Passiflora plastome sequencing reveals widespread genomic rearrangements

Abstract

Although past studies have included Passiflora among angiosperm lineages with highly rearranged plastid genomes (plastomes), knowledge about plastome organization in the genus is limited. So far only one draft and one complete plastome have been published. Expanded sampling of Passiflora plastomes is needed to understand the extent of the genomic rearrangement in the genus, which is also unusual in having biparental plastid inheritance and plastome‐genome incompatibility. We sequenced 15 Passiflora plastomes using either Illumina paired‐end or shotgun cloning and Sanger sequencing approaches. Assembled plastomes were annotated using Dual Organellar GenoMe Annotator (DOGMA) and tRNAscan‐SE. The Populus trichocarpa plastome was used as a reference to estimate genomic rearrangements in Passiflora by performing whole genome alignment in progressiveMauve. The phylogenetic distribution of rearrangements was plotted on the maximum likelihood tree generated from 64 plastid encoded protein genes. Inverted repeat (IR) expansion/contraction and loss of the two largest hypothetical open reading frames, ycf1 and ycf2, account for most plastome size variation, which ranges from 139 262 base pairs (bp) in P. biflora to 161 494 bp in P. pittieri. Passiflora plastomes have experienced numerous inversions, gene and intron losses along with multiple independent IR expansions and contractions resulting in a distinct organization in each of the three subgenera examined. Each Passiflora subgenus has a unique plastome structure in terms of gene content, order and size. The phylogenetic distribution of rearrangements shows that Passiflora has experienced widespread genomic changes, suggesting that such events may not be reliable phylogenetic markers.

Exploring the plastid genome disparity of liverworts

“…); the latter include the largest genomes as a consequence of genome rearrangements (Ruhlman & Jansen, ). Frequent genome rearrangements could cause substantial length difference among closely related species, as recently shown for the plastid genome of Passiflora (Rabah et al, ). The observed variation in the length of plastomes is arguably partly contributed by changes in gene content (Zheng et al, ) and partly by the length of non‐coding DNA.…”

Plastome Evolution in Dolomiaea (Asteraceae, Cardueae) Using Phylogenomic and Comparative Analyses

“…The expansion/contraction of IR regions has been demonstrated to be a significant contribution to substantial variation in plastome size (Ruhlman and Jansen, 2014). Occurrence of IR expansion/contraction is common in angiosperm plastomes and has been documented in several lineages, such as Pelargonium (Weng et al, 2017), Trochodendraceae (Sun et al, 2013), Plantago (Zhu et al, 2016), and Passiflora (Rabah et al, 2019). In the present study, however, no significant IR length variation was found among Dolomiaea plastomes and with plastomes of its sister genus (Saussurea) , indicating the conservative nature of plastome evolutionary history of Dolomiaea.…”

“…Due to the lack of recombination, usually uniparental inheritance and high copy numbers per cells (Wicke et al, 2011;Ruhlman and Jansen, 2014), whole plastome sequences have been extensively used in reconstructing the plant Tree of Life (e.g., Jansen et al, 2007;Moore et al, 2007;Ruhfel et al, 2014;Gitzendanner et al, 2018;Li et al, 2019). Comparative plastome studies provide the opportunity to explore sequence variation and the molecular evolutionary patterns associated with genome rearrangements (e.g., Knox, 2014;Weng et al, 2014;Rabah et al, 2019;Shrestha et al, 2019) as well as gene loss, duplication, and transfer events (e.g., Downie and Jansen, 2015;Wu and Chaw, 2016;Sun et al, 2017), while also detecting signatures of positive selection in plastid genes facilitating our understanding of plants adapting to extreme environments (e.g., alpine areas) (Bock et al, 2014;Jiang et al, 2018;Liu et al, 2018). Highly divergent regions and simple sequence repeats (SSRs) obtained from whole plastome sequence hold promise as efficient molecular markers implemented in species delimitation and population genetics Cui et al, 2019).…”

Can we use it? On the utility ofde novoand reference-based assembly of Nanopore data for plant plastome sequencing

“…Another limitation is that highly degraded DNA cannot be used for long-range PCR, which limits its use with herbarium material [61,6]. The method is also unsuitable if larger rearrangements in gene order are to be expected, as have been found for example in Passiflora L. [62]. In any case, optimization of primers for the study group will almost always be necessary to amplify all fragments (in the present study, different primers had to be used for five out of 16 fragments, and several primers were slightly modified).…”