Mitogenomes comparison of 3 species of Asparagus L shedding light on their functions due to domestication and adaptative evolution

Abstract

Background: Asparagus L., widely distributed in the old world is a genus under Asparagaceae, Asparagales. The species of the genus were mainly used as vegetables, traditional medicines as well as ornamental plants. However, the evolution and functions of mitochondrial (Mt) genomes (mitogenomes) remains largely unknown. In this study, the typical herbal medicine A. taliensis and ornamental plant A. setaceus were used to assemble and annotate the mitogenomes, and the resulting mitogenomes were further compared with published mitogenome of A. officinalis for the analysis of their functions in the context of domestication and adaptative evolution.

Results: The mitochondrial genomes of both A. taliensis and A. setaceus were assembled as complete circular ones. The phylogenetic trees based on conserved protein-coding genes of Mt genomes and whole chloroplast (Cp) genomes showed that, the phylogenetic relationship of the sampled 13 species of Asparagus L. were not exactly consistent. The collinear analyses between the nuclear (Nu) and Mt genomes confirmed the existence of mutual horizontal genes transfers (HGTs) between Nu and Mt genomes within these species. Based on RNAseq data, the Mt RNA editing were predicted and atp1 and ccmB RNA editing of A. taliensis were further confirmed by DNA sequencing. Simultaneously homologous search found 5 Nu coding gene families including pentatricopeptide-repeats (PPRs) involved in Mt RNA editing. Finally, the Mt genome variations, gene expressions and mutual HGTs between Nu and Mt were detected with correlation to the growth and developmental phenotypes respectively. The results suggest that, both Mt and Nu genomes co-evolved and maintained the Mt organella replication and energy production through TCA and oxidative phosphorylation .

Conclusion: The assembled and annotated complete mitogenomes of both A. taliensis and A. setaceus provide valuable information for their phylogeny and concerted action of Nu and Mt genomes to maintain the energy production system of Asparagus L. in the context of domestication and adaptation to environmental niches.

Keywords: Asparagus L.; Energy production system; Mitochondrial genome; Phylogenetic analysis; RNA editing.

Fig. 1

Mitogenome structure and phylogenetic analyses of Asparagus L; A, C: Mt genomes of A. taliensis and A. setaceus respectively; B, D: Cp genomes of A .taliensis and A. setaceus respectively; E, F:phylogenetic trees of the Mt and Cp genomes, bootstrap values < 50% not display in branches, classification differences between Mt and Cp in the phylogenetic trees are highlighted with light green while the numbers on the phylogenetic trees represents the bootstrap value of that branch

Fig. 2

Metabolic pathways and expressions of partial Nu genes in Asparagus L;A1-C1:partial KEGG pathway map of A. officinalis, A. taliensis and A. setaceus collinear Nu genes with their five up and downflanking genes respectively;A2-C2: collinear Nu genes heatmap expressions of A. officinalis, A. taliensis and A. setaceus with their five up and downflanking genes respectively. Where Aof_GR represent green root of A. officinalis, Aof_GS represent green stem of A. officinalis, Aof_GF represent green flowers of A. officinalis, Ata_MR represent wildtype male roots of A. taliensis, Ata_MS represent wildtype male stems of A.taliensis, Ata_MF represent wildtype male flowers of A. taliensis,Ase_L represents leaves of A. setaceus, Ase_S represents stems of A. setaceus and Ase_F represents flowers of A. setaceus

Fig. 3

RNA editing prediction and validation;A-C: RNA editing prediction of A. officinalis, A. taliensis and A. setaceus atp1 gene, the black border indicates that there may be RNA editing at the site of cytosine (C), which transforms into uracil (U, T represent represent their respective positions) during transcription into mRNA;D1-D2: PCR product sequencing and comparison of A.taliensis atp1 and ccmB, where the red dashed boxes represent RNA editing site confirmed by PCR amplification while the numbers represent the RNA editing site position in the whole sequence

Fig. 4

Motif analysis and expression of 5 RNA editing gene families in the 3 asparagus species;A-E: the motifs and heatmap expressions of some genes in the PPR, MORF, ORRM, OZ and PPO1 families of A. officinalis (Aof), A.taliensis(Ata)and A.setaceus(Ase)

Fig. 5

DEGs heatmaps of TCA cycle and Oxidative phosphorylation; all genes are expressed differently in both stem and flower organs among the three species where A. officinalis have relatively higher expression levels in differentially expressed genes encoding EC1.1.1.37, EC2.3.3.1, EC2.3.3.8 and EC4.2.1.3 enzymes, while A. setaceus have relatively higher expression levels in differentially expressed genes encoding EC1.3.5.1 related enzymes