We report the draft genome of the black cottonwood tree, Populus trichocarpa . Integration of shotgun sequence assembly with genetic mapping enabled chromosome-scale reconstruction of the genome. More than 45,000 putative protein-coding genes were identified. Analysis of the assembled genome revealed a whole-genome duplication event; about 8000 pairs of duplicated genes from that event survived in the Populus genome. A second, older duplication event is indistinguishably coincident with the divergence of the Populus and Arabidopsis lineages. Nucleotide substitution, tandem gene duplication, and gross chromosomal rearrangement appear to proceed substantially more slowly in Populus than in Arabidopsis. Populus has more protein-coding genes than Arabidopsis , ranging on average from 1.4 to 1.6 putative Populus homologs for each Arabidopsis gene. However, the relative frequency of protein domains in the two genomes is similar. Overrepresented exceptions in Populus include genes associated with lignocellulosic wall biosynthesis, meristem development, disease resistance, and metabolite transport.
In trees, production of intercellular signals and accessibility of signal conduits jointly govern dormancy cycling at the shoot apex. We identified 10 putative cell wall 1,3-b-glucanase genes (glucan hydrolase family 17 [GH17]) in Populus that could turn over 1,3-b-glucan (callose) at pores and plasmodesmata (PD) and investigated their regulation in relation to FT and CENL1 expression. The 10 genes encode orthologs of Arabidopsis thaliana BG_ppap, a PD-associated glycosylphosphatidylinositol (GPI) lipid-anchored protein, the Arabidopsis PD callose binding protein PDCB, and a birch (Betula pendula) putative lipid body (LB) protein. We found that these genes were differentially regulated by photoperiod, by chilling (58C), and by feeding of gibberellins GA 3 and GA 4 . GA 3 feeding upregulated all LB-associated GH17s, whereas GA 4 upregulated most GH17s with a GPI anchor and/or callose binding motif, but only GA 4 induced true bud burst. Chilling upregulated a number of GA biosynthesis and signaling genes as well as FT, but not CENL1, while the reverse was true for both GA 3 and GA 4 . Collectively, the results suggest a model for dormancy release in which chilling induces FT and both GPI lipid-anchored and GA 3 -inducible GH17s to reopen signaling conduits in the embryonic shoot. When temperatures rise, the reopened conduits enable movement of FT and CENL1 to their targets, where they drive bud burst, shoot elongation, and morphogenesis.
Forest ecosystems maintain a large share of Northern Hemisphere biodiversity. Boreal forests comprise roughly 30% of global forest area 1 and contain the highest tree density among climate zones 2 . Moreover, boreal regions are undergoing extensive climate change. Annual temperature increases exceeding 1.5 °C are projected to result in a warming of 4-11 °C by the end of this century, with little concomitant increase in precipitation 1 . At this pace, climate zones will shift northward at a greater speed than trees can migrate 3 . To understand how future populations of forest trees may respond to climate change, it is essential to uncover past and present signatures of molecular adaptation in their genomes. Silver birch, B. pendula, is a pioneer species in boreal forests of Eurasia. Flowering of the species can be artificially accelerated 4 , giving it an advantage over other tree species with published genome sequences (such as poplar 5 , spruce 6 , and pine 7 ) for the optimization of fiber and biomass production.Here we sequenced 150 birch individuals and assembled a B. pendula reference genome from a fourth-generation inbred line, resulting in a high-quality assembly of 435 Mb that was linked to chromosomes using a dense genetic map. We analyzed SNPs in the genomes of 80 birch individuals spanning most of the geographic range of B. pendula, as well as seven other members of Betulaceae. Population genomic analyses of these data provide insights into the deep-time evolution of the birch family and on recent natural selection acting on silver birch.Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch Silver birch (Betula pendula) is a pioneer boreal tree that can be induced to flower within 1 year. Its rapid life cycle, small (440-Mb) genome, and advanced germplasm resources make birch an attractive model for forest biotechnology. We assembled and chromosomally anchored the nuclear genome of an inbred B. pendula individual. Gene duplicates from the paleohexaploid event were enriched for transcriptional regulation, whereas tandem duplicates were overrepresented by environmental responses. Population resequencing of 80 individuals showed effective population size crashes at major points of climatic upheaval. Selective sweeps were enriched among polyploid duplicates encoding key developmental and physiological triggering functions, suggesting that local adaptation has tuned the timing of and cross-talk between fundamental plant processes. Variation around the tightlylinked light response genes PHYC and FRS10 correlated with latitude and longitude and temperature, and with precipitation for PHYC. Similar associations characterized the growth-promoting cytokinin response regulator ARR1, and the wood development genes KAK and MED5A.A full list of affiliations appears at the end of the paper.
The plant hormone ethylene is an important signal in plant growth responses to environmental cues. In vegetative growth, ethylene is generally considered as a regulator of cell expansion, but a role in the control of meristem growth has also been suggested based on pharmacological experiments and ethylene-overproducing mutants. In this study, we used transgenic ethylene-insensitive and ethylene-overproducing hybrid aspen (Populus tremula ؋ tremuloides) in combination with experiments using an ethylene perception inhibitor [1-methylcyclopropene (1-MCP)] to demonstrate that endogenous ethylene produced in response to leaning stimulates cell division in the cambial meristem. This ethylenecontrolled growth gives rise to the eccentricity of Populus stems that is formed in association with tension wood.plant hormones ͉ secondary xylem ͉ tension wood ͉ vascular cambium ͉ wood development T he vascular cambium is the meristem that produces secondary xylem and phloem by periclinal cell divisions, and it is responsible for wood production and stem diameter growth in trees. Cambial growth rate along the trunk is correlated with leaf biomass and crown structure (1). Superimposed on this intrinsic control, cambial growth is also strongly influenced by environment, where mechanical and gravitational loads imposed by wind and leaning are important (2). Wind sway induces increased diameter growth that protects against stem breakage (3), whereas a static lean results in a localized growth response known as tension wood (TW) in dicotyledonous angiosperms. TW is formed on the upper side of the leaning stem, resulting in characteristic asymmetric growth, and it serves to correct the stem position (4). In addition to the striking increase in cambial cell divisions, TW has an altered anatomy, and the fibers form an additional inner, cellulose-rich, gelatinous secondary cell wall layer (G layer) (5).Experiments with ethylene applications have revealed that this volatile plant hormone has the potential to both inhibit and stimulate growth (6). Its synthesis from S-adenosylmethionine through the action of 1-aminocyclopropane-1-carboxylate (ACC) synthase (ACS) and ACC oxidase (ACO) is triggered in vegetative tissues in response to many environmental cues. To date, concepts of ethylene function in vegetative growth have mainly implicated its role in primary tissue and cell expansion (6). However, ethylene biosynthesis increases during TW formation because of an asymmetric induction of ACO (7,8), and application of ethylene has been shown to stimulate cambial growth both in trees and herbaceous species (9, 10). Additional observations also support a potential role for ethylene in cell division. Applied ethylene stimulated endoreduplication in cucumber hypocotyls and growth of the intercalary meristem in deepwater rice (11-13). Moreover, the ethylene-overproducing Arabidopsis mutant eto1 exhibits aberrant cell divisions in the quiescent center of the root (14). However, experiments where ethylene homeostasis is artificially manipulated by a...
SummaryEthylene Response Factors (ERFs) are a large family of transcription factors that mediate responses to ethylene. Ethylene affects many aspects of wood development and is involved in tension wood formation. Thus ERFs could be key players connecting ethylene action to wood development.We identified 170 gene models encoding ERFs in the Populus trichocarpa genome. The transcriptional responses of ERF genes to ethylene treatments were determined in stem tissues of hybrid aspen (Populus tremula 9 tremuloides) by qPCR. Selected ethylene-responsive ERFs were overexpressed in wood-forming tissues and characterized for growth and wood chemotypes by FT-IR.Fifty ERFs in Populus showed more than five-fold increased transcript accumulation in response to ethylene treatments. Twenty-six ERFs were selected for further analyses. A majority of these were induced during tension wood formation. Overexpression of ERFs 18, 21, 30, 85 and 139 in wood-forming tissues of hybrid aspen modified the wood chemotype. Moreover, overexpression of ERF139 caused a dwarf-phenotype with altered wood development, and overexpression of ERF18, 34 and 35 slightly increased stem diameter.We identified ethylene-induced ERFs that respond to tension wood formation, and modify wood formation when overexpressed. This provides support for their role in ethylenemediated regulation of wood development.
We have used genotypic variation in birch (Betula pendula Roth) to investigate the roles of ozone (O 3 )-induced ethylene (ET), jasmonic acid, and salicylic acid in the regulation of tissue tolerance to O 3 . Of these hormones, ET evolution correlated best with O 3 -induced cell death. Disruption of ET perception by transformation of birch with the dominant negative mutant allele etr1-1 of the Arabidopsis ET receptor gene ETR1 or blocking of ET perception with 1-methylcyclopropene reduced but did not completely prevent the O 3 -induced cell death, when inhibition of ET biosynthesis with aminooxyacetic acid completely abolished O 3 lesion formation. This suggests the presence of an ET-signaling-independent but ET biosynthesis-dependent component in the ET-mediated stimulation of cell death in O 3 -exposed birch. Functional ET signaling was required for the O 3 induction of the gene encoding -cyanoalanine synthase, which catalyzes detoxification of the cyanide formed during ET biosynthesis. The results suggest that functional ET signaling is required to protect birch from the O 3 -induced cell death and that a decrease in ET sensitivity together with a simultaneous, high ET biosynthesis can potentially cause cell death through a deficient detoxification of cyanide.The concentration of tropospheric ozone (O 3 ) has increased during the past decades due to human activities, and it has been estimated that in year 2100, 50% of global forest area will be exposed to potentially phytotoxic O 3 concentrations (Fowler et al., 1999). In the leaves of O 3 -sensitive plants, symptoms of high O 3 are observed as rapid lesion formation. Traditionally, formation of reactive oxygen species (ROS), such as superoxide (O 2 ⅐ Ϫ ) and hydrogen peroxide (H 2 O 2 ) from the degradation of O 3 in the apoplast has been thought to alter the integrity of the plasma membrane and thus the integrity of the cell (Laisk et al., 1989; Heath, 1994). However, O 3 also induces an active and controlled apoplastic oxidative burst, the production of O 2 ⅐ Ϫ and H 2 O 2 in the leaves affected, which may initiate programmed cell death analogous to that induced by ROS in an incompatible plant-pathogen interaction (Schraudner et al., 1998;Pellinen et al., 1999Pellinen et al., , 2002Overmyer et al., 2000; Moeder et al., 2002; Wohlgemuth et al., 2002).Activation of ethylene (ET) biosynthesis by induction of the genes encoding 1-aminocyclopropane-1-carboxylate synthase (ACS) is one of the fastest and most obvious biochemical responses to O 3 and has been mechanistically linked to the regulation of O 3 lesion formation (Schlagnhaufer et al., 1997;Tuomainen et al., 1997;Vahala et al., 1998;Overmyer et al., 2000; Moeder et al., 2002). ET is perceived by a two-component His kinase receptor family (Chang et al., 1993a; Hua et al., 1995Hua et al., , 1998Sakai et al., 1998). The ET receptor can be pharmacologically blocked with a competitive inhibitor of ET action, norbornadiene, or with 1-methylcyclopropene (MCP; Serek et al., 1995), which prevents the binding ...
HighlightShort photoperiod and apical dominance trigger a shared developmental bud programme at terminal and axillary positions, while the capacity to establish photoperiod-induced dormancy is lost in maturing para-dormant axillary buds.
The role of ethylene (ET) signaling in the responses of two hybrid aspen (Populus tremula L. ϫ P. tremuloides Michx.) clones to chronic ozone (O 3 ; 75 nL L Ϫ1 ) was investigated. The hormonal responses differed between the clones; the O 3 -sensitive clone 51 had higher ET evolution than the tolerant clone 200 during the exposure, whereas the free salicylic acid concentration in clone 200 was higher than in clone 51. The cellular redox status, measured as glutathione redox balance, did not differ between the clones suggesting that the O 3 lesions were not a result of deficient antioxidative capacity. The buildup of salicylic acid during chronic O 3 exposure might have prevented the up-regulation of ET biosynthesis in clone 200. Blocking of ET perception with 1-methylcyclopropene protected both clones from the decrease in net photosynthesis during chronic exposure to O 3 . After a pretreatment with low O 3 for 9 d, an acute 1.5-fold O 3 elevation caused necrosis in the O 3 -sensitive clone 51, which increased substantially when ET perception was blocked. The results suggest that in hybrid aspen, ET signaling had a dual role depending on the severity of the stress. ET accelerated leaf senescence under low O 3 , but under acute O 3 elevation, ET signaling seemed to be required for protection from necrotic cell death.The gaseous phytohormone ethylene (ET) is a signal molecule that is active during both plant development and senescence and is synthesized as a response to several biotic and abiotic stresses (Tingey et al., 1976;Yang and Hoffman, 1984; Abeles et al., 1992;Johnson and Ecker, 1998). The ET precursor 1-aminocyclopropane-1-carboxylic acid (ACC) is synthesized from S-adenosyl-l-Met by ACC synthase (ACS; Yang and Hoffman, 1984). ACC is further converted to CO 2 , cyanide (HCN), and ET by ACC oxidase. The HCN formed is rapidly detoxified by -cyano-Ala synthase (-CAS; Yip and Yang, 1988). ET has a role in the regulation of several plant defense genes (Broglie et al., 1986;Ecker and Davis, 1987;Eyal et al., 1993;Leubner-Metzger et al., 1998), but it also has an opposite role; ET can promote cell death under oxidative stress (Overmyer et al., 2000) and pathogen attack (Ciardi et al., 2001).Tropospheric ozone (O 3 ) has been recognized as a severe air pollutant since the 1950s. Ambient O 3 concentrations in northern Europe vary usually between 20 to 50 nL L Ϫ1 during the growth season, but acute O 3 peaks exceeding 150 nL L Ϫ1 are also regularly observed. Once O 3 enters the leaf through stomata, it degrades rapidly in the apoplast to form various reactive oxygen species (ROS;Mehlhorn et al., 1990;Kanofsky and Sima, 1995;Langebartels et al., 2002). It has been proposed that this apoplastic ROS formation may alter the integrity of the plasma membrane and thus cause cellular damage (Laisk et al., 1989;Heath and Taylor, 1997). To remove and detoxify excess ROS, plants have both enzymatic and nonenzymatic antioxidant defenses such as ascorbic acid, glutathione, ␣-tocopherol, and catalase (Noctor and Foyer, 1998;V...
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