Abstract
Parasitic plants have evolved to be subtly or severely dependent on host plants to complete their life cycle. To provide new insights into the biology of parasitic plants in general, we assembled genomes for members of the sandalwood order Santalales, including a stem hemiparasite (Scurrula) and two highly modified root holoparasites (Balanophora) that possess chimaeric host–parasite tubers. Comprehensive genome comparisons reveal that hemiparasitic Scurrula has experienced a relatively minor degree of gene loss compared with autotrophic plants, consistent with its moderate degree of parasitism. Nonetheless, patterns of gene loss appear to be substantially divergent across distantly related lineages of hemiparasites. In contrast, Balanophora has experienced substantial gene loss for the same sets of genes as an independently evolved holoparasite lineage, the endoparasitic Sapria (Malpighiales), and the two holoparasite lineages experienced convergent contraction of large gene families through loss of paralogues. This unprecedented convergence supports the idea that despite their extreme and strikingly divergent life histories and morphology, the evolution of these and other holoparasitic lineages can be shaped by highly predictable modes of genome reduction. We observe substantial evidence of relaxed selection in retained genes for both hemi- and holoparasitic species. Transcriptome data also document unusual and novel interactions between Balanophora and host plants at the host–parasite tuber interface tissues, with evidence of mRNA exchange, substantial and active hormone exchange and immune responses in parasite and host.
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Data availability
The raw genomic and transcriptomic data, genome assemblies and annotations have been deposited to the China National GeneBank (CNGB) Sequence Archive (CNSA)104 with accession number CNP0003054. The genome assemblies and annotations have also been deposited to the National Genomics Data Center (NGDC) with accession number PRJCA018288. The datasets used for comparative genome analysis are listed in Supplementary Table 1a. The databases used for annotation are listed in Supplementary Table 1q. All supplementary data are available in the figshare repository at https://doi.org/10.6084/m9.figshare.21721358.
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Acknowledgements
We thank Y. Guo (Chinese Academy of Sciences), X. Li (University of British Columbia), C. Davis (Harvard University), S. Wanke (Technische Universität Dresden) and S. Stefanović (University of Toronto) for discussion. This project was supported by the Shenzhen Municipal Government of China (No. JCYJ20160331150739027 to X.C., and KCXFZ20201221173013035 to H.L.), the Key Laboratory of Genomics, Ministry of Agriculture, BGI‐Shenzhen, Shenzhen, China, and the China National GeneBank (CNGB; https://www.cngb.org/). This work is part of the 10KP project (https://db.cngb.org/10kp/).
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H.L. and X.C. led and designed the project. H.L., S.W.G. and X.C. conceived the study. X.C., D.F., S.Yang., K.D., H.F., C.W., Y.B., R.Y., S.P., W.Z. and Q.Y. contributed to sample preparation. C.W. constructed libraries for sequencing. D.F. and S.Yang. performed the genome assembly. X.C., D.F., Y.X., S.Yang., K.D., H.F., M.L., Y.L., F.W., W.M., X.G., D.S., Y.C., Y.F., S.K.S. and S.P. performed annotation and comparative genomic analyses. S.Yoshida. performed the gene family expansion and contraction analysis, and HGT analysis. X.C. and D.F. wrote the original draft manuscript. Y.X., S.K.S., Y.W., Z.-J.L., X.L., X.X., H.Y., J.W., S.Yoshida., S.W.G. and H.L. revised and edited the manuscript. All authors read and approved the final manuscript.
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Extended data
Extended Data Fig. 2 The biosynthesis pathway of carotenoid and ABA in Balanophora.
The major ABA biosynthesis pathway through ZEP is colored in blue, and the alternative ZEP-independent pathway is colored in orange. Gene products in red are absent; black are present; and skyblue are unknown (see also in Supplementary Table 3s and 5l). AAO3, abscisic aldehyde oxidase 3; AO, Aldehyde Oxidase; ABA2, ABA deficient 2; ABA3, ABA deficient 3; ABA4, ABA deficient 4; BCH, beta carotene hydroxylase; CCD, carotenoid cleavage dioxygenase; CRTISO, carotenoid isomerase; CYP97A3, cytochrome P450 97A3; CYP97C1, cytochrome P450 97C1; GA3P, glyceraldehyde-3-phosphate; GGPP, geranylgeranyl pyrophosphate; LCYB, lycopene beta cyclase; LUT, lycopene epsilon cyclase; NCED, 9-cis-epoxycarotenoid dioxygenase; NSY, neoxanthin synthase; NXS, neoxanthin synthase; PDS, phytoene desaturase; PSY, phytoene synthase; ROS, reactive oxygen species; SDR, short chain dehydrogenase; VDE, violaxanthin de-epoxidase; ZDS, z-carotene desaturase; ZEP, zeaxanthin epoxidase; Z-ISO, ζ carotene isomerase.
Extended Data Fig. 3 Hormone interaction between Balanophora and host.
a. The ABA, ABA glucosyl ester (ABA-GE), concentration in inflorescence, tuber of Balanophora, and host root. The box plot shows first quartile, median, and third quartile (n = 3 biologically independent samples). b. The expression levels of ABA signaling genes from Balanophora in different tissues and growing stages, genes in dotted box show ABA signaling and maker genes upregulated in inflorescence. c. The expression of host ABA biosynthesis genes, genes in dotted box are ABA biosynthesis genes highly expressed in tubers. d. The SA, SA 2-O-β-D-Glucoside (SAG) concentration in inflorescence, tuber of Balanophora, and host root. Box plot shows first quartile, median, and third quartile (n = 3 biologically independent samples). e. The expression of salicylic acid biosynthesis, metabolism and signaling genes from Balanophora; dotted box represents SA metabolism genes upregulated in JU1. f. The expression of host SA biosynthesis genes, genes in dotted box are SA biosynthesis genes highly expressed in tubers. Tissue abbreviations are listed in Supplementary Fig. 1d–h and Methods section. In B-C, and E-F, each row represents the expression of each gene in a different sample, and each column represents the expression of genes in each sample. The upper tree represents a cluster analysis for different samples of different groups and stages, and the left tree represents the cluster analysis for different genes from different samples. g. Putative models of hormone interactions between Balanophora and the host. Cells walls from Balanophora or host are colored in orange vs. green respectively, in tissues including the inflorescence from Balanophora (IF), root from the host (RO), parasite-root junction (JU), and chimeric tuber containing both cells of Balanophora and host (TU). Genes from Balanophora or host that are upregulated in corresponding tissues are colored in red vs. blue. Hormone biosynthesis, metabolism and signaling genes are pentagons, rectangles, and ovals, respectively. Small circles with different colors are different hormones.
Extended Data Fig. 4 The violin plot showing the distribution of nonsynonymous substitution rate (dN), synonymous substitution rate (dS), and the seletion pressure ω(dN/dS) for 2,729 orthologs in 21 species.
The grey dots represent the observed values for each species. The box plot in each violin plot shows first quartile, median, and third quartile of the dN, dS or dN/dS value from 2,729 orthologs for each species. The black circles indicate the outliers. The colors of species names indicate different types of parasitism, as in Extended Data Fig. 1 and the details of species are described in Supplementary Table 1a.
Extended Data Fig. 5 Selection intensity shift in parasitic plants.
a. Distribution of selection intensity (k value) for four lineages of parasitic plants and their autotrophic relatives across 2,729 orthologs retained in all species analysed here. Selection intensity is presented according to the k parameter in RELAX using general descriptive RELAX model. The box plot in each violin plot shows first quartile, median, and third quartile of the k value from 2,729 orthologs for each species. In addition to Arabidopsis and Vitis, four lineages of parasitic plants and their close relatives are included. The colors of species show different lifestyles of parasitism as Extended Data Fig. 1 and details of species in Supplementary Table 1a. b. Selection changes per branch are colour-coded according to the selection strength parameter k as in A. Low k (<1, red) indicates relaxation of selection, whereas high k (>1, blue) suggests selection intensification. c. The violin distribution of selection intensity according to different gene family sizes for three parasitic plants in Santalales (test species). We chose those common multiple/single gene families shared in autotrophs (cluster 3, and cluster 1 in Fig. 4a, respectively), three categories are compared between each other including: (i) remaining multigene families in each test species, respectively; (ii) those multigene families in autotrophs but change to singleton in test species; (iii) remaining single gene families in autotrophs and also in reference species. The box plot in each violin plot shows first quartile, median, and third quartile. The numbers of gene family for three categories in each species are listed. The two-sided Wilcoxon signed rank test was performed for pair of two categories, and the p values were listed.
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Chen, X., Fang, D., Xu, Y. et al. Balanophora genomes display massively convergent evolution with other extreme holoparasites and provide novel insights into parasite–host interactions. Nat. Plants 9, 1627–1642 (2023). https://doi.org/10.1038/s41477-023-01517-7
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DOI: https://doi.org/10.1038/s41477-023-01517-7
