Branching out: a new era of investigating physiological processes in forest trees using genomic tools

Branching out: a new era of investigating physiological processes in forest trees using genomic... In just over a decade since the publication of the first forest tree genome—that of Populus trichocarpa (Salicaceae; Tuskan et al. 2006)—we have witnessed tremendous advances in tree physiology leveraged from forest tree genomic resources. Prepublication release of draft sequence data from the Populus genome project (Tuskan et al. 2004), together with pioneering efforts to develop expressed sequence tag (EST) resources for Populus spp. (e.g., Sterky et al. 1998, 2004) and loblolly pine (Pinus taeda, Pinaceae; Allona et al. 1998), revolutionized the way in which the forest tree community conducts physiological experiments. Indeed, an Editorial in this journal penned by Stan Wullschleger, Jerry Tuskan and Stephen DiFazio soon after the announcement of the Populus genome project was prescient in identifying innovative new avenues in which genomics would be brought to bear on forest tree physiology, from molecular to ecosystem scales (Wullschleger et al. 2002). In this Invited Issue, entitled Tree Physiology and Genomics, we bring together 12 articles that skillfully illustrate uses of an ever-expanding forest genomics toolkit to further our insight into various physiological processes. The status of P. trichocarpa as the flagship tree genome sequence is reflected in this Invited Issue, in which half of the articles use this resource and related omic tools in their investigations. The remaining articles draw from genome sequence and transcriptomic resources developed for a number of other taxa. In recent years, advances in technologies, increased access to sequencing and bioinformatics expertise and decreased costs have spurred the community to develop significant genomic and transcriptomic resources for a dizzying number of economically, ecologically and evolutionarily important forest tree species from both the Northern and Southern hemispheres. These species represent commercially important fast-growing short rotation woody crops, ecosystem-dominating species such as slow-growing conifers, threatened species and species from fragile ecosystems, as well as species occupying key positions on the tree of life. As of early 2018, the list of forest tree genome sequences comprised several eudicot species, including additional poplar species (Populus euphratica, Salicaceae; Ma et al. 2013), gum (Eucalyptus grandis, Myrtaceae; Myburg et al. 2014), willow (Salix suchowensis, Salicaceae; Dai et al. 2014), birch (Betula pendula and Betula nana, Betulaceae; Wang et al. 2013, Salojarvi et al. 2017), ash (Fraxinus excelsior, Oleaceae; Sollars et al. 2017), oak (Quercus robur, Fagaceae; Plomion et al. 2016a) and rubber tree (Hevea brasiliensis, Euphorbiaceae; Rahman et al. 2013); the basal angiosperm Amborella trichopoda (Amborellaceae; Amborella Genome Project 2013); and the even earlier diverging giga-genome conifers Norway spruce, white spruce, loblolly pine and sugar pine (Picea abies, Picea glauca, P. taeda and Pinus lambertiana, respectively, all Pinaceae; Nystedt et al. 2013, Zimin et al. 2014, Warren et al. 2015, Stevens et al. 2016). Genome sequences of several other forest tree species have been released prior to publication (e.g., Phytozome v12; Goodstein et al. 2012), and many more are on track to be publicly released and/or published in the near- and mid-term. Genome sequences are also available for a wide array of agronomically important fruit tree species (summarized in Chagné 2015 and Neale et al. 2017), which serve as important resources for comparative genomic analyses of perennial processes. Articles in this Invited Issue illustrate how the growing diversity in genomic resources for forest tree species that are adapted to a wide range of environments and other ecological parameters provides unprecedented power to examine adaptive traits. This Invited Issue also highlights the maturation that has taken place in genomics-enabled physiology over the last decade. Wullschleger et al. (2002) envisioned that the availability of genomic-scale sequence resources would open the doors to unprecedented interdisciplinary approaches to investigate physiological processes important to forest trees’ perennial lifestyle in a more integrated, comprehensive fashion across scales of biological organization. While they predicted that these types of integrated approaches may take years to come to fruition, this promise is already beginning to be realized, as evidenced by articles in this Invited Issue. For example, systems biology approaches are now feasible for forest trees due to major technological and analytical advances in other omics domains, such as proteomics and metabolomics, together with more targeted protein and metabolite profiling methods. These omics technologies, alongside broad-scale and targeted functional genomics techniques, enable more holistic examinations of gene families, metabolic pathways and signaling networks to advance our understanding of physiological mechanisms. Working at the nexus of functional genomics, population genomics and quantitative genomics, forest tree biologists are also increasingly exploiting the natural genetic variation that exists in these undomesticated species to investigate how this natural genetic variation manifests itself in phenotypic variation associated with functional traits. Connecting genotype with phenotype is one of the grand challenges in contemporary biology, and physiology is central to this endeavor. Forest trees interact with a plethora of organisms in their natural environments, and genomics is also transforming the way in which researchers investigate forest tree interactions with symbiotic, pathogenic, saprotrophic and endophytic microbes. In tandem with the explosion in genomic-scale sequence information for forest tree species, genomic resources have been generated for hundreds of fungal species (MycoCosm; Grigoriev et al. 2011, Grigoriev et al. 2014) and other organisms such as bacteria, insects, nematodes and viruses (e.g., Büttner et al. 2013, Futai 2013, Gugerli et al. 2013, Keeling et al. 2013, Martin et al. 2017, Gschloessl et al. 2018) that interact with forest trees. These genomic resources generated remarkable new insights about how pathogenic and mycorrhizal fungal interact with their hosts (e.g., Duplessis et al. 2011, Martin et al. 2016), and have enabled new ways to finely dissect a tree host’s response to interaction with these fungi. Excitingly, it is now possible to examine host and fungal/bacterial responses simultaneously (e.g., Meyer et al. 2016). Within the above context, we introduce the 12 articles of this Invited Issue in the following sections within the broad themes of abiotic stress, development of wood and bark, cell wall biosynthesis, nitrogen metabolism, pathogen interactions and multi-omics approaches. This Invited Issue is dedicated to the memory of Dr Carl Douglas, our colleague, friend and mentor, whose life was cut tragically short in a mountaineering accident. Carl was a leader in our field in so many ways. Carl’s group was amongst the first to use molecular tools in forest trees, choosing Populus as his system of choice, and was a tireless advocate for Populus as a model genomic system. Carl played instrumental roles in developing landmark Populus genomic resources, such as his contributions to the P. trichocarpa genome sequence paper (Tuskan et al. 2006), and a unique integrated genetic, genomic and phenotypic dataset for P. trichocarpa (e.g., Porth et al. 2013; Suarez-Gonzalez et al. 2016) that will be exploited for years to come. Carl and his group published over 100 papers in Populus, Arabidopsis and other systems, making outstanding contributions to the areas of phenylpropanoid metabolism and biosynthesis of lignin, pollen exine and plant cell walls. Many of these papers appeared in the very best journals in our field. Carl took on several other leadership roles over his career, including at the University of British Columbia where he was a faculty member for nearly 30 years, and for national and international plant biology organizations. Carl was a remarkable, kind and caring individual whose presence in our international community is greatly missed. New perspectives from the fast-moving field of abiotic stress physiology The triumvirate of drought, heat and cold comprises perhaps the most persistent and widespread abiotic challenge to forests worldwide, even in non-arid regions. As the old adage about sessile plants suggests, trees cannot manipulate or avoid environmental fluctuations, but they can often tolerate and acclimate over their long lifespan. Many of the studies featured in this Invited Issue explore development and survival of long-lived organisms in a way that trees are uniquely qualified to facilitate. The study foci ranged from transcriptomic investigations of stress responses to the acquisition and curation of new gene data related to drought tolerance. Fox et al. (2018) focused on Pinus halepensis (Aleppo pine) native to semi-arid regions throughout the Mediterranean basin. Aleppo pine has played an important historical role in anti-desertification programs and forest plantations in Israel. These forests have grown well in the past, but in recent years the impact of climate change has resulted in decreased vitality. Using rooted cuttings propagated from a mature tree living in a sub-optimal environment, Fox et al. (2018) have assembled a rich body of physiological and transcriptomic data on the response course of this robust species during prolonged drought and recovery. The molecular response of P. halepensis roots to drought was reported earlier by others (Sathyan et al. 2005), but this paper examined needle response. Of more than 6000 drought-responsive transcripts, fewer than half were reported previously and the rest were assembled de novo from this study. A striking finding was the strong contribution by retrotransposons, which make up over 60% of the P. taeda genome (Neale et al. 2014), during Aleppo pine recovery from drought. Differential expression of genes potentially involved in histone modifications was also noted. As epigenetic mechanisms are known to suppress retrotransposon activity during stress (Ito et al. 2011), the authors discussed their findings regarding the interplay between epigenetics and retrotransposon activity as a potential mechanism of long-lived trees to adapt to future stress. Sena et al. (2018) report on the comparatively large family of dehydrin genes found in conifers native to Boreal forests. Dehydrins are group 2 Late Embryogenesis Abundant (LEA) proteins that confer cellular tolerance to dehydration partly via hydration-dependent conformational changes (Hanin et al. 2011). Using powerful genome search algorithms like those based on Hidden Markov principles (Eddy 1998), Sena et al. (2018) conducted comprehensive searches of dehydrin sequences in the Pinaceae as well as representative angiosperm species. Following up on their discovery that conifers may have as many as fourfold the number of dehydrin genes as angiosperms (Rigault et al. 2011), Sena and colleagues delve into the evolutionary basis for the expansion. Differences in gene structure between angiosperm and conifer dehydrins are presented, as is the drought-induced expression of a subset of conifer-specific dehydrins. Their work implies greater sub-functionalization and a broader functional repertory for dehydrins than previously estimated based on angiosperm lineages. Stress does not necessarily affect woody biomass recalcitrance Trees provide not only a host of environmental services, they also yield marketplace products. Perhaps nowhere have post-genomics era technologies had greater application than toward the post-harvest utilization of tree biomass (Grattapaglia et al. 2009). Several studies in this issue investigated the dependence of cell wall traits on environmental and circadian cues. Given the ever-changing environment and longevity of woody bioenergy crops, trees harvested for biorefineries are bound to have experienced episodic stress or sub-optimal conditions during their multi-year growth. In this regard, it is imperative to understand how wood properties change in response to stress, and whether and how such changes affect bioprocessing. Ployet et al. (2018) studied the effects of cold temperatures on wood traits in a frost-tolerant hybrid Eucalyptus gundal (E. gunnii × E. dalrympleana). Arguably the most-planted hardwood species in the world, commercial plantations of Eucalyptus remain limited to tropical and subtropical regions due to frost sensitivity (Wisniewski et al. 2014). Ployet et al. (2018) showed that cold treatments induced secondary cell wall thickening and increased deposition of lignin and extractives, reminiscent of the difference between autumn/winter wood and summer wood. This, along with increased pentose-to-hexose polysaccharide ratio in cold-stressed wood, led the authors to suggest that increased lignin and hemicellulose contributed to cell wall reinforcement against freezing damage. Coexpression network analysis with transcription factors known to regulate secondary cell wall biogenesis (Ye and Zhong 2015) identified cold-regulated transcription factors that are promising candidates to decipher the crosstalk between cell wall biogenesis and cold stress response. Wildhagen et al. (2018) investigated the genetic canalization and drought responsiveness of wood anatomical and chemical traits relevant to biofuel conversion in black poplar (Populus nigra). Three genotypes originating from habitats with varying water availability exhibited different wood anatomies, lignin contents and fermentable sugar yields. Xylem transcriptomics analysis revealed a much greater influence of genotype than drought stress per se. Drought stress reduced growth as expected. However, against the commonly held belief that drought would increase lignin accrual to strengthen cell wall support, lignin content was unchanged by drought stress in all three genotypes (Wildhagen et al. 2018). Also counter to prediction, saccharification efficiencies of drought-stressed wood relative to unstressed control was increased rather than decreased. Their findings that neither lignin content nor wood anatomical features correlated significantly with sugar yield echoed those of Studer et al. (2011), and suggested that saccharification efficiency is influenced by factors other than, or in addition to, lignin characteristics. Although cell wall carbohydrates were not analyzed in this study, gene coexpression network analysis revealed an association of saccharification efficiency with pectin methylesterification, and with the shuttling of UDP-glucuronic acid between pectin and xylose biosynthesis. It appears that even though abiotic stresses frequently lead to increased lignin accrual, wood from stressed trees as a whole is not necessarily more recalcitrant to sugar fermentation than that of unstressed trees. Pectin, a minor component with a major effect on cell wall properties The findings of Wildhagen et al. (2018) support the emerging view that pectin, though a minor component of cell wall, has a major influence on digestibility of lignocellulosic biomass (Xiao and Anderson 2013, Biswal et al. 2014, 2015). Interestingly, cell wall pectins, but not cellulose, were affected by misregulation of α-tubulin in Populus wood (Swamy et al. 2015). Following up on their findings that overexpression of α-tubulin in Populus leaves delayed stomatal closure in response to drought (Swamy et al. 2015), Harding et al. (2018) employed cell wall glycomics and transcriptomics to dissect the mechanism. The pectin constituent galacturonic acid increased in transgenic leaves at the expense of the hemicellulose component xylose, via altered utilization of and/or competition for the common precursor UDP-glucuronic acid (Harding et al. 2018). Based on published accounts of circadian regulation of cell wall biogenesis (Mahboubi et al. 2015) and poplar diurnal expression data (Filichkin et al. 2011), the authors posited that constitutive tubulin expression perturbed the diurnal provisioning of UDP-glucuronic acid for matrix polysaccharide synthesis, and altered pectin abundance and methylation, which impacted stomatal behavior in the transgenic leaves. The study showed that besides the level, the timing of transgene expression can have revelatory effects. Nevertheless, circadian regulation of gene expression remains under-investigated in tree species. The expanding omics repertoire reveals functional insights into the regulation of wood formation Proteomics and metabolomics approaches are increasingly used alongside transcriptomic analysis for functional investigation. This Invited Issue features studies that employed proteomics (Petzold et al. 2018) and metabolomics (Robinson et al. 2018) to address the post-transcriptional aspects of wood formation regulation. Petzold et al. (2018) focused on genes with wood-biased expression to develop a P. trichocarpa wood interactome. The interactome network included 179 nodes derived from protein–protein and protein–DNA interaction assays, interrogated with publicly available RNA-seq data. The most highly connected node in the network is orthologous to a snapdragon (Antirrhinum majus) MYB transcription factor DRIFs (DIV-and-RAD-interacting factors), named after their association with two other MYB proteins DIVARICATA (DIV) and RADIALIS (RAD) involved in flower asymmetry (Raimundo et al. 2013). DRIFs have not been linked to wood formation previously, but the conserved DRIF–RAD–DIV interactions in wood-forming tissues reported by Petzold et al. (2018) raise the enticing possibility of their involvement in asymmetric cambium cell divisions that give rise to xylem and phloem cells. By incorporating multiple data types, the authors showed that wood formation is governed not only by xylem-biased proteins, but also by their predicted interactions with cambium and phloem proteins occurring in neighboring tissues. Importantly, the work demonstrated that a modest scale protein–protein interaction study of tissue-biased genes combined with iterative screening (interactome walking) can identify novel regulators, and contribute to valuable community resources. Decades of research on molecular regulation and genetic engineering of the lignin biosynthetic pathway have demonstrated general conservation in a wide range of crop and woody species (Boerjan et al. 2003). This translates into relatively reproducible, and hence predictable, metabolic engineering outcomes of lignin traits (i.e., lignin content and monolignol S/G ratio) across species. However, far fewer studies have examined the metabolomic responses to lignin pathway perturbation. As many of the pathway intermediates are channeled into different phenylpropanoid branchways and subject to different modes of feedback or feedforward regulation, their responses to genetic perturbation likely exhibit a greater degree of plasticity than the lignin traits per se (Vanholme et al. 2012). In this issue, Robinson et al. (2018) conducted comparative metabolomics on two suites of transgenic poplars engineered for reduced lignin content or increased S/G ratio in two distinct hybrid aspen backgrounds, Populus tremula × alba and Populus grandidentata × alba. The previously reported changes in lignin content or S/G ratio were confirmed, with slight differences in degree. In contrast, changes in soluble metabolite profiles were less consistent between genotypes, and were influenced by the specific genetic manipulation and the analytical platform (Robinson et al. 2018). It appears that genetic perturbations leading to quantitative changes of lignin content had a greater and more consistent impact on general metabolism than did genetic modifications that altered lignin composition. This is consistent with the abnormal growth observed in lignin-reduced transgenics (Coleman et al. 2008), but not S/G-increased lines (Franke et al. 2000). The work demonstrated the utility of metabolomics approaches for identification of stable metabolic signatures as well as taxon-specific metabolic markers associated with metabolic engineering or trait variation from breeding or natural populations. New views of heartwood and bark arise from their distinctive natural product compositions Relative to significant research advances in our understanding of lignocellulosic biosynthesis and xylogenesis, heartwood development remains a less well-characterized aspect of wood formation. The slower research progress may be due in part to taxonomic and developmental constraints. Heartwood formation does not occur in all species, and it can be age-dependent, occurring as early as 1–2 years or as late as 80–100 years depending on the species (Kampe and Magel 2013). Heartwood is traditionally viewed as dead tissue, characterized by high levels of extractives that contribute to many of its desirable properties, such as durability, dark color and essential oils that are highly valued for solid wood products and specialty chemicals (Kampe and Magel 2013). In this Invited Issue, Celedon and Bohlmann (2018) present a new model to challenge the traditional view, and discuss evidence that supports retention of living cells in the heartwood of sandalwood (Santalum album). A recent functional genomics study of terpenoid biosynthesis in sandalwood identified a suite of terpene synthases and cytochrome P450 monooxygenases with biased expression in heartwood (Celedon et al. 2016). This led to the discovery and biochemical characterization of a new, heartwood-specific P450 (CYP736A167) that catalyzes the stereospecific formation of four major sandalwood oil components (Celedon et al. 2016). Celedon and Bohlmann (2018) now posit that a small number of parenchyma cells retain their viability and become specialized for sesquiterpene biosynthesis, while other heartwood cells undergo programmed cell death. This contrasts with heartwood formation models in which specialized metabolites (mostly phenolics) are thought to be synthesized exclusively or predominantly in the transition zone. The paradigm shift presented by Celedon and Bohlmann (2018) raises the interesting question of whether retention of metabolically active cells in the heartwood is the rule or the exception. Given the complexity of heartwood extractives and our limited understanding of their biosynthetic pathways, ‘learning from the (presumably) dead’ may be a fruitful approach for identification and characterization of novel genes involved in biosynthesis of specialized metabolites. While the perspective on heartwood may be changing, mature bark remains almost certainly dead. In all plants, the first line of protection against water loss and infection is the epidermis with its waxy cuticle. In tree stems, the phellogen (cork cambium) gives rise to a secondary protective layer known as the periderm, which replaces the epidermis. The periderm comprises phellum (cork) cells with suberin-enriched walls which remain as bark after phellum cell death. Suberin is ubiquitous in vascular plants, and its induction by biotic and abiotic stresses point to its importance as a protective polymer (Lulai and Corsini 1998, Lulai et al. 2008). Nevertheless, many aspects of suberin biosynthesis remain poorly understood (but see Le Provost et al. 2016). Rains et al. (2018) now report on a large-scale transcriptomic dataset for the exploration of suberin biosynthesis in relation to bark development and plant protection in poplar. Their data shed light on the possibility that many P450 monooxygenase orthologs of Arabidopsis CYP86A cutin biosynthetic genes have been co-opted for suberin biosynthesis in poplar. In the developing phellum, those genes were co-expressed with additional, as yet uncharacterized monoxygenases from other CYP families that may contribute to cork cell wall formation. Another novel CYP may catalyze hydroxylation of a suberin aliphatic, 10,16-dihydroxypalmitate, that is abundant in poplar phellum and one of numerous suberin constituent molecules and biosynthetic intermediates profiled in this study. In addition, the authors reported expression evidence on ABA transporter orthologs in developing phellum of poplar that may eventually be shown to couple bark suberization with abiotic stress signals. The discoveries of Rains et al. (2018) should pave the way for improved poplar genotypes with greater capacities to survive biotic as well as abiotic challenges. Insights into nitrogen metabolism from studies of embryogenesis and germination Over the years, many comparative studies have identified several developmental and metabolic anomalies during somatic embryogenesis and somatic embryo (SE) maturation and germination, relative to zygotic embryos (ZE) at similar developmental stages (Winkelmann 2016). Understanding the molecular underpinnings of embryogenesis holds potential to improve regeneration efficiency. For conifer systems in particular, SE is a vital component to creating transgenic plants for functional analysis of candidate genes. The work of Llebrés et al. (2018) in this Invited Issue represents one such investigation, focusing on biosynthesis and catabolism of arginine in maritime pine (Pinus pinaster Ait.). Arginine has the highest nitrogen/carbon ratio among protein amino acids and is a major storage and transport form of organic nitrogen, accounting for 40–50% of the total nitrogen reserves in seed proteins of several plant species, including pine (Winter et al. 2015). By mining the maritime pine transcriptome (Canales et al. 2014), Llebrés et al. (2018) identified putative orthologs of all known arginine biosynthetic and catabolic genes. Their transcript levels were developmentally regulated in accordance with gradually increased storage protein deposition during ZE development, as well as increased arginine degradation during seed germination. These temporal profiles, however, were not observed in corresponding SE tissues, with arginine biosynthesis and degradation occurring throughout their development. The work offers a molecular basis for the well-known deficiency of storage proteins in mature SE relative to ZE (Winkelmann 2016), and may inspire future modifications to improve SE maturation and germination. Furthermore, subcellular localization of arginine metabolic pathway proteins reported by Llebrés et al. (2018) provided convincing evidence to support, for the first time, a cytosolic pool of ornithine catalyzed by N-acetylornithine deacetylase—the only ornithine/arginine biosynthetic enzyme not localized in the plastid. This suggests that the two well-characterized pathways for ornithine biosynthesis are compartmentalized, with the canonical ‘cyclic pathway’ fueling arginine biosynthesis in plastids and the ‘linear pathway’ supporting biosynthesis of polyamines (Molesini et al. 2015, Llebrés et al. 2018). Multifaceted approaches to addressing forest health threats Climate change is affecting not only growth and geographic distribution of trees, but perhaps much more rapidly so their associated insects and pathogens. Addressing ongoing and predicted forest disease outbreaks requires multifaceted approaches, including holistic understanding of resistance mechanisms and rapid diagnosis, among others. La Mantia et al. (2018) offer important insights about the interface between biotic and abiotic stress resistance, focusing on poplar leaf rust disease, caused by the biotroph Melampsora aecidiodes. Extending previous work by Unda et al. (2017) on the relevance of galactinol to growth, abiotic stress tolerance and signaling in Populus, La Mantia et al. (2018) explored possible connections between galactinol metabolism and poplar defense against M. aecidiodes. Galactinol is an intermediate in the biosynthesis of protective raffinose family oligosaccharides (RFOs) from myo-inositol, but in this Invited Issue, La Mantia et al. (2018) showed that salicylic acid-mediated rust-resistance is compromised in transgenic poplar lines that over-produce galactinol and raffinose. Capitalizing on reports that salicylic acid SA homeostasis also interfaces with myo-inositol utilization, the authors offer metabolic competition and ROS scavenging as two mechanisms by which RFO biosynthesis may interfere with SA-mediated defense against Melampsora. The implications are far-reaching, since SA and RFO underlie separate but important stress resistance mechanisms in Populus. Mountain pine beetle (Dendroctonus ponderosae) has undergone significant range expansion during this current outbreak, which is the largest in recorded history. Mountain pine beetle carries a complex microbiome that includes multiple species of Ophiostomoid fungi, commonly referred to as the bluestain fungi. These fungi, which include Grosmannia clavigera, are necrotrophic pathogens that cause lesions within the infected tissues of their host plant. Lesion length has commonly been used as a relative measure of the tree’s defensive capacity (e.g., Arango-Velez et al. 2016), but is also used to measure fungal virulence (e.g., Rice and Langor 2008). Is lesion length an appropriate measure for either of these traits? McAllister et al. (2018) addressed this question by developing a new, more sensitive and specific quantitative PCR method that they then used to quantify amounts of G. clavigera in stems of lodgepole and jack pine. Quantitative PCR carried out using primers designed using G. clavigera genomic-scale data revealed that lesion length is not a good predictor of the extent of fungal growth along the stem, nor of total quantity of fungal growth. From this finding, McAllister et al. (2018) infer that differences in lesion length but not fungal growth between treatments or individual represent differences in defense responses. The new quantitative PCR method developed by McAllister et al. (2018) will not only allow for further examination of this question, but can be used for in situ quantification of microbial DNA in a wide range of plant tissues and other environmental samples. Continuing to push boundaries As summarized above, the collection of 12 papers that make up this Invited Issue effectively demonstrate a range of contemporary genomic techniques to investigate key physiological processes in the fields of development, metabolism and responses to biotic and abiotic factors. These papers underscore the progress that we have made as a community towards mechanistic understanding of these processes since the advent of the Populus genome sequencing project in the early 2000s. Drawing inspiration from Wullschleger et al. (2002), we can expect to see an even greater pace of innovation over the next decade. The Populus system continues to provide the richest genomic resources and biological attributes that facilitate an enviable range of experimental approaches; we anticipate that advances in technologies such as CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats)-based genome editing (Zhou et al. 2015) will lead to even more ground-breaking discoveries in the next decade. At the same time, the rapid growth of genomic resources for several other forest tree species (Plomion et al. 2016b, Neale et al. 2017) indicates that the community is moving into a post-model era of genomics, and that we can expect an increasing number of functional genomics studies for a broader range of species. We can also expect more studies that examine adaptive traits for diverse species from a wide range of ecological niches in holistic fashion. As we continue to build bridges through genomic tools with other disciplines, the community will assuredly pursue the vision of Wullschleger et al. (2002) to explore how genotype and environment shape phenotype across scales of biological organization. Throughout his career, Dr Carl Douglas was an innovator, always pushing boundaries through astute and creative hypothesis testing, early adoption of new techniques and technologies, and interdisciplinary collaboration. 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Branching out: a new era of investigating physiological processes in forest trees using genomic tools

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Oxford University Press
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Abstract

In just over a decade since the publication of the first forest tree genome—that of Populus trichocarpa (Salicaceae; Tuskan et al. 2006)—we have witnessed tremendous advances in tree physiology leveraged from forest tree genomic resources. Prepublication release of draft sequence data from the Populus genome project (Tuskan et al. 2004), together with pioneering efforts to develop expressed sequence tag (EST) resources for Populus spp. (e.g., Sterky et al. 1998, 2004) and loblolly pine (Pinus taeda, Pinaceae; Allona et al. 1998), revolutionized the way in which the forest tree community conducts physiological experiments. Indeed, an Editorial in this journal penned by Stan Wullschleger, Jerry Tuskan and Stephen DiFazio soon after the announcement of the Populus genome project was prescient in identifying innovative new avenues in which genomics would be brought to bear on forest tree physiology, from molecular to ecosystem scales (Wullschleger et al. 2002). In this Invited Issue, entitled Tree Physiology and Genomics, we bring together 12 articles that skillfully illustrate uses of an ever-expanding forest genomics toolkit to further our insight into various physiological processes. The status of P. trichocarpa as the flagship tree genome sequence is reflected in this Invited Issue, in which half of the articles use this resource and related omic tools in their investigations. The remaining articles draw from genome sequence and transcriptomic resources developed for a number of other taxa. In recent years, advances in technologies, increased access to sequencing and bioinformatics expertise and decreased costs have spurred the community to develop significant genomic and transcriptomic resources for a dizzying number of economically, ecologically and evolutionarily important forest tree species from both the Northern and Southern hemispheres. These species represent commercially important fast-growing short rotation woody crops, ecosystem-dominating species such as slow-growing conifers, threatened species and species from fragile ecosystems, as well as species occupying key positions on the tree of life. As of early 2018, the list of forest tree genome sequences comprised several eudicot species, including additional poplar species (Populus euphratica, Salicaceae; Ma et al. 2013), gum (Eucalyptus grandis, Myrtaceae; Myburg et al. 2014), willow (Salix suchowensis, Salicaceae; Dai et al. 2014), birch (Betula pendula and Betula nana, Betulaceae; Wang et al. 2013, Salojarvi et al. 2017), ash (Fraxinus excelsior, Oleaceae; Sollars et al. 2017), oak (Quercus robur, Fagaceae; Plomion et al. 2016a) and rubber tree (Hevea brasiliensis, Euphorbiaceae; Rahman et al. 2013); the basal angiosperm Amborella trichopoda (Amborellaceae; Amborella Genome Project 2013); and the even earlier diverging giga-genome conifers Norway spruce, white spruce, loblolly pine and sugar pine (Picea abies, Picea glauca, P. taeda and Pinus lambertiana, respectively, all Pinaceae; Nystedt et al. 2013, Zimin et al. 2014, Warren et al. 2015, Stevens et al. 2016). Genome sequences of several other forest tree species have been released prior to publication (e.g., Phytozome v12; Goodstein et al. 2012), and many more are on track to be publicly released and/or published in the near- and mid-term. Genome sequences are also available for a wide array of agronomically important fruit tree species (summarized in Chagné 2015 and Neale et al. 2017), which serve as important resources for comparative genomic analyses of perennial processes. Articles in this Invited Issue illustrate how the growing diversity in genomic resources for forest tree species that are adapted to a wide range of environments and other ecological parameters provides unprecedented power to examine adaptive traits. This Invited Issue also highlights the maturation that has taken place in genomics-enabled physiology over the last decade. Wullschleger et al. (2002) envisioned that the availability of genomic-scale sequence resources would open the doors to unprecedented interdisciplinary approaches to investigate physiological processes important to forest trees’ perennial lifestyle in a more integrated, comprehensive fashion across scales of biological organization. While they predicted that these types of integrated approaches may take years to come to fruition, this promise is already beginning to be realized, as evidenced by articles in this Invited Issue. For example, systems biology approaches are now feasible for forest trees due to major technological and analytical advances in other omics domains, such as proteomics and metabolomics, together with more targeted protein and metabolite profiling methods. These omics technologies, alongside broad-scale and targeted functional genomics techniques, enable more holistic examinations of gene families, metabolic pathways and signaling networks to advance our understanding of physiological mechanisms. Working at the nexus of functional genomics, population genomics and quantitative genomics, forest tree biologists are also increasingly exploiting the natural genetic variation that exists in these undomesticated species to investigate how this natural genetic variation manifests itself in phenotypic variation associated with functional traits. Connecting genotype with phenotype is one of the grand challenges in contemporary biology, and physiology is central to this endeavor. Forest trees interact with a plethora of organisms in their natural environments, and genomics is also transforming the way in which researchers investigate forest tree interactions with symbiotic, pathogenic, saprotrophic and endophytic microbes. In tandem with the explosion in genomic-scale sequence information for forest tree species, genomic resources have been generated for hundreds of fungal species (MycoCosm; Grigoriev et al. 2011, Grigoriev et al. 2014) and other organisms such as bacteria, insects, nematodes and viruses (e.g., Büttner et al. 2013, Futai 2013, Gugerli et al. 2013, Keeling et al. 2013, Martin et al. 2017, Gschloessl et al. 2018) that interact with forest trees. These genomic resources generated remarkable new insights about how pathogenic and mycorrhizal fungal interact with their hosts (e.g., Duplessis et al. 2011, Martin et al. 2016), and have enabled new ways to finely dissect a tree host’s response to interaction with these fungi. Excitingly, it is now possible to examine host and fungal/bacterial responses simultaneously (e.g., Meyer et al. 2016). Within the above context, we introduce the 12 articles of this Invited Issue in the following sections within the broad themes of abiotic stress, development of wood and bark, cell wall biosynthesis, nitrogen metabolism, pathogen interactions and multi-omics approaches. This Invited Issue is dedicated to the memory of Dr Carl Douglas, our colleague, friend and mentor, whose life was cut tragically short in a mountaineering accident. Carl was a leader in our field in so many ways. Carl’s group was amongst the first to use molecular tools in forest trees, choosing Populus as his system of choice, and was a tireless advocate for Populus as a model genomic system. Carl played instrumental roles in developing landmark Populus genomic resources, such as his contributions to the P. trichocarpa genome sequence paper (Tuskan et al. 2006), and a unique integrated genetic, genomic and phenotypic dataset for P. trichocarpa (e.g., Porth et al. 2013; Suarez-Gonzalez et al. 2016) that will be exploited for years to come. Carl and his group published over 100 papers in Populus, Arabidopsis and other systems, making outstanding contributions to the areas of phenylpropanoid metabolism and biosynthesis of lignin, pollen exine and plant cell walls. Many of these papers appeared in the very best journals in our field. Carl took on several other leadership roles over his career, including at the University of British Columbia where he was a faculty member for nearly 30 years, and for national and international plant biology organizations. Carl was a remarkable, kind and caring individual whose presence in our international community is greatly missed. New perspectives from the fast-moving field of abiotic stress physiology The triumvirate of drought, heat and cold comprises perhaps the most persistent and widespread abiotic challenge to forests worldwide, even in non-arid regions. As the old adage about sessile plants suggests, trees cannot manipulate or avoid environmental fluctuations, but they can often tolerate and acclimate over their long lifespan. Many of the studies featured in this Invited Issue explore development and survival of long-lived organisms in a way that trees are uniquely qualified to facilitate. The study foci ranged from transcriptomic investigations of stress responses to the acquisition and curation of new gene data related to drought tolerance. Fox et al. (2018) focused on Pinus halepensis (Aleppo pine) native to semi-arid regions throughout the Mediterranean basin. Aleppo pine has played an important historical role in anti-desertification programs and forest plantations in Israel. These forests have grown well in the past, but in recent years the impact of climate change has resulted in decreased vitality. Using rooted cuttings propagated from a mature tree living in a sub-optimal environment, Fox et al. (2018) have assembled a rich body of physiological and transcriptomic data on the response course of this robust species during prolonged drought and recovery. The molecular response of P. halepensis roots to drought was reported earlier by others (Sathyan et al. 2005), but this paper examined needle response. Of more than 6000 drought-responsive transcripts, fewer than half were reported previously and the rest were assembled de novo from this study. A striking finding was the strong contribution by retrotransposons, which make up over 60% of the P. taeda genome (Neale et al. 2014), during Aleppo pine recovery from drought. Differential expression of genes potentially involved in histone modifications was also noted. As epigenetic mechanisms are known to suppress retrotransposon activity during stress (Ito et al. 2011), the authors discussed their findings regarding the interplay between epigenetics and retrotransposon activity as a potential mechanism of long-lived trees to adapt to future stress. Sena et al. (2018) report on the comparatively large family of dehydrin genes found in conifers native to Boreal forests. Dehydrins are group 2 Late Embryogenesis Abundant (LEA) proteins that confer cellular tolerance to dehydration partly via hydration-dependent conformational changes (Hanin et al. 2011). Using powerful genome search algorithms like those based on Hidden Markov principles (Eddy 1998), Sena et al. (2018) conducted comprehensive searches of dehydrin sequences in the Pinaceae as well as representative angiosperm species. Following up on their discovery that conifers may have as many as fourfold the number of dehydrin genes as angiosperms (Rigault et al. 2011), Sena and colleagues delve into the evolutionary basis for the expansion. Differences in gene structure between angiosperm and conifer dehydrins are presented, as is the drought-induced expression of a subset of conifer-specific dehydrins. Their work implies greater sub-functionalization and a broader functional repertory for dehydrins than previously estimated based on angiosperm lineages. Stress does not necessarily affect woody biomass recalcitrance Trees provide not only a host of environmental services, they also yield marketplace products. Perhaps nowhere have post-genomics era technologies had greater application than toward the post-harvest utilization of tree biomass (Grattapaglia et al. 2009). Several studies in this issue investigated the dependence of cell wall traits on environmental and circadian cues. Given the ever-changing environment and longevity of woody bioenergy crops, trees harvested for biorefineries are bound to have experienced episodic stress or sub-optimal conditions during their multi-year growth. In this regard, it is imperative to understand how wood properties change in response to stress, and whether and how such changes affect bioprocessing. Ployet et al. (2018) studied the effects of cold temperatures on wood traits in a frost-tolerant hybrid Eucalyptus gundal (E. gunnii × E. dalrympleana). Arguably the most-planted hardwood species in the world, commercial plantations of Eucalyptus remain limited to tropical and subtropical regions due to frost sensitivity (Wisniewski et al. 2014). Ployet et al. (2018) showed that cold treatments induced secondary cell wall thickening and increased deposition of lignin and extractives, reminiscent of the difference between autumn/winter wood and summer wood. This, along with increased pentose-to-hexose polysaccharide ratio in cold-stressed wood, led the authors to suggest that increased lignin and hemicellulose contributed to cell wall reinforcement against freezing damage. Coexpression network analysis with transcription factors known to regulate secondary cell wall biogenesis (Ye and Zhong 2015) identified cold-regulated transcription factors that are promising candidates to decipher the crosstalk between cell wall biogenesis and cold stress response. Wildhagen et al. (2018) investigated the genetic canalization and drought responsiveness of wood anatomical and chemical traits relevant to biofuel conversion in black poplar (Populus nigra). Three genotypes originating from habitats with varying water availability exhibited different wood anatomies, lignin contents and fermentable sugar yields. Xylem transcriptomics analysis revealed a much greater influence of genotype than drought stress per se. Drought stress reduced growth as expected. However, against the commonly held belief that drought would increase lignin accrual to strengthen cell wall support, lignin content was unchanged by drought stress in all three genotypes (Wildhagen et al. 2018). Also counter to prediction, saccharification efficiencies of drought-stressed wood relative to unstressed control was increased rather than decreased. Their findings that neither lignin content nor wood anatomical features correlated significantly with sugar yield echoed those of Studer et al. (2011), and suggested that saccharification efficiency is influenced by factors other than, or in addition to, lignin characteristics. Although cell wall carbohydrates were not analyzed in this study, gene coexpression network analysis revealed an association of saccharification efficiency with pectin methylesterification, and with the shuttling of UDP-glucuronic acid between pectin and xylose biosynthesis. It appears that even though abiotic stresses frequently lead to increased lignin accrual, wood from stressed trees as a whole is not necessarily more recalcitrant to sugar fermentation than that of unstressed trees. Pectin, a minor component with a major effect on cell wall properties The findings of Wildhagen et al. (2018) support the emerging view that pectin, though a minor component of cell wall, has a major influence on digestibility of lignocellulosic biomass (Xiao and Anderson 2013, Biswal et al. 2014, 2015). Interestingly, cell wall pectins, but not cellulose, were affected by misregulation of α-tubulin in Populus wood (Swamy et al. 2015). Following up on their findings that overexpression of α-tubulin in Populus leaves delayed stomatal closure in response to drought (Swamy et al. 2015), Harding et al. (2018) employed cell wall glycomics and transcriptomics to dissect the mechanism. The pectin constituent galacturonic acid increased in transgenic leaves at the expense of the hemicellulose component xylose, via altered utilization of and/or competition for the common precursor UDP-glucuronic acid (Harding et al. 2018). Based on published accounts of circadian regulation of cell wall biogenesis (Mahboubi et al. 2015) and poplar diurnal expression data (Filichkin et al. 2011), the authors posited that constitutive tubulin expression perturbed the diurnal provisioning of UDP-glucuronic acid for matrix polysaccharide synthesis, and altered pectin abundance and methylation, which impacted stomatal behavior in the transgenic leaves. The study showed that besides the level, the timing of transgene expression can have revelatory effects. Nevertheless, circadian regulation of gene expression remains under-investigated in tree species. The expanding omics repertoire reveals functional insights into the regulation of wood formation Proteomics and metabolomics approaches are increasingly used alongside transcriptomic analysis for functional investigation. This Invited Issue features studies that employed proteomics (Petzold et al. 2018) and metabolomics (Robinson et al. 2018) to address the post-transcriptional aspects of wood formation regulation. Petzold et al. (2018) focused on genes with wood-biased expression to develop a P. trichocarpa wood interactome. The interactome network included 179 nodes derived from protein–protein and protein–DNA interaction assays, interrogated with publicly available RNA-seq data. The most highly connected node in the network is orthologous to a snapdragon (Antirrhinum majus) MYB transcription factor DRIFs (DIV-and-RAD-interacting factors), named after their association with two other MYB proteins DIVARICATA (DIV) and RADIALIS (RAD) involved in flower asymmetry (Raimundo et al. 2013). DRIFs have not been linked to wood formation previously, but the conserved DRIF–RAD–DIV interactions in wood-forming tissues reported by Petzold et al. (2018) raise the enticing possibility of their involvement in asymmetric cambium cell divisions that give rise to xylem and phloem cells. By incorporating multiple data types, the authors showed that wood formation is governed not only by xylem-biased proteins, but also by their predicted interactions with cambium and phloem proteins occurring in neighboring tissues. Importantly, the work demonstrated that a modest scale protein–protein interaction study of tissue-biased genes combined with iterative screening (interactome walking) can identify novel regulators, and contribute to valuable community resources. Decades of research on molecular regulation and genetic engineering of the lignin biosynthetic pathway have demonstrated general conservation in a wide range of crop and woody species (Boerjan et al. 2003). This translates into relatively reproducible, and hence predictable, metabolic engineering outcomes of lignin traits (i.e., lignin content and monolignol S/G ratio) across species. However, far fewer studies have examined the metabolomic responses to lignin pathway perturbation. As many of the pathway intermediates are channeled into different phenylpropanoid branchways and subject to different modes of feedback or feedforward regulation, their responses to genetic perturbation likely exhibit a greater degree of plasticity than the lignin traits per se (Vanholme et al. 2012). In this issue, Robinson et al. (2018) conducted comparative metabolomics on two suites of transgenic poplars engineered for reduced lignin content or increased S/G ratio in two distinct hybrid aspen backgrounds, Populus tremula × alba and Populus grandidentata × alba. The previously reported changes in lignin content or S/G ratio were confirmed, with slight differences in degree. In contrast, changes in soluble metabolite profiles were less consistent between genotypes, and were influenced by the specific genetic manipulation and the analytical platform (Robinson et al. 2018). It appears that genetic perturbations leading to quantitative changes of lignin content had a greater and more consistent impact on general metabolism than did genetic modifications that altered lignin composition. This is consistent with the abnormal growth observed in lignin-reduced transgenics (Coleman et al. 2008), but not S/G-increased lines (Franke et al. 2000). The work demonstrated the utility of metabolomics approaches for identification of stable metabolic signatures as well as taxon-specific metabolic markers associated with metabolic engineering or trait variation from breeding or natural populations. New views of heartwood and bark arise from their distinctive natural product compositions Relative to significant research advances in our understanding of lignocellulosic biosynthesis and xylogenesis, heartwood development remains a less well-characterized aspect of wood formation. The slower research progress may be due in part to taxonomic and developmental constraints. Heartwood formation does not occur in all species, and it can be age-dependent, occurring as early as 1–2 years or as late as 80–100 years depending on the species (Kampe and Magel 2013). Heartwood is traditionally viewed as dead tissue, characterized by high levels of extractives that contribute to many of its desirable properties, such as durability, dark color and essential oils that are highly valued for solid wood products and specialty chemicals (Kampe and Magel 2013). In this Invited Issue, Celedon and Bohlmann (2018) present a new model to challenge the traditional view, and discuss evidence that supports retention of living cells in the heartwood of sandalwood (Santalum album). A recent functional genomics study of terpenoid biosynthesis in sandalwood identified a suite of terpene synthases and cytochrome P450 monooxygenases with biased expression in heartwood (Celedon et al. 2016). This led to the discovery and biochemical characterization of a new, heartwood-specific P450 (CYP736A167) that catalyzes the stereospecific formation of four major sandalwood oil components (Celedon et al. 2016). Celedon and Bohlmann (2018) now posit that a small number of parenchyma cells retain their viability and become specialized for sesquiterpene biosynthesis, while other heartwood cells undergo programmed cell death. This contrasts with heartwood formation models in which specialized metabolites (mostly phenolics) are thought to be synthesized exclusively or predominantly in the transition zone. The paradigm shift presented by Celedon and Bohlmann (2018) raises the interesting question of whether retention of metabolically active cells in the heartwood is the rule or the exception. Given the complexity of heartwood extractives and our limited understanding of their biosynthetic pathways, ‘learning from the (presumably) dead’ may be a fruitful approach for identification and characterization of novel genes involved in biosynthesis of specialized metabolites. While the perspective on heartwood may be changing, mature bark remains almost certainly dead. In all plants, the first line of protection against water loss and infection is the epidermis with its waxy cuticle. In tree stems, the phellogen (cork cambium) gives rise to a secondary protective layer known as the periderm, which replaces the epidermis. The periderm comprises phellum (cork) cells with suberin-enriched walls which remain as bark after phellum cell death. Suberin is ubiquitous in vascular plants, and its induction by biotic and abiotic stresses point to its importance as a protective polymer (Lulai and Corsini 1998, Lulai et al. 2008). Nevertheless, many aspects of suberin biosynthesis remain poorly understood (but see Le Provost et al. 2016). Rains et al. (2018) now report on a large-scale transcriptomic dataset for the exploration of suberin biosynthesis in relation to bark development and plant protection in poplar. Their data shed light on the possibility that many P450 monooxygenase orthologs of Arabidopsis CYP86A cutin biosynthetic genes have been co-opted for suberin biosynthesis in poplar. In the developing phellum, those genes were co-expressed with additional, as yet uncharacterized monoxygenases from other CYP families that may contribute to cork cell wall formation. Another novel CYP may catalyze hydroxylation of a suberin aliphatic, 10,16-dihydroxypalmitate, that is abundant in poplar phellum and one of numerous suberin constituent molecules and biosynthetic intermediates profiled in this study. In addition, the authors reported expression evidence on ABA transporter orthologs in developing phellum of poplar that may eventually be shown to couple bark suberization with abiotic stress signals. The discoveries of Rains et al. (2018) should pave the way for improved poplar genotypes with greater capacities to survive biotic as well as abiotic challenges. Insights into nitrogen metabolism from studies of embryogenesis and germination Over the years, many comparative studies have identified several developmental and metabolic anomalies during somatic embryogenesis and somatic embryo (SE) maturation and germination, relative to zygotic embryos (ZE) at similar developmental stages (Winkelmann 2016). Understanding the molecular underpinnings of embryogenesis holds potential to improve regeneration efficiency. For conifer systems in particular, SE is a vital component to creating transgenic plants for functional analysis of candidate genes. The work of Llebrés et al. (2018) in this Invited Issue represents one such investigation, focusing on biosynthesis and catabolism of arginine in maritime pine (Pinus pinaster Ait.). Arginine has the highest nitrogen/carbon ratio among protein amino acids and is a major storage and transport form of organic nitrogen, accounting for 40–50% of the total nitrogen reserves in seed proteins of several plant species, including pine (Winter et al. 2015). By mining the maritime pine transcriptome (Canales et al. 2014), Llebrés et al. (2018) identified putative orthologs of all known arginine biosynthetic and catabolic genes. Their transcript levels were developmentally regulated in accordance with gradually increased storage protein deposition during ZE development, as well as increased arginine degradation during seed germination. These temporal profiles, however, were not observed in corresponding SE tissues, with arginine biosynthesis and degradation occurring throughout their development. The work offers a molecular basis for the well-known deficiency of storage proteins in mature SE relative to ZE (Winkelmann 2016), and may inspire future modifications to improve SE maturation and germination. Furthermore, subcellular localization of arginine metabolic pathway proteins reported by Llebrés et al. (2018) provided convincing evidence to support, for the first time, a cytosolic pool of ornithine catalyzed by N-acetylornithine deacetylase—the only ornithine/arginine biosynthetic enzyme not localized in the plastid. This suggests that the two well-characterized pathways for ornithine biosynthesis are compartmentalized, with the canonical ‘cyclic pathway’ fueling arginine biosynthesis in plastids and the ‘linear pathway’ supporting biosynthesis of polyamines (Molesini et al. 2015, Llebrés et al. 2018). Multifaceted approaches to addressing forest health threats Climate change is affecting not only growth and geographic distribution of trees, but perhaps much more rapidly so their associated insects and pathogens. Addressing ongoing and predicted forest disease outbreaks requires multifaceted approaches, including holistic understanding of resistance mechanisms and rapid diagnosis, among others. La Mantia et al. (2018) offer important insights about the interface between biotic and abiotic stress resistance, focusing on poplar leaf rust disease, caused by the biotroph Melampsora aecidiodes. Extending previous work by Unda et al. (2017) on the relevance of galactinol to growth, abiotic stress tolerance and signaling in Populus, La Mantia et al. (2018) explored possible connections between galactinol metabolism and poplar defense against M. aecidiodes. Galactinol is an intermediate in the biosynthesis of protective raffinose family oligosaccharides (RFOs) from myo-inositol, but in this Invited Issue, La Mantia et al. (2018) showed that salicylic acid-mediated rust-resistance is compromised in transgenic poplar lines that over-produce galactinol and raffinose. Capitalizing on reports that salicylic acid SA homeostasis also interfaces with myo-inositol utilization, the authors offer metabolic competition and ROS scavenging as two mechanisms by which RFO biosynthesis may interfere with SA-mediated defense against Melampsora. The implications are far-reaching, since SA and RFO underlie separate but important stress resistance mechanisms in Populus. Mountain pine beetle (Dendroctonus ponderosae) has undergone significant range expansion during this current outbreak, which is the largest in recorded history. Mountain pine beetle carries a complex microbiome that includes multiple species of Ophiostomoid fungi, commonly referred to as the bluestain fungi. These fungi, which include Grosmannia clavigera, are necrotrophic pathogens that cause lesions within the infected tissues of their host plant. Lesion length has commonly been used as a relative measure of the tree’s defensive capacity (e.g., Arango-Velez et al. 2016), but is also used to measure fungal virulence (e.g., Rice and Langor 2008). Is lesion length an appropriate measure for either of these traits? McAllister et al. (2018) addressed this question by developing a new, more sensitive and specific quantitative PCR method that they then used to quantify amounts of G. clavigera in stems of lodgepole and jack pine. Quantitative PCR carried out using primers designed using G. clavigera genomic-scale data revealed that lesion length is not a good predictor of the extent of fungal growth along the stem, nor of total quantity of fungal growth. From this finding, McAllister et al. (2018) infer that differences in lesion length but not fungal growth between treatments or individual represent differences in defense responses. The new quantitative PCR method developed by McAllister et al. (2018) will not only allow for further examination of this question, but can be used for in situ quantification of microbial DNA in a wide range of plant tissues and other environmental samples. Continuing to push boundaries As summarized above, the collection of 12 papers that make up this Invited Issue effectively demonstrate a range of contemporary genomic techniques to investigate key physiological processes in the fields of development, metabolism and responses to biotic and abiotic factors. These papers underscore the progress that we have made as a community towards mechanistic understanding of these processes since the advent of the Populus genome sequencing project in the early 2000s. Drawing inspiration from Wullschleger et al. (2002), we can expect to see an even greater pace of innovation over the next decade. The Populus system continues to provide the richest genomic resources and biological attributes that facilitate an enviable range of experimental approaches; we anticipate that advances in technologies such as CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats)-based genome editing (Zhou et al. 2015) will lead to even more ground-breaking discoveries in the next decade. At the same time, the rapid growth of genomic resources for several other forest tree species (Plomion et al. 2016b, Neale et al. 2017) indicates that the community is moving into a post-model era of genomics, and that we can expect an increasing number of functional genomics studies for a broader range of species. We can also expect more studies that examine adaptive traits for diverse species from a wide range of ecological niches in holistic fashion. As we continue to build bridges through genomic tools with other disciplines, the community will assuredly pursue the vision of Wullschleger et al. (2002) to explore how genotype and environment shape phenotype across scales of biological organization. Throughout his career, Dr Carl Douglas was an innovator, always pushing boundaries through astute and creative hypothesis testing, early adoption of new techniques and technologies, and interdisciplinary collaboration. 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Tree PhysiologyOxford University Press

Published: Mar 1, 2018

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