High-quality assembly and methylome of a Tibetan wild tree peony genome (Paeonia ludlowii) reveal the evolution of giant genome architecture.

Tree peony belongs to one of the Saxifragales families, Paeoniaceae. It is one of the most famous ornamental plants, and is also a promising woody oil plant. Although two Paeoniaceae genomes have been released, their assembly qualities are still to be improved. Additionally, more genomes from wild peonies are needed to accelerate genomic-assisted breeding. Here we assemble a high-quality and chromosome-scale 10.3-Gb genome of a wild Tibetan tree peony, Paeonia ludlowii, which features substantial sequence divergence, including around 75% specific sequences and gene-level differentials compared with other peony genomes. Our phylogenetic analyses suggest that Saxifragales and Vitales are sister taxa and, together with rosids, they are the sister taxon to asterids. The P. ludlowii genome is characterized by frequent chromosome reductions, centromere rearrangements, broadly distributed heterochromatin, and recent continuous bursts of transposable element (TE) movement in peony, although it lacks recent whole-genome duplication. These recent TE bursts appeared during the uplift and glacial period of the Qinghai-Tibet Plateau, perhaps contributing to adaptation to rapid climate changes. Further integrated analyses with methylome data revealed that genome expansion in peony might be dynamically affected by complex interactions among TE proliferation, TE removal, and DNA methylation silencing. Such interactions also impact numerous recently duplicated genes, particularly those related to oil biosynthesis and flower traits. This genome resource will not only provide the genomic basis for tree peony breeding but also shed light on the study of the evolution of huge genome structures as well as their protein-coding genes.

The content and diversity of carotenoids associated with high-altitude adaptation in Tibetan peach fruit.

Carotenoids are important secondary metabolites that may participate in response to extreme environments. Fruit color changes were observed in peaches growing at altitude on the Tibetan Plateau. Here, we qualitatively and quantitatively analyzed 43 kinds of carotenoids in 96 Tibetan peach and 12 cultivated peach fruit samples. Comparative analysis revealed that 25 kinds of carotenoids accumulated at significantly different levels between Tibetan peaches and cultivated peaches. Based on a population structure analysis, the carotenoid levels of Tibetan peaches were divided into two groups, which are mainly affected by the environmental factors light and temperature. The correlation analysis implied that the levels of 9 carotenoids were significantly correlated with altitude. qRT-PCR results showed that PSY, CCD4 and BCH were significantly differently expressed between the low and high altitude Tibetan peaches. In summary, this study showed that the abundant variation in carotenoids was highly associated with high-altitude adaptations in Tibetan peach fruit.

Genomic basis of high-altitude adaptation in Tibetan Prunus fruit trees.

The Great Himalayan Mountains and their foothills are believed to be the place of origin and development of many plant species. The genetic basis of adaptation to high plateaus is a fascinating topic that is poorly understood at the population level. We comprehensively collected and sequenced 377 accessions of Prunus germplasm along altitude gradients ranging from 2,067 to 4,492 m in the Himalayas. We de novo assembled three high-quality genomes of Tibetan Prunus species. A comparative analysis of Prunus genomes indicated a remarkable expansion of the SINE retrotransposons occurred in the genomes of Tibetan species. We observed genetic differentiation between Tibetan peaches from high and low altitudes and that genes associated with light stress signaling, especially UV stress signaling, were enriched in the differentiated regions. By profiling the metabolomes of Tibetan peach fruit, we determined 379 metabolites had significant genetic correlations with altitudes and that in particular phenylpropanoids were positively correlated with altitudes. We identified 62 Tibetan peach-specific SINEs that colocalized with metabolites differentially accumualted in Tibetan relative to cultivated peach. We demonstrated that two SINEs were inserted in a locus controlling the accumulation of 3-O-feruloyl quinic acid. SINE1 was specific to Tibetan peach. SINE2 was predominant in high altitudes and associated with the accumulation of 3-O-feruloyl quinic acid. These genomic and metabolic data for Prunus populations native to the Himalayan region indicate that the expansion of SINE retrotransposons helped Tibetan Prunus species adapt to the harsh environment of the Himalayan plateau by promoting the accumulation of beneficial metabolites.

Male Sterility is linked to the Flavonoid Biosynthesis Pathways in Prunus mira.

Sterility plays an important role in plant adaptation and evolution and has contributed to the development of high yielding crop hybrids. We used the widely targeted metabolomics profiling to survey the metabolites and biological pathways associated with male sterility in Prunus mira by comparing flowers from fertile and sterile trees. Male sterile flowers displayed abnormal stamen, uncolored anthers, and distorted and shrunken pollen grains with an apparent lack of turgidity. We report 566 metabolites in six flower samples and 140 differentially accumulated metabolites (DAMs) between both flower types. Most of the DAMs belong to the phenyl propanoid biosynthesis pathway, particularly flavonoid, flavone and flavonol biosynthesis pathways, implying that alterations in these key pathways link to male sterility in P. mira. The known link between low levels of flavonoid metabolites, weak expression levels of several structural genes from the phenyl propanoid biosynthesis pathway and hyper accumulation of reactive oxygen species were highlighted for understanding the underlying mechanism leading to the abnormal or aborted pollen grains observed in the sterile flowers. Data on the molecular mechanism of male sterility in Prunus mira will facilitate further in-depth investigations on this important agronomic and ecological trait.

Transcriptomic and metabolomic profiling provide novel insights into fruit development and flesh coloration in Prunus mira Koehne, a special wild peach species.

BACKGROUND: Flesh color is one of the most important traits for the commercial value of peach fruit. To unravel the underlying regulatory network in Prunus mira, we performed an integrated analysis of the transcriptome and metabolome of 3 fruit types with various flesh pigmentations (milk-white, yellow and blood) at 3 developmental stages (pit-hardening, cell enlargement and fruit ripening). RESULTS: Transcriptome analysis showed that an intense transcriptional adjustment is required for the transition from the pit-hardening to the cell enlargement stage. In contrast, few genes were differentially expressed (DEGs) from the cell enlargement to the fruit ripening stage and importantly, the 3 fruits displayed diverse transcriptional activities, indicating that difference in fruit flesh pigmentations mainly occurred during the ripening stage. We further investigated the DEGs between pairs of fruit types during the ripening stage and identified 563 DEGs representing the 'core transcriptome' associated with major differentiations between the 3 fruit types, including flesh pigmentation. Meanwhile, we analyzed the metabolome, particularly, at the ripening stage and uncovered 40 differential metabolites ('core metabolome') between the 3 fruit types including 5 anthocyanins, which may be the key molecules associated with flesh coloration. Finally, we constructed the regulatory network depicting the interactions between anthocyanins and important transcripts involved in fruit flesh coloration. CONCLUSIONS: The major metabolites and transcripts involved in fruit flesh coloration in P. mira were unraveled in this study providing valuable information which will undoubtedly assist in breeding towards improved fruit quality in peach.

Identification of Potential Metabolites Mediating Bird's Selective Feeding on Prunus mira Flowers.

In peach orchards, birds severely damage flowers during blossom season, decreasing the fruit yield potential. However, the wild peach species Prunus mira shows intraspecific variations of bird damage, indicating that some of the wild trees have developed strategies to avert bird foraging. Motivated by this observation, we formulated the present study to identify the potential flower metabolites mediating the bird's selective feeding behavior in P. mira flowers. The birds' preferred (FG) and avoided (BFT) flowers were collected from wild P. mira trees at three different locations, and their metabolite contents were detected, quantified, and compared. The widely-targeted metabolomics approach was employed to detect a diverse set of 603 compounds, predominantly, organic acids, amino acid derivatives, nucleotide and its derivatives, and flavones. By quantitatively comparing the metabolite contents between FG and BFT, three candidate metabolites, including Eriodictiol 6-C-hexoside 8-C-hexoside-O-hexoside, Luteolin O-hexosyl-O-hexosyl-O-hexoside, and Salvianolic acid A, were differentially accumulated and showed the same pattern across the three sampling locations. Distinctly, Salvianolic acid A was abundantly accumulated in FG but absent in BFT, implying that it may be the potential metabolite attracting birds in some P. mira flowers. Overall, this study sheds light on the diversity of the floral metabolome in P. mira and suggests that the bird's selective feeding behavior may be mediated by variations in floral metabolite contents.