using Pyrolysis‐GC‐MS in mature wood of 268 trees from 99 genotypes.
                
                
                  
                    Abundant variation was observed for lignin content and composition, and genome‐wide association study identified proteins in the pentose phosphate pathway and arabinogalactan protein glycosylation among the top‐ranked genes that are associated with these traits. Variation in gene expression and the associated genetic polymorphism was revealed through the identification of 312 705 local and 292 003 distant expression quantitative trait loci (eQTL). A co‐expression network analysis suggested modularization of lignin biosynthesis and novel functions for the lignin‐biosynthetic CINNAMYL ALCOHOL DEHYDROGENASE 2 and CAFFEOYL‐CoA O‐METHYLTRANSFERASE 3.
                    PHENYLALANINE AMMONIA LYASE 3
                    was co‐expressed with
                    HOMEOBOX PROTEIN 5
                    (HB5), and the role of HB5 in stimulating lignification was demonstrated in transgenic trees.
                  
                
                
                  The systems genetic approach allowed linking natural variation in lignin biosynthesis to trees´ responses to external cues such as mechanical stimulus and nutrient availability.},
	language = {en},
	number = {6},
	urldate = {2024-08-30},
	journal = {New Phytologist},
	author = {Luomaranta, Mikko and Grones, Carolin and Choudhary, Shruti and Milhinhos, Ana and Kalman, Teitur Ahlgren and Nilsson, Ove and Robinson, Kathryn M. and Street, Nathaniel R. and Tuominen, Hannele},
	month = sep,
	year = {2024},
	keywords = {GWAS, HD-Zip III, Populus, aspen, eQTL, lignin biosynthesis, wood formation},
	pages = {2157--2174},
}

Summary The genetic control underlying natural variation in lignin content and composition in trees is not fully understood. We performed a systems genetic analysis to uncover the genetic regulation of lignin biosynthesis in a natural ‘SwAsp’ population of aspen ( Populus tremula ) trees. We analyzed gene expression by RNA sequencing (RNA‐seq) in differentiating xylem tissues, and lignin content and composition using Pyrolysis‐GC‐MS in mature wood of 268 trees from 99 genotypes. Abundant variation was observed for lignin content and composition, and genome‐wide association study identified proteins in the pentose phosphate pathway and arabinogalactan protein glycosylation among the top‐ranked genes that are associated with these traits. Variation in gene expression and the associated genetic polymorphism was revealed through the identification of 312 705 local and 292 003 distant expression quantitative trait loci (eQTL). A co‐expression network analysis suggested modularization of lignin biosynthesis and novel functions for the lignin‐biosynthetic CINNAMYL ALCOHOL DEHYDROGENASE 2 and CAFFEOYL‐CoA O‐METHYLTRANSFERASE 3. PHENYLALANINE AMMONIA LYASE 3 was co‐expressed with HOMEOBOX PROTEIN 5 (HB5), and the role of HB5 in stimulating lignification was demonstrated in transgenic trees. The systems genetic approach allowed linking natural variation in lignin biosynthesis to trees´ responses to external cues such as mechanical stimulus and nutrient availability.

@article{escamez_genetic_2023,
	title = {Genetic markers and tree properties predicting wood biorefining potential in aspen ({Populus} tremula) bioenergy feedstock},
	volume = {16},
	issn = {2731-3654},
	url = {https://doi.org/10.1186/s13068-023-02315-1},
	doi = {10.1186/s13068-023-02315-1},
	abstract = {Wood represents the majority of the biomass on land and constitutes a renewable source of biofuels and other bioproducts. However, wood is recalcitrant to bioconversion, raising a need for feedstock improvement in production of, for instance, biofuels. We investigated the properties of wood that affect bioconversion, as well as the underlying genetics, to help identify superior tree feedstocks for biorefining.},
	number = {1},
	urldate = {2023-04-14},
	journal = {Biotechnology for Biofuels and Bioproducts},
	author = {Escamez, Sacha and Robinson, Kathryn M. and Luomaranta, Mikko and Gandla, Madhavi Latha and Mähler, Niklas and Yassin, Zakiya and Grahn, Thomas and Scheepers, Gerhard and Stener, Lars-Göran and Jansson, Stefan and Jönsson, Leif J. and Street, Nathaniel R. and Tuominen, Hannele},
	month = apr,
	year = {2023},
	keywords = {Bioenergy, Biomass, Biorefining, Feedstock recalcitrance, Forest feedstocks, Saccharification},
	pages = {65},
}

Wood represents the majority of the biomass on land and constitutes a renewable source of biofuels and other bioproducts. However, wood is recalcitrant to bioconversion, raising a need for feedstock improvement in production of, for instance, biofuels. We investigated the properties of wood that affect bioconversion, as well as the underlying genetics, to help identify superior tree feedstocks for biorefining.

@article{lihavainen_salicylic_2023,
	title = {Salicylic acid metabolism and signalling coordinate senescence initiation in aspen in nature},
	volume = {14},
	copyright = {2023 The Author(s)},
	issn = {2041-1723},
	url = {https://www.nature.com/articles/s41467-023-39564-5},
	doi = {10.1038/s41467-023-39564-5},
	abstract = {Deciduous trees exhibit a spectacular phenomenon of autumn senescence driven by the seasonality of their growth environment, yet there is no consensus which external or internal cues trigger it. Senescence starts at different times in European aspen (Populus tremula L.) genotypes grown in same location. By integrating omics studies, we demonstrate that aspen genotypes utilize similar transcriptional cascades and metabolic cues to initiate senescence, but at different times during autumn. The timing of autumn senescence initiation appeared to be controlled by two consecutive “switches”; 1) first the environmental variation induced the rewiring of the transcriptional network, stress signalling pathways and metabolic perturbations and 2) the start of senescence process was defined by the ability of the genotype to activate and sustain stress tolerance mechanisms mediated by salicylic acid. We propose that salicylic acid represses the onset of leaf senescence in stressful natural conditions, rather than promoting it as often observed in annual plants.},
	language = {en},
	number = {1},
	urldate = {2023-07-21},
	journal = {Nature Communications},
	author = {Lihavainen, Jenna and Šimura, Jan and Bag, Pushan and Fataftah, Nazeer and Robinson, Kathryn Megan and Delhomme, Nicolas and Novák, Ondřej and Ljung, Karin and Jansson, Stefan},
	month = jul,
	year = {2023},
	note = {Number: 1
Publisher: Nature Publishing Group},
	keywords = {Metabolomics, Plant physiology, Regulatory networks, Senescence},
	pages = {4288},
}

Deciduous trees exhibit a spectacular phenomenon of autumn senescence driven by the seasonality of their growth environment, yet there is no consensus which external or internal cues trigger it. Senescence starts at different times in European aspen (Populus tremula L.) genotypes grown in same location. By integrating omics studies, we demonstrate that aspen genotypes utilize similar transcriptional cascades and metabolic cues to initiate senescence, but at different times during autumn. The timing of autumn senescence initiation appeared to be controlled by two consecutive “switches”; 1) first the environmental variation induced the rewiring of the transcriptional network, stress signalling pathways and metabolic perturbations and 2) the start of senescence process was defined by the ability of the genotype to activate and sustain stress tolerance mechanisms mediated by salicylic acid. We propose that salicylic acid represses the onset of leaf senescence in stressful natural conditions, rather than promoting it as often observed in annual plants.

@article{rendon-anaya_adaptive_2021,
	title = {Adaptive introgression facilitate adaptation to high latitudes in {European} aspen ({Populus} tremula {L}.)},
	volume = {38},
	issn = {1537-1719},
	url = {https://doi.org/10.1093/molbev/msab229},
	doi = {10.1093/molbev/msab229},
	abstract = {Understanding local adaptation has become a key research area given the ongoing climate challenge and the concomitant requirement to conserve genetic resources. Perennial plants, such as forest trees, are good models to study local adaptation given their wide geographic distribution, largely outcrossing mating systems and demographic histories. We evaluated signatures of local adaptation in European aspen (Populus tremula) across Europe by means of whole genome re-sequencing of a collection of 411 individual trees. We dissected admixture patterns between aspen lineages and observed a strong genomic mosaicism in Scandinavian trees, evidencing different colonization trajectories into the peninsula from Russia, Central and Western Europe. As a consequence of the secondary contacts between populations after the last glacial maximum (LGM), we detected an adaptive introgression event in a genome region of ∼500kb in chromosome 10, harboring a large-effect locus that has previously been shown to contribute to adaptation to the short growing seasons characteristic of northern Scandinavia. Demographic simulations and ancestry inference suggest an Eastern origin - probably Russian - of the adaptive Nordic allele which nowadays is present in a homozygous state at the north of Scandinavia. The strength of introgression and positive selection signatures in this region is a unique feature in the genome. Furthermore, we detected signals of balancing selection, shared across regional populations, that highlight the importance of standing variation as a primary source of alleles that facilitate local adaptation. Our results therefore emphasize the importance of migration-selection balance underlying the genetic architecture of key adaptive quantitative traits.},
	language = {eng},
	number = {11},
	journal = {Molecular Biology and Evolution},
	author = {Rendón-Anaya, Martha and Wilson, Jonathan and Sveinsson, Sæmundur and Fedorkov, Aleksey and Cottrell, Joan and Bailey, Mark E. S. and Ruņģis, Dainis and Lexer, Christian and Jansson, Stefan and Robinson, Kathryn M. and Street, Nathaniel R. and Ingvarsson, Pär K.},
	month = jul,
	year = {2021},
	pages = {5034--5050},
}

Understanding local adaptation has become a key research area given the ongoing climate challenge and the concomitant requirement to conserve genetic resources. Perennial plants, such as forest trees, are good models to study local adaptation given their wide geographic distribution, largely outcrossing mating systems and demographic histories. We evaluated signatures of local adaptation in European aspen (Populus tremula) across Europe by means of whole genome re-sequencing of a collection of 411 individual trees. We dissected admixture patterns between aspen lineages and observed a strong genomic mosaicism in Scandinavian trees, evidencing different colonization trajectories into the peninsula from Russia, Central and Western Europe. As a consequence of the secondary contacts between populations after the last glacial maximum (LGM), we detected an adaptive introgression event in a genome region of ∼500kb in chromosome 10, harboring a large-effect locus that has previously been shown to contribute to adaptation to the short growing seasons characteristic of northern Scandinavia. Demographic simulations and ancestry inference suggest an Eastern origin - probably Russian - of the adaptive Nordic allele which nowadays is present in a homozygous state at the north of Scandinavia. The strength of introgression and positive selection signatures in this region is a unique feature in the genome. Furthermore, we detected signals of balancing selection, shared across regional populations, that highlight the importance of standing variation as a primary source of alleles that facilitate local adaptation. Our results therefore emphasize the importance of migration-selection balance underlying the genetic architecture of key adaptive quantitative traits.

@article{bag_atlas_2021,
	title = {An atlas of the {Norway} spruce needle seasonal transcriptome},
	volume = {108},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/tpj.15530},
	doi = {10.1111/tpj.15530},
	abstract = {Boreal conifers possess a tremendous ability to survive and remain evergreen during harsh winter conditions and resume growth during summer. This is enabled by coordinated regulation of major cellular functions at the level of gene expression, metabolism, and physiology. Here we present a comprehensive characterization of the annual changes in the global transcriptome of Norway spruce (Picea abies) needles as a resource to understand needle development and acclimation processes throughout the year. In young, growing needles (May 15 until June 30), cell walls, organelles, etc., were formed, and this developmental program heavily influenced the transcriptome, explained by over-represented Gene Ontology (GO) categories. Later changes in gene expression were smaller but four phases were recognized: summer (July–August), autumn (September–October), winter (November–February), and spring (March–April), where over-represented GO categories demonstrated how the needles acclimated to the various seasons. Changes in the seasonal global transcriptome profile were accompanied by differential expression of members of the major transcription factor families. We present a tentative model of how cellular activities are regulated over the year in needles of Norway spruce, which demonstrates the value of mining this dataset, accessible in ConGenIE together with advanced visualization tools.},
	language = {en},
	number = {6},
	urldate = {2021-11-04},
	journal = {The Plant Journal},
	author = {Bag, Pushan and Lihavainen, Jenna and Delhomme, Nicolas and Riquelme, Thomas and Robinson, Kathryn M and Jansson, Stefan},
	month = oct,
	year = {2021},
	keywords = {Conifers, Norway spruce, Seasonal adaptation, Transcriptomics, conifers, resource, seasonal adaptation, transcriptomics},
}

Boreal conifers possess a tremendous ability to survive and remain evergreen during harsh winter conditions and resume growth during summer. This is enabled by coordinated regulation of major cellular functions at the level of gene expression, metabolism, and physiology. Here we present a comprehensive characterization of the annual changes in the global transcriptome of Norway spruce (Picea abies) needles as a resource to understand needle development and acclimation processes throughout the year. In young, growing needles (May 15 until June 30), cell walls, organelles, etc., were formed, and this developmental program heavily influenced the transcriptome, explained by over-represented Gene Ontology (GO) categories. Later changes in gene expression were smaller but four phases were recognized: summer (July–August), autumn (September–October), winter (November–February), and spring (March–April), where over-represented GO categories demonstrated how the needles acclimated to the various seasons. Changes in the seasonal global transcriptome profile were accompanied by differential expression of members of the major transcription factor families. We present a tentative model of how cellular activities are regulated over the year in needles of Norway spruce, which demonstrates the value of mining this dataset, accessible in ConGenIE together with advanced visualization tools.

@article{bandau_european_2021,
	title = {European aspen with high compared to low constitutive tannin defenses grow taller in response to anthropogenic nitrogen enrichment},
	volume = {487},
	issn = {03781127},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S0378112721000748},
	doi = {10/gjd7k2},
	language = {en},
	urldate = {2021-06-03},
	journal = {Forest Ecology and Management},
	author = {Bandau, Franziska and Albrectsen, Benedicte Riber and Robinson, Kathryn M. and Gundale, Michael J.},
	month = may,
	year = {2021},
	pages = {118985},
}

@article{lihavainen_stem_2021,
	title = {Stem girdling affects the onset of autumn senescence in aspen in interaction with metabolic signals},
	volume = {172},
	issn = {0031-9317, 1399-3054},
	url = {https://onlinelibrary.wiley.com/doi/10.1111/ppl.13319},
	doi = {10.1111/ppl.13319},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Physiologia Plantarum},
	author = {Lihavainen, Jenna and Edlund, Erik and Björkén, Lars and Bag, Pushan and Robinson, Kathryn M. and Jansson, Stefan},
	month = may,
	year = {2021},
	pages = {201--217},
}

@article{robinson_variation_2021,
	title = {Variation in non-target traits in genetically modified hybrid aspens does not exceed natural variation},
	volume = {64},
	issn = {1871-6784},
	url = {https://www.sciencedirect.com/science/article/pii/S1871678421000625},
	doi = {10.1016/j.nbt.2021.05.005},
	abstract = {Genetically modified hybrid aspens (Populus tremula L. x P. tremuloides Michx.), selected for increased growth under controlled conditions, have been grown in highly replicated field trials to evaluate how the target trait (growth) translated to natural conditions. Moreover, the variation was compared among genotypes of ecologically important non-target traits: number of shoots, bud set, pathogen infection, amount of insect herbivory, composition of the insect herbivore community and flower bud induction. This variation was compared with the variation in a population of randomly selected natural accessions of P. tremula grown in common garden trials, to estimate how the “unintended variation” present in transgenic trees, which in the future may be commercialized, compares with natural variation. The natural variation in the traits was found to be typically significantly greater. The data suggest that when authorities evaluate the potential risks associated with a field experiment or commercial introduction of transgenic trees, risk evaluation should focus on target traits and that unintentional variation in non-target traits is of less concern.},
	language = {en},
	urldate = {2021-09-21},
	journal = {New Biotechnology},
	author = {Robinson, Kathryn M. and Möller, Linus and Bhalerao, Rishikesh P. and Hertzberg, Magnus and Nilsson, Ove and Jansson, Stefan},
	month = sep,
	year = {2021},
	keywords = {European aspen, Field experiment, Genetically modified, Hybrid aspen, Natural variation, Non-target traits},
	pages = {27--36},
}

Genetically modified hybrid aspens (Populus tremula L. x P. tremuloides Michx.), selected for increased growth under controlled conditions, have been grown in highly replicated field trials to evaluate how the target trait (growth) translated to natural conditions. Moreover, the variation was compared among genotypes of ecologically important non-target traits: number of shoots, bud set, pathogen infection, amount of insect herbivory, composition of the insect herbivore community and flower bud induction. This variation was compared with the variation in a population of randomly selected natural accessions of P. tremula grown in common garden trials, to estimate how the “unintended variation” present in transgenic trees, which in the future may be commercialized, compares with natural variation. The natural variation in the traits was found to be typically significantly greater. The data suggest that when authorities evaluate the potential risks associated with a field experiment or commercial introduction of transgenic trees, risk evaluation should focus on target traits and that unintentional variation in non-target traits is of less concern.

@article{muller_single_2020,
	title = {A single gene underlies the dynamic evolution of poplar sex determination},
	volume = {6},
	issn = {2055-0278},
	url = {http://www.nature.com/articles/s41477-020-0672-9},
	doi = {10.1038/s41477-020-0672-9},
	language = {en},
	number = {6},
	urldate = {2021-06-07},
	journal = {Nature Plants},
	author = {Müller, Niels A. and Kersten, Birgit and Leite Montalvão, Ana P. and Mähler, Niklas and Bernhardsson, Carolina and Bräutigam, Katharina and Carracedo Lorenzo, Zulema and Hoenicka, Hans and Kumar, Vikash and Mader, Malte and Pakull, Birte and Robinson, Kathryn M. and Sabatti, Maurizio and Vettori, Cristina and Ingvarsson, Pär K. and Cronk, Quentin and Street, Nathaniel R. and Fladung, Matthias},
	month = jun,
	year = {2020},
	pages = {630--637},
}

@article{apuli_inferring_2020,
	title = {Inferring the {Genomic} {Landscape} of {Recombination} {Rate} {Variation} in {European} {Aspen} ( {Populus} tremula )},
	volume = {10},
	issn = {2160-1836},
	url = {https://academic.oup.com/g3journal/article/10/1/299/6020315},
	doi = {10/gjctk2},
	abstract = {Abstract
            The rate of meiotic recombination is one of the central factors determining genome-wide levels of linkage disequilibrium which has important consequences for the efficiency of natural selection and for the dissection of quantitative traits. Here we present a new, high-resolution linkage map for Populus tremula that we use to anchor approximately two thirds of the P. tremula draft genome assembly on to the expected 19 chromosomes, providing us with the first chromosome-scale assembly for P. tremula (Table 2). We then use this resource to estimate variation in recombination rates across the P. tremula genome and compare these results to recombination rates based on linkage disequilibrium in a large number of unrelated individuals. We also assess how variation in recombination rates is associated with a number of genomic features, such as gene density, repeat density and methylation levels. We find that recombination rates obtained from the two methods largely agree, although the LD-based method identifies a number of genomic regions with very high recombination rates that the map-based method fails to detect. Linkage map and LD-based estimates of recombination rates are positively correlated and show similar correlations with other genomic features, showing that both methods can accurately infer recombination rate variation across the genome. Recombination rates are positively correlated with gene density and negatively correlated with repeat density and methylation levels, suggesting that recombination is largely directed toward gene regions in P. tremula.},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {G3 Genes{\textbar}Genomes{\textbar}Genetics},
	author = {Apuli, Rami-Petteri and Bernhardsson, Carolina and Schiffthaler, Bastian and Robinson, Kathryn M and Jansson, Stefan and Street, Nathaniel R and Ingvarsson, Pär K},
	month = jan,
	year = {2020},
	pages = {299--309},
}

Abstract The rate of meiotic recombination is one of the central factors determining genome-wide levels of linkage disequilibrium which has important consequences for the efficiency of natural selection and for the dissection of quantitative traits. Here we present a new, high-resolution linkage map for Populus tremula that we use to anchor approximately two thirds of the P. tremula draft genome assembly on to the expected 19 chromosomes, providing us with the first chromosome-scale assembly for P. tremula (Table 2). We then use this resource to estimate variation in recombination rates across the P. tremula genome and compare these results to recombination rates based on linkage disequilibrium in a large number of unrelated individuals. We also assess how variation in recombination rates is associated with a number of genomic features, such as gene density, repeat density and methylation levels. We find that recombination rates obtained from the two methods largely agree, although the LD-based method identifies a number of genomic regions with very high recombination rates that the map-based method fails to detect. Linkage map and LD-based estimates of recombination rates are positively correlated and show similar correlations with other genomic features, showing that both methods can accurately infer recombination rate variation across the genome. Recombination rates are positively correlated with gene density and negatively correlated with repeat density and methylation levels, suggesting that recombination is largely directed toward gene regions in P. tremula.

@article{mahler_leaf_2020,
	title = {Leaf shape in {Populus} tremula is a complex, omnigenic trait},
	volume = {10},
	issn = {2045-7758, 2045-7758},
	url = {https://onlinelibrary.wiley.com/doi/10.1002/ece3.6691},
	doi = {10.1002/ece3.6691},
	language = {en},
	number = {21},
	urldate = {2021-06-07},
	journal = {Ecology and Evolution},
	author = {Mähler, Niklas and Schiffthaler, Bastian and Robinson, Kathryn M. and Terebieniec, Barbara K. and Vučak, Matej and Mannapperuma, Chanaka and Bailey, Mark E. S. and Jansson, Stefan and Hvidsten, Torgeir R. and Street, Nathaniel R.},
	month = nov,
	year = {2020},
	pages = {11922--11940},
}

@article{wang_major_2018,
	title = {A major locus controls local adaptation and adaptive life history variation in a perennial plant},
	volume = {19},
	issn = {1474-760X},
	url = {https://genomebiology.biomedcentral.com/articles/10.1186/s13059-018-1444-y},
	doi = {10.1186/s13059-018-1444-y},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Genome Biology},
	author = {Wang, Jing and Ding, Jihua and Tan, Biyue and Robinson, Kathryn M. and Michelson, Ingrid H. and Johansson, Anna and Nystedt, Björn and Scofield, Douglas G. and Nilsson, Ove and Jansson, Stefan and Street, Nathaniel R. and Ingvarsson, Pär K.},
	month = dec,
	year = {2018},
	pages = {72},
}

@article{michelson_autumn_2018,
	title = {Autumn senescence in aspen is not triggered by day length},
	volume = {162},
	issn = {00319317},
	url = {http://doi.wiley.com/10.1111/ppl.12593},
	doi = {10.1111/ppl.12593},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Physiologia Plantarum},
	author = {Michelson, Ingrid H. and Ingvarsson, Pär K. and Robinson, Kathryn M. and Edlund, Erik and Eriksson, Maria E. and Nilsson, Ove and Jansson, Stefan},
	month = jan,
	year = {2018},
	pages = {123--134},
}

@article{albrectsen_both_2018,
	title = {Both plant genotype and herbivory shape aspen endophyte communities},
	volume = {187},
	issn = {0029-8549, 1432-1939},
	url = {http://link.springer.com/10.1007/s00442-018-4097-3},
	doi = {10/gdrvmw},
	language = {en},
	number = {2},
	urldate = {2021-06-07},
	journal = {Oecologia},
	author = {Albrectsen, Benedicte Riber and Siddique, Abu Bakar and Decker, Vicki Huizu Guo and Unterseher, Martin and Robinson, Kathryn M.},
	month = jun,
	year = {2018},
	pages = {535--545},
}

@article{lin_functional_2018,
	title = {Functional and evolutionary genomic inferences in \textit{{Populus}} through genome and population sequencing of {American} and {European} aspen},
	volume = {115},
	issn = {0027-8424, 1091-6490},
	url = {http://www.pnas.org/lookup/doi/10.1073/pnas.1801437115},
	doi = {10.1073/pnas.1801437115},
	abstract = {The
              Populus
              genus is one of the major plant model systems, but genomic resources have thus far primarily been available for poplar species, and primarily
              Populus trichocarpa
              (Torr. \& Gray), which was the first tree with a whole-genome assembly. To further advance evolutionary and functional genomic analyses in
              Populus
              , we produced genome assemblies and population genetics resources of two aspen species,
              Populus tremula
              L. and
              Populus tremuloides
              Michx. The two aspen species have distributions spanning the Northern Hemisphere, where they are keystone species supporting a wide variety of dependent communities and produce a diverse array of secondary metabolites. Our analyses show that the two aspens share a similar genome structure and a highly conserved gene content with
              P. trichocarpa
              but display substantially higher levels of heterozygosity. Based on population resequencing data, we observed widespread positive and negative selection acting on both coding and noncoding regions. Furthermore, patterns of genetic diversity and molecular evolution in aspen are influenced by a number of features, such as expression level, coexpression network connectivity, and regulatory variation. To maximize the community utility of these resources, we have integrated all presented data within the PopGenIE web resource (
              PopGenIE.org
              ).},
	language = {en},
	number = {46},
	urldate = {2021-06-07},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Lin, Yao-Cheng and Wang, Jing and Delhomme, Nicolas and Schiffthaler, Bastian and Sundström, Görel and Zuccolo, Andrea and Nystedt, Björn and Hvidsten, Torgeir R. and de la Torre, Amanda and Cossu, Rosa M. and Hoeppner, Marc P. and Lantz, Henrik and Scofield, Douglas G. and Zamani, Neda and Johansson, Anna and Mannapperuma, Chanaka and Robinson, Kathryn M. and Mähler, Niklas and Leitch, Ilia J. and Pellicer, Jaume and Park, Eung-Jun and Van Montagu, Marc and Van de Peer, Yves and Grabherr, Manfred and Jansson, Stefan and Ingvarsson, Pär K. and Street, Nathaniel R.},
	month = nov,
	year = {2018},
	pages = {E10970--E10978},
}

The Populus genus is one of the major plant model systems, but genomic resources have thus far primarily been available for poplar species, and primarily Populus trichocarpa (Torr. & Gray), which was the first tree with a whole-genome assembly. To further advance evolutionary and functional genomic analyses in Populus , we produced genome assemblies and population genetics resources of two aspen species, Populus tremula L. and Populus tremuloides Michx. The two aspen species have distributions spanning the Northern Hemisphere, where they are keystone species supporting a wide variety of dependent communities and produce a diverse array of secondary metabolites. Our analyses show that the two aspens share a similar genome structure and a highly conserved gene content with P. trichocarpa but display substantially higher levels of heterozygosity. Based on population resequencing data, we observed widespread positive and negative selection acting on both coding and noncoding regions. Furthermore, patterns of genetic diversity and molecular evolution in aspen are influenced by a number of features, such as expression level, coexpression network connectivity, and regulatory variation. To maximize the community utility of these resources, we have integrated all presented data within the PopGenIE web resource ( PopGenIE.org ).

@article{grimberg_storage_2018,
	title = {Storage lipid accumulation is controlled by photoperiodic signal acting via regulators of growth cessation and dormancy in hybrid aspen},
	volume = {219},
	issn = {0028646X},
	url = {http://doi.wiley.com/10.1111/nph.15197},
	doi = {10.1111/nph.15197},
	language = {en},
	number = {2},
	urldate = {2021-06-07},
	journal = {New Phytologist},
	author = {Grimberg, Åsa and Lager, Ida and Street, Nathaniel R. and Robinson, Kathryn M. and Marttila, Salla and Mähler, Niklas and Ingvarsson, Pär K. and Bhalerao, Rishikesh P.},
	month = jul,
	year = {2018},
	pages = {619--630},
}

@article{soolanayakanahally_comparative_2015,
	title = {Comparative physiology of allopatric {Populus} species: geographic clines in photosynthesis, height growth, and carbon isotope discrimination in common gardens},
	volume = {6},
	issn = {1664-462X (Print) 1664-462X (Linking)},
	shorttitle = {Comparative physiology of allopatric {Populus} species},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/26236324},
	doi = {10.3389/fpls.2015.00528},
	abstract = {Populus species with wide geographic ranges display strong adaptation to local environments. We studied the clinal patterns in phenology and ecophysiology in allopatric Populus species adapted to similar environments on different continents under common garden settings. As a result of climatic adaptation, both Populus tremula L. and Populus balsamifera L. display latitudinal clines in photosynthetic rates (A), whereby high-latitude trees of P. tremula had higher A compared to low-latitude trees and nearly so in P. balsamifera (p = 0.06). Stomatal conductance (g s) and chlorophyll content index (CCI) follow similar latitudinal trends. However, foliar nitrogen was positively correlated with latitude in P. balsamifera and negatively correlated in P. tremula. No significant trends in carbon isotope composition of the leaf tissue (delta(13)C) were observed for both species; but, intrinsic water-use efficiency (WUEi) was negatively correlated with the latitude of origin in P. balsamifera. In spite of intrinsically higher A, high-latitude trees in both common gardens accomplished less height gain as a result of early bud set. Thus, shoot biomass was determined by height elongation duration (HED), which was well approximated by the number of days available for free growth between bud flush and bud set. We highlight the shortcoming of unreplicated outdoor common gardens for tree improvement and the crucial role of photoperiod in limiting height growth, further complicating interpretation of other secondary effects.},
	language = {English},
	urldate = {2021-06-07},
	journal = {Front Plant Sci},
	author = {Soolanayakanahally, R. Y. and Guy, R. D. and Street, N. R. and Robinson, K. M. and Silim, S. N. and Albrectsen, B. R. and Jansson, S.},
	year = {2015},
	note = {Edition: 2015/08/04},
	keywords = {Photosynthesis, bud set, carbon isotope discrimination, common garden, comparative physiology, latitude, photosynthesis, poplar, water-use efficiency},
	pages = {528},
}

Populus species with wide geographic ranges display strong adaptation to local environments. We studied the clinal patterns in phenology and ecophysiology in allopatric Populus species adapted to similar environments on different continents under common garden settings. As a result of climatic adaptation, both Populus tremula L. and Populus balsamifera L. display latitudinal clines in photosynthetic rates (A), whereby high-latitude trees of P. tremula had higher A compared to low-latitude trees and nearly so in P. balsamifera (p = 0.06). Stomatal conductance (g s) and chlorophyll content index (CCI) follow similar latitudinal trends. However, foliar nitrogen was positively correlated with latitude in P. balsamifera and negatively correlated in P. tremula. No significant trends in carbon isotope composition of the leaf tissue (delta(13)C) were observed for both species; but, intrinsic water-use efficiency (WUEi) was negatively correlated with the latitude of origin in P. balsamifera. In spite of intrinsically higher A, high-latitude trees in both common gardens accomplished less height gain as a result of early bud set. Thus, shoot biomass was determined by height elongation duration (HED), which was well approximated by the number of days available for free growth between bud flush and bud set. We highlight the shortcoming of unreplicated outdoor common gardens for tree improvement and the crucial role of photoperiod in limiting height growth, further complicating interpretation of other secondary effects.

@article{robinson_relative_2015,
	title = {Relative impacts of environmental variation and evolutionary history on the nestedness and modularity of tree-herbivore networks},
	volume = {5},
	issn = {2045-7758 (Print) 2045-7758 (Linking)},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/26306175},
	doi = {10/f3nt2b},
	abstract = {Nestedness and modularity are measures of ecological networks whose causative effects are little understood. We analyzed antagonistic plant-herbivore bipartite networks using common gardens in two contrasting environments comprised of aspen trees with differing evolutionary histories of defence against herbivores. These networks were tightly connected owing to a high level of specialization of arthropod herbivores that spend a large proportion of the life cycle on aspen. The gardens were separated by ten degrees of latitude with resultant differences in abiotic conditions. We evaluated network metrics and reported similar connectance between gardens but greater numbers of links per species in the northern common garden. Interaction matrices revealed clear nestedness, indicating subsetting of the bipartite interactions into specialist divisions, in both the environmental and evolutionary aspen groups, although nestedness values were only significant in the northern garden. Variation in plant vulnerability, measured as the frequency of herbivore specialization in the aspen population, was significantly partitioned by environment (common garden) but not by evolutionary origin of the aspens. Significant values of modularity were observed in all network matrices. Trait-matching indicated that growth traits, leaf morphology, and phenolic metabolites affected modular structure in both the garden and evolutionary groups, whereas extra-floral nectaries had little influence. Further examination of module configuration revealed that plant vulnerability explained considerable variance in web structure. The contrasting conditions between the two gardens resulted in bottom-up effects of the environment, which most strongly influenced the overall network architecture, however, the aspen groups with dissimilar evolutionary history also showed contrasting degrees of nestedness and modularity. Our research therefore shows that, while evolution does affect the structure of aspen-herbivore bipartite networks, the role of environmental variations is a dominant constraint.},
	language = {en},
	number = {14},
	urldate = {2021-06-07},
	journal = {Ecol Evol},
	author = {Robinson, K. M. and Hauzy, C. and Loeuille, N. and Albrectsen, B. R.},
	month = jul,
	year = {2015},
	note = {Edition: 2015/08/26},
	keywords = {Antagonism, arthropod, aspen, bipartite networks, degree of specialization, modularity, nestedness, trophic strength},
	pages = {2898--915},
}

Nestedness and modularity are measures of ecological networks whose causative effects are little understood. We analyzed antagonistic plant-herbivore bipartite networks using common gardens in two contrasting environments comprised of aspen trees with differing evolutionary histories of defence against herbivores. These networks were tightly connected owing to a high level of specialization of arthropod herbivores that spend a large proportion of the life cycle on aspen. The gardens were separated by ten degrees of latitude with resultant differences in abiotic conditions. We evaluated network metrics and reported similar connectance between gardens but greater numbers of links per species in the northern common garden. Interaction matrices revealed clear nestedness, indicating subsetting of the bipartite interactions into specialist divisions, in both the environmental and evolutionary aspen groups, although nestedness values were only significant in the northern garden. Variation in plant vulnerability, measured as the frequency of herbivore specialization in the aspen population, was significantly partitioned by environment (common garden) but not by evolutionary origin of the aspens. Significant values of modularity were observed in all network matrices. Trait-matching indicated that growth traits, leaf morphology, and phenolic metabolites affected modular structure in both the garden and evolutionary groups, whereas extra-floral nectaries had little influence. Further examination of module configuration revealed that plant vulnerability explained considerable variance in web structure. The contrasting conditions between the two gardens resulted in bottom-up effects of the environment, which most strongly influenced the overall network architecture, however, the aspen groups with dissimilar evolutionary history also showed contrasting degrees of nestedness and modularity. Our research therefore shows that, while evolution does affect the structure of aspen-herbivore bipartite networks, the role of environmental variations is a dominant constraint.

@article{robinson_populus_2014,
	title = {Populus tremula ({European} aspen) shows no evidence of sexual dimorphism},
	volume = {14},
	issn = {1471-2229},
	url = {http://bmcplantbiol.biomedcentral.com/articles/10.1186/s12870-014-0276-5},
	doi = {10/f25brv},
	language = {en},
	number = {1},
	urldate = {2021-06-08},
	journal = {BMC Plant Biology},
	author = {Robinson, Kathryn M and Delhomme, Nicolas and Mähler, Niklas and Schiffthaler, Bastian and Önskog, Jenny and Albrectsen, Benedicte R and Ingvarsson, Pär K and Hvidsten, Torgeir R and Jansson, Stefan and Street, Nathaniel R},
	month = dec,
	year = {2014},
	pages = {276},
}

@article{bernhardsson_geographic_2013,
	title = {Geographic structure in metabolome and herbivore community co-occurs with genetic structure in plant defence genes},
	volume = {16},
	issn = {1461023X},
	url = {http://doi.wiley.com/10.1111/ele.12114},
	doi = {10/f25rz6},
	language = {en},
	number = {6},
	urldate = {2021-06-08},
	journal = {Ecology Letters},
	author = {Bernhardsson, Carolina and Robinson, Kathryn M. and Abreu, Ilka N. and Jansson, Stefan and Albrectsen, Benedicte R. and Ingvarsson, Pär K.},
	editor = {Eubanks, Micky},
	month = jun,
	year = {2013},
	pages = {791--798},
}

@article{robinson_genetic_2012,
	title = {Genetic {Variation} in {Functional} {Traits} {Influences} {Arthropod} {Community} {Composition} in {Aspen} ({Populus} tremula {L}.)},
	volume = {7},
	issn = {1932-6203},
	url = {https://dx.plos.org/10.1371/journal.pone.0037679},
	doi = {10/f24ksj},
	language = {en},
	number = {5},
	urldate = {2021-06-08},
	journal = {PLoS ONE},
	author = {Robinson, Kathryn M. and Ingvarsson, Pär K. and Jansson, Stefan and Albrectsen, Benedicte R.},
	editor = {Kliebenstein, Daniel J.},
	month = may,
	year = {2012},
	pages = {e37679},
}

@article{rae_five_2009,
	title = {Five {QTL} hotspots for yield in short rotation coppice bioenergy poplar: {The} {Poplar} {Biomass} {Loci}},
	volume = {9},
	copyright = {2009 Rae et al; licensee BioMed Central Ltd.},
	issn = {1471-2229},
	shorttitle = {Five {QTL} hotspots for yield in short rotation coppice bioenergy poplar},
	url = {https://bmcplantbiol.biomedcentral.com/articles/10.1186/1471-2229-9-23},
	doi = {10/dj94rg},
	abstract = {Concern over land use for non-food bioenergy crops requires breeding programmes that focus on producing biomass on the minimum amount of land that is economically-viable. To achieve this, the maximum potential yield per hectare is a key target for improvement. For long lived tree species, such as poplar, this requires an understanding of the traits that contribute to biomass production and their genetic control. An important aspect of this for long lived plants is an understanding of genetic interactions at different developmental stages, i.e. how genes or genetic regions impact on yield over time. QTL mapping identified regions of genetic control for biomass yield. We mapped consistent QTL across multiple coppice cycles and identified five robust QTL hotspots on linkage groups III, IV, X, XIV and XIX, calling these 'Poplar Biomass Loci' (PBL 1–5). In total 20\% of the variation in final harvest biomass yield was explained by mapped QTL. We also investigated the genetic correlations between yield related traits to identify 'early diagnostic' indicators of yield showing that early biomass was a reasonable predictor of coppice yield and that leaf size, cell number and stem and sylleptic branch number were also valuable traits. These findings provide insight into the genetic control of biomass production and correlation to 'early diagnostic' traits determining yield in poplar SRC for bioenergy. QTL hotspots serve as useful targets for directed breeding for improved biomass productivity that may also be relevant across additional poplar hybrids.},
	language = {en},
	number = {1},
	urldate = {2021-08-20},
	journal = {BMC Plant Biology},
	author = {Rae, Anne M. and Street, Nathaniel Robert and Robinson, Kathryn Megan and Harris, Nicole and Taylor, Gail},
	month = dec,
	year = {2009},
	note = {Number: 1
Publisher: BioMed Central},
	keywords = {Biomass Yield, Linkage Group VIIIa, Short Rotation Coppice, Stem Number, Sylleptic Branch},
	pages = {1--13},
}

Concern over land use for non-food bioenergy crops requires breeding programmes that focus on producing biomass on the minimum amount of land that is economically-viable. To achieve this, the maximum potential yield per hectare is a key target for improvement. For long lived tree species, such as poplar, this requires an understanding of the traits that contribute to biomass production and their genetic control. An important aspect of this for long lived plants is an understanding of genetic interactions at different developmental stages, i.e. how genes or genetic regions impact on yield over time. QTL mapping identified regions of genetic control for biomass yield. We mapped consistent QTL across multiple coppice cycles and identified five robust QTL hotspots on linkage groups III, IV, X, XIV and XIX, calling these 'Poplar Biomass Loci' (PBL 1–5). In total 20% of the variation in final harvest biomass yield was explained by mapped QTL. We also investigated the genetic correlations between yield related traits to identify 'early diagnostic' indicators of yield showing that early biomass was a reasonable predictor of coppice yield and that leaf size, cell number and stem and sylleptic branch number were also valuable traits. These findings provide insight into the genetic control of biomass production and correlation to 'early diagnostic' traits determining yield in poplar SRC for bioenergy. QTL hotspots serve as useful targets for directed breeding for improved biomass productivity that may also be relevant across additional poplar hybrids.

@article{albrectsen_large_2009,
	title = {Large scale geographic clines of parasite damage to \textit{{Populus} tremula} {L}},
	issn = {09067590, 16000587},
	url = {http://doi.wiley.com/10.1111/j.1600-0587.2009.05982.x},
	doi = {10/c38874},
	language = {en},
	urldate = {2021-06-08},
	journal = {Ecography},
	author = {Albrectsen, Benedicte R. and Witzell, Johanna and Robinson, Kathryn M. and Wulff, Sören and Luquez, Virginia M. C. and Ågren, Rickard and Jansson, Stefan},
	month = oct,
	year = {2009},
}

@article{robinson_defining_2004,
	title = {Defining leaf traits linked to yield in short-rotation coppice {Salix}},
	volume = {26},
	issn = {0961-9534},
	url = {https://www.sciencedirect.com/science/article/pii/S0961953403001600},
	doi = {10/ctstfz},
	abstract = {Short-rotation coppice Salix genotypes of differing biomass yields were studied over two growing seasons with the long-term aim of identifying traits definitive of high yield for the breeding of elite energy crops. In the first season, basic leaf and stem traits were measured in six Salix genotypes, to identify morphological characteristics associated with high biomass yields. Thereafter, S. viminalis L. ‘L78183’ (low yield) and the hybrid genotype S. schwerinii E. Wolf× S. viminalis L. ‘Tora’ (high yield) were compared. Maximum stem heights and stem diameters increased with biomass yield. ‘Tora’ produced more sylleptic branches on the leading stems than ‘L78183’. Leaf traits differed significantly between the two genotypes: individual leaf area and cell number per leaf was greater in ‘Tora’, whereas cell area was greater in ‘L78183’, suggesting that final leaf areas were attained in ‘Tora’ through the production of many, small cells, and in ‘L78183’ through fewer, large cells. Leaf extension rates were higher in ‘Tora’ than ‘L78183’. This result was mirrored for leaf production rate. Leaf area index, examined at two coppice stages, was higher in ‘L78183’ (values of 2.06 and 1.67) than in ‘Tora’ (maximum value 1.43) which had a very open canopy. Furthermore, A/Ci analysis revealed the low-yielding genotype as the most photosynthetically efficient at the individual leaf level whereas light response curves suggest that ‘Tora’ utilised light more efficiently. The results presented in this study suggest that leaf extension rate, final leaf size and cell number per leaf may be indicative of yield, and may be useful as selection criteria for potentially high-yielding hybrids for biomass use.},
	language = {en},
	number = {5},
	urldate = {2021-08-23},
	journal = {Biomass and Bioenergy},
	author = {Robinson, K. M and Karp, A and Taylor, Gail},
	month = may,
	year = {2004},
	keywords = {Cell area, Leaf area, Leaf extension rate, Short-rotation coppice, Yield physiology},
	pages = {417--431},
}

Short-rotation coppice Salix genotypes of differing biomass yields were studied over two growing seasons with the long-term aim of identifying traits definitive of high yield for the breeding of elite energy crops. In the first season, basic leaf and stem traits were measured in six Salix genotypes, to identify morphological characteristics associated with high biomass yields. Thereafter, S. viminalis L. ‘L78183’ (low yield) and the hybrid genotype S. schwerinii E. Wolf× S. viminalis L. ‘Tora’ (high yield) were compared. Maximum stem heights and stem diameters increased with biomass yield. ‘Tora’ produced more sylleptic branches on the leading stems than ‘L78183’. Leaf traits differed significantly between the two genotypes: individual leaf area and cell number per leaf was greater in ‘Tora’, whereas cell area was greater in ‘L78183’, suggesting that final leaf areas were attained in ‘Tora’ through the production of many, small cells, and in ‘L78183’ through fewer, large cells. Leaf extension rates were higher in ‘Tora’ than ‘L78183’. This result was mirrored for leaf production rate. Leaf area index, examined at two coppice stages, was higher in ‘L78183’ (values of 2.06 and 1.67) than in ‘Tora’ (maximum value 1.43) which had a very open canopy. Furthermore, A/Ci analysis revealed the low-yielding genotype as the most photosynthetically efficient at the individual leaf level whereas light response curves suggest that ‘Tora’ utilised light more efficiently. The results presented in this study suggest that leaf extension rate, final leaf size and cell number per leaf may be indicative of yield, and may be useful as selection criteria for potentially high-yielding hybrids for biomass use.

@article{rae_morphological_2004,
	title = {Morphological and physiological traits influencing biomass productivity in short-rotation coppice poplar},
	volume = {34},
	issn = {0045-5067},
	url = {https://cdnsciencepub.com/doi/10.1139/x04-033},
	doi = {10/d4fjbn},
	number = {7},
	urldate = {2021-08-23},
	journal = {Canadian Journal of Forest Research},
	author = {Rae, A M and Robinson, K M and Street, N R and Taylor, G},
	month = jul,
	year = {2004},
	note = {Publisher: NRC Research Press},
	pages = {1488--1498},
}

@article{ferris_leaf_2002,
	title = {Leaf stomatal and epidermal cell development: identification of putative quantitative trait loci in relation to elevated carbon dioxide concentration in poplar},
	volume = {22},
	issn = {0829-318X},
	shorttitle = {Leaf stomatal and epidermal cell development},
	url = {https://doi.org/10.1093/treephys/22.9.633},
	doi = {10.1093/treephys/22.9.633},
	abstract = {Genetic variation in stomatal initiation and density, and epidermal cell size and number were examined in a hybrid pedigree of Populus trichocarpa T. \& G. and P. deltoides Marsh in both ambient ([aCO2]) and elevated ([eCO2]) concentrations of CO2. We aimed to link anatomical traits with the underlying genetic map of F2 Family 331, composed of 350 markers across 19 linkage groups. Leaf stomatal and epidermal cell traits showed pronounced differences between the original parents. We considered the following traits in the F2 population: stomatal density (SD), stomatal index (SI), epidermal cell area (ECA) and the number of epidermal cells per leaf (ECN). In [eCO2], adaxial SD and SI were reduced in the F2 population, whereas ECA increased and ECN remained unchanged. In [aCO2], four putative quantitative trait loci (QTL) with logarithm of the odds ratio (LOD) scores greater than 2.9 were found for stomatal traits on linkage group B: adaxial SI (LOD scores of 5.4 and 5.2); abaxial SI (LOD score of 3.3); and SD (LOD score of 3.2). These results imply that QTL for SI and SD share linkage group B and are under genetic control. More moderate LOD scores (LOD scores \>/= 2.5) suggest QTL for SI on linkage groups A and B and for SD on linkage groups B, D and X with a probable co-locating quantitative trait locus for SI and SD on linkage group D (position 46.3 cM). The QTL in both [aCO2] and [eCO2] for adaxial SD were co-located on linkage group X (LOD scores of 3.5 and 2.6, respectively) indicating a similar response across both treatments. Putative QTL were located on linkage group A (position 89.2 cM) for both leaf size and ECN in [aCO2] and for ECA at almost the same position. The data provide preliminary evidence that leaf stomatal and cell traits are amenable to QTL analysis.},
	number = {9},
	urldate = {2021-10-19},
	journal = {Tree Physiology},
	author = {Ferris, Rachel and Long, L. and Bunn, S. M. and Robinson, K. M. and Bradshaw, H. D. and Rae, A. M. and Taylor, Gail},
	month = jun,
	year = {2002},
	pages = {633--640},
}

Genetic variation in stomatal initiation and density, and epidermal cell size and number were examined in a hybrid pedigree of Populus trichocarpa T. & G. and P. deltoides Marsh in both ambient ([aCO2]) and elevated ([eCO2]) concentrations of CO2. We aimed to link anatomical traits with the underlying genetic map of F2 Family 331, composed of 350 markers across 19 linkage groups. Leaf stomatal and epidermal cell traits showed pronounced differences between the original parents. We considered the following traits in the F2 population: stomatal density (SD), stomatal index (SI), epidermal cell area (ECA) and the number of epidermal cells per leaf (ECN). In [eCO2], adaxial SD and SI were reduced in the F2 population, whereas ECA increased and ECN remained unchanged. In [aCO2], four putative quantitative trait loci (QTL) with logarithm of the odds ratio (LOD) scores greater than 2.9 were found for stomatal traits on linkage group B: adaxial SI (LOD scores of 5.4 and 5.2); abaxial SI (LOD score of 3.3); and SD (LOD score of 3.2). These results imply that QTL for SI and SD share linkage group B and are under genetic control. More moderate LOD scores (LOD scores >/= 2.5) suggest QTL for SI on linkage groups A and B and for SD on linkage groups B, D and X with a probable co-locating quantitative trait locus for SI and SD on linkage group D (position 46.3 cM). The QTL in both [aCO2] and [eCO2] for adaxial SD were co-located on linkage group X (LOD scores of 3.5 and 2.6, respectively) indicating a similar response across both treatments. Putative QTL were located on linkage group A (position 89.2 cM) for both leaf size and ECN in [aCO2] and for ECA at almost the same position. The data provide preliminary evidence that leaf stomatal and cell traits are amenable to QTL analysis.