Expression divergence of expansin genes drive the heteroblasty in Ceratopteris chingii
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Date
Authors
Zhang, Yue
Van de Peer, Yves
Lu. Bei
Zhang, Sisi
Che, Jingru
Chen, Jinming
Marchal, Kathleen
Yang, Xingyu
Journal Title
Journal ISSN
Volume Title
Publisher
BMC
Abstract
BACKGROUND : Sterile-fertile heteroblasty is a common phenomenon observed in ferns, where the leaf shape
of a fern sporophyll, responsible for sporangium production, differs from that of a regular trophophyll. However,
due to the large size and complexity of most fern genomes, the molecular mechanisms that regulate the formation
of these functionally different heteroblasty have remained elusive. To shed light on these mechanisms, we generated
a full-length transcriptome of Ceratopteris chingii with PacBio Iso-Seq from five tissue samples. By integrating
Illumina-based sequencing short reads, we identified the genes exhibiting the most significant differential expression
between sporophylls and trophophylls.
RESULTS : The long reads were assembled, resulting in a total of 24,024 gene models. The differential expressed genes
between heteroblasty primarily involved reproduction and cell wall composition, with a particular focus on expansin
genes. Reconstructing the phylogeny of expansin genes across 19 plant species, ranging from green algae
to seed plants, we identified four ortholog groups for expansins. The observed high expression of expansin genes
in the young sporophylls of C. chingii emphasizes their role in the development of heteroblastic leaves. Through gene
coexpression analysis, we identified highly divergent expressions of expansin genes both within and between species.
CONCLUSIONS : The specific regulatory interactions and accompanying expression patterns of expansin genes are associated
with variations in leaf shapes between sporophylls and trophophylls.
Description
AVAILABILITY OF DATA AND MATERIALS : The PacBio full-length sequencing dataset generated for this work is accessible through NCBI Sequence Read Archive (SRA) under accession number PRJNA924672 [74]. The Illumina RNA-seq dataset is accessible through NCBI SRA accession number PRJNA924581 [75].
ADDITIONAL FILE 1. FIG. S1. Density distribution of raw reads and full-length non-chimeric reads obtained by PacBio Iso-seq. FIG. S2. RT-PCR validation of nine high-confident gene models. FIG. S3. The UpSet plot summarizes the presence of genes in five databases. FIG. S4. The pie diagrams showing the number of transcription factors in different families. FIG. S5. GO enrichment analysis of differentially expressed genes in the comparisons of sporophyll-S1 vs trophophyll-S2, sporophyll-S2 vs trophophyll-S1, and sporophyll-S2 vs trophophyll-S2. FIG. S6. Heatmap showing the differential and non-differential expression of the expansin genes in different pairwise comparisons as obtained from transcriptome analysis. FIG. S7. Phylogenetic tree of expansins in C. chingii and A. thaliana, built with Maximum likelihood. FIG. S8. Analysis of conserved domains of the CcEXP proteins. FIG. S9. Phylogenetic profiling of four groups of expansin genes in 19 species. FIG. S10. Bar plots showing the differentially expressed expansin genes in pteridophyte-specific groups. FIG. S11. GO enrichment analysis of genes that were identified to be significantly coexpressed with CcEXP genes. FIG. S12. Heatmap showing the member number of transcription factors in different families that are coexpressed with at least one CcEXP gene in the four groups. FIG. S13. Yeast two-hybrid assay showing how CcFL01489 interacts with three transcription factor (CcFL09745, CcFL03547, and CcFL06843). FIG. S14. Gene coexpression networks of CrEXP (A) and AtEXP (B) genes of the different groups. FIG. S15. GO enrichment analysis of genes that were identified to be significantly coexpressed with AtEXP (A) and CcEXP (B) genes in group IV.
ADDITIONAL FILE 2. TABLE S1. EXP genes in C. chingii. TABLE S2. Topology of EXP gene tree of 19 species. TABLE S3. Correlation coefficient of FPKM and relative expression in CcEXP genes. TABLE S4. Summer of lncRNA targeted genes. TABLE S5. Summary of the RNA-Seq samples in this study. TABLE S6. Summary of the RT-PCR primer for validating the splicing events. TABLE S7. Summary of the qRT-PCR primer for expansin genes. TABLE S8. Summer of Yeast two-hybrid primer.
ADDITIONAL FILE 1. FIG. S1. Density distribution of raw reads and full-length non-chimeric reads obtained by PacBio Iso-seq. FIG. S2. RT-PCR validation of nine high-confident gene models. FIG. S3. The UpSet plot summarizes the presence of genes in five databases. FIG. S4. The pie diagrams showing the number of transcription factors in different families. FIG. S5. GO enrichment analysis of differentially expressed genes in the comparisons of sporophyll-S1 vs trophophyll-S2, sporophyll-S2 vs trophophyll-S1, and sporophyll-S2 vs trophophyll-S2. FIG. S6. Heatmap showing the differential and non-differential expression of the expansin genes in different pairwise comparisons as obtained from transcriptome analysis. FIG. S7. Phylogenetic tree of expansins in C. chingii and A. thaliana, built with Maximum likelihood. FIG. S8. Analysis of conserved domains of the CcEXP proteins. FIG. S9. Phylogenetic profiling of four groups of expansin genes in 19 species. FIG. S10. Bar plots showing the differentially expressed expansin genes in pteridophyte-specific groups. FIG. S11. GO enrichment analysis of genes that were identified to be significantly coexpressed with CcEXP genes. FIG. S12. Heatmap showing the member number of transcription factors in different families that are coexpressed with at least one CcEXP gene in the four groups. FIG. S13. Yeast two-hybrid assay showing how CcFL01489 interacts with three transcription factor (CcFL09745, CcFL03547, and CcFL06843). FIG. S14. Gene coexpression networks of CrEXP (A) and AtEXP (B) genes of the different groups. FIG. S15. GO enrichment analysis of genes that were identified to be significantly coexpressed with AtEXP (A) and CcEXP (B) genes in group IV.
ADDITIONAL FILE 2. TABLE S1. EXP genes in C. chingii. TABLE S2. Topology of EXP gene tree of 19 species. TABLE S3. Correlation coefficient of FPKM and relative expression in CcEXP genes. TABLE S4. Summer of lncRNA targeted genes. TABLE S5. Summary of the RNA-Seq samples in this study. TABLE S6. Summary of the RT-PCR primer for validating the splicing events. TABLE S7. Summary of the qRT-PCR primer for expansin genes. TABLE S8. Summer of Yeast two-hybrid primer.
Keywords
Expansin, Ferns, Ceratopteris chingii, Phylogeny, Coexpression network, Heteroblasty, SDG-15: Life on land
Sustainable Development Goals
SDG-15:Life on land
Citation
Zhang, Y., Van de Peer, Y., Lu, B. et al. 2023, 'Expression divergence of expansin genes drive the heteroblasty in Ceratopteris chingii', BMC Biology, vol. 21, no. 1, art. 244, pp. 1-16. DOI : 10.1186/s12915-023-01743-7.