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Plant secondary growth derives from the meristematic activity of the vascular cambium. In Arabidopsis thaliana, cell divisions in the cambium are regulated by the transcription factor WOX4, a key target of the CLAVATA3 (CLV3)/EMBRYO SURROUNDING REGION (ESR)-RELATED 41 (CLE41) signaling pathway. However, function of the WOX4-like genes in plants that are dependent on a much more prolific secondary growth, such as trees, remains unclear. Here, we investigate the role of WOX4 and CLE41 homologs for stem secondary growth in Populus trees. In Populus, PttWOX4 genes are specifically expressed in the cambial region during vegetative growth, but not after growth cessation and during dormancy, possibly involving a regulation by auxin. In PttWOX4a/b RNAi trees, primary growth was not affected whereas the width of the vascular cambium was severely reduced and secondary growth was greatly diminished. Our data show that in Populus trees, PttWOX4 genes control cell division activity in the vascular cambium, and hence growth in stem girth. This activity involves the positive regulation of PttWOX4a/b through PttCLE41-related genes. Finally, expression profiling suggests that the CLE41 signaling pathway is an evolutionarily conserved program for the regulation of vascular cambium activity between angiosperm and gymnosperm tree species.

• The seasonally synchronized annual growth cycle that is regulated mainly by photoperiod and temperature cues is a crucial adaptive strategy for perennial plants in boreal and temperate ecosystems. • Phytochrome B (phyB), as a light and thermal sensor, has been extensively studied in Arabidopsis. However, the specific mechanisms for how the phytochrome photoreceptors control the phenology in tree species remain poorly understood. • We characterized the functions of PHYB genes and their downstream PHYTOCHROME INTERACTING FACTOR (PIF) targets in the regulation of shade avoidance and seasonal growth in hybrid aspen trees. We show that while phyB1 and phyB2, as phyB in other plants, act as suppressors of shoot elongation during vegetative growth, they act as promoters of tree seasonal growth. Furthermore, while the Populus homologs of both PIF4 and PIF8 are involved in the shade avoidance syndrome (SAS), only PIF8 plays a major role as a suppressor of seasonal growth. • Our data suggest that the PHYB-PIF8 regulon controls seasonal growth through the regulation of FT and CENL1 expression while a genome-wide transcriptome analysis suggests how, in Populus trees, phyB coordinately regulates SAS responses and seasonal growth cessation.

Both light and temperature have dramatic effects on plant development. Phytochrome photoreceptors regulate plant responses to the environment in large part by controlling the abundance of PHYTOCHROME INTERACTING FACTOR (PIF) transcription factors. However, the molecular determinants of this essential signaling mechanism still remain largely unknown. Here, we present evidence that the BLADE-ON-PETIOLE (BOP) genes, which have previously been shown to control leaf and flower development in Arabidopsis, are involved in controlling the abundance of PIF4. Genetic analysis shows that BOP2 promotes photo-morphogenesis and modulates thermomorphogenesis by suppressing PIF4 activity, through a reduction in PIF4 protein level. In red-light-grown seedlings PIF4 ubiquitination was reduced in the bop2 mutant. Moreover, we found that BOP proteins physically interact with both PIF4 and CULLIN3A and that a CULLIN3-BOP2 complex ubiquitinates PIF4 in vitro. This shows that BOP proteins act as substrate adaptors in a CUL3BOP1/BOP2 E3 ubiquitin ligase complex, targeting PIF4 proteins for ubiquitination and subsequent degradation.

Plants time flowering through temperature-sensing mechanisms involving differential RNA abundance, alternative splicing, and protein stability. [Also see Report by Lee et al. ] Temperature is one of the most important cues that plants use to flower at the right time of the year—a process crucial for adaptation and reproductive success. We live in a world where climate change is already affecting our everyday lives and where, in the not too distant future, we will likely face huge challenges associated with increasing global temperatures ( 1 ). One of these challenges is to understand how flowering and growth of agricultural crops and trees will be affected by changing temperatures. The report by Lee et al. on page 628 of this issue ( 2 ), together with a recently published paper by Posé et al. ( 3 ), provide insight into the basic mechanisms controlling temperature regulation of plant growth and development.

Trees represent the largest terrestrial carbon sink and a renewable source of ligno-cellulose. There is significant scope for yield and quality improvement in these largely undomesticated species, and efforts to engineer elite varieties will benefit from improved understanding of the transcriptional network underlying cambial growth and wood formation. We generated highspatial- resolution RNA sequencing data spanning the secondary phloem, vascular cambium, and wood-forming tissues of Populus tremula. The transcriptome comprised 28,294 expressed, annotated genes, 78 novel protein-coding genes, and 567 putative long intergenic noncoding RNAs. Most paralogs originating from the Salicaceae whole-genome duplication had diverged expression, with the exception of those highly expressed during secondary cell wall deposition. Coexpression network analyses revealed that regulation of the transcriptome underlying cambial growth and wood formation comprises numerous modules forming a continuum of active processes across the tissues. A comparative analysis revealed that a majority of these modules are conserved in Picea abies. The high spatial resolution of our data enabled identification of novel roles for characterized genes involved in xylan and cellulose biosynthesis, regulators of xylem vessel and fiber differentiation and lignification. An associated web resource (AspWood, http://aspwood.popgenie.org) provides interactive tools for exploring the expression profiles and coexpression network.

Background Spliceosomes are large evolutionary conserved ribonucleoprotein complexes containing at their core heptameric rings of Sm (or LSm) proteins and U-rich snRNAs. The role of Sm proteins in animal development is well established, and recent research has begun to link mutations in these genes to growth defects in plants. One of the most studied Sm genes is SmE1/PCP , mutants of which display a temperature-dependent phenotype in Arabidopsis thaliana. Results This study provides a first glimpse into the function of a core splicing protein in the regulation of growth in a perennial species. Phylogenetic analysis identified two paralogous SmE genes in poplar, named SmEa and SmEb , that encode identical proteins and are orthologs of SmEs from Arabidopsis , as suggested by Y2H and in vivo experiments. CRISPR/Cas9 mutagenesis in hybrid aspen identified a role for SmEs in development in plants grown in an environment simulating seasonal photoperiod and temperature changes. Unlike in Arabidopsis, low temperatures had no or only a very minor effect on the development of sme mutants in aspen. Conclusions We identified specific aspects of SmE in poplar, highlighting the importance of examining the physiological and evolutionary differences that define this gene family in woody compared to herbaceous plants.

Plants that live at high latitudes and altitudes must adapt to growth in cold environments. Trees survive freezing winter conditions by ceasing growth and forming protective winter buds at the end of the growing season. To optimize growth and adaptation, the timing of growth cessation and bud set is critical. Like the well-studied Populus species (poplars, aspens, cottonwoods), many trees respond to the shortening photoperiods of fall to induce growth cessation. Temperature also has a role in this process, but the mechanism is unknown. Here, we show that the PHYTOCHROME B ( PHYB )- PHYTOCHROME INTERACTING FACTOR4 ( PIF4 ) module controls the interplay between photoperiod cues and temperature to prevent premature growth cessation and bud set at cooler temperatures. PHYB is essential for the ability of aspen trees to maintain growth under lower temperatures in permissive long days. This is mediated through PIF4, which promotes growth cessation, specifically in response to low temperatures rather than to changes in photoperiod. PIF4 can directly bind to the promoter region of the vegetative growth marker gene FLOWERING LOCUS T2 ( FT2 ). In contrast to annual plants, it does so to suppress its transcription. Furthermore, lower temperatures can suppress PIF4 function at the transcriptional and protein levels to prevent premature growth cessation. These data show how poplar trees balance the antagonistic roles of PHYB and PIF4 to optimise the timing of growth cessation and bud set in cold environments, and this has been achieved with contrasting mechanisms compared to the annual plant model. Trees in cold climates, as revealed by Zhang et al., utilize the proteins PHYB and PIF4 to precisely time their winter dormancy, allowing them to grow under fluctuating temperatures without ceasing growth too early. This unique adaptation enhances forest resilience in a changing climate by optimizing seasonal growth and minimizing frost damage.

The maintenance of variation (i.e., different phenotypes) for heritable traits that are under selection, despite expectations of selection eroding variation and favouring only the fittest phenotype, represents an evolutionary paradox. Here, we studied variation in life‐history traits in five populations of colour polymorphic tawny owls (Strix aluco) across Europe that have been individually studied for 13 years. Tawny owls show heritable plumage colour variation ranging from less pigmented (grey) to more heavily pigmented (brown‐red). The breeding life span (BLS), lifetime egg production (LEP), lifetime reproductive success (LRS) and the number of years skipped between breeding attempts (NYS) varied between the study populations, with LEP and LRS varying across colour morphs in a population‐specific fashion. Thus, grey tawny owl females have higher lifetime fledgling and egg production than brown‐red females in some populations, but vice versa in others. Hence, our findings demonstrate disruptive selection of tawny owl plumage colourations across their European range, which may be one factor maintaining variation in heritable tawny owl colourations. Wide geographical‐scale investigation of life‐history among different tawny owl plumage colour phenotypes across Europe. Our findings highlight the complexity of reproductive strategies between different populations and within single populations over large spatial scales, suggesting that factors influencing eggs and fledglings production vary across different regions.

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.

Background The initiation of growth cessation and dormancy represent critical life-history trade-offs between survival and growth and have important fitness effects in perennial plants. Such adaptive life-history traits often show strong local adaptation along environmental gradients but, despite their importance, the genetic architecture of these traits remains poorly understood. Results We integrate whole genome re-sequencing with environmental and phenotypic data from common garden experiments to investigate the genomic basis of local adaptation across a latitudinal gradient in European aspen ( Populus tremula ). A single genomic region containing the PtFT2 gene mediates local adaptation in the timing of bud set and explains 65% of the observed genetic variation in bud set. This locus is the likely target of a recent selective sweep that originated right before or during colonization of northern Scandinavia following the last glaciation. Field and greenhouse experiments confirm that variation in PtFT 2 gene expression affects the phenotypic variation in bud set that we observe in wild natural populations. Conclusions Our results reveal a major effect locus that determines the timing of bud set and that has facilitated rapid adaptation to shorter growing seasons and colder climates in European aspen. The discovery of a single locus explaining a substantial fraction of the variation in a key life-history trait is remarkable, given that such traits are generally considered to be highly polygenic. These findings provide a dramatic illustration of how loci of large-effect for adaptive traits can arise and be maintained over large geographical scales in natural populations.