Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Systematic Botany Australian Systematic Botany Society
Taxonomy, biogeography and evolution of plants
RESEARCH ARTICLE

Evolution of Geosiris (Iridaceae): historical biogeography and plastid-genome evolution in a genus of non-photosynthetic tropical rainforest herbs disjunct across the Indian Ocean

Elizabeth M. Joyce https://orcid.org/0000-0001-8291-8058 A B C E , Darren M. Crayn https://orcid.org/0000-0001-6614-4216 A B C , Vivienne K. Y. Lam D , Wesley K. Gerelle D , Sean W. Graham D and Lars Nauheimer https://orcid.org/0000-0002-2847-0966 A B C
+ Author Affiliations
- Author Affiliations

A Australian Tropical Herbarium, James Cook University, 14–88 McGregor Road, Smithfield, Qld 4878, Australia.

B College of Science and Engineering, James Cook University, 14–88 McGregor Road, Smithfield, Qld 4878, Australia.

C Centre for Tropical Environmental Sustainability Science, James Cook University—Cairns, 14–88 McGregor Road, Smithfield, Qld 4878, Australia.

D Department of Botany, University of British Columbia, 6270 University Boulevard, Vancouver, BC, V6T 1Z4, Canada.

E Corresponding author. Email: lizzy.joyce@my.jcu.edu.au

Australian Systematic Botany 31(6) 504-522 https://doi.org/10.1071/SB18028
Submitted: 2 May 2018  Accepted: 14 October 2018   Published: 13 December 2018

Abstract

Mycoheterotrophs, i.e. plants that acquire carbon from root-associated soil fungi, often have highly degraded plastomes, reflecting relaxed selective constraints on plastid genes following the loss of photosynthesis. Geosiris Baill. is the only mycoheterotrophic genus in Iridaceae and comprises two species in Madagascar and nearby islands, and a third recently discovered species in north-eastern Australia. Here, we characterise the plastomes of the Australian and one Madagascan species to compare patterns of plastome degradation in relation to autotrophic and other mycoheterotrophic taxa and investigate the evolutionary and biogeographical history of the genus in Iridaceae. Both examined species have lost approximately half their plastid-encoded genes and a small but significant reduction in purifying selection in retained non-photosynthetic genes was observed. Geosiris is confirmed as monophyletic, with initial divergence of the genus occurring c. 53 million years ago, and subsequent diversification occurring c. 30 million years ago. Africa (including Madagascar) is reconstructed as the most likely ancestral area of the genus, implying a major range-expansion event of one lineage to Australia after its divergence in the Oligocene. Our study has highlighted the dynamic evolutionary history of Geosiris, contributed to the characterisation of mycoheterotrophic plastomes, and furthered our understanding of plastome structure and function.

Additional keywords: degradation, heterotrophic, monocot, mycoheterotroph, plastome.


References

Akaike H (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.
A new look at the statistical model identification.Crossref | GoogleScholarGoogle Scholar |

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.
Basic local alignment search tool.Crossref | GoogleScholarGoogle Scholar |

Angiosperm Phylogeny Group Chase MW, Christenhusz MJM, Fay MF, Byng JW, Judd WS, Soltis DE, Mabberley DJ, Sennikov AN, Soltis PS, Stevens PF (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181, 1–20.
An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV.Crossref | GoogleScholarGoogle Scholar |

Baillon HE (1894) Une Iridacée sans matière verte. Bulletin Mensuel de la Société Linnéenne de Paris 2, 1149–1150.

Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19, 455–477.
SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing.Crossref | GoogleScholarGoogle Scholar |

Barcelona JF, Nickrent DL, LaFrankie JV, Callado JRC, Pelser PB (2013) Co’s Digital Flora of the Philippines: plant identification and conservation through cybertaxonomy. Philippine Journal of Science 142, 57–67.

Barrett CF, Davis JI (2012) The plastid genome of the mycoheterotrophic Corallorhiza striata (Orchidaceae) is in the relatively early stages of degradation. American Journal of Botany 99, 1513–1523.
The plastid genome of the mycoheterotrophic Corallorhiza striata (Orchidaceae) is in the relatively early stages of degradation.Crossref | GoogleScholarGoogle Scholar |

Barrett CF, Freudenstein JV, Li J, Mayfield-Jones DR, Perez L, Pires JC, Santos C (2014) Investigating the path of plastid genome degradation in an early transitional clade of heterotrophic orchids, and implications for heterotrophic angiosperms. Molecular Biology and Evolution 31, 3095–3112.
Investigating the path of plastid genome degradation in an early transitional clade of heterotrophic orchids, and implications for heterotrophic angiosperms.Crossref | GoogleScholarGoogle Scholar |

Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society – B. Methodological 57, 289–300.

Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537
BEAST 2: a software platform for Bayesian evolutionary analysis.Crossref | GoogleScholarGoogle Scholar |

Braukmann TWA, Broe MB, Stefanović S, Freudenstein JV (2017) On the brink: the highly reduced plastomes of nonphotosynthetic Ericaceae. New Phytologist 216, 254–266.
On the brink: the highly reduced plastomes of nonphotosynthetic Ericaceae.Crossref | GoogleScholarGoogle Scholar |

Bromham L, Cowman PF, Lanfear R (2013) Parasitic plants have increased rates of molecular evolution across all three genomes. BMC Evolutionary Biology 13, 126
Parasitic plants have increased rates of molecular evolution across all three genomes.Crossref | GoogleScholarGoogle Scholar |

Brummitt RK, Pando F, Hollis S, Brummitt NA (2001) ‘World Geographical Scheme for Recording Plant Distributions.’ (International Working Group on Taxonomic Databases for Plant Sciences, TDWG: Pittsburgh, PA, USA)

Chase MW, Duvall MR, Hills HG, Conran JG, Cox AV, Eguiarte LE, Hartwell J, Fay MF, Caddick LR, Cameron KM, Hoot SB (1995) Molecular phylogenetics of Lilianae. In ‘Monocotyledons: Systematics and Evolution’. (Eds P Rudall, PJ Cribb, DF Cutler, CJ Humphries) pp. 109–137. (Royal Botanic Gardens, Kew: London, UK)

Cody S, Richardson JE, Rull V, Ellis C, Pennington RT (2010) The great American biotic interchange revisited. Ecography 33, 326–332.

Cooper WE (2017) Thismia hawkesii W.E.Cooper and T. lanternatus W.E.Cooper (Thismiaceae), two new fairy lantern species from the Wet Tropics Bioregion, Queensland, Australia. Austrobaileya 10, 130–138.

Crayn DM, Costion C, Harrington MG (2015) The Sahul–Sunda floristic exchange: dated molecular phylogenies document Cenozoic intercontinental dispersal dynamics. Journal of Biogeography 42, 11–24.
The Sahul–Sunda floristic exchange: dated molecular phylogenies document Cenozoic intercontinental dispersal dynamics.Crossref | GoogleScholarGoogle Scholar |

Cusimano N, Wicke S (2016) Massive intracellular gene transfer during plastid genome reduction in nongreen Orobanchaceae. New Phytologist 210, 680–693.
Massive intracellular gene transfer during plastid genome reduction in nongreen Orobanchaceae.Crossref | GoogleScholarGoogle Scholar |

Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772
jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar |

Doyle J, Doyle JL (1987) Genomic plant DNA preparation from fresh tissue-CTAB method. Phytochemical Bulletin 19, 11–15.

Drummond AJ, Ho SY, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88
Relaxed phylogenetics and dating with confidence.Crossref | GoogleScholarGoogle Scholar |

Eriksson O, Kainulainen K (2011) The evolutionary ecology of dust seeds. Perspectives in Plant Ecology, Evolution and Systematics 13, 73–87.
The evolutionary ecology of dust seeds.Crossref | GoogleScholarGoogle Scholar |

Goldblatt P, Manning JC (2008) ‘The Iris family: Natural History and Classification.’ (Timber Press: Portland, OR, USA)

Goldblatt P, Manning JC (2010) Iridaceae. Geosiris albiflora (Geosiridoideae), a new species from the Comoro Archipelago. Bothalia 40, 169–171.

Goldblatt P, Rodriguez A, Powell MP, Davies TJ, Manning JC, van der Bank M, Savolainen V (2008) Iridaceae ‘out of Australasia’? Phylogeny, biogeography, and divergence time based on plastid DNA sequences. Systematic Botany 33, 495–508.
Iridaceae ‘out of Australasia’? Phylogeny, biogeography, and divergence time based on plastid DNA sequences.Crossref | GoogleScholarGoogle Scholar |

Graham SW, Reeves PA, Burns ACE, Olmstead RG (2000) Microstructural changes in noncoding chloroplast DNA: interpretation, evolution and utility of indels and inversions in basal angiosperm phylogenetic inference. International Journal of Plant Sciences 161, S83–S96.
Microstructural changes in noncoding chloroplast DNA: interpretation, evolution and utility of indels and inversions in basal angiosperm phylogenetic inference.Crossref | GoogleScholarGoogle Scholar |

Graham SW, Lam VKY, Merckx VSFT (2017) Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes. New Phytologist 214, 48–55.
Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes.Crossref | GoogleScholarGoogle Scholar |

Gray B, Low YW (2017) First record of Geosiris (Iridaceae: Geosiridoideae) from Australasia: a new record and a new species from the Wet Tropics of Queensland, Australia. Candollea 72, 249–255.
First record of Geosiris (Iridaceae: Geosiridoideae) from Australasia: a new record and a new species from the Wet Tropics of Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

Iles WJD, Smith SY, Gandolfo MA, Graham SW (2015) Monocot fossils suitable for molecular dating analyses. Botanical Journal of the Linnean Society 178, 346–374.
Monocot fossils suitable for molecular dating analyses.Crossref | GoogleScholarGoogle Scholar |

Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar |

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar |

Kim HT, Kim JS, Moore MJ, Neubig KM, Williams NH, Whitten WM, Kim J-H (2015) Seven new complete plastome sequences reveal rampant independent loss of the ndh gene family across orchids and associated instability of the inverted repeat/small single-copy region boundaries. PLoS One 10, e0142215
Seven new complete plastome sequences reveal rampant independent loss of the ndh gene family across orchids and associated instability of the inverted repeat/small single-copy region boundaries.Crossref | GoogleScholarGoogle Scholar |

Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23, 1289–1291.
Enhancements and modifications of primer design program Primer3.Crossref | GoogleScholarGoogle Scholar |

Lam VKY, Merckx VSFT, Graham SW (2016) A few-gene phylogenetic framework for mycoheterotrophic monocots. American Journal of Botany 103, 692–708.
A few-gene phylogenetic framework for mycoheterotrophic monocots.Crossref | GoogleScholarGoogle Scholar |

Lam VKY, Darby H, Merckx VSFT, Lim G, Yukawa T, Neubig KM, Abbott JR, Beatty GE, Provan J, Soto Gomez M, Graham SW (2018) Phylogenomic inference in extremis: a case study with mycoheterotroph plastomes. American Journal of Botany 105, 480–494.
Phylogenomic inference in extremis: a case study with mycoheterotroph plastomes.Crossref | GoogleScholarGoogle Scholar | [https://doi.org/]

Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.

Lim GS, Barrett CF, Pang C-C, Davis JI (2016) Drastic reduction of plastome size in the mycoheterotrophic Thismia tentaculata relative to that of its autotrophic relative Tacca chantrieri. American Journal of Botany 103, 1129–1137.
Drastic reduction of plastome size in the mycoheterotrophic Thismia tentaculata relative to that of its autotrophic relative Tacca chantrieri.Crossref | GoogleScholarGoogle Scholar |

Logacheva MD, Schelkunov MI, Nuraliev MS, Samigullin TH, Penin AA (2014) The plastid genome of mycoheterotrophic monocot Petrosavia stellaris exhibits both gene losses and multiple rearrangements. Genome Biology and Evolution 6, 238–246.
The plastid genome of mycoheterotrophic monocot Petrosavia stellaris exhibits both gene losses and multiple rearrangements.Crossref | GoogleScholarGoogle Scholar |

Lohan AJ, Wolfe KH (1998) A subset of conserved tRNA genes in plastid DNA of nongreen plants. Genetics 150, 425–433.

Lohse M, Drechsel O, Kahlau S, Bock R (2013) OrganellarGenomeDRAW: a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Research 41, W575–W581.
OrganellarGenomeDRAW: a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets.Crossref | GoogleScholarGoogle Scholar |

Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25, 955–964.
tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence.Crossref | GoogleScholarGoogle Scholar |

Magallón S, Gómez-Acevedo S, Sánchez-Reyes LL, Hernández-Hernández T (2015) A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist 207, 437–453.
A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity.Crossref | GoogleScholarGoogle Scholar |

Matzke NJ (2014) Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades. Systematic Biology 63, 951–970.
Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades.Crossref | GoogleScholarGoogle Scholar |

McLoughlin S (2001) The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism. Australian Journal of Botany 49, 271–300.
The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism.Crossref | GoogleScholarGoogle Scholar |

Merckx VSFT (2013) Mycoheterotrophy: an introduction. In ‘Mycoheterotrophy. The Biology of Plants Living on Fungi’. (Ed VSFT Merckx) pp. 1–17. (Springer Science and Business Media: New York, NY, USA)

Merckx VSFT, Mennes CB, Peay KG, Geml J (2013a) Evolution and diversification. In ‘Mycoheterotrophy. The Biology of Plants Living on Fungi’. (Ed. VSFT Merckx) pp. 215–244. (Springer Science and Business Media: New York, NY, USA)

Merckx VSFT, Smets EF, Specht CD (2013b) Biogeography and conservation. ‘Mycoheterotrophy. The Biology of Plants Living on Fungi’. (Ed. VSFT Merckx) pp. 103–156. (Springer Science and Business Media: New York, NY, USA)

Merckx VS, Gomes SI, Wapstra M, Hunt C, Steenbeeke G, Mennes CB, Walsh N, Smissen R, Hsieh T-H, Smets EF (2017) The biogeographical history of the interaction between mycoheterotrophic Thismia (Thismiaceae) plants and mycorrhizal Rhizophagus (Glomeraceae) fungi. Journal of Biogeography 44, 1869–1879.
The biogeographical history of the interaction between mycoheterotrophic Thismia (Thismiaceae) plants and mycorrhizal Rhizophagus (Glomeraceae) fungi.Crossref | GoogleScholarGoogle Scholar |

Molina J, Hazzouri KM, Nickrent D, Geisler M, Meyer RS, Pentony MM, Flowers JM, Pelser P, Barcelona J, Inovejas SA (2014) Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae). Molecular Biology and Evolution 31, 793–803.
Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae).Crossref | GoogleScholarGoogle Scholar |

Morley RJ (2003) Interplate dispersal paths for megathermal angiosperms. Perspectives in Plant Ecology, Evolution and Systematics 6, 5–20.
Interplate dispersal paths for megathermal angiosperms.Crossref | GoogleScholarGoogle Scholar |

Muellner-Riehl AN, Weeks A, Clayton JW, Buerki S, Nauheimer L, Chiang Y-C, Cody S, Pell SK (2016) Molecular phylogenetics and molecular clock dating of Sapindales based on plastid rbcL, atpB and trnL–trnF DNA sequences. Taxon 65, 1019–1036.
Molecular phylogenetics and molecular clock dating of Sapindales based on plastid rbcL, atpB and trnL–trnF DNA sequences.Crossref | GoogleScholarGoogle Scholar |

Naumann J, Der JP, Wafula EK, Jones SS, Wagner ST, Honaas LA, Ralph PE, Bolin JF, Maass E, Neinhuis C (2016) Detecting and characterizing the highly divergent plastid genome of the nonphotosynthetic parasitic plant Hydnora visseri (Hydnoraceae). Genome Biology and Evolution 8, 345–363.
Detecting and characterizing the highly divergent plastid genome of the nonphotosynthetic parasitic plant Hydnora visseri (Hydnoraceae).Crossref | GoogleScholarGoogle Scholar |

Rai HS, O’Brien HE, Reeves PA, Olmstead RG, Graham SW (2003) Inference of higher-order relationships in the cycads from a large chloroplast data set. Molecular Phylogenetics and Evolution 29, 350–359.
Inference of higher-order relationships in the cycads from a large chloroplast data set.Crossref | GoogleScholarGoogle Scholar |

Ree RH, Smith SA (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57, 4–14.
Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis.Crossref | GoogleScholarGoogle Scholar |

Reeves C (2014) The position of Madagascar within Gondwana and its movements during Gondwana dispersal. Journal of African Earth Sciences 94, 45–57.
The position of Madagascar within Gondwana and its movements during Gondwana dispersal.Crossref | GoogleScholarGoogle Scholar |

Reeves G, Chase MW, Goldblatt P, Rudall P, Fay MF, Cox AV, Lejeune B, Souza-Chies T (2001) Molecular systematics of Iridaceae: evidence from four plastid DNA regions. American Journal of Botany 88, 2074–2087.
Molecular systematics of Iridaceae: evidence from four plastid DNA regions.Crossref | GoogleScholarGoogle Scholar |

Ronquist F (1997) Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology 46, 195–203.
Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography.Crossref | GoogleScholarGoogle Scholar |

Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar |

Sanmartín I, Ronquist F (2004) Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns. Systematic Biology 53, 216–243.
Southern hemisphere biogeography inferred by event-based models: plant versus animal patterns.Crossref | GoogleScholarGoogle Scholar |

Sanmartín I, Enghoff H, Ronquist F (2001) Patterns of animal dispersal, vicariance and diversification in the Holarctic. Biological Journal of the Linnean Society. Linnean Society of London 73, 345–390.
Patterns of animal dispersal, vicariance and diversification in the Holarctic.Crossref | GoogleScholarGoogle Scholar |

Sauquet H (2013) A practical guide to molecular dating. Comptes Rendus. Palévol 12, 355–367.
A practical guide to molecular dating.Crossref | GoogleScholarGoogle Scholar |

Schelkunov MI, Shtratnikova VY, Nuraliev MS, Selosse M-A, Penin AA, Logacheva MD (2015) Exploring the limits for reduction of plastid genomes: a case study of the mycoheterotrophic orchids Epipogium aphyllum and Epipogium roseum. Genome Biology and Evolution 7, 1179–1191.
Exploring the limits for reduction of plastid genomes: a case study of the mycoheterotrophic orchids Epipogium aphyllum and Epipogium roseum.Crossref | GoogleScholarGoogle Scholar |

Sinn BT, Sedmak DD, Kelly LM, Freudenstein JV (2018) Total duplication of the small single copy region in the angiosperm plastome: rearrangement and inverted repeat instability in Asarum. American Journal of Botany 105, 71–84.
Total duplication of the small single copy region in the angiosperm plastome: rearrangement and inverted repeat instability in Asarum.Crossref | GoogleScholarGoogle Scholar |

Souza-Chies TT, Bittar G, Nadot S, Carter L, Besin E, Lejeune B (1997) Phylogenetic analysis of Iridaceae with parsimony and distance methods using the plastid gene rps4. Plant Systematics and Evolution 204, 109–123.
Phylogenetic analysis of Iridaceae with parsimony and distance methods using the plastid gene rps4.Crossref | GoogleScholarGoogle Scholar |

Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar |

Swiatek M, Kuras R, Sokolenko A, Higgs D, Olive J, Cinque G, Müller B, Eichacker LA, Stern DB, Bassi R, Herrmann RG, Wollman FA (2001) The chloroplast gene ycf9 encodes a Photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture. The Plant Cell 13, 1347–1368.
The chloroplast gene ycf9 encodes a Photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture.Crossref | GoogleScholarGoogle Scholar |

Thorne RF (1972) Major disjunctions in the geographic ranges of seed plants. The Quarterly Review of Biology 47, 365–411.
Major disjunctions in the geographic ranges of seed plants.Crossref | GoogleScholarGoogle Scholar |

Tiffney BH (1985) Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America. Journal of the Arnold Arboretum 66, 73–94.
Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America.Crossref | GoogleScholarGoogle Scholar |

Töpel M, Zizka A, Calió MF, Scharn R, Silvestro D, Antonelli A (2016) SpeciesGeoCoder: fast categorization of species occurrences for analyses of biodiversity, biogeography, ecology, and evolution. Systematic Biology 66, 145–151.

Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research 35, W71–W74.
Primer3Plus, an enhanced web interface to Primer3.Crossref | GoogleScholarGoogle Scholar |

Wertheim JO, Murrell B, Smith MD, Kosakovsky Pond SL, Scheffler K (2015) RELAX: detecting relaxed selection in a phylogenetic framework. Molecular Biology and Evolution 32, 820–832.
RELAX: detecting relaxed selection in a phylogenetic framework.Crossref | GoogleScholarGoogle Scholar |

Wicke S, Naumann J (2018) Molecular evolution of plastid genomes in parasitic flowering plants. Advances in Botanical Research 85, 315–347.
Molecular evolution of plastid genomes in parasitic flowering plants.Crossref | GoogleScholarGoogle Scholar |

Wicke S, Müller KF, de Pamphilis CW, Quandt D, Wickett NJ, Zhang Y, Renner SS, Schneeweiss GM (2013) Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family. The Plant Cell 25, 3711–3725.
Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family.Crossref | GoogleScholarGoogle Scholar |

Wicke S, Müller KF, dePamphilis CW, Quandt D, Bellot S, Schneeweiss GM (2016) Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants. Proceedings of the National Academy of Sciences of the United States of America 113, 9045–9050.
Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants.Crossref | GoogleScholarGoogle Scholar |

Wikström N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proceedings of the Royal Society of London – B. Biological Sciences 268, 2211–2220.
Evolution of the angiosperms: calibrating the family tree.Crossref | GoogleScholarGoogle Scholar |

Wolfe KH, Li W-H, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences of the United States of America 84, 9054–9058.
Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs.Crossref | GoogleScholarGoogle Scholar |

Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20, 3252–3255.
Automatic annotation of organellar genomes with DOGMA.Crossref | GoogleScholarGoogle Scholar |

Yang Z (1998) Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Molecular Biology and Evolution 15, 568–573.
Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution.Crossref | GoogleScholarGoogle Scholar |

Yang Z (2007) PAML4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24, 1586–1591.
PAML4: phylogenetic analysis by maximum likelihood.Crossref | GoogleScholarGoogle Scholar |

Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693.
Trends, rhythms, and aberrations in global climate 65 Ma to present.Crossref | GoogleScholarGoogle Scholar |

Zachos JC, Dickens GR, Zeebe RE (2008) An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451, 279–283.
An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics.Crossref | GoogleScholarGoogle Scholar |

Zhang J, Ruhlman TA, Sabir JSM, Blazier JC, Weng M-L, Park S, Jansen RK (2016) Coevolution between nuclear-encoded DNA replication, recombination, and repair genes and plastid genome complexity. Genome Biology and Evolution 8, 622–634.
Coevolution between nuclear-encoded DNA replication, recombination, and repair genes and plastid genome complexity.Crossref | GoogleScholarGoogle Scholar |

Zhou L, Su YCF, Thomas DC, Saunders RMK (2012) ‘Out-of-Africa’ dispersal of tropical floras during the Miocene climatic optimum: evidence from Uvaria (Annonaceae). Journal of Biogeography 39, 322–335.
‘Out-of-Africa’ dispersal of tropical floras during the Miocene climatic optimum: evidence from Uvaria (Annonaceae).Crossref | GoogleScholarGoogle Scholar |

Zhu A, Guo W, Gupta S, Fan W, Mower JP (2016) Evolutionary dynamics of the plastid inverted repeat: the effects of expansion, contraction, and loss on substitution rates. New Phytologist 209, 1747–1756.
Evolutionary dynamics of the plastid inverted repeat: the effects of expansion, contraction, and loss on substitution rates.Crossref | GoogleScholarGoogle Scholar |