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Genome-wide association studies (GWAS) have great promise for identifying the loci that contribute to adaptive variation, but the complex genetic architecture of many quantitative traits presents a substantial challenge. We measured 14 morphological and physiological traits and identified single nucleotide polymorphism (SNP)-phenotype associations in a Populus trichocarpa population distributed from California, USA to British Columbia, Canada. We used whole-genome resequencing data of 882 trees with more than 6.78 million SNPs, coupled with multitrait association to detect polymorphisms with potentially pleiotropic effects. Candidate genes were validated with functional data. Broad-sense heritability (H²) ranged from 0.30 to 0.56 for morphological traits and 0.08 to 0.36 for physiological traits. In total, 4 and 20 gene models were detected using the single-trait and multitrait association methods, respectively. Several of these associations were corroborated by additional lines of evidence, including co-expression networks, metabolite analyses, and direct confirmation of gene function through RNAi. Multitrait association identified many more significant associations than single-trait association, potentially revealing pleiotropic effects of individual genes. This approach can be particularly useful for challenging physiological traits such as water-use efficiency or complex traits such as leaf morphology, for which we were able to identify credible candidate genes by combining multitrait association with gene co-expression and co-methylation data.

How plants adapt their developmental patterns to regular seasonal changes is an important question in biology. The annual growth cycle in perennial long-lived trees is yet another example of how plants can adapt to seasonal changes. The two main signals that plants rely on to respond to seasonal changes are photoperiod and temperature, and these signals have critical roles in the temporal regulation of the annual growth cycle of trees. This review presents the latest findings to provide insight into the molecular mechanisms that underlie how photoperiodic and temperature signals regulate seasonal growth in trees. The results point to a high level of conservation in the signalling pathways that mediate photoperiodic control of seasonal growth in trees and flowering in annual plants such as arabidopsis. Furthermore, the data indicate that symplastic communication may mediate certain aspects of seasonal growth. Although considerable insight into the control of phenology in model plants such as poplar and spruce has been obtained, the future challenge is extending these studies to other, non-model trees.

Summary In the present study, PeSTZ1, a cysteine‐2/histidine‐2‐type zinc finger transcription factor, was isolated from the desert poplar, Populus euphratica, which serves as a model stress adaptation system for trees. PeSTZ1 was preferentially expressed in the young stems and was significantly up‐regulated during chilling and freezing treatments. PeSTZ1 was localized to the nucleus and bound specifically to the PeAPX2 promoter. To examine the potential functions of PeSTZ1, we overexpressed it in poplar 84K hybrids (Populus alba × Populus glandulosa), which are known to be stress‐sensitive. Upon exposure to freezing stress, transgenic poplars maintained higher photosynthetic activity and dissipated more excess light energy (in the form of heat) than wild‐type poplars. Thus, PeSTZ1 functions as a transcription activator to enhance freezing tolerance without sacrificing growth. Under freezing stress, PeSTZ1 acts upstream of ASCORBATE PEROXIDASE2 (PeAPX2) and directly regulates its expression by binding to its promoter. Activated PeAPX2 promotes cytosolic APX that scavenges reactive oxygen species (ROS) under cold stress. PeSTZ1 may operate in parallel with C‐REPEAT‐BINDING FACTORS to regulate COLD‐REGULATED gene expression. Moreover, PeSTZ1 up‐regulation reduces malondialdehyde and ROS accumulation by activating the antioxidant system. Taken together, these results suggested that overexpressing PeSTZ1 in 84K poplar enhances freezing tolerance through the modulation of ROS scavenging via the direct regulation of PeAPX2 expression.

  Background To investigate the salt tolerance of Populus talassica  ×  Populus euphratica , morphological and physiological parameters were measured on the second day after the 15th, 30th and 45th days of NaCl treatment, revealing significant effects of NaCl on growth. To further elucidate the mechanisms underlying salt tolerance, transcriptomic and metabolomic analysis were conducted under different NaCl treatments. Results The results of morphological and physiological indexes showed that under low salt treatment, P. talassica  ×  P. euphratica was able to coordinate the growth of aboveground and belowground parts. Under high salt concentration, the growth and water balance of P. talassica  ×  P. euphratica were markedly inhibited. The most significant differences between treatments were observed on the second day after the 45th day of NaCl treatment. Transcriptomic analysis showed that the pathways of gene enrichment in the roots and stems of P. talassica  ×  P. euphratica were different in the salt resistance response. And it involves several core pathways such as plant hormone signal transduction, phenylpropanoid biosynthesis, MAPK signaling pathway—plant, plant- pathogen interaction, carbon metabolism, biosynthesis of amino acids, and several key Transcription factors (TFs) such as AP2/ERF, NAC, WRKY and bZIP. Metabolomic analysis revealed that KEGG pathway enrichment analysis showed unique metabolic pathways were enriched in P. talassica  ×  P. euphratica under both 200 mM and 400 mM NaCl treatments. Additionally, while there were some differences in the metabolic pathways enriched in the roots and stems, both tissues commonly enriched pathways related to the biosynthesis of secondary metabolites, biosynthesis of cofactors, biosynthesis of amino acids, flavonoid biosynthesis, and ABC transporters. Association analysis further indicated that biosynthesis of amino acids and plant hormone signal transduction pathway play key roles in the response of P. talassica  ×  P. euphratica to salt stress. The interactions between the differentially expressed genes (DEGs) and several differentially accumulated metabolites (DAMs), especially the strong association between LOC105124002 and Jasmonoyl-L-Isoleucine (pme2074), were again revealed by the interactions analysis. Conclusions In this study, we resolved the changes of metabolic pathways in roots and stems of P. talassica  ×  P. euphratica under different NaCl treatments and explored the associations between characteristic DEGs and DAMs, which provided insights into the mechanisms of P. talassica  ×  P. euphratica in response to salt stress.

Recent findings were able to show significant variability of stomatal dynamics between species, but not much is known about factors influencing stomatal dynamics and its consequences on biomass production, transpiration and water-use efficiency (WUE). We assessed the dynamics of stomatal conductance (g(s)) to a change of irradiance or vapour-pressure deficit (VPD) in two Populus euramericana and two Populus nigra genotypes grown under control and drought conditions. Our objectives were to determine the diversity of stomatal dynamics among poplar genotypes, and if soil water deficit can alter it. Physiological and morphological factors were investigated to find their potential links with stomatal morphology, WUE and its components at the whole-plant level. We found significant genotypic variability of g(s) dynamics to both irradiance and VPD. Genotypes with faster stomatal dynamics were correlated with higher stomatal density and smaller stomata, and the implications of these correlations are discussed. Drought slowed g(s) dynamics, depending on genotype and especially during stomatal closing. This finding is contrary to previous research on more drought-tolerant species. Independently of the treatment, faster stomatal dynamics were negatively correlated with daily whole-plant transpiration, presenting new evidence of a previously hypothesized contribution of stomatal dynamics to whole-plant water use.

The effect of temperature on stomatal conductance (g s) and corresponding gas exchange parameters was studied in two tree species with contrasting leaf anatomy and ecophysiology—a broadleaf angiosperm, Populus deltoides x nigra (poplar), and a needle-leaf gymnosperm, Pinus taeda (loblolly pine). Experiments were conducted in growth chambers across a leaf temperature range of 19–48°C. Manipulations of temperature were done in well-watered and drought soil conditions and under ambient (400 ppm) and elevated (800 ppm) air CO₂ concentrations. Increases in leaf temperature caused stomatal opening at both ambient and elevated [CO₂]. The g s increased by 42% in poplar and by 40% in loblolly pine when leaf temperature increased from 30°C to 40°C at a vapour pressure difference of 1 kPa. Stomatal limitation to photosynthesis decreased in elevated temperature in loblolly pine but not in poplar. The ratio of net photosynthesis to g s depended on leaf temperature, especially at high temperatures. Evaporative cooling of transpiring leaves resulted in reductions in leaf temperature up to 9°C in well-watered poplar but only 1°C in drought-stressed poplar and in loblolly pine. As global mean temperatures rise and temperature extremes become more frequent and severe, understanding the effect of temperature on g s, and modelling that relationship, will become increasingly important.

Plants develop tolerance to drought by activating genes with altered levels of epigenetic modifications. Specific transcription factors are involved in this activation, but the molecular connections within the regulatory system are unclear. Here, we analyzed genome-wide acetylated lysine residue 9 of histone H3 (H3K9ac) enrichment and examined its association with transcriptomes in Populus trichocarpa under drought stress. We revealed that abscisic acid-Responsive Element (ABRE) motifs in promoters of the drought-responsive genes PtrNAC006, PtrNAC007, and PtrNAC120 are involved in H3K9ac enhancement and activation of these genes. Overexpressing these PtrNAC genes in P. trichocarpa resulted in strong drought-tolerance phenotypes. We showed that the ABRE binding protein PtrAREB1-2 binds to ABRE motifs associated with these PtrNAC genes and recruits the histone acetyltransferase unit ADA2b-GCN5, forming AREB1-ADA2b-GCN5 ternary protein complexes. Moreover, this recruitment enables GCN5-mediated histone acetylation to enhance H3K9ac and enrich RNA polymerase II specifically at these PtrNAC genes for the development of drought tolerance. CRISPR editing or RNA interference-mediated downregulation of any of the ternary members results in highly drought-sensitive P. trichocarpa. Thus, the combinatorial function of the ternary proteins establishes a coordinated histone acetylation and transcription factor-mediated gene activation for drought response and tolerance in Populus species.

Water deficiency is a critical environmental condition that is seriously reducing global plant production. Improved water‐use efficiency (WUE) and drought tolerance are effective strategies to address this problem. In this study, PdEPF1, a member of the EPIDERMAL PATTERNING FACTOR (EPF) family, was isolated from the fast‐growing poplar clone NE‐19 [Populus nigra × (Populus deltoides × Populus nigra)]. Significantly, higher PdEPF1 levels were detected after induction by dehydration and abscisic acid. To explore the biological functions of PdEPF1, transgenic triploid white poplars (Populus tomentosa ‘YiXianCiZhu B385’) overexpressing PdEPF1 were constructed. PdEPF1 overexpression resulted in increased water deficit tolerance and greater WUE. We confirmed that the transgenic lines with greater instantaneous WUE had approximately 30% lower transpiration but equivalent CO₂ assimilation. Lower transpiration was associated with a 28% reduction in abaxial stomatal density. PdEPF1 overexpression not only strongly enhanced WUE, but also greatly improved drought tolerance, as measured by the leaf relative water content and water potential, under limited water conditions. In addition, the growth of these oxPdEPF1 plants was less adversely affected by reduced water availability than plants with a higher stomatal density, indicating that plants with a low stomatal density may be well suited to grow in water‐scarce environments. Taken together, our data suggest that PdEPF1 improves WUE and confers drought tolerance in poplar; thus, it could be used to breed drought‐tolerant plants with increased production under conditions of water deficiency.

Background Growth-regulating factors (GRFs) are plant-specific transcription factors that control organ size. Nineteen GRF genes were identified in the Populus trichocarpa genome and one was reported to control leaf size mainly by regulating cell expansion. In this study, we further characterize the roles of the other poplar GRFs in leaf size control in a similar manner. Results The 19 poplar GRF genes were clustered into six groups according to their phylogenetic relationship with Arabidopsis GRFs. Bioinformatic analysis, degradome, and transient transcription assays showed that 18 poplar GRFs were regulated by miR396, with GRF12b the only exception. The functions of PagGRF6b ( Pag , Populus alba × P. glandulosa ), PagGRF7a , PagGRF12a , and PagGRF12b , representing three different groups, were investigated. The results show that PagGRF6b may have no function on leaf size control, while PagGRF7a functions as a negative regulator of leaf size by regulating cell expansion. By contrast, PagGRF12a and PagGRF12b may function as positive regulators of leaf size control by regulating both cell proliferation and expansion, primarily cell proliferation. Conclusions The diversity of poplar GRFs in leaf size control may facilitate the specific, coordinated regulation of poplar leaf development through fine adjustment of cell proliferation and expansion.

Annual plants grow vegetatively at early developmental stages and then transition to the reproductive stage, followed by senescence in the same year. In contrast, after successive years of vegetative growth at early ages, woody perennial shoot meristems begin repeated transitions between vegetative and reproductive growth at sexual maturity. However, it is unknown how these repeated transitions occur without a developmental conflict between vegetative and reproductive growth. We report that functionally diverged paralogs FLOWERING LOCUS T1 (FT1) and FLOWERING LOCUS T2 (FT2), products of whole-genome duplication and homologs of Arabidopsis thaliana gene FLOWERING LOCUS T (FT), coordinate the repeated cycles of vegetative and reproductive growth in woody perennial poplar (Populus spp.). Our manipulative physiological and genetic experiments coupled with field studies, expression profiling, and network analysis reveal that reproductive onset is determined by FT1 in response to winter temperatures, whereas vegetative growth and inhibition of bud set are promoted by FT2 in response to warm temperatures and long days in the growing season. The basis for functional differentiation between FT1 and FT2 appears to be expression pattern shifts, changes in proteins, and divergence in gene regulatory networks. Thus, temporal separation of reproductive onset and vegetative growth into different seasons via FT1 and FT2 provides seasonality and demonstrates the evolution of a complex perennial adaptive trait after genome duplication.