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.
SummaryCytokinins are a major class of plant hormones that are involved in various aspects of plant development, ranging from organ formation and apical dominance to leaf senescence. Cytokinin and auxin have long been known to interact antagonistically, and more recent studies have shown that cytokinins also interact with other plant hormones to regulate plant development. A growing body of research has begun to elucidate the molecular and genetic underpinnings of this extensive crosstalk. The rich interconnections between the synthesis, perception and transport networks of these plant hormones provide a wide range of opportunities for them to modulate, amplify or buffer one another. Here, we review this exciting and rapidly growing area of cytokinin research.
We investigated the short day (SD)-induced transition to dormancy in wild-type hybrid poplar (Populus tremula 3 P. tremuloides) and its absence in transgenic poplar overexpressing heterologous PHYTOCHROME A (PHYA). CENTRORADIALIS-LIKE1 (CENL1), a poplar ortholog of Arabidopsis thaliana TERMINAL FLOWER1 (TFL1), was markedly downregulated in the wild-type apex coincident with SD-induced growth cessation. By contrast, poplar overexpressing a heterologous Avena sativa PHYA construct (P35S:AsPHYA), with PHYA accumulating in the rib meristem (RM) and adjacent tissues but not in the shoot apical meristem (SAM), upregulated CENL1 in the RM area coincident with an acceleration of stem elongation. In SD-exposed heterografts, both P35S:AsPHYA and wild-type scions ceased growth and formed buds, whereas only the wild type assumed dormancy and P35S:AsPHYA showed repetitive flushing. This shows that the transition is not dictated by leaf-produced signals but dependent on RM and SAM properties. In view of this, callose-enforced cell isolation in the SAM, associated with suspension of indeterminate growth during dormancy, may require downregulation of CENL1 in the RM. Accordingly, upregulation of CENL1/TFL1 might promote stem elongation in poplar as well as in Arabidopsis during bolting. Together, the results suggest that the RM is particularly sensitive to photoperiodic signals and that CENL1 in the RM influences transition to dormancy in hybrid poplar.
SUMMARYThe complex inflorescences (capitula) of Asteraceae consist of different types of flowers. In Gerbera hybrida (gerbera), the peripheral ray flowers are bilaterally symmetrical and lack functional stamens while the central disc flowers are more radially symmetrical and hermaphroditic. Proteins of the CYC2 subclade of the CYC/TB1-like TCP domain transcription factors have been recruited several times independently for parallel evolution of bilaterally symmetrical flowers in various angiosperm plant lineages, and have also been shown to regulate flower-type identity in Asteraceae. The CYC2 subclade genes in gerbera show largely overlapping gene expression patterns. At the level of single flowers, their expression domain in petals shows a spatial shift from the dorsal pattern known so far in species with bilaterally symmetrical flowers, suggesting that this change in expression may have evolved after the origin of Asteraceae. Functional analysis indicates that GhCYC2, GhCYC3 and GhCYC4 mediate positional information at the proximal-distal axis of the inflorescence, leading to differentiation of ray flowers, but that they also regulate ray flower petal growth by affecting cell proliferation until the final size and shape of the petals is reached. Moreover, our data show functional diversification for the GhCYC5 gene. Ectopic activation of GhCYC5 increases flower density in the inflorescence, suggesting that GhCYC5 may promote the flower initiation rate during expansion of the capitulum. Our data thus indicate that modification of the ancestral network of TCP factors has, through gene duplications, led to the establishment of new expression domains and to functional diversification.
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 ...
SummaryIn many trees, a short photoperiod (SD) triggers substantial physiological adjustments necessary for overwintering. We have used transgenic ethylene-insensitive birches (Betula pendula), which express the Arabidopsis ethylene receptor gene ETR1 carrying the dominant mutation etr1-1, to investigate the role of ethylene in SD-induced responses in the shoot apical meristem (SAM). Under SD, the ethylene-insensitive trees ceased elongation growth comparably to the wild-type. In contrast, the formation of terminal buds, which in trees is typically induced by SD, was abolished. However, although delayed, endo-dormancy did eventually develop in the ethylene-insensitive trees. This, together with the rapid resumption of growth in the ethylene-insensitive trees after transfer from non-permissive to permissive conditions suggests that ethylene facilitates the SD-induced terminal bud formation, as well as growth arrest. In addition, apical buds of the ethylene-insensitive birch did not accumulate abscisic acid (ABA) under SD, suggesting interaction between ethylene and ABA signalling in the bud. Alterations in SAM functioning were further exemplified by reduced apical dominance and early flowering in ethylene-insensitive birches. Gene expression analysis of shoot apices revealed that the ethylene-insensitive birch lacked the marked increase in expression of a beta-xylosidase gene typical to the SD-exposed wild-type. The ethylene-dependent beta-xylosidase gene expression is hypothesized to relate to modification of cell walls in terminal buds during SD-induced growth cessation. Our results suggest that ethylene is involved in terminal bud formation and in the timely suppression of SAM activity, not only in the shoot apex, but also in axillary and reproductive meristems.
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.
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