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Fruits are the defining feature of angiosperms, likely have contributed to angiosperm successes by protecting and dispersing seeds, and provide foods to humans and other animals, with many morphological types and important ecological and agricultural implications. Rosaceae is a family with ∼3000 species and an extraordinary spectrum of distinct fruits, including fleshy peach, apple, and strawberry prized by their consumers, as well as dry achenetum and follicetum with features facilitating seed dispersal, excellent for studying fruit evolution. To address Rosaceae fruit evolution and other questions, we generated 125 new transcriptomic and genomic datasets and identified hundreds of nuclear genes to reconstruct a well-resolved Rosaceae phylogeny with highly supported monophyly of all subfamilies and tribes. Molecular clock analysis revealed an estimated age of ∼101.6 Ma for crown Rosaceae and divergence times of tribes and genera, providing a geological and climate context for fruit evolution. Phylogenomic analysis yielded strong evidence for numerous whole genome duplications (WGDs), supporting the hypothesis that the apple tribe had a WGD and revealing another one shared by fleshy fruit-bearing members of this tribe, with moderate support for WGDs in the peach tribe and other groups. Ancestral character reconstruction for fruit types supports independent origins of fleshy fruits from dry-fruit ancestors, including the evolution of drupes (e.g., peach) and pomes (e.g., apple) from follicetum, and drupetum (raspberry and blackberry) from achenetum. We propose that WGDs and environmental factors, including animals, contributed to the evolution of the many fruits in Rosaceae, which provide a foundation for understanding fruit evolution.

Phylogenetic relationships in Rosaceae have long been problematic because of frequent hybridisation, apomixis and presumed rapid radiation, and their historical diversification has not been clarified. With 87 genera representing all subfamilies and tribes of Rosaceae and six of the other eight families of Rosales (outgroups), we analysed 130 newly sequenced plastomes together with 12 from GenBank in an attempt to reconstruct deep relationships and reveal temporal diversification of this family. Our results highlight the importance of improving sequence alignment and the use of appropriate substitution models in plastid phylogenomics. Three subfamilies and 16 tribes (as previously delimited) were strongly supported as monophyletic, and their relationships were fully resolved and strongly supported at most nodes. Rosaceae were estimated to have originated during the Late Cretaceous with evidence for rapid diversification events during several geological periods. The major lineages rapidly diversified in warm and wet habits during the Late Cretaceous, and the rapid diversification of genera from the early Oligocene onwards occurred in colder and drier environments. Plastid phylogenomics offers new and important insights into deep phylogenetic relationships and the diversification history of Rosaceae. The robust phylogenetic backbone and time estimates we provide establish a framework for future comparative studies on rosaceous evolution.

Background Cerasus sachalinensis is widely used in cool regions as a sweet cherry rootstock and is known for its sensitivity to soil waterlogging and waterlogging stress. However, the limited availability of Cerasus genomic resources has considerably restricted the exploration of its waterlogging response mechanism. To understand its reaction to short-term waterlogging, we analyzed the physiology and transcriptomes of C. sachalinensis roots in response to different waterlogging durations. Results In this study, 12,487 differentially expressed genes (DEGs) were identified from Cerasus sachalinensis roots under different waterlogging durations. Carbon metabolism and energy maintenance formed the first coping mechanism stage of C. sachalinensis in response to low oxygen conditions. Root energy processes, including root respiration and activities of the fermentation enzymes alcohol dehydrogenase, pyruvate decarboxylase, and lactate dehydrogenase, showed unique changes after 0 h, 3 h, 6 h, and 24 h of waterlogging exposure. Ribonucleic acid sequencing was used to analyze transcriptome changes in C. sachalinensis roots treated with 3 h, 6 h, and 24 h of waterlogging stress. After de novo assembly, 597,474 unigenes were recognized, of which 355,350 (59.47%) were annotated. To identify the most important pathways represented by DEGs, Gene Ontology and Kyoto Encyclopedia of Genes and Genomes databases were used to compare these genes. The first stage of root reaction to waterlogging stress was activation of carbohydrate metabolism to produce more glucose and maintain energy levels. At 3 h, the glycolytic and fermentation pathways were activated to maintain adenosine triphosphate production. At 24 h, pathways involved in the translation of proteins were activated to further assist the plant in tolerating waterlogging stress. These findings will facilitate a further understanding of the potential mechanisms of plant responses to waterlogging at physiological and transcriptome levels. Conclusions Carbon metabolism and energy maintenance formed the first coping mechanism C. sachalinensis in response to low oxygen conditions, and they may be responsible for its short-term waterlogging response. Our study not only provides the assessment of genomic resources of Cerasus but also paves the way for probing the metabolic and molecular mechanisms underlying the short-term waterlogging response in C. sachalinensis .

Prunus mume (mei), which was domesticated in China more than 3,000 years ago as ornamental plant and fruit, is one of the first genomes among Prunus subfamilies of Rosaceae been sequenced. Here, we assemble a 280M genome by combining 101-fold next-generation sequencing and optical mapping data. We further anchor 83.9% of scaffolds to eight chromosomes with genetic map constructed by restriction-site-associated DNA sequencing. Combining P. mume genome with available data, we succeed in reconstructing nine ancestral chromosomes of Rosaceae family, as well as depicting chromosome fusion, fission and duplication history in three major subfamilies. We sequence the transcriptome of various tissues and perform genome-wide analysis to reveal the characteristics of P. mume , including its regulation of early blooming in endodormancy, immune response against bacterial infection and biosynthesis of flower scent. The P. mume genome sequence adds to our understanding of Rosaceae evolution and provides important data for improvement of fruit trees. The Prunus mume was domesticated in China over 3,000 years ago and is an important ornamental plant and fruit. Here Qixiang Zhang et al. obtain the first assembly of its genome with a combination of next-generation sequencing, whole-genome mapping and restriction-site-associated DNA.

The irreversible nature of reactions catalysed by P450s makes these enzymes landmarks in the evolution of plant metabolic pathways. Founding members of P450 families are often associated with general (i.e. primary) metabolic pathways, restricted to single copy or very few representatives, indicative of purifying selection. Recruitment of those and subsequent blooms into multi-member gene families generates genetic raw material for functional diversification, which is an inherent characteristic of specialized (i.e. secondary) metabolism. However, a growing number of highly specialized P450s from not only the CYP71 clan indicate substantial contribution of convergent and divergent evolution to the observed general and specialized metabolite diversity. We will discuss examples of how the genetic and functional diversification of plant P450s drives chemical diversity in light of plant evolution. Even though it is difficult to predict the function or substrate of a P450 based on sequence similarity, grouping with a family or subfamily in phylogenetic trees can indicate association with metabolism of particular classes of compounds. Examples will be given that focus on multi-member gene families of P450s involved in the metabolic routes of four classes of specialized metabolites: cyanogenic glucosides, glucosinolates, mono- to triterpenoids and phenylpropanoids.

DNA N6-methyladenine (6 mA) is one of the most vital epigenetic modifications and involved in controlling the various gene expression levels. With the avalanche of DNA sequences generated in numerous databases, the accurate identification of 6 mA plays an essential role for understanding molecular mechanisms. Because the experimental approaches are time-consuming and costly, it is desirable to develop a computation model for rapidly and accurately identifying 6 mA. To the best of our knowledge, we first proposed a computational model named i6mA-Fuse to predict 6 mA sites from the Rosaceae genomes, especially in Rosa chinensis and Fragaria vesca. We implemented the five encoding schemes, i.e., mononucleotide binary, dinucleotide binary, k-space spectral nucleotide, k-mer, and electron–ion interaction pseudo potential compositions, to build the five, single-encoding random forest (RF) models. The i6mA-Fuse uses a linear regression model to combine the predicted probability scores of the five, single encoding-based RF models. The resultant species-specific i6mA-Fuse achieved remarkably high performances with AUCs of 0.982 and 0.978 and with MCCs of 0.869 and 0.858 on the independent datasets of Rosa chinensis and Fragaria vesca, respectively. In the F. vesca-specific i6mA-Fuse, the MBE and EIIP contributed to 75% and 25% of the total prediction; in the R. chinensis-specific i6mA-Fuse, Kmer, MBE, and EIIP contribute to 15%, 65%, and 20% of the total prediction. To assist high-throughput prediction for DNA 6 mA identification, the i6mA-Fuse is publicly accessible at https://kurata14.bio.kyutech.ac.jp/i6mA-Fuse/.Key messageThe existing prediction models are not suitable to identify 6mA in the Rosaceae genome because the existing algorithms are species-specific. Thus, a novel predictor is desired to be established to identify 6mA sites in the Rosaceae genome. To the best of our knowledge, we first propose a computation model named i6mA-Fuse (Identification of N6-MethylAdenine sites by Fusing multiple feature representation) to predict 6mA sites from the Rosaceae genomes, especially in Rosa chinensis and Fragaria vesca.

Background The control of plant anthocyanin accumulation is via transcriptional regulation of the genes encoding the biosynthetic enzymes. A key activator appears to be an R2R3 MYB transcription factor. In apple fruit, skin anthocyanin levels are controlled by a gene called MYBA or MYB1 , while the gene determining fruit flesh and foliage anthocyanin has been termed MYB10 . In order to further understand tissue-specific anthocyanin regulation we have isolated orthologous MYB genes from all the commercially important rosaceous species. Results We use gene specific primers to show that the three MYB activators of apple anthocyanin ( MYB10/MYB1/MYBA) are likely alleles of each other. MYB transcription factors, with high sequence identity to the apple gene were isolated from across the rosaceous family (e.g. apples, pears, plums, cherries, peaches, raspberries, rose, strawberry). Key identifying amino acid residues were found in both the DNA-binding and C-terminal domains of these MYBs. The expression of these MYB10 genes correlates with fruit and flower anthocyanin levels. Their function was tested in tobacco and strawberry. In tobacco, these MYBs were shown to induce the anthocyanin pathway when co-expressed with bHLHs, while over-expression of strawberry and apple genes in the crop of origin elevates anthocyanins. Conclusions This family-wide study of rosaceous R2R3 MYBs provides insight into the evolution of this plant trait. It has implications for the development of new coloured fruit and flowers, as well as aiding the understanding of temporal-spatial colour change.

Background Gretchen Hagen 3 (GH3), one of the important auxin-responsive gene families, plays essential roles in plant growth, development process, and stress response by regulating hormone homeostasis. However, the evolutionary analysis of the GH3 gene family in Rosaceae species has not been well-studied and the specifc functions of Fragaria ananassa are not well-documented. Results In the current study, 64 members of the GH3 family genes were identifed from five Rosaceae species and divided into 8 groups. According to the comprehensive analysis of evolutionary relationship, collinearity, selection pressure and codon bias, the GH3 gene family was found to be highly conserved across these Rosaceae species, suggesting that purifying selection was a significant force in the evolution of GH3 genes, and the expansion of the GH3 gene family in Rosaceae species might be attributed to fragment duplication. Meanwhile, the codon bias of GH3s in subfamily G and K showed a relatively strong codon bias. Significantly, both FaGH3.17 and FaGH3.18 were localized in the cytoplasm and nucleus. Additionally, compared with the wild type (WT), the malondialdehyde (MDA) content and relative conductivity of FaGH3.17 and FaGH3.18 transgenic Arabidopsis were decreased, while the superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) activities were increased under drought stress. The above results indicate that overexpression of FaGH3.17 and FaGH3.18 signifcantly enhanced the tolerance to drought in transgenic Arabidopsis . Conclusions The study provides crucial insights into the evolution of the GH3 gene family in Rosaceae species and provides a theoretical basis for further investigation on the function of FaGH3s .

Abscisic acid (ABA) is a phytohormone that plays important roles in the regulation of plant growth, seed germination, and stress responses. The pyrabactin resistance 1-like (PYR/PYL) protein, an ABA receptor, was involved in the initial step in ABA signal transduction. However, the evolutionary history and characteristics of PYL genes expression remain unclear in Chinese white pear ( Pyrus bretschneideri ) or other Rosaceae species. In this study, 67 PYL genes were identified in eight Rosaceae species, and have been classified into three subgroups based on specific motifs and phylogenetic analysis. Intriguingly, we observed that whole-genome duplication (WGD) and dispersed duplication (DSD) have a major contribution to PYL family expansion. Purifying selection was the major force in PYL genes evolution. Expression analysis finds that PYL genes may function in multiple pear tissues. qRT-PCR validation of 11 PbrPYL genes indicates their roles in seed germination and abiotic stress responses. Our study provides a basis for further elucidation of the function of PYL genes and analysis of their expansion, evolution and expression patterns, which helps to understand the molecular mechanism of pear response to seed germination and seedling abiotic stress.

The GATA gene family is one of the most important transcription factors (TFs). It extensively exists in plants, contributes to diverse biological processes such as the development process, and responds to environmental stress. Although the GATA gene family has been comprehensively and systematically studied in many species, less is known about GATA genes in Chinese pears (Pyrus bretschneideri). In the current study, the GATA gene family in the four Rosaceae genomes was identified, its structural characteristics identified, and a comparative analysis of its properties was carried out. Ninety-two encoded GATA proteins were authenticated in the four Rosaceae genomes (Pyrus bretschneideri, Prunus avium, Prunus mume, and Prunus persica) and categorized into four subfamilies (Ⅰ–Ⅳ) according to phylogeny. The majority of GATA genes contained one to two introns and conserved motif composition analysis revealed their functional divergence. Whole-genome duplications (WGDs) and dispersed duplication (DSD) played a key role in the expansion of the GATA gene family. The microarray indicated that, among P. bretschneideri, P. avium, P. mume and P. persica, GATA duplicated regions were more conserved between Pyrus bretschneideri and Prunus persica with 32 orthologous genes pairs. The physicochemical parameters, duplication patterns, non-synonymous (ka), and synonymous mutation rate (ks) and GO annotation ontology were performed using different bioinformatics tools. cis-elements respond to various phytohormones, abiotic/biotic stress, and light-responsive were found in the promoter regions of GATA genes which were induced via stimuli. Furthermore, subcellular localization of the PbGATA22 gene product was investigated, showing that it was present in the nucleus of tobacco (Nicotiana tabacum) epidermal cells. Finally, in silico analysis was performed on various organs (bud, leaf, stem, ovary, petal, and sepal) and different developmental stages of fruit. Subsequently, the expression profiles of PbGATA genes were extensively expressed under exogenous hormonal treatments of SA (salicylic acid), MeJA (methyl jasmonate), and ABA (abscisic acid) indicating that play important role in hormone signaling pathways. A comprehensive analysis of GATA transcription factors was performed through systematic biological approaches and comparative genomics to establish a theoretical base for further structural and functional investigations in Rosaceae species.