@article{donev_glucuronoyl_2025,
	title = {Glucuronoyl {Esterase} of {Pathogenic} {Phanerochaete} carnosa {Induces} {Immune} {Responses} in {Aspen} {Independently} of {Its} {Enzymatic} {Activity}},
	volume = {n/a},
	copyright = {© 2025 The Author(s). Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley \& Sons Ltd.},
	issn = {1467-7652},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/pbi.70357},
	doi = {10.1111/pbi.70357},
	abstract = {Microbial enzymes expressed in plants add new functionalities but occasionally trigger undesirable immune responses. Phanerochaete carnosa glucuronoyl esterase (PcGCE) hydrolyses the bond between lignin and 4-O-methyl-α-D-glucuronic acid substituent of glucuronoxylan. PcGCE constitutively expressed in Arabidopsis or hybrid aspen (Populus tremula × tremuloides) improved saccharification but also induced premature leaf senescence. To understand what triggered this senescence, we characterised PcGCE-expressing hybrid aspen by microscopy and omics approaches, supplemented by grafting and recombinant protein application experiments. PcGCE induced massive immune responses followed by senescence in the leaves. Expressing an inactive (PcGCES217A) enzyme has led to similar phenotypes, excluding a possibility that damage-associated molecular patterns (DAMPs) released by glucuronoyl esterase triggered immune responses. Grafting experiments showed that PcGCE transcripts are not mobile but they induce systemic responses. Recombinant PcGCE protein applied to leaves did not induce such responses; thus, PcGCE is probably not perceived as a pathogen-associated molecular pattern (PAMP). We suggest that the observed high expression of PcGCE from the 35S promoter triggers the unfolded protein response. Indeed, restricting PcGCE expression to short-lived xylem cells by using the wood-specific promoter avoided all detrimental effects. Thus, wood-specific expression is a viable strategy for PcGCE deployment in planta, which might be applicable for other stress-inducing proteins.},
	language = {en},
	number = {n/a},
	urldate = {2025-09-19},
	journal = {Plant Biotechnology Journal},
	author = {Donev, Evgeniy N. and Derba-Maceluch, Marta and Liu, Xiao-Kun and Bwanika, Henri Colyn and Dobrowolska, Izabela and Thapa, Mohit and Leśniewska, Joanna and Šimura, Jan and Yi-Lin Tsai, Alex and Krajewski, Konrad S. and Boström, Dan and Kleczkowski, Leszek A. and Eriksson, Maria E. and Ljung, Karin and Master, Emma R. and Mellerowicz, Ewa J.},
	year = {2025},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/pbi.70357},
	keywords = {PTI, Populus, biotic stress, glucuronoyl esterase, lignocellulose improvement, transgenic crops, unfolded protein response},
}

Microbial enzymes expressed in plants add new functionalities but occasionally trigger undesirable immune responses. Phanerochaete carnosa glucuronoyl esterase (PcGCE) hydrolyses the bond between lignin and 4-O-methyl-α-D-glucuronic acid substituent of glucuronoxylan. PcGCE constitutively expressed in Arabidopsis or hybrid aspen (Populus tremula × tremuloides) improved saccharification but also induced premature leaf senescence. To understand what triggered this senescence, we characterised PcGCE-expressing hybrid aspen by microscopy and omics approaches, supplemented by grafting and recombinant protein application experiments. PcGCE induced massive immune responses followed by senescence in the leaves. Expressing an inactive (PcGCES217A) enzyme has led to similar phenotypes, excluding a possibility that damage-associated molecular patterns (DAMPs) released by glucuronoyl esterase triggered immune responses. Grafting experiments showed that PcGCE transcripts are not mobile but they induce systemic responses. Recombinant PcGCE protein applied to leaves did not induce such responses; thus, PcGCE is probably not perceived as a pathogen-associated molecular pattern (PAMP). We suggest that the observed high expression of PcGCE from the 35S promoter triggers the unfolded protein response. Indeed, restricting PcGCE expression to short-lived xylem cells by using the wood-specific promoter avoided all detrimental effects. Thus, wood-specific expression is a viable strategy for PcGCE deployment in planta, which might be applicable for other stress-inducing proteins.

@article{marien_natures_2025,
	title = {Nature’s {Master} of {Ceremony}: {The} {Populus} {Circadian} {Clock} as {Orchestrator} of {Tree} {Growth} and {Phenology}},
	volume = {2},
	copyright = {2025 The Author(s)},
	issn = {2948-281X},
	shorttitle = {Nature’s {Master} of {Ceremony}},
	url = {https://www.nature.com/articles/s44323-025-00034-4},
	doi = {10.1038/s44323-025-00034-4},
	abstract = {Understanding the timely regulation of plant growth and phenology is crucial for assessing a terrestrial ecosystem’s productivity and carbon budget. The circadian clock, a system of genetic oscillators, acts as ‘Master of Ceremony’ during plant physiological processes. The mechanism is particularly elusive in trees despite its relevance. The primary and secondary tree growth, leaf senescence, bud set, and bud burst timing were investigated in 68 constructs transformed into Populus hybrids and compared with untransformed or transformed controls grown in natural or controlled conditions. The results were analyzed using generalized additive models with ordered-factor-smooth interaction smoothers. This meta-analysis shows that several genetic components are associated with the clock. Especially core clock-regulated genes affected tree growth and phenology in both controlled and field conditions. Our results highlight the importance of field trials and the potential of using the clock to generate trees with improved characteristics for sustainable silviculture (e.g., reprogrammed to new photoperiodic regimes and increased growth).},
	language = {en},
	number = {1},
	urldate = {2025-04-11},
	journal = {npj Biological Timing and Sleep},
	publisher = {Nature Publishing Group},
	author = {Mariën, Bertold and Robinson, Kathryn M. and Jurca, Manuela and Michelson, Ingrid H. and Takata, Naoki and Kozarewa, Iwanka and Pin, Pierre A. and Ingvarsson, Pär K. and Moritz, Thomas and Ibáñez, Cristian and Nilsson, Ove and Jansson, Stefan and Penfield, Steve and Yu, Jun and Eriksson, Maria E.},
	month = apr,
	year = {2025},
	keywords = {Biological techniques, Plant sciences},
	pages = {1--19},
}

Understanding the timely regulation of plant growth and phenology is crucial for assessing a terrestrial ecosystem’s productivity and carbon budget. The circadian clock, a system of genetic oscillators, acts as ‘Master of Ceremony’ during plant physiological processes. The mechanism is particularly elusive in trees despite its relevance. The primary and secondary tree growth, leaf senescence, bud set, and bud burst timing were investigated in 68 constructs transformed into Populus hybrids and compared with untransformed or transformed controls grown in natural or controlled conditions. The results were analyzed using generalized additive models with ordered-factor-smooth interaction smoothers. This meta-analysis shows that several genetic components are associated with the clock. Especially core clock-regulated genes affected tree growth and phenology in both controlled and field conditions. Our results highlight the importance of field trials and the potential of using the clock to generate trees with improved characteristics for sustainable silviculture (e.g., reprogrammed to new photoperiodic regimes and increased growth).

@article{ibanez_circadian_2025,
	title = {The circadian clock of {Populus} affects physiological, transcriptional and metabolomic responses to osmotic and ionic components of salt stress},
	volume = {2},
	copyright = {2025 The Author(s)},
	issn = {2948-281X},
	url = {https://www.nature.com/articles/s44323-025-00052-2},
	doi = {10.1038/s44323-025-00052-2},
	abstract = {The circadian oscillator is an innate timing mechanism present in most organisms, including plants. In this study, Populus tremula × P. tremuloides (Populus) trees with reduced expression of circadian clock components were exposed to gradually increases in the osmotic and ionic components of salt stress. Reduced levels of the morning components PttLATE ELONGATED HYPOCOTYL 1 and 2 (PttLHY1,2) or of the evening components PttPSEUDO-RESPONSE REGULATOR 7a and b (PttPRR7a,b) and PttGIGANTEA1,2 (PttGI1,2) affected growth adaptation under stress conditions. PttLHY1,2 regulated growth under NaCl treatment via the control of PttCyclin D3 expression. PttPRR7a,b and PttGI1,2 were instrumental in maintaining growth in roots by enabling effective adaptation of the metabolome. Major changes in the root metabolome under prolonged stress included alterations in carbohydrate, amino acids, and fatty acids. This study places the circadian clock at the centre of adaptation to adverse conditions in trees and will help the development of stress-resistant trees.},
	language = {en},
	number = {1},
	urldate = {2025-10-03},
	journal = {npj Biological Timing and Sleep},
	publisher = {Nature Publishing Group},
	author = {Ibáñez, Cristian and Vergara, Alexander and Castro, David and Bascunan-Godoy, Luisa and Sjölander, Johan and Jurca, Manuela and Pin, Pierre A. and Nilsson, Ove and Eriksson, Maria E.},
	month = oct,
	year = {2025},
	keywords = {Circadian rhythm signalling peptides and proteins, Plant sciences},
	pages = {34},
}

The circadian oscillator is an innate timing mechanism present in most organisms, including plants. In this study, Populus tremula × P. tremuloides (Populus) trees with reduced expression of circadian clock components were exposed to gradually increases in the osmotic and ionic components of salt stress. Reduced levels of the morning components PttLATE ELONGATED HYPOCOTYL 1 and 2 (PttLHY1,2) or of the evening components PttPSEUDO-RESPONSE REGULATOR 7a and b (PttPRR7a,b) and PttGIGANTEA1,2 (PttGI1,2) affected growth adaptation under stress conditions. PttLHY1,2 regulated growth under NaCl treatment via the control of PttCyclin D3 expression. PttPRR7a,b and PttGI1,2 were instrumental in maintaining growth in roots by enabling effective adaptation of the metabolome. Major changes in the root metabolome under prolonged stress included alterations in carbohydrate, amino acids, and fatty acids. This study places the circadian clock at the centre of adaptation to adverse conditions in trees and will help the development of stress-resistant trees.

@article{lazaro-gimeno_circadian_2024,
	title = {The circadian clock participates in seasonal growth in {Norway} spruce ({Picea} abies)},
	volume = {44},
	issn = {1758-4469},
	url = {https://doi.org/10.1093/treephys/tpae139},
	doi = {10.1093/treephys/tpae139},
	abstract = {The boreal forest ecosystems of the northern hemisphere are dominated by conifers, of which Norway spruce (Picea abies [L.] H. Karst.) is one of the most common species. Due to its economic interest to the agroforestry industry, as well as its ecological significance, it is important to understand seasonal growth and biomass production in Norway spruce. Solid evidence that the circadian clock regulates growth in conifers has proved elusive, however, resulting in significant gaps in our knowledge of clock function in these trees. Here, we reassess the impact of the circadian clock on growth in Norway spruce. Using a combination of approaches monitoring the physiology of vegetative growth, transcriptomics and bioinformatics, we determined that the clock could be playing a decisive role in enabling growth, acting in specific developmental processes influenced by season and geographical location to guide bud burst and growth. Thus, the evidence indicates that there is time for spruce.},
	number = {11},
	urldate = {2024-11-29},
	journal = {Tree Physiology},
	author = {Lázaro-Gimeno, David and Ferrari, Camilla and Delhomme, Nico and Johansson, Mikael and Sjölander, Johan and Singh, Rajesh Kumar and Mutwil, Marek and Eriksson, Maria E},
	month = nov,
	year = {2024},
	pages = {tpae139},
}

The boreal forest ecosystems of the northern hemisphere are dominated by conifers, of which Norway spruce (Picea abies [L.] H. Karst.) is one of the most common species. Due to its economic interest to the agroforestry industry, as well as its ecological significance, it is important to understand seasonal growth and biomass production in Norway spruce. Solid evidence that the circadian clock regulates growth in conifers has proved elusive, however, resulting in significant gaps in our knowledge of clock function in these trees. Here, we reassess the impact of the circadian clock on growth in Norway spruce. Using a combination of approaches monitoring the physiology of vegetative growth, transcriptomics and bioinformatics, we determined that the clock could be playing a decisive role in enabling growth, acting in specific developmental processes influenced by season and geographical location to guide bud burst and growth. Thus, the evidence indicates that there is time for spruce.

@incollection{johansson_monitoring_2022,
	address = {New York, NY},
	series = {Methods in {Molecular} {Biology}},
	title = {Monitoring {Seasonal} {Bud} {Set}, {Bud} {Burst}, and {Cold} {Hardiness} in {Populus}},
	isbn = {978-1-07-161912-4},
	url = {https://doi.org/10.1007/978-1-0716-1912-4_17},
	abstract = {Using a perennial model plant allows the study of reoccurring seasonal events in a way that is not possible using a fast-growing annual such as A. thaliana (Arabidopsis). In this study, we present a hybrid aspen (Populus tremula × P. tremuloides) as our perennial model plant. These plants can be grown in growth chambers to shorten growth periods and manipulate day length and temperature in ways that would be impossible under natural conditions. In addition, the use of growth chambers allows easy monitoring of height and diameter expansion, accelerating the collection of data from new strategies that allow evaluation of promoters or inhibitors of growth. Here, we describe how to study and quantify responses to seasonal changes (mainly using P. tremula × P. tremuloides) by measuring growth rate and key events under different photoperiodic cycles.},
	language = {en},
	urldate = {2021-12-01},
	booktitle = {Plant {Circadian} {Networks}: {Methods} and {Protocols}},
	publisher = {Springer US},
	author = {Johansson, Mikael and Takata, Naoki and Ibáñez, Cristian and Eriksson, Maria E.},
	editor = {Staiger, Dorothee and Davis, Seth and Davis, Amanda Melaragno},
	month = jan,
	year = {2022},
	keywords = {Bud burst, Bud set, Cold acclimation, Critical day length, Freezing tolerance, Perennial, Photoperiod, Populus},
	pages = {215--226},
}

Using a perennial model plant allows the study of reoccurring seasonal events in a way that is not possible using a fast-growing annual such as A. thaliana (Arabidopsis). In this study, we present a hybrid aspen (Populus tremula × P. tremuloides) as our perennial model plant. These plants can be grown in growth chambers to shorten growth periods and manipulate day length and temperature in ways that would be impossible under natural conditions. In addition, the use of growth chambers allows easy monitoring of height and diameter expansion, accelerating the collection of data from new strategies that allow evaluation of promoters or inhibitors of growth. Here, we describe how to study and quantify responses to seasonal changes (mainly using P. tremula × P. tremuloides) by measuring growth rate and key events under different photoperiodic cycles.

@incollection{johansson_perennial_2022,
	address = {New York, NY},
	series = {Methods in {Molecular} {Biology}},
	title = {The {Perennial} {Clock} {Is} an {Essential} {Timer} for {Seasonal} {Growth} {Events} and {Cold} {Hardiness}},
	isbn = {978-1-07-161912-4},
	url = {https://doi.org/10.1007/978-1-0716-1912-4_18},
	abstract = {Over the last several decades, changes in global temperatures have led to changes in local environments affecting the growth conditions for many species. This is a trend that makes it even more important to understand how plants respond to local variations and seasonal changes in climate.To detect daily and seasonal changes as well as acute stress factors such as cold and drought, plants rely on a circadian clock. This chapter introduces the current knowledge and literature about the setup and function of the circadian clock in various tree and perennial species, with a focus on the Populus genus.},
	language = {en},
	urldate = {2021-12-01},
	booktitle = {Plant {Circadian} {Networks}: {Methods} and {Protocols}},
	publisher = {Springer US},
	author = {Johansson, Mikael and Ibáñez, Cristian and Takata, Naoki and Eriksson, Maria E.},
	editor = {Staiger, Dorothee and Davis, Seth and Davis, Amanda Melaragno},
	month = jan,
	year = {2022},
	keywords = {Bud burst, Bud set, Circadian clock, Cold tolerance, Growth, Perennial plants, Populus, Seasonal regulation},
	pages = {227--242},
}

Over the last several decades, changes in global temperatures have led to changes in local environments affecting the growth conditions for many species. This is a trend that makes it even more important to understand how plants respond to local variations and seasonal changes in climate.To detect daily and seasonal changes as well as acute stress factors such as cold and drought, plants rely on a circadian clock. This chapter introduces the current knowledge and literature about the setup and function of the circadian clock in various tree and perennial species, with a focus on the Populus genus.

@article{jurca_zeitlupe_2022,
	title = {{ZEITLUPE} {Promotes} {ABA}-{Induced} {Stomatal} {Closure} in {Arabidopsis} and {Populus}},
	volume = {13},
	issn = {1664-462X},
	url = {https://www.frontiersin.org/article/10.3389/fpls.2022.829121},
	abstract = {Plants balance water availability with gas exchange and photosynthesis by controlling stomatal aperture. This control is regulated in part by the circadian clock, but it remains unclear how signalling pathways of daily rhythms are integrated into stress responses. The serine/threonine protein kinase OPEN STOMATA 1 (OST1) contributes to the regulation of stomatal closure via activation of S-type anion channels. OST1 also mediates gene regulation in response to ABA/drought stress. We show that ZEITLUPE (ZTL), a blue light photoreceptor and clock component, also regulates ABA-induced stomatal closure in Arabidopsis thaliana, establishing a link between clock and ABA-signalling pathways. ZTL sustains expression of OST1 and ABA-signalling genes. Stomatal closure in response to ABA is reduced in ztl mutants, which maintain wider stomatal apertures and show higher rates of gas exchange and water loss than wild-type plants. Detached rosette leaf assays revealed a stronger water loss phenotype in ztl-3, ost1-3 double mutants, indicating that ZTL and OST1 contributed synergistically to the control of stomatal aperture. Experimental studies of Populus sp., revealed that ZTL regulated the circadian clock and stomata, indicating ZTL function was similar in these trees and Arabidopsis. PSEUDO-RESPONSE REGULATOR 5 (PRR5), a known target of ZTL, affects ABA-induced responses, including stomatal regulation. Like ZTL, PRR5 interacted physically with OST1 and contributed to the integration of ABA responses with circadian clock signalling. This suggests a novel mechanism whereby the PRR proteins—which are expressed from dawn to dusk—interact with OST1 to mediate ABA-dependent plant responses to reduce water loss in time of stress.},
	urldate = {2022-03-02},
	journal = {Frontiers in Plant Science},
	author = {Jurca, Manuela and Sjölander, Johan and Ibáñez, Cristian and Matrosova, Anastasia and Johansson, Mikael and Kozarewa, Iwanka and Takata, Naoki and Bakó, Laszlo and Webb, Alex A. R. and Israelsson-Nordström, Maria and Eriksson, Maria E.},
	month = mar,
	year = {2022},
	keywords = {⛔ No DOI found},
}

Plants balance water availability with gas exchange and photosynthesis by controlling stomatal aperture. This control is regulated in part by the circadian clock, but it remains unclear how signalling pathways of daily rhythms are integrated into stress responses. The serine/threonine protein kinase OPEN STOMATA 1 (OST1) contributes to the regulation of stomatal closure via activation of S-type anion channels. OST1 also mediates gene regulation in response to ABA/drought stress. We show that ZEITLUPE (ZTL), a blue light photoreceptor and clock component, also regulates ABA-induced stomatal closure in Arabidopsis thaliana, establishing a link between clock and ABA-signalling pathways. ZTL sustains expression of OST1 and ABA-signalling genes. Stomatal closure in response to ABA is reduced in ztl mutants, which maintain wider stomatal apertures and show higher rates of gas exchange and water loss than wild-type plants. Detached rosette leaf assays revealed a stronger water loss phenotype in ztl-3, ost1-3 double mutants, indicating that ZTL and OST1 contributed synergistically to the control of stomatal aperture. Experimental studies of Populus sp., revealed that ZTL regulated the circadian clock and stomata, indicating ZTL function was similar in these trees and Arabidopsis. PSEUDO-RESPONSE REGULATOR 5 (PRR5), a known target of ZTL, affects ABA-induced responses, including stomatal regulation. Like ZTL, PRR5 interacted physically with OST1 and contributed to the integration of ABA responses with circadian clock signalling. This suggests a novel mechanism whereby the PRR proteins—which are expressed from dawn to dusk—interact with OST1 to mediate ABA-dependent plant responses to reduce water loss in time of stress.

@article{singh_growing_2021,
	title = {Growing in time: exploring the molecular mechanisms of tree growth},
	volume = {41},
	issn = {1758-4469},
	shorttitle = {Growing in time},
	url = {https://academic.oup.com/treephys/article/41/4/657/5848548},
	doi = {10.1093/treephys/tpaa065},
	abstract = {Abstract
            Trees cover vast areas of the Earth’s landmasses. They mitigate erosion, capture carbon dioxide, produce oxygen and support biodiversity, and also are a source of food, raw materials and energy for human populations. Understanding the growth cycles of trees is fundamental for many areas of research. Trees, like most other organisms, have evolved a circadian clock to synchronize their growth and development with the daily and seasonal cycles of the environment. These regular changes in light, daylength and temperature are perceived via a range of dedicated receptors and cause resetting of the circadian clock to local time. This allows anticipation of daily and seasonal fluctuations and enables trees to co-ordinate their metabolism and physiology to ensure vital processes occur at the optimal times. In this review, we explore the current state of knowledge concerning the regulation of growth and seasonal dormancy in trees, using information drawn from model systems such as Populus spp.},
	language = {en},
	number = {4},
	urldate = {2021-06-07},
	journal = {Tree Physiology},
	author = {Singh, Rajesh Kumar and Bhalerao, Rishikesh P. and Eriksson, Maria E.},
	editor = {Polle, Andrea},
	month = apr,
	year = {2021},
	pages = {657--678},
}

Abstract Trees cover vast areas of the Earth’s landmasses. They mitigate erosion, capture carbon dioxide, produce oxygen and support biodiversity, and also are a source of food, raw materials and energy for human populations. Understanding the growth cycles of trees is fundamental for many areas of research. Trees, like most other organisms, have evolved a circadian clock to synchronize their growth and development with the daily and seasonal cycles of the environment. These regular changes in light, daylength and temperature are perceived via a range of dedicated receptors and cause resetting of the circadian clock to local time. This allows anticipation of daily and seasonal fluctuations and enables trees to co-ordinate their metabolism and physiology to ensure vital processes occur at the optimal times. In this review, we explore the current state of knowledge concerning the regulation of growth and seasonal dormancy in trees, using information drawn from model systems such as Populus spp.

@article{parry_current_2020,
	title = {Current status of the multinational {Arabidopsis} community},
	volume = {4},
	issn = {2475-4455},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1002/pld3.248},
	doi = {10/gpn668},
	abstract = {The multinational Arabidopsis research community is highly collaborative and over the past thirty years these activities have been documented by the Multinational Arabidopsis Steering Committee (MASC). Here, we (a) highlight recent research advances made with the reference plant Arabidopsis thaliana; (b) provide summaries from recent reports submitted by MASC subcommittees, projects and resources associated with MASC and from MASC country representatives; and (c) initiate a call for ideas and foci for the “fourth decadal roadmap,” which will advise and coordinate the global activities of the Arabidopsis research community.},
	language = {en},
	number = {7},
	urldate = {2022-03-14},
	journal = {Plant Direct},
	author = {Parry, Geraint and Provart, Nicholas J. and Brady, Siobhan M. and Uzilday, Baris and Committee, The Multinational Arabidopsis Steering},
	year = {2020},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/pld3.248},
	keywords = {Arabidopsis thaliana, Research Network, collaboration, roadmap},
	pages = {e00248},
}

The multinational Arabidopsis research community is highly collaborative and over the past thirty years these activities have been documented by the Multinational Arabidopsis Steering Committee (MASC). Here, we (a) highlight recent research advances made with the reference plant Arabidopsis thaliana; (b) provide summaries from recent reports submitted by MASC subcommittees, projects and resources associated with MASC and from MASC country representatives; and (c) initiate a call for ideas and foci for the “fourth decadal roadmap,” which will advise and coordinate the global activities of the Arabidopsis research community.

@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{edwards_circadian_2018,
	title = {Circadian clock components control daily growth activities by modulating cytokinin levels and cell division-associated gene expression in \textit{{Populus}} trees: {Control} of growth in {Populus}.},
	volume = {41},
	issn = {01407791},
	shorttitle = {Circadian clock components control daily growth activities by modulating cytokinin levels and cell division-associated gene expression in \textit{{Populus}} trees},
	url = {http://doi.wiley.com/10.1111/pce.13185},
	doi = {10/gd8xdq},
	language = {en},
	number = {6},
	urldate = {2021-06-07},
	journal = {Plant, Cell \& Environment},
	author = {Edwards, Kieron D. and Takata, Naoki and Johansson, Mikael and Jurca, Manuela and Novák, Ondřej and Hényková, Eva and Liverani, Silvia and Kozarewa, Iwanka and Strnad, Miroslav and Millar, Andrew J. and Ljung, Karin and Eriksson, Maria E.},
	month = jun,
	year = {2018},
	pages = {1468--1482},
}

@article{ding_gigantea-like_2018,
	title = {{GIGANTEA}-like genes control seasonal growth cessation in {Populus}},
	volume = {218},
	copyright = {© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust},
	issn = {1469-8137},
	url = {https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/nph.15087},
	doi = {10/gdt24k},
	abstract = {Survival of trees growing in temperate zones requires cycling between active growth and dormancy. This involves growth cessation in the autumn triggered by a photoperiod shorter than the critical day length. Variations in GIGANTEA (GI)-like genes have been associated with phenology in a range of different tree species, but characterization of the functions of these genes in the process is still lacking. We describe the identification of the Populus orthologs of GI and their critical role in short-day-induced growth cessation. Using ectopic expression and silencing, gene expression analysis, protein interaction and chromatin immunoprecipitation experiments, we show that PttGIs are likely to act in a complex with PttFKF1s (FLAVIN-BINDING, KELCH REPEAT, F-BOX 1) and PttCDFs (CYCLING DOF FACTOR) to control the expression of PttFT2, the key gene regulating short-day-induced growth cessation in Populus. In contrast to Arabidopsis, in which the GI-CONSTANS (CO)-FLOWERING LOCUS T (FT) regulon is a crucial day-length sensor for flowering time, our study suggests that, in Populus, PttCO-independent regulation of PttFT2 by PttGI is more important in the photoperiodic control of growth cessation and bud set.},
	language = {en},
	number = {4},
	urldate = {2021-06-21},
	journal = {New Phytologist},
	author = {Ding, Jihua and Böhlenius, Henrik and Rühl, Mark Georg and Chen, Peng and Sane, Shashank and Zambrano, Jose A. and Zheng, Bo and Eriksson, Maria E. and Nilsson, Ove},
	year = {2018},
	note = {\_eprint: https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.15087},
	keywords = {FLOWERING LOCUS (FT), GIGANTEA (GI), Populus, growth cessation, photoperiod},
	pages = {1491--1503},
}

Survival of trees growing in temperate zones requires cycling between active growth and dormancy. This involves growth cessation in the autumn triggered by a photoperiod shorter than the critical day length. Variations in GIGANTEA (GI)-like genes have been associated with phenology in a range of different tree species, but characterization of the functions of these genes in the process is still lacking. We describe the identification of the Populus orthologs of GI and their critical role in short-day-induced growth cessation. Using ectopic expression and silencing, gene expression analysis, protein interaction and chromatin immunoprecipitation experiments, we show that PttGIs are likely to act in a complex with PttFKF1s (FLAVIN-BINDING, KELCH REPEAT, F-BOX 1) and PttCDFs (CYCLING DOF FACTOR) to control the expression of PttFT2, the key gene regulating short-day-induced growth cessation in Populus. In contrast to Arabidopsis, in which the GI-CONSTANS (CO)-FLOWERING LOCUS T (FT) regulon is a crucial day-length sensor for flowering time, our study suggests that, in Populus, PttCO-independent regulation of PttFT2 by PttGI is more important in the photoperiodic control of growth cessation and bud set.

@article{noren_circadian_2016,
	title = {Circadian and {Plastid} {Signaling} {Pathways} {Are} {Integrated} to {Ensure} {Correct} {Expression} of the {CBF} and {COR} {Genes} during {Photoperiodic} {Growth}},
	volume = {171},
	issn = {0032-0889},
	url = {https://doi.org/10.1104/pp.16.00374},
	doi = {10/f3rvjv},
	abstract = {The circadian clock synchronizes a wide range of biological processes with the day/night cycle, and correct circadian regulation is essential for photosynthetic activity and plant growth. We describe here a mechanism where a plastid signal converges with the circadian clock to fine-tune the regulation of nuclear gene expression in Arabidopsis (Arabidopsis thaliana). Diurnal oscillations of tetrapyrrole levels in the chloroplasts contribute to the regulation of the nucleus-encoded transcription factors C-REPEAT BINDING FACTORS (CBFs). The plastid signal triggered by tetrapyrrole accumulation inhibits the activity of cytosolic HEAT SHOCK PROTEIN90 and, as a consequence, the maturation and stability of the clock component ZEITLUPE (ZTL). ZTL negatively regulates the transcription factor LONG HYPOCOTYL5 (HY5) and PSEUDO-RESPONSE REGULATOR5 (PRR5). Thus, low levels of ZTL result in a HY5- and PRR5-mediated repression of CBF3 and PRR5-mediated repression of CBF1 and CBF2 expression. The plastid signal thereby contributes to the rhythm of CBF expression and the downstream COLD RESPONSIVE expression during day/night cycles. These findings provide insight into how plastid signals converge with, and impact upon, the activity of well-defined clock components involved in circadian regulation.},
	number = {2},
	urldate = {2021-06-07},
	journal = {Plant Physiology},
	author = {Norén, Louise and Kindgren, Peter and Stachula, Paulina and Rühl, Mark and Eriksson, Maria E. and Hurry, Vaughan and Strand, Åsa},
	month = jun,
	year = {2016},
	pages = {1392--1406},
}

The circadian clock synchronizes a wide range of biological processes with the day/night cycle, and correct circadian regulation is essential for photosynthetic activity and plant growth. We describe here a mechanism where a plastid signal converges with the circadian clock to fine-tune the regulation of nuclear gene expression in Arabidopsis (Arabidopsis thaliana). Diurnal oscillations of tetrapyrrole levels in the chloroplasts contribute to the regulation of the nucleus-encoded transcription factors C-REPEAT BINDING FACTORS (CBFs). The plastid signal triggered by tetrapyrrole accumulation inhibits the activity of cytosolic HEAT SHOCK PROTEIN90 and, as a consequence, the maturation and stability of the clock component ZEITLUPE (ZTL). ZTL negatively regulates the transcription factor LONG HYPOCOTYL5 (HY5) and PSEUDO-RESPONSE REGULATOR5 (PRR5). Thus, low levels of ZTL result in a HY5- and PRR5-mediated repression of CBF3 and PRR5-mediated repression of CBF1 and CBF2 expression. The plastid signal thereby contributes to the rhythm of CBF expression and the downstream COLD RESPONSIVE expression during day/night cycles. These findings provide insight into how plastid signals converge with, and impact upon, the activity of well-defined clock components involved in circadian regulation.

@incollection{john_wiley__sons_ltd_plant_2016,
	address = {Chichester, UK},
	title = {Plant {Circadian} {Rhythms}},
	isbn = {978-0-470-01590-2 978-0-470-01617-6},
	url = {http://doi.wiley.com/10.1002/9780470015902.a0020113.pub2},
	doi = {10.1002/9780470015902.a0020113.pub2},
	language = {en},
	urldate = {2021-06-07},
	booktitle = {{eLS}},
	publisher = {John Wiley \& Sons, Ltd},
	author = {McWatters, Harriet G and Eriksson, Maria E.},
	editor = {{John Wiley \& Sons Ltd}},
	month = may,
	year = {2016},
	pages = {1--10},
}

@incollection{anderson_role_2015,
	address = {Cham},
	title = {Role of the {Circadian} {Clock} in {Cold} {Acclimation} and {Winter} {Dormancy} in {Perennial} {Plants}},
	isbn = {978-3-319-14450-4 978-3-319-14451-1},
	url = {http://link.springer.com/10.1007/978-3-319-14451-1_3},
	doi = {10.1007/978-3-319-14451-1_3},
	language = {en},
	urldate = {2021-06-07},
	booktitle = {Advances in {Plant} {Dormancy}},
	publisher = {Springer International Publishing},
	author = {Johansson, Mikael and Ramos-Sánchez, José M. and Conde, Daniel and Ibáñez, Cristian and Takata, Naoki and Allona, Isabel and Eriksson, Maria E.},
	editor = {Anderson, James V.},
	year = {2015},
	pages = {51--74},
}

@article{eriksson_transgenic_2015,
	title = {Transgenic hybrid aspen trees with increased gibberellin ({GA}) concentrations suggest that {GA} acts in parallel with {FLOWERING} {LOCUS} {T2} to control shoot elongation},
	volume = {205},
	issn = {1469-8137},
	url = {https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/nph.13144},
	doi = {10/f3nxc2},
	abstract = {Bioactive gibberellins (GAs) have been implicated in short day (SD)-induced growth cessation in Populus, because exogenous applications of bioactive GAs to hybrid aspens (Populus tremula × tremuloides) under SD conditions delay growth cessation. However, this effect diminishes with time, suggesting that plants may cease growth following exposure to SDs due to a reduction in sensitivity to GAs. In order to validate and further explore the role of GAs in growth cessation, we perturbed GA biosynthesis or signalling in hybrid aspen plants by overexpressing AtGA20ox1, AtGA2ox2 and PttGID1.3 (encoding GA biosynthesis enzymes and a GA receptor). We found trees with elevated concentrations of bioactive GA, due to overexpression of AtGA20ox1, continued to grow in SD conditions and were insensitive to the level of FLOWERING LOCUS T2 (FT2) expression. As transgenic plants overexpressing the PttGID1.3 GA receptor responded in a wild-type (WT) manner to SD conditions, this insensitivity did not result from limited receptor availability. As high concentrations of bioactive GA during SD conditions were sufficient to sustain shoot elongation growth in hybrid aspen trees, independent of FT2 expression levels, we conclude elongation growth in trees is regulated by both GA- and long day-responsive pathways, similar to the regulation of flowering in Arabidopsis thaliana.},
	language = {en},
	number = {3},
	urldate = {2021-08-31},
	journal = {New Phytologist},
	author = {Eriksson, Maria E. and Hoffman, Daniel and Kaduk, Mateusz and Mauriat, Mélanie and Moritz, Thomas},
	year = {2015},
	note = {\_eprint: https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.13144},
	keywords = {Flowering Locus T2 (FT2), Populus, gibberellins (GA), growth cessation, photoperiod},
	pages = {1288--1295},
}

Bioactive gibberellins (GAs) have been implicated in short day (SD)-induced growth cessation in Populus, because exogenous applications of bioactive GAs to hybrid aspens (Populus tremula × tremuloides) under SD conditions delay growth cessation. However, this effect diminishes with time, suggesting that plants may cease growth following exposure to SDs due to a reduction in sensitivity to GAs. In order to validate and further explore the role of GAs in growth cessation, we perturbed GA biosynthesis or signalling in hybrid aspen plants by overexpressing AtGA20ox1, AtGA2ox2 and PttGID1.3 (encoding GA biosynthesis enzymes and a GA receptor). We found trees with elevated concentrations of bioactive GA, due to overexpression of AtGA20ox1, continued to grow in SD conditions and were insensitive to the level of FLOWERING LOCUS T2 (FT2) expression. As transgenic plants overexpressing the PttGID1.3 GA receptor responded in a wild-type (WT) manner to SD conditions, this insensitivity did not result from limited receptor availability. As high concentrations of bioactive GA during SD conditions were sufficient to sustain shoot elongation growth in hybrid aspen trees, independent of FT2 expression levels, we conclude elongation growth in trees is regulated by both GA- and long day-responsive pathways, similar to the regulation of flowering in Arabidopsis thaliana.

@incollection{staiger_monitoring_2014,
	address = {New York, NY},
	title = {Monitoring {Seasonal} {Bud} {Set}, {Bud} {Burst}, and {Cold} {Hardiness} in {Populus}},
	volume = {1158},
	isbn = {978-1-4939-0699-4 978-1-4939-0700-7},
	url = {http://link.springer.com/10.1007/978-1-4939-0700-7_21},
	doi = {10.1007/978-1-4939-0700-7_21},
	urldate = {2021-06-08},
	booktitle = {Plant {Circadian} {Networks}},
	publisher = {Springer New York},
	author = {Johansson, Mikael and Takata, Naoki and Ibáñez, Cristian and Eriksson, Maria E.},
	editor = {Staiger, Dorothee},
	year = {2014},
	note = {Series Title: Methods in Molecular Biology},
	pages = {313--324},
}

@incollection{staiger_perennial_2014,
	address = {New York, NY},
	title = {The {Perennial} {Clock} {Is} an {Essential} {Timer} for {Seasonal} {Growth} {Events} and {Cold} {Hardiness}},
	volume = {1158},
	isbn = {978-1-4939-0699-4 978-1-4939-0700-7},
	url = {http://link.springer.com/10.1007/978-1-4939-0700-7_20},
	doi = {10.1007/978-1-4939-0700-7_20},
	urldate = {2021-06-08},
	booktitle = {Plant {Circadian} {Networks}},
	publisher = {Springer New York},
	author = {Johansson, Mikael and Ibáñez, Cristian and Takata, Naoki and Eriksson, Maria E.},
	editor = {Staiger, Dorothee},
	year = {2014},
	note = {Series Title: Methods in Molecular Biology},
	pages = {297--311},
}

@article{takata_simple_2012,
	title = {A simple and efficient transient transformation for hybrid aspen ({Populus} tremula × {P}. tremuloides)},
	volume = {8},
	issn = {1746-4811},
	url = {http://plantmethods.biomedcentral.com/articles/10.1186/1746-4811-8-30},
	doi = {10/f236z7},
	language = {en},
	number = {1},
	urldate = {2021-06-08},
	journal = {Plant Methods},
	author = {Takata, Naoki and Eriksson, Maria E.},
	year = {2012},
	pages = {30},
}

@article{cooke_dynamic_2012,
	title = {The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms: {Bud} dormancy in trees},
	volume = {35},
	issn = {01407791},
	shorttitle = {The dynamic nature of bud dormancy in trees},
	url = {http://doi.wiley.com/10.1111/j.1365-3040.2012.02552.x},
	doi = {10/f22v73},
	language = {en},
	number = {10},
	urldate = {2021-06-08},
	journal = {Plant, Cell \& Environment},
	author = {Cooke, Janice E. K. and Eriksson, Maria E. and Junttila, Olavi},
	month = oct,
	year = {2012},
	pages = {1707--1728},
}

@article{ashelford_full_2011,
	title = {Full genome re-sequencing reveals a novel circadian clock mutation in {Arabidopsis}},
	volume = {12},
	issn = {1465-6906},
	url = {http://genomebiology.biomedcentral.com/articles/10.1186/gb-2011-12-3-r28},
	doi = {10/dzpfvk},
	language = {en},
	number = {3},
	urldate = {2021-06-08},
	journal = {Genome Biology},
	author = {Ashelford, Kevin and Eriksson, Maria E. and Allen, Christopher M and D'Amore, Rosalinda and Johansson, Mikael and Gould, Peter and Kay, Suzanne and Millar, Andrew J and Hall, Neil and Hall, Anthony},
	year = {2011},
	pages = {R28},
}

@article{johansson_partners_2011,
	title = {Partners in {Time}: {EARLY} {BIRD} {Associates} with {ZEITLUPE} and {Regulates} the {Speed} of the {Arabidopsis} {Clock}},
	volume = {155},
	issn = {1532-2548},
	shorttitle = {Partners in {Time}},
	url = {https://academic.oup.com/plphys/article/155/4/2108/6108867},
	doi = {10/bgh2rc},
	abstract = {Abstract
            The circadian clock of the model plant Arabidopsis (Arabidopsis thaliana) is made up of a complex series of interacting feedback loops whereby proteins regulate their own expression across day and night. early bird (ebi) is a circadian mutation that causes the clock to speed up: ebi plants have short circadian periods, early phase of clock gene expression, and are early flowering. We show that EBI associates with ZEITLUPE (ZTL), known to act in the plant clock as a posttranslational mediator of protein degradation. However, EBI is not degraded by its interaction with ZTL. Instead, ZTL counteracts the effect of EBI during the day and increases it at night, modulating the expression of key circadian components. The partnership of EBI with ZTL reveals a novel mechanism involved in controlling the complex transcription-translation feedback loops of the clock. This work highlights the importance of cross talk between the ubiquitination pathway and transcriptional control for regulation of the plant clock.},
	language = {en},
	number = {4},
	urldate = {2021-06-08},
	journal = {Plant Physiology},
	author = {Johansson, Mikael and McWatters, Harriet G. and Bakó, László and Takata, Naoki and Gyula, Péter and Hall, Anthony and Somers, David E. and Millar, Andrew J. and Eriksson, Maria E.},
	month = mar,
	year = {2011},
	pages = {2108--2122},
}

Abstract The circadian clock of the model plant Arabidopsis (Arabidopsis thaliana) is made up of a complex series of interacting feedback loops whereby proteins regulate their own expression across day and night. early bird (ebi) is a circadian mutation that causes the clock to speed up: ebi plants have short circadian periods, early phase of clock gene expression, and are early flowering. We show that EBI associates with ZEITLUPE (ZTL), known to act in the plant clock as a posttranslational mediator of protein degradation. However, EBI is not degraded by its interaction with ZTL. Instead, ZTL counteracts the effect of EBI during the day and increases it at night, modulating the expression of key circadian components. The partnership of EBI with ZTL reveals a novel mechanism involved in controlling the complex transcription-translation feedback loops of the clock. This work highlights the importance of cross talk between the ubiquitination pathway and transcriptional control for regulation of the plant clock.

@article{eriksson_plant_2011,
	title = {Plant cell responses to cold are all about timing},
	volume = {14},
	issn = {13695266},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S1369526611001282},
	doi = {10/bwjm2f},
	language = {en},
	number = {6},
	urldate = {2021-06-08},
	journal = {Current Opinion in Plant Biology},
	author = {Eriksson, Maria E. and Webb, Alex AR},
	month = dec,
	year = {2011},
	pages = {731--737},
}

@article{kozarewa_alteration_2010,
	title = {Alteration of {PHYA} expression change circadian rhythms and timing of bud set in {Populus}},
	volume = {73},
	issn = {0167-4412, 1573-5028},
	url = {http://link.springer.com/10.1007/s11103-010-9619-2},
	doi = {10/dp553q},
	language = {en},
	number = {1-2},
	urldate = {2021-06-08},
	journal = {Plant Molecular Biology},
	author = {Kozarewa, Iwanka and Ibáñez, Cristian and Johansson, Mikael and Ögren, Erling and Mozley, David and Nylander, Eva and Chono, Makiko and Moritz, Thomas and Eriksson, Maria E.},
	month = may,
	year = {2010},
	pages = {143--156},
}

@article{hoffman_changes_2010,
	title = {Changes in diurnal patterns within the {Populus} transcriptome and metabolome in response to photoperiod variation},
	volume = {33},
	issn = {1365-3040},
	doi = {10/d2xk8m},
	abstract = {Changes in seasonal photoperiod provides an important environmental signal that affects the timing of winter dormancy in perennial, deciduous, temperate tree species, such as hybrid aspen (Populus tremula x Populus tremuloides). In this species, growth cessation, cold acclimation and dormancy are induced in the autumn by the detection of day-length shortening that occurs at a given critical day length. Important components in the detection of such day-length changes are photoreceptors and the circadian clock, and many plant responses at both the gene regulation and metabolite levels are expected to be diurnal. To directly examine this expectation and study components in these events, here we report transcriptomic and metabolomic responses to a change in photoperiod from long to short days in hybrid aspen. We found about 16\% of genes represented on the arrays to be diurnally regulated, as assessed by our pre-defined criteria. Furthermore, several of these genes were involved in circadian-associated processes, including photosynthesis and primary and secondary metabolism. Metabolites affected by the change in photoperiod were mostly involved in carbon metabolism. Taken together, we have thus established a molecular catalog of events that precede a response to winter.},
	language = {eng},
	number = {8},
	journal = {Plant, Cell \& Environment},
	author = {Hoffman, Daniel E. and Jonsson, Pär and Bylesjö, Max and Trygg, Johan and Antti, Henrik and Eriksson, Maria E. and Moritz, Thomas},
	month = aug,
	year = {2010},
	keywords = {Carbohydrate Metabolism, Circadian Rhythm, DNA, Complementary, Gene Expression Profiling, Gene Expression Regulation, Plant, Genes, Plant, Metabolome, Oligonucleotide Array Sequence Analysis, Photoperiod, Populus, Seasons},
	pages = {1298--1313},
}

Changes in seasonal photoperiod provides an important environmental signal that affects the timing of winter dormancy in perennial, deciduous, temperate tree species, such as hybrid aspen (Populus tremula x Populus tremuloides). In this species, growth cessation, cold acclimation and dormancy are induced in the autumn by the detection of day-length shortening that occurs at a given critical day length. Important components in the detection of such day-length changes are photoreceptors and the circadian clock, and many plant responses at both the gene regulation and metabolite levels are expected to be diurnal. To directly examine this expectation and study components in these events, here we report transcriptomic and metabolomic responses to a change in photoperiod from long to short days in hybrid aspen. We found about 16% of genes represented on the arrays to be diurnally regulated, as assessed by our pre-defined criteria. Furthermore, several of these genes were involved in circadian-associated processes, including photosynthesis and primary and secondary metabolism. Metabolites affected by the change in photoperiod were mostly involved in carbon metabolism. Taken together, we have thus established a molecular catalog of events that precede a response to winter.

@article{ibanez_circadian_2010,
	title = {Circadian {Clock} {Components} {Regulate} {Entry} and {Affect} {Exit} of {Seasonal} {Dormancy} as {Well} as {Winter} {Hardiness} in \textit{{Populus}} {Trees}},
	volume = {153},
	issn = {1532-2548},
	url = {https://academic.oup.com/plphys/article/153/4/1823/6111276},
	doi = {10/dzmr76},
	abstract = {Abstract
            This study addresses the role of the circadian clock in the seasonal growth cycle of trees: growth cessation, bud set, freezing tolerance, and bud burst. Populus tremula × Populus tremuloides (Ptt) LATE ELONGATED HYPOCOTYL1 (PttLHY1), PttLHY2, and TIMING OF CAB EXPRESSION1 constitute regulatory clock components because down-regulation by RNA interference of these genes leads to altered phase and period of clock-controlled gene expression as compared to the wild type. Also, both RNA interference lines show about 1-h-shorter critical daylength for growth cessation as compared to the wild type, extending their period of growth. During winter dormancy, when the diurnal variation in clock gene expression stops altogether, down-regulation of PttLHY1 and PttLHY2 expression compromises freezing tolerance and the expression of C-REPEAT BINDING FACTOR1, suggesting a role of these genes in cold hardiness. Moreover, down-regulation of PttLHY1 and PttLHY2 causes a delay in bud burst. This evidence shows that in addition to a role in daylength-controlled processes, PttLHY plays a role in the temperature-dependent processes of dormancy in Populus such as cold hardiness and bud burst.},
	language = {en},
	number = {4},
	urldate = {2021-06-08},
	journal = {Plant Physiology},
	author = {IbÁñez, Cristian and Kozarewa, Iwanka and Johansson, Mikael and Ögren, Erling and Rohde, Antje and Eriksson, Maria E.},
	month = aug,
	year = {2010},
	pages = {1823--1833},
}

Abstract This study addresses the role of the circadian clock in the seasonal growth cycle of trees: growth cessation, bud set, freezing tolerance, and bud burst. Populus tremula × Populus tremuloides (Ptt) LATE ELONGATED HYPOCOTYL1 (PttLHY1), PttLHY2, and TIMING OF CAB EXPRESSION1 constitute regulatory clock components because down-regulation by RNA interference of these genes leads to altered phase and period of clock-controlled gene expression as compared to the wild type. Also, both RNA interference lines show about 1-h-shorter critical daylength for growth cessation as compared to the wild type, extending their period of growth. During winter dormancy, when the diurnal variation in clock gene expression stops altogether, down-regulation of PttLHY1 and PttLHY2 expression compromises freezing tolerance and the expression of C-REPEAT BINDING FACTOR1, suggesting a role of these genes in cold hardiness. Moreover, down-regulation of PttLHY1 and PttLHY2 causes a delay in bud burst. This evidence shows that in addition to a role in daylength-controlled processes, PttLHY plays a role in the temperature-dependent processes of dormancy in Populus such as cold hardiness and bud burst.

@incollection{mcwatters_plant_2007,
	title = {Plant {Circadian} {Rhythms}},
	copyright = {Copyright © 2007 John Wiley \& Sons, Ltd. All rights reserved.},
	isbn = {978-0-470-01590-2},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1002/9780470015902.a0020113},
	doi = {10.1002/9780470015902.a0020113},
	abstract = {Circadian clocks are found in most eukaryotic organisms. By allowing anticipation of daily and seasonal changes they enable coordination of metabolism and life cycle with the natural rhythms of the environment. Plant circadian rhythms are generated by a series of interlocking feedback loops of ribonucleic acid (RNA) and protein expression that respond to environmental cycles of light and temperature. They control essential processes in the plant's development, such as the transition to flowering or growth cessation.},
	language = {en},
	urldate = {2021-06-10},
	booktitle = {{eLS}},
	publisher = {American Cancer Society},
	author = {McWatters, Harriet G. and Eriksson, Maria E.},
	year = {2007},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/9780470015902.a0020113},
	keywords = {Arabidopsis thaliana, Populus, bud set, circadian clock, entrainment, photoperiodism},
}

Circadian clocks are found in most eukaryotic organisms. By allowing anticipation of daily and seasonal changes they enable coordination of metabolism and life cycle with the natural rhythms of the environment. Plant circadian rhythms are generated by a series of interlocking feedback loops of ribonucleic acid (RNA) and protein expression that respond to environmental cycles of light and temperature. They control essential processes in the plant's development, such as the transition to flowering or growth cessation.

@article{kevei_forward_2006,
	title = {Forward genetic analysis of the circadian clock separates the multiple functions of {ZEITLUPE}},
	volume = {140},
	issn = {0032-0889},
	doi = {10/bx2pxd},
	abstract = {The circadian system of Arabidopsis ( Arabidopsis thaliana) includes feedback loops of gene regulation that generate 24-h oscillations. Components of these loops remain to be identified; none of the known components is completely understood, including ZEITLUPE (ZTL), a gene implicated in regulated protein degradation. ztl mutations affect both circadian and developmental responses to red light, possibly through ZTL interaction with PHYTOCHROME B (PHYB). We conducted a large-scale genetic screen that identified additional clock-affecting loci. Other mutants recovered include 11 new ztl alleles encompassing mutations in each of the ZTL protein domains. Each mutation lengthened the circadian period, even in darkgrown seedlings entrained to temperature cycles. A mutation of the LIGHT, OXYGEN, VOLTAGE (LOV)/Period-ARNT-Sim ( PAS) domain was unique in retaining wild-type responses to red light both for the circadian period and for control of hypocotyl elongation. This uncoupling of ztl phenotypes indicates that interactions of ZTL protein with multiple factors must be disrupted to generate the full ztl mutant phenotype. Protein interaction assays showed that the ztl mutant phenotypes were not fully explained by impaired interactions with previously described partner proteins Arabidopsis S-phase kinase-related protein 1, TIMING OF CAB EXPRESSION 1, and PHYB. Interaction with PHYB was unaffected by mutation of any ZTL domain. Mutation of the kelch repeat domain affected protein binding at both the LOV/PAS and the F-box domains, indicating that interaction among ZTL domains leads to the strong phenotypes of kelch mutations. Forward genetics continues to provide insight regarding both known and newly discovered components of the circadian system, although current approaches have saturated mutations at some loci.},
	language = {English},
	number = {3},
	journal = {Plant Physiology},
	publisher = {Amer Soc Plant Biologists},
	author = {Kevei, E. and Gyula, P. and Hall, A. and Kozma-Bognar, L. and Kim, W. Y. and Eriksson, M. E. and Toth, R. and Hanano, S. and Feher, B. and Southern, M. M. and Bastow, R. M. and Viczian, A. and Hibberd, V. and Davis, S. J. and Somers, D. E. and Nagy, F. and Millar, A. J.},
	month = mar,
	year = {2006},
	note = {Place: Rockville
WOS:000235868900013},
	keywords = {arabidopsis-thaliana, degradation, encodes, flowering time, light, photoreceptors, phytochrome interacting factor-3, protein, rhythms, system},
	pages = {933--945},
}

The circadian system of Arabidopsis ( Arabidopsis thaliana) includes feedback loops of gene regulation that generate 24-h oscillations. Components of these loops remain to be identified; none of the known components is completely understood, including ZEITLUPE (ZTL), a gene implicated in regulated protein degradation. ztl mutations affect both circadian and developmental responses to red light, possibly through ZTL interaction with PHYTOCHROME B (PHYB). We conducted a large-scale genetic screen that identified additional clock-affecting loci. Other mutants recovered include 11 new ztl alleles encompassing mutations in each of the ZTL protein domains. Each mutation lengthened the circadian period, even in darkgrown seedlings entrained to temperature cycles. A mutation of the LIGHT, OXYGEN, VOLTAGE (LOV)/Period-ARNT-Sim ( PAS) domain was unique in retaining wild-type responses to red light both for the circadian period and for control of hypocotyl elongation. This uncoupling of ztl phenotypes indicates that interactions of ZTL protein with multiple factors must be disrupted to generate the full ztl mutant phenotype. Protein interaction assays showed that the ztl mutant phenotypes were not fully explained by impaired interactions with previously described partner proteins Arabidopsis S-phase kinase-related protein 1, TIMING OF CAB EXPRESSION 1, and PHYB. Interaction with PHYB was unaffected by mutation of any ZTL domain. Mutation of the kelch repeat domain affected protein binding at both the LOV/PAS and the F-box domains, indicating that interaction among ZTL domains leads to the strong phenotypes of kelch mutations. Forward genetics continues to provide insight regarding both known and newly discovered components of the circadian system, although current approaches have saturated mutations at some loci.

@article{israelsson_changes_2003,
	title = {Changes in gene expression in the wood-forming tissue of transgenic hybrid aspen with increased secondary growth},
	volume = {52},
	issn = {1573-5028},
	url = {https://doi.org/10.1023/A:1025097410445},
	doi = {10/b7zwj2},
	abstract = {Transgenic lines of hybrid aspen with elevated levels of gibberellin (GA) show greatly increased numbers of xylem fibres and increases in xylem fibre length. These plants therefore provide excellent models for studying secondary growth. We have used cDNA microarry analysis to investigate how gene transcription in the developing xylem is affected by GA-induced growth. A recent investigation has shown that genes encoding lignin and cellulose biosynthetic enzymes, as well as a number of transcription factors and other potential regulators of xylogenesis, are under developmental-stage-specific transcriptional control. The present study shows that the highest transcript changes in our transgenic trees occurs in genes generally restricted to the early stages of xylogenesis, including cell division, early expansion and late expansion. The results reveal genes among those arrayed that are up-regulated with an increased xylem production, thus indicating key components in the production of wood.},
	language = {en},
	number = {4},
	urldate = {2022-03-11},
	journal = {Plant Molecular Biology},
	author = {Israelsson, Maria and Eriksson, Maria E. and Hertzberg, Magnus and Aspeborg, Henrik and Nilsson, Peter and Moritz, Thomas},
	month = jul,
	year = {2003},
	pages = {893--903},
}

Transgenic lines of hybrid aspen with elevated levels of gibberellin (GA) show greatly increased numbers of xylem fibres and increases in xylem fibre length. These plants therefore provide excellent models for studying secondary growth. We have used cDNA microarry analysis to investigate how gene transcription in the developing xylem is affected by GA-induced growth. A recent investigation has shown that genes encoding lignin and cellulose biosynthetic enzymes, as well as a number of transcription factors and other potential regulators of xylogenesis, are under developmental-stage-specific transcriptional control. The present study shows that the highest transcript changes in our transgenic trees occurs in genes generally restricted to the early stages of xylogenesis, including cell division, early expansion and late expansion. The results reveal genes among those arrayed that are up-regulated with an increased xylem production, thus indicating key components in the production of wood.

@article{eriksson_daylength_2002,
	title = {Daylength and spatial expression of a gibberellin 20-oxidase isolated from hybrid aspen ({Populus} tremula {L}. × {P}. tremuloides {Michx}.)},
	volume = {214},
	issn = {1432-2048},
	url = {https://doi.org/10.1007/s00425-001-0703-3},
	doi = {10/bn4z3p},
	abstract = {Physiologically active gibberellins (GAs) are key regulators of shoot growth in trees. To investigate this mechanism of GA-controlled growth in hybrid aspen, we cloned cDNAs encoding gibberellin 20-oxidase (GA 20-oxidase), a key, highly regulated enzyme in the biosynthesis of GAs. Clones were isolated from leaf and cambium cDNA libraries using probes generated by polymerase chain reaction, based on conserved domains of GA 20-oxidases. Upon expression in Escherichia coli, the GST-fusion protein was shown to oxidise GA12 as well as oxidising the 13-hydroxylated substrate GA53, successively to GA9 and GA20, respectively. The gene PttGA20ox1 was expressed in meristematic cells and growing tissues such as expanding internodes, leaves and roots. The expression was negatively regulated by both GA4 and overexpression of phytochrome A. RNA analysis also showed that the expression was down-regulated in late-expanding leaf tissue in response to short days (SDs). Actively growing tissues such as early elongating internodes, petioles and leaf blades had the highest levels of C19-GAs. Upon transfer to SDs an accumulation of GA19 was observed in early elongating internodes and leaf blades. The levels of C19-GAs were also to some extent changed upon transfer to SDs. The levels of GA20 were down-regulated in internodes, and those of GA1 were significantly reduced in early expanding leaf blades. In roots the metabolites GA19 and GA8 decreased upon shifts to SDs, while GA20 accumulated slightly. The down-regulation of GA 20-oxidase activity in response to SDs was further indicated by studies of [14C]GA12 metabolism in shoots, demonstrating that the substrate for GA 20-oxidase, [14C]GA53, accumulates in SDs.},
	language = {en},
	number = {6},
	urldate = {2021-10-19},
	journal = {Planta},
	author = {Eriksson, Maria E. and Moritz, Thomas},
	month = apr,
	year = {2002},
	pages = {920--930},
}

Physiologically active gibberellins (GAs) are key regulators of shoot growth in trees. To investigate this mechanism of GA-controlled growth in hybrid aspen, we cloned cDNAs encoding gibberellin 20-oxidase (GA 20-oxidase), a key, highly regulated enzyme in the biosynthesis of GAs. Clones were isolated from leaf and cambium cDNA libraries using probes generated by polymerase chain reaction, based on conserved domains of GA 20-oxidases. Upon expression in Escherichia coli, the GST-fusion protein was shown to oxidise GA12 as well as oxidising the 13-hydroxylated substrate GA53, successively to GA9 and GA20, respectively. The gene PttGA20ox1 was expressed in meristematic cells and growing tissues such as expanding internodes, leaves and roots. The expression was negatively regulated by both GA4 and overexpression of phytochrome A. RNA analysis also showed that the expression was down-regulated in late-expanding leaf tissue in response to short days (SDs). Actively growing tissues such as early elongating internodes, petioles and leaf blades had the highest levels of C19-GAs. Upon transfer to SDs an accumulation of GA19 was observed in early elongating internodes and leaf blades. The levels of C19-GAs were also to some extent changed upon transfer to SDs. The levels of GA20 were down-regulated in internodes, and those of GA1 were significantly reduced in early expanding leaf blades. In roots the metabolites GA19 and GA8 decreased upon shifts to SDs, while GA20 accumulated slightly. The down-regulation of GA 20-oxidase activity in response to SDs was further indicated by studies of [14C]GA12 metabolism in shoots, demonstrating that the substrate for GA 20-oxidase, [14C]GA53, accumulates in SDs.

@article{eriksson_increased_2000,
	title = {Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length},
	volume = {18},
	copyright = {2000 Nature America Inc.},
	issn = {1546-1696},
	url = {https://www.nature.com/articles/nbt0700_784},
	doi = {10.1038/77355},
	abstract = {In most tree-breeding programs worldwide, increasing the trees' growth rates and stem volumes and shortening their rotation times are important aims. Such trees would yield more biomass per unit area. Here we show that overexpressing a key regulatory gene in the biosynthesis of the plant hormone gibberellin (GA) in hybrid aspen (Populus tremula × P. tremuloides) improves growth rate and biomass. In addition, these transgenic trees have more numerous and longer xylem fibers than unmodified wild-type (wt) plants. Long fibers are desirable in the production of strong paper, but it has not as yet proved possible to influence this trait by traditional breeding techniques. We also show that GA has an antagonistic effect on root initiation, as the transgenic lines showed poorer rooting than the control plants when potted in soil. However, the negative effect on rooting efficiencies in the initial establishment of young plantlets in the growth chamber did not significantly affect root growth at later stages.},
	language = {en},
	number = {7},
	urldate = {2021-11-08},
	journal = {Nature Biotechnology},
	publisher = {Nature Publishing Group},
	author = {Eriksson, Maria E. and Israelsson, Maria and Olsson, Olof and Moritz, Thomas},
	month = jul,
	year = {2000},
	note = {Bandiera\_abtest: a
Cg\_type: Nature Research Journals
Number: 7
Primary\_atype: Research},
	keywords = {Agriculture, Bioinformatics, Biomedical Engineering/Biotechnology, Biomedicine, Biotechnology, Life Sciences, general},
	pages = {784--788},
}

In most tree-breeding programs worldwide, increasing the trees' growth rates and stem volumes and shortening their rotation times are important aims. Such trees would yield more biomass per unit area. Here we show that overexpressing a key regulatory gene in the biosynthesis of the plant hormone gibberellin (GA) in hybrid aspen (Populus tremula × P. tremuloides) improves growth rate and biomass. In addition, these transgenic trees have more numerous and longer xylem fibers than unmodified wild-type (wt) plants. Long fibers are desirable in the production of strong paper, but it has not as yet proved possible to influence this trait by traditional breeding techniques. We also show that GA has an antagonistic effect on root initiation, as the transgenic lines showed poorer rooting than the control plants when potted in soil. However, the negative effect on rooting efficiencies in the initial establishment of young plantlets in the growth chamber did not significantly affect root growth at later stages.

@article{olsen_ectopic_1997,
	title = {Ectopic expression of oat phytochrome {A} in hybrid aspen changes critical daylength for growth and prevents cold acclimatization},
	volume = {12},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1046/j.1365-313x.1997.12061339.x},
	doi = {10/c5z6sf},
	abstract = {Survival of temperate-zone tree species under the normal summer-winter cycle is dependent on proper timing of apical growth cessation and cold acclimatization. This timing is primarily based on the perception of daylength, and through evolution many tree species have developed photoperiodic ecotypes which are closely adapted to the local light conditions. The longest photoperiod inducing growth cessation, the critical photoperiod, is inherited as a quantitative character. The phytochrome pigment family is the probable receptor of daylength, but the exact role of phytochrome and the physiological basis for the different responses between photoperiodic ecotypes are not known. This report shows for the first time that over-expression of the oat phytochrome A gene (PHYA) in a tree significantly changes the critical daylength and effectively prevents cold acclimatization. While the critical daylength for elongation growth in the wild-type of hybrid aspen (Populus tremula × tremuloides) was approximately 15 h, transgenic lines with a strong expression of the oat PHYA gene did not stop growing even under a photoperiod of 6 h. Quantitative analysis of gibberellins (GA) as well as indole-3-acetic acid (IAA) revealed that levels of these were not down-regulated under short days in the transgenic plants expressing high levels of oat PHYA, as in the wild-type. These results indicate that photoperiodic responses in trees might be regulated by the amount of PHYA gene expressed in the plants, and that the amount of phytochrome A (phyA) affects the metabolism of GAs and IAA.},
	language = {en},
	number = {6},
	urldate = {2022-03-11},
	journal = {The Plant Journal},
	author = {Olsen, Jorunn E. and Junttila, Olavi and Nilsen, Jarle and Eriksson, Maria E. and Martinussen, Inger and Olsson, Olof and Sandberg, Göran and Moritz, Thomas},
	year = {1997},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-313x.1997.12061339.x},
	pages = {1339--1350},
}

Survival of temperate-zone tree species under the normal summer-winter cycle is dependent on proper timing of apical growth cessation and cold acclimatization. This timing is primarily based on the perception of daylength, and through evolution many tree species have developed photoperiodic ecotypes which are closely adapted to the local light conditions. The longest photoperiod inducing growth cessation, the critical photoperiod, is inherited as a quantitative character. The phytochrome pigment family is the probable receptor of daylength, but the exact role of phytochrome and the physiological basis for the different responses between photoperiodic ecotypes are not known. This report shows for the first time that over-expression of the oat phytochrome A gene (PHYA) in a tree significantly changes the critical daylength and effectively prevents cold acclimatization. While the critical daylength for elongation growth in the wild-type of hybrid aspen (Populus tremula × tremuloides) was approximately 15 h, transgenic lines with a strong expression of the oat PHYA gene did not stop growing even under a photoperiod of 6 h. Quantitative analysis of gibberellins (GA) as well as indole-3-acetic acid (IAA) revealed that levels of these were not down-regulated under short days in the transgenic plants expressing high levels of oat PHYA, as in the wild-type. These results indicate that photoperiodic responses in trees might be regulated by the amount of PHYA gene expressed in the plants, and that the amount of phytochrome A (phyA) affects the metabolism of GAs and IAA.