Expansions and contractions of the inverted repeat, as well as gene loss and potential pseudogenization shape plastome evolution in Hechtioideae (Bromeliaceae, Poales)
Ivón M. Ramírez-Morillo1, Laura A. Espinosa-Barrera1,2(), Carolina Granados Mendoza3, Sandra I. Vera-Paz3,4, Daniel D. Díaz Contreras Díaz3,4, Katya J. Romero-Soler1,3()
Expansions and contractions of the inverted repeat, as well as gene loss and potential pseudogenization shape plastome evolution in Hechtioideae (Bromeliaceae, Poales)
Full plastomes have recently proven to be a valuable data source for resolving recalcitrant phylogenetic relationships in the flowering plant family Bromeliaceae. The study of complete plastomes has additionally led to the discovery of new structural rearrangements and advanced our understanding of bromeliad plastome diversity and evolution. Here, we focus on the study of full plastomes of the bromeliad subfamily Hechtioideae to assess phylogenetic relationships, marker informativeness, and plastome structure and evolution. Using whole-genome sequencing data, we de novo assembled and annotated new plastid genomes of 19 Hechtioideae species plus one representative each from the Pitcairnioideae and Puyoideae subfamilies and compared them with four additional available plastomes from other bromeliad subfamilies. Our phylogenetic analysis using complete plastome sequences not only recovered the three currently recognized genera of Hechtioideae as monophyletic, strongly supporting Mesoamerantha as sister of Bakerantha and Hechtia, but also improved statistical support at different phylogenetic depths within the subfamily. We identified a set of highly informative loci, some of them explored for the first time in Hechtioideae. Structural rearrangements, including expansions and contractions of the inverted repeats, large inversions, and gene loss and potential pseudogenization were detected mainly within the genus Hechtia. Evolutionary trait rate shifts were associated with the size and guanine–cytosine content of the small single copy and inverted repeats.
Bromeliaceae / Hechtioideae / ndh gene family / phylogenetic informativeness / phylogenomics / plastid genome / structural rearrangements
1 | JJ Ancona, JP Pinzón-Esquivel, E Ruiz-Sánchez, C Palma-Silva, JJ Ortiz-Díaz, J Tun-Garrido, G Carnevali, NE Raigoza. 2022. Multilocus data analysis reveal the diversity of cryptic species in the Tillandsia ionantha (Bromeliaceae: Tillansioideae) complex. Plants 11(13): 1706. |
2 | A Amiryousefi, J Hyv?nen, P Poczai. 2018. IRscope: An online program to visualize the junction sites of chloroplast genomes. Bioinformatics 34(17): 3030–3031. |
3 | S Andrews. 2018. FastQC: A quality control tool for high throughput sequence data [online]. Available from [accessed 10 November 2022] |
4 | MHJ Barfuss, W Till, EM Leme, JP Pinzón, JM Manzanares, H Halbritter, R Samuel, GK Brown. 2016. Taxonomic revision of Bromeliaceae subfam. Tillandsioideae based on a multi-locus DNA sequence phylogeny and morphology. Phytotaxa 279: 1–97. |
5 | CF Barrett, BT Sinn, AH Kennedy. 2019. Unprecedented parallel photosynthetic losses in a heterotrophic Orchid genus. Molecular Biology and Evolution 36(9): 1884–1901. |
6 | AM Bolger, M Lohse, B Usadel. 2014. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30(15): 2114–2120. |
7 | T Borsch, D Quandt. 2009. Mutational dynamics and phylogenetic utility of noncoding chloroplast DNA. Plant Systematics and Evolution 282: 169–199. |
8 | F Bratzel, J Paule, J Leebens-Mack, EMC Leme, RC Forzza, MA Koch, S Heller, G Zizka. 2023. Target-enrichment sequencing reveals for the first time a well-resolved phylogeny of the core Bromelioideae (family Bromeliaceae). Taxon 72(1): 47–63. |
9 | LV Castello, MH Barfuss, W Till, L Galetto, JO Chiapella. 2016. Disentangling the Tillandsia capillaris complex: Phylogenetic relationships and taxon boundaries in Andean populations. Botanical Journal of the Linnean Society 181: 391–414. |
10 | J Castresana. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540–552. |
11 | PP Chan, TM Lowe. 2019. tRNAscan-SE: Searching for tRNA genes in genomic sequences. In: Kollmar M ed. Gene prediction: Methods and protocols. New York: Springer. 1–14. |
12 | JC Chávez-Galarza, S Cardenas-Ninasivincha, R Contreras, R Ferro-Mauricio, W Huanca-Mamani. 2021a. Chloroplast genoma of Tillandsia marconae Till & Vitek (Bromeliaceae), a hyperarid desert endangered species. Mitochondrial DNA Part B 6(9): 2562–2564. |
13 | JC Chávez-Galarza, S Cardenas-Ninasivincha, R Contreras, R Ferro-Mauricio, W Huanca-Mamani. 2021b. Chloroplast genome of Tillandsia landbeckii Phil. (Bromeliaceae) a species adapted to the hyper-arid conditions of the Atacama and Peruvian desert. Mitochondrial DNA Part B 6(12): 3375–3377. |
14 | MT Clegg, BS Gaut, GH Learn, BR Morton. 1994. Rates and patterns of chloroplast DNA evolution. Proceedings of the National Academy of Sciences United States of America 91: 6795–6801. |
15 | W Dong, C Xu, C Li, J Sun, Y Zuo, S Shi, T Cheng, J Guo, S Zhou. 2015. ycf1, the most promising plastid DNA barcode of land plants. Scientific Reports 5: 8348. |
16 | JJ Doyle, JL Doyle. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15. |
17 | BC Faircloth, J Chang, ME Alfaro. 2012. TAPIR enables high-throughput estimation and comparison of phylogenetic informativeness using locus-specific substitution models. arXiv. Available from |
18 | L Gao, YJ Su, T Wang. 2010. Plastid genome sequencing, comparative genomics, and phylogenomics: Current status and prospects. Journal of Systematics and Evolution 48: 77–93. |
19 | MA Gitzendanner, PS Soltis, TS Yi, DZ Li, DE Soltis. 2018. Chapter Ten—Plastome phylogenetics: 30 years of inferences into plant evolution. In: Chaw SM, Jansen RK eds. Advances in botanical research. Cambridge: Academic Press. 293–313. |
20 | TJ Givnish, MH Barfuss, B Van Ee, R Riina, K Schulte, R Horres, PA Gonsiska, RS Jabaily, DM Crayn, JA Smith. 2011. Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: Insights from an eight-locus plastid phylogeny. American Journal of Botany 98: 872–895. |
21 | TJ Givnish, KC Millam, PE Berry, KJ Sytsma. 2007. Phylogeny, adaptive radiation, and historical biogeography of Bromeliaceae inferred from ndhF sequence data. Aliso 23: 3–26. |
22 | M Goetze, CM Zanella, C Palma-Silva, MV Büttow, F Bered. 2017. Incomplete lineage sorting and hybridization in the evolutionary history of closely related, endemic yellow-flowered Aechmea species of subgenus Ortgiesia (Bromeliaceae). American Journal of Botany 104: 1073–1087. |
23 | EJ Gouda, D Butcher, CS Gouda. 2023. Encyclopaedia of bromeliads, version 5. Utrecht: University Botanic Gardens. Available from [accessed 20 January 2023]. |
24 | C Granados Mendoza, M Jost, E Hágsater, S Magallón, C van den Berg, EM Lemmon, AR Lemmon, GA Salazar, S Wanke. 2020. Target nuclear and off-target plastid hybrid enrichment data inform a range of evolutionary depths in the orchid genus Epidendrum. Frontiers in Plant Science 10: 1761. |
25 | MM Guisinger, TW Chumley, JV Kuehl, JL Boore, RK Jansen. 2010. Implications of the plastid genome sequence of Typha (Typhaceae, Poales) for understanding genome evolution in Poaceae. Journal of Molecular Evolution 70: 149–166. |
26 | RS Jabaily, KJ Sytsma. 2010. Phylogenetics of Puya (Bromeliaceae): Placement, major lineages, and evolution of Chilean species. American Journal of Botany 97(2): 337–356. |
27 | RK Jansen, TA Ruhlman. 2012. Plastid genomes of seed plants. In: Bock R, Knoop V eds. Genomics of chloroplasts and mitochondria. Dordrecht: Springer. 103–126. |
28 | JJ Jin, WB Yu, JB Yang, Y Song, CW Depamphilis, TS Yi, DZ Li. 2020. GetOrganelle: A fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biology 21: 241. |
29 | K Katoh, DM Standley. 2013. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. |
30 | M Kearse, R Moir, A Wilson, S Stones-Havas, M Cheung, S Sturrock, S Buxton, A Cooper, S Markowitz, C Duran. 2012. Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649. |
31 | K K?nyves, J Bilsborrow, MD Christodoulou, A Culham, J David. 2021. Comparative plastomics of Amaryllidaceae: Inverted repeat expansion and the degradation of the ndh genes in Strumaria truncata Jacq. PeerJ 9: e12400. |
32 | EMC Leme, G Zizka, J Paule, J Aguirre-Santoro, S Heller, IM Ramírez-Morillo, H Halbritter, JEA Mariath, JDT Carvalho, RC Forzza. 2021. Re-evaluation of the Amazonian Hylaeaicum (Bromeliaceae: Bromelioideae) based on neglected morphological traits and molecular evidence. Phytotaxa 499: 1–60. |
33 | F-W Li, L-Y Kuo, KM Pryer, CJ Rothfels. 2016. Genes translocated into the plastid inverted repeat show decelerated substitution rates and elevated GC content. Genome Biology and Evolution 8(8): 2452–2458. |
34 | H Li, R Durbin. 2009. Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 25: 1754–1760. |
35 | H Li, B Handsaker, A Wysoker, T Fennell, J Ruan, N Homer, G Marth, G Abecasis, R Durbin. 2009. The sequence Alignment/Map format and SAMtools. Bioinformatics 25(16): 2078–2079. |
36 | CS Lin, J Chen, YT Huang, M-T Chan, H Daniell, WJ Chang, C-T Hsu, DC Liao, F-H Wu, S-Y Lin, C-F Liao, MK Deyholos, G K-S Wong, VA Albert, M-L Chou, C-Y Chen, MC Shih. 2015. The location and translocation of ndh genes of chloroplast origin in the Orchidaceae family. Scientific Reports 5: 9040. |
37 | L Liu, YQ Zhang, L Tumi, ML Suni, M Arakaki, KS Burgess, XJ Ge. 2022. Genetic markers in Andean Puya species (Bromeliaceae) with implications on plastome evolution and phylogeny. Ecology and Evolution 12(8): e9159. |
38 | M Lohse, O Drechsel, S Kahlau, R Bock. 2013. OrganellarGenomeDRAW—A suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Research 41: 575–581. |
39 | O Loiseau, T Mota Machado, M Paris, D Koubínová, KG Dexter, LM Versieux, C Lexer, N Salamin. 2021. Genome skimming reveals widespread hybridization in a Neotropical flowering plant radiation. Frontiers in Ecology and Evolution 9: 668281. |
40 | TM Lowe, PP Chan. 2016. tRNAscan-SE on-line: Integrating search and context for analysis of transfer RNA genes. Nucleic Acids Research 44: W54–W57. |
41 | TM Machado, O Loiseau, M Paris, A Weigand, LM Versieux, JR Stehmann, C Lexer, N Salamin. 2020. Systematics of Vriesea (Bromeliaceae): Phylogenetic relationships based on nuclear gene and partial plastome sequences. Botanical Journal of the Linnean Society 192: 656–674. |
42 | M Martín, B Sabater. 2010. Plastid ndh genes in plant evolution. Plant Physiology and Biochemistry 48: 636–645. |
43 | S Matuszak-Renger, J Paule, S Heller, EMC Leme, GM Steinbeisser, MHJ Barfuss, G Zizka. 2018. Phylogenetic relationships among Ananas and related taxa (Bromelioideae, Bromeliaceae) based on nuclear, plastid and AFLP data. Plant Systematics and Evolution 304: 841–851. |
44 | MA Miller, W Pfeiffer, T Schwartz. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans: IEEE. 1–8. |
45 | I Milne, G Stephen, M Bayer, PJA Cock, L Pritchard, L Cardle, PD Shaw, D Marshall. 2013. Using Tablet for visual exploration of second-generation sequencing data. Briefings in Bioinformatics 14(2): 193–202. |
46 | J M?bus, C Kiefer, D Quandt, MH Barfuss, MA Koch. 2021. Setting the evolutionary timeline: Tillandsia landbeckii in the Chilean Atacama Desert. Plant Systematics and Evolution 307: 39. |
47 | JP Mower, TL Vickrey. 2018. Chapter Nine—Structural diversity among plastid genomes of land plants. In: Chaw SM, Jansen RK eds. Advances in botanical research. Cambridge: Academic Press. 263–292. |
48 | JP Mower, W Guo, R Partha, W Fan, N Levsen, K Wolff, JM Nugent, N Pabon-Mora, F Gonzalez. 2021. Plastomes from tribe Plantagineae (Plantaginaceae) reveal infrageneric structural synapormorphies and localized hypermutation for Plantago and functional loss of ndh genes from Littorella. Molecular Phylogenetics and Evolution 162: 107217. |
49 | Y Naciri, HP Linder. 2015. Species delimitation and relationships: The dance of the seven veils. Taxon 64: 3–16. |
50 | K Nashima, S Terakami, C Nishitani, M Kunihisa, M Shoda, M Takeuchi, N Urasaki, K Tarora, T Yamamoto, H Katayama. 2015. Complete chloroplast genome sequence of pineapple (Ananas comosus). Tree Genetics and Genomes 11: 60. |
51 | AE Ortiz-Rodríguez, JF Ornelas, E Ruiz-Sanchez. 2018. A jungle tale: Molecular phylogeny and divergence time estimates of the Desmopsis-Stenanona clade (Annonaceae) in Mesoamerica. Molecular Phylogenetics and Evolution 122: 80–94. |
52 | C Palma-Silva, BSS Leal, CJN Chaves, MF Fay. 2016. Advances in and perspectives on evolution in Bromeliaceae. Botanical Journal of the Linnean Society 181: 305–322. |
53 | JD Palmer. 1983. Chloroplast DNA exists in two orientations. Nature 301: 92–93. |
54 | JD Palmer. 1991. Plastid chromosomes: Structure and evolution. In: Bogorad L, Vasil IK eds. The molecular biology of plastids. Cambridge: Academic Press. 5–53. |
55 | E Paradis, K Schliep. 2019. ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35: 526–528. |
56 | J Paule, R Schmickl, T Fér, S Matuszak-Renger, H Halbritter, G Zizka. 2020. Phylogenomic insights into the Fascicularia-Ochagavia group (Bromelioideae, Bromeliaceae). Botanical Journal of the Linnean Society 192(4): 642–655. |
57 | M Plummer, N Best, K Cowles, K Vines. 2006. CODA: Convergence diagnosis and output analysis for MCMC. R News 6: 7–11. |
58 | P Poczai, J Hyv?nen. 2017. The complete chloroplast genome sequence of the CAM epiphyte Spanish moss (Tillandsia usneoides, Bromeliaceae) and its comparative analysis. PLoS One 12: 1–25. |
59 | SLK Pond, SDW Frost, SV Muse. 2005. HyPhy: Hypothesis testing using phylogenies. Bioinformatics 21: 676–679. |
60 | R Core Team. 2022. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. |
61 | DL Rabosky. 2014. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS One 9: e89543. |
62 | IM Ramírez-Morillo, G Carnevali, JP Pinzón, K Romero-Soler, N Raigoza, N Hornung-Leoni, R Duno, JL Tapia-Mu?oz, I Echevarría. 2018a. Phylogenetic relationships of Hechtia (Hechtioideae; Bromeliaceae). Phytotaxa 376: 227–253. |
63 | IM Ramírez-Morillo, K Romero-Soler, G Carnevali, JP Pinzón, N Raigoza, C Hornung-Leoni, R Duno, JL Tapia-Mu?oz. 2018b. The reestablishment of Bakerantha, and a new genus in Hechtioideae (Bromeliaceae) in Megamexico, Mesoamerantha. Harvard Papers in Botany 23: 301–312. |
64 | RM Redwan, A Saidin, SV Kumar. 2015. Complete chloroplast genome sequence of MD-2 pineapple and its comparative analysis among nine other plants from the subclass Commelinidae. BMC Plant Biology 15: 196. |
65 | LJ Revell. 2012. phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3: 217–223. |
66 | R Rivera-Martínez, IM Ramírez-Morillo, JA De-Nova, G Carnevali, JP Pinzón, KJ Romero-Soler, N Raigoza. 2022. Spatial phylogenetics in Hechtioideae (Bromeliaceae) reveals a recent speciation and dispersal. Botanical Science 100(3): 692–709. |
67 | KJ Romero-Soler, IM Ramírez-Morillo, E Ruiz-Sánchez, C Hornung-Leoni, G Carnevali, N Raigoza. 2022a. Phylogenetic relationships within the Mexican genus Bakerantha (Hechtioideae, Bromeliaceae) based on plastid and nuclear DNA: Implications for taxonomy. Journal of Systematics and Evolution 60: 55–72. |
68 | KJ Romero-Soler, IM Ramírez-Morillo, E Ruiz-Sánchez, C Hornung-Leoni, G Carnevali. 2022b. Historical biogeography and comparative phylogeography of the Mexican bromeliad genus Bakerantha: Insights into evolution and diversification. Botanical Journal of the Linnean Society 199(1): 109–127. |
69 | TA Ruhlman, WJ Chang, JJW Chen, YT Huang, MT Chan, J Zhang, DC Liao, JC Blazier, X Jin, MC Shih, RK Jansen, CS Lin. 2015. NDH expression marks major transitions in plant evolution and reveals coordinate intracellular gene loss. BMC Plant Biology 15: 100. |
70 | MJ Sanderson, D Copetti, A Burquez, E Bustamante, JL Charboneau, LE Eguiarte, S Kumar, HO Lee, J Lee, M McMahon, K Steele, R Wing, T-J Yang, D Zwickl, MF Wojciechowski. 2015. Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea): Loss of the ndh gene suite and inverted repeat. American Journal of Botany 102: 1115–1127. |
71 | C Sass, CD Specht. 2010. Phylogenetic estimation of the core Bromelioids with emphasis on the genus Aechmea (Bromeliaceae). Molecular Phylogenetics and Evolution 55: 559–571. |
72 | J Shaw, HL Shafer, OR Leonard, MJ Kovach, M Schorr, AB Morris. 2014. Chloroplast DNA sequence utility for the lowest phylogenetic and phylogeographic inferences in angiosperms: The tortoise and the hare IV. American Journal of Botany 101(11): 1987–2004. |
73 | SA Smith, MJ Donoghue. 2008. Rates of molecular evolution are linked to life history in flowering plants. Science 322: 86–89. |
74 | A Stamatakis. 2014. RAxML Version 8: A tool for phylogenetic analysis and post–analysis of large phylogenies. Bioinformatics 30: 1312–1313. |
75 | DD Strand, L D'Andrea, R Bock. 2019. The plastid NAD(P)H dehydrogenase-like complex: Structure, function and evolutionary dynamics. Biochemical Journal 476: 2743–2756. |
76 | JP Townsend. 2007. Profiling phylogenetic informativeness. Systematic Biology 56: 222–231. |
77 | SI Vera-Paz, DD Díaz Contreras Díaz, M Jost, S Wanke, AJ Rossado, R Hernández-Gutiérrez, GA Salazar, S Magallón, EJ Gouda, IM Ramírez-Morillo, S Donadío, C Granados Mendoza. 2022. New plastome structural rearrangements discovered in core Tillandsioideae (Bromeliaceae) support recently adopted taxonomy. Frontiers in Plant Science 13: 924922. |
78 | SI Vera-Paz, C Granados Mendoza, DD Díaz Contreras Díaz, M Jost, GA Salazar, AJ Rossado, CA Montes-Azcué, R Hernández-Gutiérrez, S Magallón, LA Sánchez-González, EJ Gouda, LI Cabrera, IM Ramírez-Morillo, M Flores-Cruz, X Granados-Aguilar, AL Martínez-García, CT Hornung-Leoni, MHJ Barfuss, S Wanke. 2023. Plastome phylogenomics reveals an early Pliocene North- and Central America colonization by long-distance dispersal from South America of a highly diverse bromeliad lineage. Frontiers in Plant Science 14: 1205511. |
79 | RJ Wang, CL Cheng, CC Chang, CL Wu, TM Su, SM Chaw. 2008. Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evolutionary Biology 8: 36. |
80 | T Yang, S Kumar Sahu, L Yang, Y Liu, W Mu, X Liu, M Lenz Strube, H Liu, B Zhong. 2022. Comparative analyses of 3,654 plastid genomes unravel insights into evolutionary dynamics and phylogenetic discordance of green plants. Frontiers in Plant Science 13: 808156. |
81 | G Yao, JJ Jin, HT Li, JB Yang, VS Mandala, M Croley, R Mostow, NA Douglas, MW Chase, MJM Christenhusz, DE Soltis, PS Soltis, SA Smith, SF Brockington, MJ Moore, TS Yi, DZ Li. 2019. Plastid phylogenomic insights into the evolution of Caryophyllales. Molecular Phylogenetics and Evolution 134: 74–86. |
82 | G Yardeni, J Viruel, M Paris, J Hess, C Groot Crego, M de La Harpe, N Rivera, MHJ Barfuss, W Till, V Guzmán-Jacob, T Kr?mer, C Lexer, O Paun, T Leroy. 2022. Taxon-specific or universal? Using target capture to study the evolutionary history of rapid radiations. Molecular Ecology Resources 22: 927–945. |
83 | A Zhu, W Guo, S Gupta, W Fan, JP Mower. 2016. Evolutionary dynamics of the plastid inverted repeat: The effects of expansion, contraction, and loss on substitution rates. New Phytologist 209: 1747–1756. |
/
〈 | 〉 |