Transit From Autotrophism to Heterotrophism: Sequence Variation and Evolution of Chloroplast Genomes in Orobanchaceae Species

Abstract

The family Orobanchaceae including autotrophic, hemiparasitic, and holoparasitic species, is becoming a key taxa to study the evolution of chloroplast genomes in different lifestyles. But the early evolutionary trajectory in the transit from autotrophism to hemiparasitism still maintains unclear for the inadequate sampling. In this study, we compared 50 complete chloroplast genomes in Orobanchaceae, containing four newly sequenced plastomes from hemiparasitic Pedicularis , to elucidate the sequence variation patterns in the evolution of plastomes. Contrasted to the sequence and structural hypervariabilities in holoparasites, hemiparasitic plastomes exhibited high similarity to those of autotrophs in gene and GC contents. They are generally characterized with functional or physical loss of ndh /tRNA genes and the inverted small-single-copy region. Gene losses in Orobanchaceae were lineage-specific and convergent, possibly related to structural reconfiguration and expansion/contraction of the inverted region. Pseudogenization of ndh genes was unique in hemiparasites. At least in Pedicularis , the ndhF gene might be most sensitive to the environmental factors and easily pseudogenized when autotrophs transit to hemiparasites. And the changes in gene contents and structural variation potentially deeply rely on the feeding type. Selective pressure, together with mutational bias, was the dominant factor of shaping the codon usage patterns. The relaxed selective constraint, potentially with genome-based GC conversion (gBGC) and preferential codon usage, drive the fluctuation of GC contents among taxa with different lifestyles. Phylogenetic analysis in Orobanchaceae supported that parasitic species were single-originated while holoparasites were multiple-originated. Overall, the comparison of plastomes provided a good opportunity to understand the evolution process in Orobanchaceae with different lifestyles.

Plastid NDH Pseudogenization and Gene Loss in a Recently Derived Lineage from the Largest Hemiparasitic Plant Genus Pedicularis (Orobanchaceae)

“…This evolutionary pattern indicated that the degradation of the NDH genes in Pedicularis was a gradual process from functional to non-functional. Moreover, gene loss and pseudogenization of NDH genes likely occurred independently across the 13 major clades in Pedicularis ( Zhang et al. 2020 ), which is similar to the pattern of evolution proposed for vegetative and corolla characters ( Ree 2005 , Yu et al.…”

Comparative Analysis of Codon Bias in the Chloroplast Genomes of Theaceae Species

“…The effective number of codons (ENc) evaluates codon use bias at the genomic level; the lower the ENc value is, the more significant the codon use preference is ( Wright, 1990 ; Zhang et al, 2020 ). …”

Chloroplast Genome Evolution in Four Montane Zingiberaceae Taxa in China

“…Before calculation, gaps and stop codons between the compared sequences were removed. As the YN model considers sequence evolution characteristics (e.g., transition/transversion ratio and codon usage frequency), it has been used increasingly in molecular evolution research ( Yang and Nielsen, 2000 ; Zeng et al, 2017 ; Zhang R. T. et al, 2020 ). Thus, the YN algorithm was chosen in KaKs_calculator ( Zhang et al, 2006 ) to illustrate the Ka/Ks value and perform selective pressure analysis.…”