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In plants, parasitism triggers the reductive evolution of plastid genomes (plastomes). To disentangle the molecular evolutionary associations between feeding on other plants below- or aboveground and general transitions from facultative to obligate parasitism, we analyzed 34 complete plastomes of autotrophic, root- and stem-feeding hemiparasitic, and holoparasitic Santalales. We observed inexplicable losses of housekeeping genes and tRNAs in hemiparasites and dramatic genomic reconfiguration in holoparasitic Balanophoraceae, whose plastomes have exceptionally low GC contents. Genomic changes are related primarily to the evolution of hemi- or holoparasitism, whereas the transition from a root- to a stem-feeding mode plays no major role. In contrast, the rate of molecular evolution accelerates in a stepwise manner from autotrophs to root- and then stem-feeding parasites. Already the ancestral transition to root-parasitism coincides with a relaxation of selection in plastomes. Another significant selectional shift in plastid genes occurs as stem-feeders evolve, suggesting that this derived form coincides with trophic specialization despite the retention of photosynthetic capacity. Parasitic Santalales fill a gap in our understanding of parasitism-associated plastome degeneration. We reveal that lifestyle-genome associations unfold interdependently over trophic specialization and feeding mode transitions, where holoparasitic Balanophoraceae provide a system for exploring the functional realms of plastomes.

Background Genome sequencing has been widely used in plant research to construct reference genomes and provide evolutionary insights. However, few plant species have had their whole genome sequenced, thus restraining the utility of these data. We collected 1,093 samples of vascular plant species growing in the Ruili Botanical Garden, located in southwest China. Of these, we sequenced 761 samples and collected voucher specimens stored in the Herbarium of China National GeneBank. Results The 761 sequenced samples represented 689 vascular plant species from 137 families belonging to 49 orders. Of these, 257 samples were identified to the species level and 504 to the family level, using specimen and chloroplast sequences. In total, we generated 54 Tb of sequencing data, with an average sequencing depth of 60X per species, as estimated from genome sizes. A reference phylogeny was reconstructed with 78 chloroplast genes for molecular identification and other possible applications. Conclusions The large dataset of vascular plant genomes generated in this study, which includes both high-depth whole-genome sequencing data and associated voucher specimens, is valuable for plant genome research and other applications. This project also provides insight into the feasibility and technical requirements for “planetary-scale” projects such as the 10,000 Plant Genomes Project and the Earth BioGenome Project.

Genetic and environmental factors collectively determine plant growth and yield. In the past 20 years, genome-wide association studies (GWAS) have been conducted on crops to decipher genetic loci that contribute to growth and yield, however, plant genotype appears to be insufficient to explain the trait variations. Here, we unravel the associations between genotypic, phenotypic, and rhizoplane microbiota variables of 827 foxtail millet cultivars by an integrated GWAS, microbiome-wide association studies (MWAS) and microbiome genome-wide association studies (mGWAS) method. We identify 257 rhizoplane microbial biomarkers associated with six key agronomic traits and validated the microbial-mediated growth effects on foxtail millet using marker strains isolated from the field. The rhizoplane microbiota composition is mainly driven by variations in plant genes related to immunity, metabolites, hormone signaling and nutrient uptake. Among these, the host immune gene FLS2 and transcription factor bHLH35 are widely associated with the microbial taxa of the rhizoplane. We further uncover a plant genotype-microbiota interaction network that contributes to phenotype plasticity. The microbial-mediated growth effects on foxtail millet are dependent on the host genotype, suggesting that precision microbiome management could be used to engineer high-yielding cultivars in agriculture systems.

Summary Dipterocarpaceae are typical tropical plants (dipterocarp forests) that are famous for their high economic value because of their production of fragrant oleoresins, top‐quality timber and usage in traditional Chinese medicine. Currently, the lack of Dipterocarpaceae genomes has been a limiting factor to decipher the fragrant oleoresin biosynthesis and gain evolutionary insights into high‐quality wood formation in Dipterocarpaceae. We generated chromosome‐level genome assemblies for two representative Dipterocarpaceae species viz. Dipterocarpus turbinatus Gaertn. f. and Hopea hainanensis Merr. et Chun. Our whole‐genome duplication (WGD) analysis revealed that Dipterocarpaceae underwent a shared WGD event, which showed significant impacts on increased copy numbers of genes related to the biosynthesis of terpene, BAHD acyltransferases, fatty acid and benzenoid/phenylpropanoid, which probably confer to the formation of their characteristic fragrant oleoresin. Additionally, compared with common soft wood plants, the expansion of gene families was also found to be associated with wood formation, such as in CESA (cellulose synthase), CSLE (cellulose synthase‐like protein E), laccase and peroxidase in Dipterocarpaceae genomes, which might also contribute to the formation of harder, stronger and high‐density timbers. Finally, an integrative analysis on a combination of genomic, transcriptomic and metabolic data from different tissues provided further insights into the molecular basis of fragrant oleoresins biosynthesis and high‐quality wood formation of Dipterocarpaceae. Our study contributes the first two representative genomes for Dipterocarpaceae, which are valuable genetic resources for further researches on the fragrant oleoresins and superior‐quality timber, genome‐assisted breeding and improvement, and conservation biology of this family.