Characterization of novel pollen-expressed transcripts reveals their potential roles in pollen heat stress response in Arabidopsis thaliana

Key message: Arabidopsis pollen transcriptome analysis revealed new intergenic transcripts of unknown function, many of which are long non-coding RNAs, that may function in pollen-specific processes, including the heat stress response. Abstract: The male gametophyte is the most heat sensitive of all plant tissues. In recent years, long noncoding RNAs (lncRNAs) have emerged as important components of cellular regulatory networks involved in most biological processes, including response to stress. While examining RNAseq datasets of developing and germinating Arabidopsis thaliana pollen exposed to heat stress (HS), we identified 66 novel and 246 recently annotated intergenic expressed loci (XLOCs) of unknown function, with the majority encoding lncRNAs. Comparison with HS in cauline leaves and other RNAseq experiments indicated that 74% of the 312 XLOCs are pollen-specific, and at least 42% are HS-responsive. Phylogenetic analysis revealed that 96% of the genes evolved recently in Brassicaceae. We found that 50 genes are putative targets of microRNAs and that 30% of the XLOCs contain small open reading frames (ORFs) with homology to protein sequences. Finally, RNAseq of ribosome-protected RNA fragments together with predictions of periodic footprint of the ribosome P-sites indicated that 23 of these ORFs are likely to be translated. Our findings indicate that many of the 312 unknown genes might be functional and play a significant role in pollen biology, including the HS response

Serine/Threonine protein kinases from bacteria, archaea and eukarya share a common evolutionary origin deeply rooted in the tree of life

The main family of serine/threonine/tyrosine protein kinases present in eukarya was defined and described by Hanks et al. in 1988 (Science, 241, 42–52). It was initially believed that these kinases do not exist in bacteria, but extensive genome sequencing revealed their existence in many bacteria. For historical reasons, the term “eukaryotic-type kinases” propagated in the literature to describe bacterial members of this protein family. Here, we argue that this term should be abandoned as a misnomer, and we provide several lines of evidence to support this claim. Our comprehensive phylostratigraphic analysis suggests that Hanks-type kinases present in eukarya, bacteria and archaea all share a common evolutionary origin in the lineage leading to the last universal common ancestor (LUCA). We found no evidence to suggest substantial horizontal transfer of genes encoding Hanks-type kinases from eukarya to bacteria. Moreover, our systematic structural comparison suggests that bacterial Hanks-type kinases resemble their eukaryal counterparts very closely, while their structures appear to be dissimilar from other kinase families of bacterial origin. This indicates that a convergent evolution scenario, by which bacterial kinases could have evolved a kinase domain similar to that of eukaryal Hanks-type kinases, is not very likely. Overall, our results strongly support a monophyletic origin of all Hanks-type kinases, and we therefore propose that this term should be adopted as a universal name for this protein family

Strong evidence for the adaptive walk model of gene evolution in Drosophila and Arabidopsis

Understanding the dynamics of species adaptation to their environments has long been a central focus of the study of evolution. Theories of adaptation propose that populations evolve by “walking” in a fitness landscape. This “adaptive walk” is characterised by a pattern of diminishing returns, where populations further away from their fitness optimum take larger steps than those closer to their optimal conditions. Hence, we expect young genes to evolve faster and experience mutations with stronger fitness effects than older genes because they are further away from their fitness optimum. Testing this hypothesis, however, constitutes an arduous task. Young genes are small, encode proteins with a higher degree of intrinsic disorder, are expressed at lower levels, and are involved in species-specific adaptations. Since all these factors lead to increased protein evolutionary rates, they could be masking the effect of gene age. While controlling for these factors, we used population genomic data sets of Arabidopsis and Drosophila and estimated the rate of adaptive substitutions across genes from different phylostrata. We found that a gene’s evolutionary age significantly impacts the molecular rate of adaptation. Moreover, we observed that substitutions in young genes tend to have larger physicochemical effects. Our study, therefore, provides strong evidence that molecular evolution follows an adaptive walk model across a large evolutionary timescale

Genome-wide and single-base resolution DNA methylomes of the Pacific oyster <i>Crassostrea gigas</i> provide insight into the evolution of invertebrate CpG methylation

BACKGROUND: Studies of DNA methylomes in a wide range of eukaryotes have revealed both conserved and divergent characteristics of DNA methylation among phylogenetic groups. However, data on invertebrates particularly molluscs are limited, which hinders our understanding of the evolution of DNA methylation in metazoa. The sequencing of the Pacific oyster Crassostrea gigas genome provides an opportunity for genome-wide profiling of DNA methylation in this model mollusc. RESULTS: Homologous searches against the C. gigas genome identified functional orthologs for key genes involved in DNA methylation: DNMT1, DNMT2, DNMT3, MBD2/3 and UHRF1. Whole-genome bisulfite sequencing (BS-seq) of the oyster’s mantle tissues revealed that more than 99% methylation modification was restricted to cytosines in CpG context and methylated CpGs accumulated in the bodies of genes that were moderately expressed. Young repeat elements were another major targets of CpG methylation in oysters. Comparison with other invertebrate methylomes suggested that the 5’-end bias of gene body methylation and the negative correlation between gene body methylation and gene length were the derived features probably limited to the insect lineage. Interestingly, phylostratigraphic analysis showed that CpG methylation preferentially targeted genes originating in the common ancestor of eukaryotes rather than the oldest genes originating in the common ancestor of cellular organisms. CONCLUSIONS: Comparative analysis of the oyster DNA methylomes and that of other animal species revealed that the characteristics of DNA methylation were generally conserved during invertebrate evolution, while some unique features were derived in the insect lineage. The preference of methylation modification on genes originating in the eukaryotic ancestor rather than the oldest genes is unexpected, probably implying that the emergence of methylation regulation in these 'relatively young’ genes was critical for the origin and radiation of eukaryotes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1119) contains supplementary material, which is available to authorized users

Comparative transcriptone analysis in the moss Physcomitrella patens and the genetic basis of key reproductive innovations

During land plant evolution plants underwent extensive transformations. For the successful adaptation to the terrestrial environment the vegetative tissues were modified to cope with low water availability while new reproductive organs and strategies emerged to ensure plant dispersal and survival. Importantly, plant life cycles were dramatically modified, evolving from gametophyte dominant in early land plants such as Bryophytes to sporophyte dominance as it is observed in flowering plants.(...

Genomic phylostratigraphy

Makroevolucija, često definirana kao “evolucija iznad razine vrste”, tradicionalno se proučava analizom fosila, komparativnom morfologijom ili tzv. evo-devo pristupom. Korištenjem komparativne genomike moguće je rekonstruirati evolucijsku povijest na dodatnoj razini, metodom genomske filostratigrafije. Genomsku filostratigrafiju razvio je Tomislav Domazet-Lošo s Instituta Ruđer Bošković u Zagrebu. Ova novija statistička metoda koristi se za povezivanje evolucijskog porijekla obitelji osnivačkih gena s određenim makroevolucijskim tranzicijama. Pretpostavka je da će porijeklo složenih fenotipskih inovacija biti udruženo s pojavom takvih osnivačkih gena čiji se potomci mogu pronaći u danas živućim organizmima. Suština metode je podjela genoma u tzv. filostratume – skupine gena definiranih na temelju njihovog evolucijskog porijekla. Ovom je metodom postalo moguće identificirati sve orphan gene koji su doveli do postojećih genoma unutar evolucijskih linija, ali i pratiti važne makroevolucijske adaptacije kao što su pojava zametnih listića ili porijeklo gena povezanih uz nastanak raka. Također, genomska filostratigrafija potvrdila je postojanje filotipske faze u razvoju životinja i biljaka. Ipak, mogu li računalne simulacije stvarno obuhvatiti pravu kompleksnost evolucije?Macroevolution, which is often defined as “evolution above the species level”, is traditionally studied by fossil analysis, comparative morphology or evo-devo approaches. With the use of comparative genomics one can nowadays reconstruct the evolutionary history on additional level of analysis by genomic phylostratigraphy. Genomic phylostratigraphy was developed by Tomislav Domazet-Lošo at the Ruđer Bošković Institute in Zagreb, Croatia. This novel statistical method is used to correlate the evolutionary origin of founder gene families to particular macroevolutionary transitions. It is assumed that the origin of complex phenotypic innovations will be accompanied by the emergence of such founder genes, the descendants of which can still be traced in extant organisms. Method is based on the genome divison into phylostrata - classes of genes according to their evolutionary origin in the history of life. With this method it has become possible to identify all orphan genes within the evolutionary lineages that have led to a particular extant genome and to trace the origin of major macroevolutionary adaptations such as emergence of germ layers or origin of cancer genes. Also, genomic phylostratigraphy confirmed the existence of phylotypic stage in animal and plant development. However, how well can computer simulations really capture the true complexity of evolution

Pluripotency and the origin of animal multicellularity

Funding: This study was supported by funds from the Australian Research Council (B.M.D. and S.M.D.).A widely held—but rarely tested—hypothesis for the origin of animals is that they evolved from a unicellular ancestor, with an apical cilium surrounded by a microvillar collar, that structurally resembled modern sponge choanocytes and choanoflagellates1,2,3,4. Here we test this view of animal origins by comparing the transcriptomes, fates and behaviours of the three primary sponge cell types—choanocytes, pluripotent mesenchymal archaeocytes and epithelial pinacocytes—with choanoflagellates and other unicellular holozoans. Unexpectedly, we find that the transcriptome of sponge choanocytes is the least similar to the transcriptomes of choanoflagellates and is significantly enriched in genes unique to either animals or sponges alone. By contrast, pluripotent archaeocytes upregulate genes that control cell proliferation and gene expression, as in other metazoan stem cells and in the proliferating stages of two unicellular holozoans, including a colonial choanoflagellate. Choanocytes in the sponge Amphimedon queenslandica exist in a transient metastable state and readily transdifferentiate into archaeocytes, which can differentiate into a range of other cell types. These sponge cell-type conversions are similar to the temporal cell-state changes that occur in unicellular holozoans5. Together, these analyses argue against homology of sponge choanocytes and choanoflagellates, and the view that the first multicellular animals were simple balls of cells with limited capacity to differentiate. Instead, our results are consistent with the first animal cell being able to transition between multiple states in a manner similar to modern transdifferentiating and stem cells.PostprintPeer reviewe