Transcription factors in Orinus: novel insights into transcription regulation for speciation adaptation on the Qinghai-Xizang (Tibet) Plateau

Abstract

Background: Transcription factors (TFs) are crucial regulators of plant growth, development, and resistance to environmental stresses. However, comprehensive understanding of the roles of TFs in speciation of Orinus, an extreme-habitat plant on the Qinghai-Xizang (Tibet) Plateau, is limited.

Results: Here, we identified 52 TF families, including 2125 members in Orinus, by methodically analysing domain findings, gene structures, chromosome locations, conserved motifs, and phylogenetic relationships. Phylogenetic trees were produced for each Orinus TF family using protein sequences together with wheat (Triticum aestivum L.) TFs to indicate the subgroups. The differences between Orinus and wheat species in terms of TF family size implies that both Orinus- and wheat-specific subfamily contractions (and expansions) contributed to the high adaptability of Orinus. Based on deep mining of RNA-Seq data between two species of Orinus, O. thoroldii and O. kokonoricus, we obtained differentially expressed TFs (DETFs) in 20 families, most of which were expressed higher in O. thoroldii than in O. kokonoricus. In addition, Cis-element analysis shows that MYC and G-box elements are enriched in the promoter region of DETFs, suggesting that jasmonic acid (JA) and abscisic acid (ABA) act synergistically in Orinus to enhance the signalling of related abiotic stress responses, ultimately leading to an improvement in the stress tolerance and speciation adaptation of Orinus.

Conclusions: Our data serve as a genetic resource for Orinus, not only filling the gap in studies of TF families within this genus but also providing preliminary insights into the molecular mechanisms underlying speciation in Orinus.

Keywords: Orinus; Phylogenetic relationship; Speciation adaptation; Transcription factor; Transcriptional regulation.

Fig. 1

Characterisation of TFs in Orinus. A Schematic computational pipeline for the identification of TFs in Orinus. B Distribution of Orinus TFs in 52 families showing the minimum number of members identified in each of the 52 TF families found in the Orinus dataset. C Protein lengths of all identified TFs in Orinus. D Isoelectric point (pI) of all the identified TFs in Orinus

Fig. 2

Phylogenetic tree of AP2/ERF genes in Orinus and wheat. The phylogenetic tree was generated using the maximum-likelihood approach, based on the alignment of the AP2/ERF domains. Only bootstrap values exceeding 50% are shown (calculated with 1000 replicates to verify the reliability of the tree topology). These AP2/ERF proteins are clustered into 13 clades. The red star indicates the new subfamily discovered in Orinus

Fig. 3

Phylogenetic tree of bHLH genes in Orinus and wheat. The phylogenetic tree was generated using the maximum-likelihood approach, based on the alignment of the bHLH domains. The parameters are consistent with Fig. 2. These bHLH proteins are clustered into 25 clades. The red star indicates the new subfamily discovered in Orinus and the blue star indicates the subfamily that is missing in Orinus

Fig. 4

Phylogenetic tree of C2H2 genes in Orinus and wheat. The phylogenetic tree was generated using the maximum-likelihood approach, based on the alignment of the C2H2 domains. The parameters are consistent with Fig. 2. These C2H2 proteins are clustered into five clades. The red stars indicate the new subfamilies discovered in Orinus

Fig. 5

Phylogenetic tree of GRAS genes in Orinus and wheat. The phylogenetic tree was generated using the maximum-likelihood approach, based on the alignment of the GRAS domains. The parameters are consistent with Fig. 2. These GRAS proteins are clustered into 12 clades. The blue stars indicate the subfamilies that are missing in Orinus

Fig. 6

Phylogenetic tree of MADS-box genes in Orinus and wheat. The phylogenetic tree was generated using the maximum-likelihood approach, based on the alignment of the MADS-box domains. The parameters are consistent with Fig. 2. These MADS-box proteins are clustered into 13 clades. The blue star indicates the subfamily that is missing in Orinus

Fig. 7

Intraspecies synteny analysis of 10 TF families. A Intraspecies synteny analysis in AP2/ERF, bHLH, C2H2, GRAS, HD-ZIP, MADS-box, R2R3-MYB, NAC, TALE, and WRKY (1–20 represent LG1–LG20, the 20 chromosomes in Orinus). B Homologous gene pairs in these 10 families. C The numbers of homologous genes in these 10 families

Fig. 8

Distribution of cis-acting elements in the 2.0-kb promoter regions of DETFs in Orinus. A Expression heatmap: expressed more in O. thoroldii than in O. kokonoricus or vice versa. B The existence of abiotic and biotic stress-related elements in the promoter regions of DETFs. C The existence of phytohormone-responsive-related elements in the promoter regions of DETFs. D The existence of plant-growth- and development-related elements in the promoter regions of DETFs