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Chromosomal-scale genome assembly and full spidroin gene set of T. clavata
To explore dragline silk production in T. clavata, we sought to assemble a high-quality genome of this species. Thus, we first performed a cytogenetic analysis of T. clavata captured from the wild in Dali City, Yunnan Province, China, and found a chromosomal complement of 2n = 26 in females and 2n = 24 in males, comprising eleven pairs of autosomal elements and unpaired sex chromosomes (X1X1X2X2 in females and X1X2 in males) (Fig. 1a). Then, DNA from adult T. clavata was used to generate long-read (Oxford Nanopore Technologies (ONT)), short-read (Illumina), and Hi-C data (Supplementary Data 1). A total of 349.95 Gb of Nanopore reads, 199.55 Gb of Illumina reads, and ~438.41 Gb of Hi-C raw data were generated. Our sequential assembly approach (Supplementary Fig. 1c) resulted in a 2.63 Gb genome with a scaffold N50 of 202.09 Mb and a Benchmarking Universal Single-Copy Ortholog (BUSCO) genome completeness score of 93.70% (Table 1; Supplementary Data 3). Finally, the genome was assembled into 13 pseudochromosomes. Sex-specific Pool-Seq analysis of spiders indicated that Chr12 and Chr13 were sex chromosomes (Fig. 1b; Supplementary Fig. 2). Based on the MAKER2 pipeline34 (Supplementary Fig. 1e), we annotated 37,607 protein-encoding gene models and predicted repetitive elements with a collective length of 1.42 Gb, accounting for 53.94% of the genome.Table 1 Characteristics of the T. clavata genome assemblyFull size tableTo identify T. clavata spidroin genes, we searched the annotated gene models for sequences similar to 443 published spidroins (Supplementary Data 6) and performed a phylogenetic analysis of the putative spidroin sequences for classification (Supplementary Fig. 12a). Based on the knowledge that a typical spidroin gene consists of a long repeat domain sandwiched between the nonrepetitive N/C-terminal domains16, 128 nonrepetitive hits were primarily identified. These candidates were further validated and reconstructed using full-length transcript isoform sequencing (Iso-seq) and transcriptome sequencing (RNA-seq) data. We thus identified 28 spidroin genes, among which 26 were full-length (Supplementary Fig. 11a), including 9 MaSps, 5 minor ampullate spidroins (MiSps), 2 flagelliform spidroins (FlSps), 1 tubuliform spidroin (TuSp), 2 aggregate spidroins (AgSp), 1 aciniform spidroin (AcSp), 1 pyriform spidroin (PySp), and 5 other spidroins. This full set of spidroin genes was located across nine of the 13 T. clavata chromosomes. Interestingly, we found that the MaSp1a–c & MaSp2e, MaSp2a–d, and MiSp-a–e genes were distributed in three independent groups on chromosomes 4, 7, and 6, respectively (Fig. 1c). Notably, using the genomic data of another orb-weaving spider species, Trichonephila antipodiana35, we identified homologous group distributions of spidroin genes on T. antipodiana chromosomes (Fig. 1d), which indicated the reliability of the grouping results of our study. When we compared the spidroin gene catalog of T. clavata and those of five other orb-web spider species with genomic data28,29,36,37, we found that T. clavata and Trichonephila clavipes possessed the largest number of spidroin genes (28 genes in both species; Fig. 1e).To further explore the expression of spidroin genes in different glands, all morphologically distinct glands (major and minor ampullate- (Ma and Mi), flagelliform- (Fl), tubuliform- (Tu), and aggregate (Ag) glands) were cleanly and separately dissected from adult female T. clavata spiders except for the aciniform and pyriform glands, which could not be cleanly separated because of their proximal anatomical locations and were therefore treated as a combined sample (aciniform & pyriform gland (Ac & Py)). After RNA sequencing of these silk glands, we performed expression clustering analysis of transcriptomic data and found that the Ma and Mi glands showed the closest relationship in terms of both morphological structure (Fig. 1g) and gene expression (Fig. 1f, h). We noted that the expression profiles of spidroin genes were largely consistent with their putative roles in the corresponding morphologically distinct silk glands; for example, MaSp expression was found in the Ma gland (Fig. 1h). However, some spidroin transcripts, such as MiSps and TuSp, were expressed in several silk glands (Fig. 1h). Unclassified spidroin genes, such as Sp-GP-rich, did not appear to show gland-specific expression (Fig. 1h).In summary, the chromosomal-scale genome of T. clavata allowed us to obtain detailed structural and location information for all spidroin genes of this species. We also found a relatively diverse set of spidroin genes and a grouped distribution of MaSps and MiSps in T. clavata.Dragline silk origin and the functional character of the Ma gland segmentsTo further evaluate the detailed molecular characteristics of the Ma gland-mediated secretion of dragline silk, we performed integrated analyses of the transcriptomes of the three T. clavata Ma gland segments and the proteome and metabolome of T. clavata dragline silk (Fig. 2a). Sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS–PAGE) analysis of dragline silk mainly showed a thick band above 240 kDa, suggesting a relatively small variety of total proteins (Fig. 2b). Subsequent liquid chromatography–mass spectrometry (LC–MS) analysis identified 28 proteins, including ten spidroins (nine MaSps and one MiSp) and 18 nonspidroin proteins (one glucose dehydrogenase (GDH), one mucin-19, one venom protein, and 15 SpiCEs of dragline silk (SpiCE-DS)) (Fig. 2b; Supplementary Data 10). Among these proteins, we found that the core protein components of dragline silk in order of intensity-based absolute quantification (iBAQ) percentages were MaSp1c (37.7%), MaSp1b (12.2%), SpiCE-DS1 (11.9%, also referred to as SpiCE-NMa1 in a previous study28), MaSp1a (10.4%), and MaSp-like (7.2%), accounting for approximately 80% of the total protein abundance in dragline silk (Fig. 2b). These results revealed potential protein components that might be highly correlated with the excellent strength and toughness of dragline silk.Fig. 2: Dragline silk origin and the functional character of the Ma gland segments.a Schematic illustration of Ma gland segmentation. b Sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS–PAGE) (left) and LC–MS (right) analyses of dragline silk protein. iBAQ, intensity-based absolute quantification. Similar results were obtained in three independent experiments and summarized in Source data. c Classification of the identified metabolites in dragline silk. d LC–MS analyses of the metabolites. e LC–MS analyses of the golden extract from T. clavata dragline silk. The golden pigment was extracted with 80% methanol. The extracted ion chromatograms (EICs) showed a peak at m/z 206 [M + H]+ for xanthurenic acid. f Pearson correlation of different Ma gland segments (Tail, Sac, and Duct). g Expression clustering of the Tail, Sac, and Duct. The transcriptomic data were clustered according to the hierarchical clustering (HC) method. h Combinational analysis of the transcriptome and proteome showing the expression profile of the dragline silk genes in the Tail, Sac, and Duct. i Concise biosynthetic pathway of xanthurenic acid (tryptophan metabolism) in the T. clavata Ma gland. Gene expression levels mapped to tryptophan metabolism are shown in three segments of the Ma gland. Enzymes involved in the pathway are indicated in red, and the genes encoding the enzymes are shown beside them. j Gene Ontology (GO) enrichment analysis of Ma gland segment-specific genes indicating the biological functions of the Tail, Sac, and Duct. The top 12 significantly enriched GO terms are shown for each segment of the Ma gland. A P-value  2) were identified in the 2 kb regions upstream and downstream of genes, and 10,501,151 (Tail), 11,356,55 (Sac), and 9,778,368 (Duct) significant ATAC peaks (RPKM  > 2) were identified at the whole-genome level. The Tail (mean RPKM: 1.78) and Sac (mean RPKM: 2.04) plots showed genes with more accessible chromatin than the Duct (mean RPKM: 1.59) plots (Fig. 3a). We then analyzed the genome-wide DNA methylation level in the Tail, Sac, and Duct. We found the highest levels of DNA methylation in the CG context (beta value: 0.12 in Tail, 0.13 in Sac, and 0.10 in Duct) and only a small amount in the CHH (beta value: 0.04 in Tail, 0.05 in Sac, and 0.03 in Duct) and CHG (beta value: 0.04 in Tail, 0.05 in Sac, and 0.04 in Duct) contexts (Fig. 3b). Overall, there was no significant difference in methylation levels among the Tail, Sac, and Duct. Taken together, our results suggest a potential regulatory role of CA rather than DNA methylation in the transcription of dragline silk genes.Fig. 3: Comprehensive epigenetic features and ceRNA network of the tri-sectional Ma gland.a Metagene plot of ATAC-seq signals and heatmap of the ATAC-seq read densities in the Tail, Sac, and Duct. The chromatin accessibility was indicated by the mean RPKM value (upper) and the blue region (bottom). b Metagene plot of DNA methylation levels in CG/CHG/CHH contexts in the Tail, Sac, and Duct. (c, d) Screenshots of the methylation and ATAC-seq tracks of the MaSp1b (c) and MaSp2b (d) genes within the Tail, Sac, and Duct. The potential TF motifs (E-value More

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