Chloroplast Genomic Insights into Adaptive Evolution and Rapid Radiation in the Genus Passiflora (Passifloraceae)

Overview

Journal BMC Plant Biol

Publisher Biomed Central

Specialty Biology

Date 2025 Feb 13

PMID 39948451

Authors

Luiz Augusto Cauz-Santos

Zirlane Portugal da Costa

Mariela Analia Sader

Cassio van den Berg

Maria Lucia Carneiro Vieira

Affiliations

Soon will be listed here.

Abstract

Chloroplasts are essential organelles in plants and eukaryotic algae, responsible for photosynthesis, fatty acid synthesis, amino acid production, and stress responses. The genus Passiflora, known for its species diversity and dynamic chloroplast (cp) genome evolution, serves as an excellent model for studying structural variations. This study investigates evolutionary relationships within Passiflora by sequencing 11 new chloroplast genomes, assessing selective pressures on cp genes, and comparing plastid and nuclear phylogenies. Passiflora cp genomes showed significant variations in size, gene content, and structure, ranging from 132,736 to 163,292 base pairs, especially in Decaloba. Structural rearrangements and species-specific repeat patterns were identified. Selective pressure tests revealed significant adaptive evolution in certain lineages, with several genes, including clpP and petL, under positive selection. Phylogenetic analyses confirmed the monophyly of subgenera Astrophea, Passiflora, and Decaloba, while Deidamioides appeared polyphyletic. Nuclear phylogenetic analysis based on 35S rDNA sequences supported the monophyly of Astrophea but showed inconsistencies within subgenus Passiflora compared to cp genome data. This study highlights the evolutionary complexity of Passiflora cp genomes, demonstrating significant structural variations and adaptive evolution. The findings underscore the effectiveness of plastid phylogenomics in resolving phylogenetic relationships and provide insights into adaptive mechanisms shaping cp genome diversity in angiosperms.

References

Cosner M, Raubeson L, Jansen R . Chloroplast DNA rearrangements in Campanulaceae: phylogenetic utility of highly rearranged genomes. BMC Evol Biol. 2004; 4:27. PMC: 516026. DOI: 10.1186/1471-2148-4-27. View

Ma P, Zhang Y, Zeng C, Guo Z, Li D . Chloroplast phylogenomic analyses resolve deep-level relationships of an intractable bamboo tribe Arundinarieae (poaceae). Syst Biol. 2014; 63(6):933-50. DOI: 10.1093/sysbio/syu054. View

Dierckxsens N, Mardulyn P, Smits G . NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res. 2017; 45(4):e18. PMC: 5389512. DOI: 10.1093/nar/gkw955. View

Zhang Y, Zhang A, Li X, Lu C . The Role of Chloroplast Gene Expression in Plant Responses to Environmental Stress. Int J Mol Sci. 2020; 21(17). PMC: 7503970. DOI: 10.3390/ijms21176082. View

Scobeyeva V, Artyushin I, Krinitsina A, Nikitin P, Antipin M, Kuptsov S . Gene Loss, Pseudogenization in Plastomes of Genus (), and Putative Selection for Adaptation to Environmental Conditions. Front Genet. 2021; 12:674783. PMC: 8296844. DOI: 10.3389/fgene.2021.674783. View

Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones E, Fischer A, Bock R . GeSeq - versatile and accurate annotation of organelle genomes. Nucleic Acids Res. 2017; 45(W1):W6-W11. PMC: 5570176. DOI: 10.1093/nar/gkx391. View

Takamatsu T, Baslam M, Inomata T, Oikawa K, Itoh K, Ohnishi T . Optimized Method of Extracting Rice Chloroplast DNA for High-Quality Plastome Resequencing and Assembly. Front Plant Sci. 2018; 9:266. PMC: 5835797. DOI: 10.3389/fpls.2018.00266. View

Wojciechowski M, Lavin M, Sanderson M . A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am J Bot. 2011; 91(11):1846-62. DOI: 10.3732/ajb.91.11.1846. View

Cauz-Santos L, Munhoz C, Rodde N, Cauet S, Santos A, Penha H . The Chloroplast Genome of (Passifloraceae) Assembled from Long Sequence Reads: Structural Organization and Phylogenomic Studies in Malpighiales. Front Plant Sci. 2017; 8:334. PMC: 5345083. DOI: 10.3389/fpls.2017.00334. View

10.

Sugiura M . The chloroplast genome. Plant Mol Biol. 1992; 19(1):149-68. DOI: 10.1007/BF00015612. View

11.

McMahon M, Sanderson M . Phylogenetic supermatrix analysis of GenBank sequences from 2228 papilionoid legumes. Syst Biol. 2006; 55(5):818-36. DOI: 10.1080/10635150600999150. View

12.

Sang T . Utility of low-copy nuclear gene sequences in plant phylogenetics. Crit Rev Biochem Mol Biol. 2002; 37(3):121-47. DOI: 10.1080/10409230290771474. View

13.

Lavin M, Doyle J, Palmer J . EVOLUTIONARY SIGNIFICANCE OF THE LOSS OF THE CHLOROPLAST-DNA INVERTED REPEAT IN THE LEGUMINOSAE SUBFAMILY PAPILIONOIDEAE. Evolution. 2017; 44(2):390-402. DOI: 10.1111/j.1558-5646.1990.tb05207.x. View

14.

Alvarez I, Wendel J . Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol. 2003; 29(3):417-34. DOI: 10.1016/s1055-7903(03)00208-2. View

15.

Wortley A, Rudall P, Harris D, Scotland R . How much data are needed to resolve a difficult phylogeny?: case study in Lamiales. Syst Biol. 2005; 54(5):697-709. DOI: 10.1080/10635150500221028. View

16.

Haberle R, Fourcade H, Boore J, Jansen R . Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and tRNA genes. J Mol Evol. 2008; 66(4):350-61. DOI: 10.1007/s00239-008-9086-4. View

17.

Muschner V, Zamberlan P, Bonatto S, Freitas L . Phylogeny, biogeography and divergence times in Passiflora (Passifloraceae). Genet Mol Biol. 2013; 35(4 (suppl)):1036-43. PMC: 3571420. DOI: 10.1590/s1415-47572012000600019. View

18.

Xi Z, Ruhfel B, Schaefer H, Amorim A, Sugumaran M, Wurdack K . Phylogenomics and a posteriori data partitioning resolve the Cretaceous angiosperm radiation Malpighiales. Proc Natl Acad Sci U S A. 2012; 109(43):17519-24. PMC: 3491498. DOI: 10.1073/pnas.1205818109. View

19.

Katoh K, Standley D . MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4):772-80. PMC: 3603318. DOI: 10.1093/molbev/mst010. View

20.

Erixon P, Oxelman B . Whole-gene positive selection, elevated synonymous substitution rates, duplication, and indel evolution of the chloroplast clpP1 gene. PLoS One. 2008; 3(1):e1386. PMC: 2148103. DOI: 10.1371/journal.pone.0001386. View