Tropical plants evolve faster than their temperate relatives: a case from the bamboos (Poaceae: Bambusoideae) based on chloroplast genome data

References

• Kreft H, Jetz W. Global patterns and determinants of vascular plant diversity. Proc Natl Acad Sci USA. 2007;104(14):5925–5930.
   PubMed Web of Science ®Google Scholar
• Keil P, Chase JM. Global patterns and drivers of tree diversity integrated across a continuum of spatial grains. Nat Ecol Evol. 2019;3(3):390–399.
   PubMed Web of Science ®Google Scholar
• Burivalova Z, Miteva D, Salafsky N, Butler RA, et al. Evidence types and trends in tropical forest conservation literature. Trends Ecol Evol (Amst). 2019;34(7):669–679.
   PubMed Web of Science ®Google Scholar
• Bromham L. Why do species vary in their rate of molecular evolution?. Biol Lett. 2009;5(3):401–404.
   PubMed Web of Science ®Google Scholar
• Brown JH. Why are there so many species in the tropics?. J Biogeogr. 2014;41(1):8–22.
   PubMed Web of Science ®Google Scholar
• Gillman LN, Wright SD. Patterns of evolutionary speed: in search of a causal mechanism. Diversity. 2013;5(4):811–823.
   Google Scholar
• Orton MG, May JA, Ly W, et al. Is molecular evolution faster in the tropics? Heredity (Edinb)). 2019;122(5):513–524.
   PubMed Web of Science ®Google Scholar
• Wright SD, Gray RD, Gardner RC. Energy and the rate of evolution: inferences from plant rDNA substitution rates in the western Pacific. Evolution. 2003;57(12):2893–2898.
   PubMed Web of Science ®Google Scholar
• Gillman LN, Wright SD. Species richness and evolutionary speed: the influence of temperature, water and area. J Biogeogr. 2013;41(1):39–51.
   Web of Science ®Google Scholar
• Davies TJ, Savolainen V, Chase MW, et al. Environmental energy and evolutionary rates in flowering plants. Proc Biol Sci. 2004;271(1553):2195–2200.
   PubMed Web of Science ®Google Scholar
• Gillman LN, Keeling DJ, Gardner RC, et al. Faster evolution of highly conserved DNA in tropical plants. J Evol Biol. 2010;23(6):1327–1330.
   PubMed Web of Science ®Google Scholar
• Wang W, Franklin SB, Lu Z, et al. Delayed flowering in bamboo: evidence from Fargesia qinlingensis in the Qinling Mountains of China. Front Plant Sci. 2016;7:151.
   PubMed Web of Science ®Google Scholar
• Wang W, Chen S, Zhang X. Whole-genome comparison reveals divergent IR borders and mutation hotspots in chloroplast genomes of herbaceous bamboos (Bambusoideae: Olyreae). Molecules. 2018;23(7):1537.
   PubMed Web of Science ®Google Scholar
• Barrett CF, Baker WJ, Comer JR, et al. Plastid genomes reveal support for deep phylogenetic relationships and extensive rate variation among palms and other commelinid monocots. New Phytol. 2016;209(2):855–870.
   PubMed Web of Science ®Google Scholar
• Williams AM, Friso G, van Wijk KJ, et al. Extreme variation in rates of evolution in the plastid Clp protease complex. Plant J. 2019;98(2):243–259.
   PubMed Web of Science ®Google Scholar
• Zervas A, Petersen G, Seberg O. Mitochondrial genome evolution in parasitic plants. BMC Evol Biol. 2019;19(1):87.
   PubMed Web of Science ®Google Scholar
• Smith SA, Donoghue MJ. Rates of molecular evolution are linked to life history in flowering plants. Science. 2008;322(5898):86–89.
   PubMed Web of Science ®Google Scholar
• Lanfear R, Ho SY, Davies TJ, et al. Taller plants have lower rates of molecular evolution. Nat Commun. 2013;4:1879.
   PubMed Web of Science ®Google Scholar
• Shrestha B, Weng ML, Theriot EC, et al. Highly accelerated rates of genomic rearrangements and nucleotide substitutions in plastid genomes of Passiflora subgenus Decaloba. Mol Phylogenet Evol. 2019;138:53–64.
   PubMed Web of Science ®Google Scholar
• Lanfear R, Welch JJ, Bromham L. Watching the clock: studying variation in rates of molecular evolution between species. Trends Ecol Evol (Amst). 2010;25(9):495–503.
   PubMed Web of Science ®Google Scholar
• Gaut BS, Yang L, Takuno S, et al. The patterns and causes of variation in plant nucleotide substitution rates. Annu Rev Ecol Evol Syst. 2011;42(1):245–266.
   Web of Science ®Google Scholar
• Gaut BS, Clark LG, Wendel JF, et al. Comparisons of the molecular evolutionary process at rbcL and ndhF in the grass family (Poaceae). Mol Biol Evol. 1997;14(7):769–777.
   PubMed Web of Science ®Google Scholar
• Clark LG, Londoño X, Ruiz-Sanchez E. Bamboo taxonomy and habitat. In: Liese W, Kohl M, editors. Bamboo, tropical forestry. Switzerland: Springer International Publishing; 2015. p. 1–30.
   Google Scholar
• Soreng RJ, Peterson PM, Romaschenko K, et al. A worldwide phylogenetic classification of the Poaceae (Gramineae). J Syst Evol. 2015;53(2):117–137.
   Web of Science ®Google Scholar
• Canavan S, Richardson DM, Visser V, et al. The global distribution of bamboos: assessing correlates of introduction and invasion. AoB Plants. 2017;9:plw078. DOI:.
   Web of Science ®Google Scholar
• Kelchner SA, BPG (Bamboo Phylogeny Group). Higher level phylogenetic relationships within the bamboos (Poaceae: Bambusoideae) based on five plastid markers. Mol Phylogenet Evol. 2013;67(2):404–413.
   PubMed Web of Science ®Google Scholar
• Zhang X-Z, Zeng C-X, Ma P-F, et al. Multi-locus plastid phylogenetic biogeography supports the Asian hypothesis of the temperate woody bamboos (Poaceae: Bambusoideae). Mol Phylogenet Evol. 2016;96:118–129.
   PubMed Web of Science ®Google Scholar
• Ma P-F, Vorontsova MS, Nanjarisoa OP, et al. Negative correlation between rates of molecular evolution and flowering cycles in temperate woody bamboos revealed by plastid phylogenomics. BMC Plant Biol. 2017;17(1):260.
   PubMed Web of Science ®Google Scholar
• Makita A. The significance of the mode of clonal growth in the life history of bamboos. Plant Species Biol. 1998;13(2–3):85–92.
   Google Scholar
• Tachiki Y, Makita A, Suyama Y, et al. A spatially explicit model for flowering time in bamboos: long rhizomes drive the evolution of delayed flowering. J Ecol. 2015;103(3):585–593.
   Web of Science ®Google Scholar
• Wicke S, Schneeweiss GM. Next-generation organellar genomics: potentials and pitfalls of high-throughput technologies for molecular evolutionary studies and plant systematics. In: Hörandl E, Appelhans MS, editors. Next-generation sequencing in plant systematics. Bratislava: International Association for Plant Taxonomy (IAPT); 2015. p. 1–35.
   Google Scholar
• Li HT, Yi TS, Gao LM, et al. Origin of angiosperms and the puzzle of the Jurassic gap. Nat Plants. 2019;5(5):461–470.
   PubMed Web of Science ®Google Scholar
• Doyle JJ. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 1987;19:11–15.
   Google Scholar
• Altschul SF, Gish W, Miller W, et al. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–410.
   PubMed Web of Science ®Google Scholar
• Wyman SK, Jansen RK, Boore JL. Automatic annotation of organellar genomes with DOGMA. Bioinformatics. 2004;20(17):3252–3255.
   PubMed Web of Science ®Google Scholar
• Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 2005;33(Web Server issue):W686–W689.
   PubMed Web of Science ®Google Scholar
• Saarela JM, Burke SV, Wysocki WP, et al. A 250 plastome phylogeny of the grass family (Poaceae): topological support under different data partitions. Peer J. 2018;6:e4299.
   PubMed Web of Science ®Google Scholar
• Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–780.
   PubMed Web of Science ®Google Scholar
• Tamura K, Peterson D, Peterson N, et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28(10):2731–2739.
   PubMed Web of Science ®Google Scholar
• Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE); 2010 November 14; New Orleans, LA, USA; 2010. p. 1–8.
   Google Scholar
• Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–1313.
   PubMed Web of Science ®Google Scholar
• Ma P-F, Zhang Y-X, Zeng C-X, et al. Chloroplast phylogenomic analyses resolve deep-level relationships of an intractable bamboo tribe Arundinarieae (Poaceae). Syst Biol. 2014;63(6):933–950.
   PubMed Web of Science ®Google Scholar
• Ronquist F, Teslenko M, Van Der Mark P, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–542.
   PubMed Web of Science ®Google Scholar
• Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7:214.
   PubMed Web of Science ®Google Scholar
• Drummond AJ, Suchard MA, Xie D, et al. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29(8):1969–1973.
   PubMed Web of Science ®Google Scholar
• Wysocki WP, Clark LG, Attigala L, et al. Evolution of the bamboos (Bambusoideae; Poaceae): a full plastome phylogenomic analysis. BMC Evol Biol. 2015;15:50.
   PubMed Web of Science ®Google Scholar
• Rambaut A, Drummond A. 2009. Tracer v1. 5: MCMC trace analyses tool. Available from http://beast.bio.ed.ac.uk/Tracer.
   Google Scholar
• Kearse M, Moir R, Wilson A, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28(12):1647–1649.
   PubMed Web of Science ®Google Scholar
• Zhang Y-J, Ma P-F, Li D-Z. High-throughput sequencing of six bamboo chloroplast genomes: phylogenetic implications for temperate woody bamboos (Poaceae: Bambusoideae). PLoS One. 2011;6(5):e20596.
   PubMed Web of Science ®Google Scholar
• Wang W, Chen S, Zhang X. Chloroplast genome evolution in Actinidiaceae: clpP loss, heterogenous divergence and phylogenomic practice. PLoS One. 2016;11(9):e0162324.
   PubMed Web of Science ®Google Scholar
• Wang W, Chen S, Zhang X. Whole-genome comparison reveals heterogeneous divergence and mutation hotspots in chloroplast genome of Eucommia ulmoides Oliver. IJMS. 2018;19(4):1037.
   Web of Science ®Google Scholar
• Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–1797.
   PubMed Web of Science ®Google Scholar
• Judziewicz EJ, Clark LG, Londoño X, et al. American bamboos. Washington, DC: Smithsonian Institution Press; 1999. p. 1–60.
   Google Scholar
• Li DZ, W ZP, Zhu ZD, et al. Bambuseae (Poaceae). Beijing and St. Louis: Science Press and Missouri Botanical Garden Press; 2006. p. 1–60.
   Google Scholar
• Attigala L, Wysocki WP, Duvall MR, et al. Phylogenetic estimation and morphological evolution of Arundinarieae (Bambusoideae: Poaceae) based on plastome phylogenomic analysis. Mol Phylogenet Evol. 2016;101:111–121.
   PubMed Web of Science ®Google Scholar
• Maddison WP, Maddison DR. 2015. Mesquite: a modular system for evolutionary analysis. Version 2.75. Available from http://mesquiteproject.org.
   Google Scholar
• Wu F-H, Kan D-P, Lee S-B, et al. Complete nucleotide sequence of Dendrocalamus latiflorus and Bambusa oldhamii chloroplast genomes. Tree Physiol. 2009;29(6):847–856.
   PubMed Web of Science ®Google Scholar
• Zhang X-Z, Chen S-Y. Genome skimming reveals the complete chloroplast genome of Ampelocalamus naibunensis (Poaceae: Bambusoideae: Arundinarieae) with phylogenomic implication. Mitochondrial DNA B. 2016;1(1):635–637.
   PubMed Web of Science ®Google Scholar
• Zhang X-Z, Chen S-Y, Chen P, et al. The complete chloroplast genome of Ampelocalamus actinotrichus (Bambusoideae: Arundinarieae). Mitochondrial DNA B. 2019;4(1):145–146.
   Web of Science ®Google Scholar
• Sungkaew S, Stapleton CM, Salamin N, et al. Non-monophyly of the woody bamboos (Bambuseae; Poaceae): a multi-gene region phylogenetic analysis of Bambusoideae s.s. J Plant Res. 2009;122(1):95–108.
   PubMed Web of Science ®Google Scholar
• Vieira LDN, Anjos KGD, Faoro H, et al. Phylogenetic inference and SSR characterization of tropical woody bamboos tribe Bambuseae (Poaceae: Bambusoideae) based on complete plastid genome sequences. Curr Genet. 2016;62(2):443–411.
   PubMed Web of Science ®Google Scholar
• Wu M, Lan S, Cai B, et al. The complete chloroplast genome of Guadua angustifolia and comparative analyses of neotropical-paleotropical bamboos. PLoS One. 2015;10(12):e0143792.
   PubMed Web of Science ®Google Scholar
• Yang Y, Moore MJ, Brockington SF, et al. Dissecting molecular evolution in the highly diverse plant clade Caryophyllales using transcriptome sequencing. Mol Biol Evol. 2015;32(8):2001–2014.
   PubMed Web of Science ®Google Scholar
• Igea J, Tanentzap AJ. Angiosperm speciation speeds up near the poles. bioRxiv. 2020; 619064. DOI:. Accessed 2020 Feb.
   Google Scholar
• Nie Y, Foster CS, Zhu T, et al. Accounting for uncertainty in the evolutionary timescale of green plants through clock-partitioning and fossil calibration strategies. Syst Biol. 2020;69(1):1–16.
   PubMed Web of Science ®Google Scholar
• Lin G, Huang Z, Wang L, et al. Evolutionary rates of bumblebee genomes are faster at lower elevations. Mol Biol Evol. 2019;36(6):1215–1219.
   PubMed Web of Science ®Google Scholar
• Sebastián-González E, Barbosa JM, Pérez-García JM, et al. Scavenging in the Anthropocene: human impact drives vertebrate scavenger species richness at a global scale. Glob Chang Biol. 2019;25(9):3005–3017.
   PubMed Web of Science ®Google Scholar
• Adams RI, Hadly EA. Genetic diversity within vertebrate species is greater at lower latitudes. Evol Ecol. 2013;27(1):133–143.
   Web of Science ®Google Scholar
• Oppold A-M, Pedrosa JAM, Bálint M, et al. Support for the evolutionary speed hypothesis from intraspecific population genetic data in the non-biting midge Chironomus riparius. Proc Biol Sci. 2016;283(1825):20152413.
   PubMed Web of Science ®Google Scholar
• Loeza-Quintana T, Carr CM, Khan T, et al. Recalibrating the molecular clock for Arctic marine invertebrates based on DNA barcodes 1. Genome. 2019;62(3):200–216.
   PubMed Web of Science ®Google Scholar
• Eo SH, Wares JP, Carroll JP. Population divergence in plant species reflects latitudinal biodiversity gradients. Biol Lett. 2008;4(4):382–384.
   PubMed Web of Science ®Google Scholar
• Pennell MW. What explains latitudinal diversity gradients? Trends Ecol Evol. 2019;34(5):390–392.
   Google Scholar
• Hu J. Evolution of body mass in Coleoptera: insights from museum specimens and DNA barcodes [doctoral dissertation]. Guelph, Canada: University of Guelph; 2019.
   Google Scholar
• Janzen DH. Why bamboos wait so long to flower. Annu Rev Ecol Syst. 1976;7(1):347–391.
   Google Scholar
• Campbell J. Bamboo flowering patterns: a global view with special reference to East Asia. J Am Bamboo Soc (USA). 1985;6:17–35.
   Google Scholar
• Guerreiro C. Flowering cycles of woody bamboos native to southern South America. J Plant Res. 2014;127(2):307–313.
   PubMed Web of Science ®Google Scholar
• Bradburd GS, Ralph PL. Spatial population genetics: it’s about time. Annu Rev Ecol Evol Syst. 2019;50(1):427–449.
   Web of Science ®Google Scholar
• Veller C, Nowak MA, Davis CC. Extended flowering intervals of bamboos evolved by discrete multiplication. Ecol Lett. 2015;18(7):653–659.
   PubMed Web of Science ®Google Scholar
• Sloan DB, Alverson AJ, Wu M, et al. Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol Evol. 2012;4(3):294–306.
   PubMed Web of Science ®Google Scholar
• Krüger M, Abeyawardana OA, Juříček M, et al. Variation in plastid genomes in the gynodioecious species Silene vulgaris. BMC Plant Biol. 2019;19(1):1–15.
   PubMed Web of Science ®Google Scholar
• Shahzadi I, Mehmood F, Ali Z, et al. Comparative analyses of chloroplast genomes among three Firmiana species: identification of mutational hotspots and phylogenetic relationship with other species of Malvaceae. Plant Gene. 2019;19:100199.
   Google Scholar
• Henriquez CL, Ahmed I, Carlsen MM, et al. Evolutionary dynamics in chloroplast genome of subfamily Aroideae (Araceae). Genomics. 2020. DOI:.
   PubMed Web of Science ®Google Scholar
• Zhao DN, Ren Y, Zhang JQ. Conservation and innovation: Plastome evolution during rapid radiation of Rhodiola on the Qinghai-Tibetan Plateau. Mol Phylogenet Evol. 2020;144:106713.
   PubMed Web of Science ®Google Scholar
• Osteryoung KW, Nunnari J. The division of endosymbiotic organelles. Science. 2003;302(5651):1698–1704.
   PubMed Web of Science ®Google Scholar
• Charlesworth B. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet. 2009;10(3):195–205.
   PubMed Web of Science ®Google Scholar
• Han TS, Zheng QJ, Onstein RE, et al. Polyploidy promotes species diversification of Allium through ecological shifts. New Phytol. 2020;225(1):571–583.
   PubMed Web of Science ®Google Scholar