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.
Several key processes in plant development are regulated by TCP transcription factors. CYCLOIDEA-like (CYC-like) TCP domain proteins have been shown to control flower symmetry in distantly related plant lineages. Gerbera hybrida, a member of one of the largest clades of angiosperms, the sunflower family (Asteraceae), is an interesting model for developmental studies because its elaborate inflorescence comprises different types of flowers that have specialized structures and functions. The morphological differentiation of flower types involves gradual changes in flower size and symmetry that follow the radial organization of the densely packed inflorescence. Differences in the degree of petal fusion further define the distinct shapes of the Gerbera flower types. To study the role of TCP transcription factors during specification of this complex inflorescence organization, we characterized the CYC-like homolog GhCYC2 from Gerbera. The expression of GhCYC2 follows a gradient along the radial axis of the inflorescence. GhCYC2 is expressed in the marginal, bilaterally symmetrical ray flowers but not in the centermost disk flowers, which are nearly radially symmetrical and have significantly less fused petals. Overexpression of GhCYC2 causes disk flowers to obtain morphologies similar to ray flowers. Both expression patterns and transgenic phenotypes suggest that GhCYC2 is involved in differentiation among Gerbera flower types, providing the first molecular evidence that CYC-like TCP factors take part in defining the complex inflorescence structure of the Asteraceae, a major determinant of the family's evolutionary success.CYCLOIDEA ͉ flower development ͉ evo-devo ͉ organ fusion
SummaryWe have used Gerbera hybrida (the cultivated ornamental, gerbera) to investigate the molecular basis of flower development in Asteraceae, a family of flowering plants that have heteromorphic flowers and specialized floral organs. Flowers of the same genotype may differ in a number of parameters, including sex expression, symmetry, sympetaly and pigmentation. In order to study the role of organ identity determination in these phenomena we isolated and functionally analysed six MADS box genes from gerbera; these were shown by phylogenetic analysis to be orthologous to well characterized regulatory genes described from Arabidopsis and Antirrhinum. Expression analysis suggests that the two gerbera agamous orthologues, the globosa orthologue and one of the deficiens orthologues may have functional equivalency to their counterparts, participating in the C and B functions, respectively. However, the function of a second deficiens orthologue appears unrelated to the B function, and that of a squamosa orthologue seems distinct from squamosa as well as from the A function. The induction patterns of gerbera MADS box genes conform spatiotemporally to the multi-flowered, head-like inflorescence typical of Asteraceae. Furthermore, gerbera plants transgenic for the newly isolated MADS box genes shed light onto the mechanistic basis for some floral characteristics that are typical for Asteraceae. We can conclude, therefore, that the pappus bristles are sepals highly modified for seed dispersal, and that organ abortion in the female marginal flowers is dependent upon organ
Plant-specific TCP domain transcription factors have been shown to regulate morphological novelties during plant evolution, including the complex architecture of the Asteraceae inflorescence that involves different types of flowers. We conducted comparative analysis of the CYCLOIDEA/TEOSINTE BRANCHED1 (CYC/TB1) gene family in Gerbera hybrida (gerbera) and Helianthus annuus (sunflower), two species that represent distant tribes within Asteraceae. Our data confirm that the CYC/TB1 gene family has expanded in Asteraceae, a condition that appears to be connected with the increased developmental complexity and evolutionary success of this large plant family. Phylogenetic analysis of the CYC/TB1 gene family revealed both shared and lineage-specific duplications in gerbera and sunflower, corresponding to the three gene lineages previously identified as specific to core eudicots: CYC1, CYC2, and CYC3. Expression analyses of early stages of flower primordia development indicated that especially within the CYC2 clade, with the greatest number of secondary gene duplications, gene expression patterns are conserved between the species and associated with flower and inflorescence development. All sunflower and gerbera CYC2 clade genes showed differential expression between developing flower types, being upregulated in marginal ray (and trans) flowers. One gene in gerbera (GhCYC3) and two in sunflower (HaCYC2d and HaCYC2c) were indicated to be strong candidates as regulators of ray flower identity, a function that is specific for Asteraceae. Our data further showed that other CYC2 clade genes are likely to have more specialized functions at the level of single flowers, including the late functions in floral reproductive organs that may be more conserved across plant families. The expression patterns of CYC1 and CYC3 clade genes showed more differences between the two species but still pointed to possible conserved functions during vegetative plant development. Pairwise protein-protein interaction assays gave the first molecular evidence that CYC/TB1-like proteins function in complexes. Compared with sunflower, the gerbera proteins showed higher capacity for dimerization, between as well as within CYC clades. Our data from two distant species within the Asteraceae suggest that the expansion and the apparent conservation of especially the CYC2 clade CYC/TB1-like genes are associated with the evolution of the increased complexity of the Asteraceae inflorescence architecture.
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