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Phylogenetic Relationships and Divergence Times of the Family Araucariaceae Based on the DNA Sequences of Eight Genes

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Phylogenetic Relationships and Divergence Times of the Family Araucariaceae Based on the DNA Sequences of Eight Genes Chinese Science Bulletin © 2009 SCIENCE IN CHINA PRESS Springer Phylogenetic relationships and divergence times of the family Araucariaceae based on the DNA sequences of eight genes LIU Nian1, ZHU Yong1, WEI ZongXian2, CHEN Jie1, WANG QingBiao1, JIAN ShuGuang4, ZHOU DangWei5, SHI Jing1, YANG Yong6 & ZHONG Yang1,3† 1 Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan Univer- sity, Shanghai 200433, China; 2 Lushan Botanical Garden, Chinese Academy of Sciences, Lushan 332900, China; 3 Shanghai Center for Bioinformation Technology, Shanghai 200235, China; 4 South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China; 5 Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China; 6 Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China Araucariaceae is one of the most primitive families of the living conifers, and its phylogenetic rela- tionships and divergence times are critically important issues. The DNA sequences of 8 genes, i.e., nuclear ribosomal 18S and 26S rRNA, chloroplast 16S rRNA, rbcL, matK and rps4, and mitochondrial coxI and atp1, obtained from this study and GenBank were used for constructing the molecular phy- logenetic trees of Araucariaceae, indicating that the phylogenetic relationships among the three genera of this family should be ((Wollemia, Agathis), Araucaria). On the basis of the fossil calibrations of Wol- lemia and the two tribes Araucaria and Eutacta of the genus Araucaria, the divergence time of Arauca- riaceae was estimated to be (308 ± 53) million years ago, that is, the origin of the family was in the Late Carboniferous rather than Triassic as a traditional view. With the same gene combination, the diver- gence times of the genera Araucaria and Agathis were (246 ± 47) and (61 ± 15) Ma, respectively. Statis- tical analyses on the phylogenetic trees generated by using different genes and comparisons of the divergence times estimated by using those genes suggested that the chloroplast matK and rps4 genes are most suitable for investigating the phylogenetic relationships and divergence times of the family Araucariaceae. Araucariaceae, nrDNA 18S rRNA, nrDNA 26S rRNA, cpDNA 16S rRNA, cpDNA rbcL, cpDNA matK, cpDNA rps4, mtDNA coxl, mtDNA atp1, phylogeny, divergence time Araucariaceae is one of the most primitive families of origin and divergence of Araucariaceae can be helpful the living conifers. Its extant species are mainly distrib- for better understanding the geological climate change uted in tropical and subtropical zones of the southern of the paleocontinent. hemisphere, including Australia, New Zealand, New Received January 16, 2009; accepted March 27, 2009 Guinea, New Caledonia and other South Pacific Islands, doi: 10.1007/s11434-009-0373-2 †Corresponding author (email: [email protected]) as well as South America. The fossil records indicate Supported by the National Infrastructure of Natural Resources for Science and that this family had a wide distribution both in the Technology (Grant No. 2005DKA21403), MOST Basic Science and Technology (Grant No. 2007FY110100), Shanghai Leading Academic Discipline Project (Grant southern and northern hemispheres during the Mesozoic No. B111), Shanghai Science and Technology Committee (Grant No. 07XD14025), era, and gradually extinct in the northern hemisphere the Graduate Students Innovation Foundation of Fudan University (Grant No. EYH1322098) and National Science Fund for Fostering Talents in Basic Science after the Late Cretaceous. Therefore, investigation of the (Grant No. J0630643) Citation: Liu N, Zhu Y, Wei Z X, et al. Phylogenetic relationships and divergence times of the family Araucariaceae based on the DNA sequences of eight genes. Chinese Sci Bull, 2009, 54: 2648―2655, doi: 10.1007/s11434-009-0373-2 The family Araucariaceae consists of 41 species and 1 effects of the eight genes on the phylogenetic recon- subspecies in three genera, i.e., Araucaria, Agathis, and struction and estimation of the divergence times of the ARTICLES Wollemia [1], among which Wollemia is a monotypic ge- family were also discussed. nus discovered in 1994[2,3], dubbed “a living dinosaur on earth”, because the fossil records proved that Wollemia 1 Materials and methods [4] occurred in the Cretaceous period . When W. nobilis 1.1 Materials was found, only 26 adults and 14 juveniles existed in the W. nobilis was provided by Wollemi Pine International Wollemi National Park in New South Wales, Australia. Pty Ltd. and Araucaria araucana was provided by Ham- Since it shares the morphological characteristics of burg Botanical Garden, Germany. Other samples used in Araucaria and Agathis[5], the W. nobilis cone scale re- this study, including 7 species of Araucariaceae, two sembles that of the tribe Eutacta of Araucaria, and the species of Podocarpaceae, one species of Cephalotax- winged seeds are free from the cone scale like Agathis[6]. aceae, one species of Taxaceae, one species of Sciado- Recently, molecular phylogenetics has provided a pityaceae, two species of Taxodiaceae, two species of new method to identify the controversial phylogenetic Cupressaceae, and two species of Pinaceae, were col- relationships among the 3 genera of the family Arauca- [7] lected from the South China Botanical Garden. Voucher riaceae. Setoguchi et al. constructed a phylogenetic specimens were stored in the Institute of Biodiversity tree of W. nobilis, 10 Agathis species and 19 Araucaria Science at Fudan University. Fresh leaves were immedi- species based on the chloroplast rbcL gene. In this tree, [8,9] ately dried by silica gel after collection for further DNA which has been supported by many paleontologists , W. nobilis lies in the basal position of the Araucariaceae, extraction and sequencing. and Agathis is sister to Araucaria. However, a number 1.2 DNA extraction [10,11] of authors disagreed with this conclusion . They Total DNA were extracted using CTAB method[19]. believed that Agathis is sister to Wollemia, and Arauca- 1.3 Amplification and sequencing ria is a basal lineage of the Araucariaceae. There are two main reasons for the incongruence. One is about differ- Primer sequences were synthesized according to refer- [14,20–22] ent outgroups selected for constructing the phylogenetic ences or self-designed. The total PCR reaction tree. The class Coniferopsida was regarded as mono- volume was 50 μL, containing 1 μL DNA template, 1.5 [11,12] phyletic in some studies , while in other studies, mmol/L MgCl2, 0.2 mmol/L dNTPs, 1×PCR buffer, 1 paraphyletic[13,14]. Previous studies indicated that the μmol/L of each primer, and 2.5 U Taq DNA polymerase. Pinaceae, Sciadopityaceae, Podocarpaceae, or Cupres- The PCR cycling parameters were 1 cycle of 5 min at saceae was regarded as the closest group to the family 94℃ for denaturation; 35 cycles of 0.5 min at 94℃, 0.5 Araucariaceae[13,15–18]. In the work of Setoguchi et al.[7], min of 45－56℃ for primer annealing and 1.5－2 min the families Taxodiaceae, Cupressaceae and Podocar- at 72℃ for primer extension; 1 cycle of 7 min at 72℃. paceae were chosen as outgroups, while in other work, PCR products were isolated by electrophoresis in 1.2% the outgroups were from Coniferopsida, even Gymno- agarose gel and purified by gel extraction kit, cloned to [10,11] spermae . Another reason is about the different pMD19-T vector and sequenced by an ABI 377 DNA genes used in phylogenetic analyses. In previous studies, automated sequencer. The GenBank accession numbers a phylogenetic tree was generated with a single gene, yet of the DNA sequences used in this study are listed in MOLECULAR REVOLUTION a gene tree may have different topology from other gene Table 1. trees. Therefore, we collected the samples of Araucari- 1.4 Sequence analyses and statistical tests aceae worldwide and conducted a combined phyloge- netic analysis based on the DNA sequences of nuclear Multiple sequence alignment of DNA sequences from 15 18S and 26S rRNA sequences, chloroplast 16S rRNA, genera in Coniferopsida (9 families) containing 8 genes rbcL, matK and rps4 genes, and mitochondrial coxI and was obtained by using CLUSTAL X[23]. The best model atp1 genes in this study. The fossil records of Wollemia parameters were estimated with Modeltest 3.7[24]. Sin- and two tribes Araucaria and Eutacta of the genus gle-gene maximum likelihood (ML) trees and the com- Araucaria were used as calibrations for dating the di- bined ML tree were constructed by using PHYML[25], vergence times of the Araucariaceae. In addition, the with 1000 bootstrap replicates. Liu N et al. Chinese Science Bulletin | August 2009 | vol. 54 | no. 15 2649 Table 1 DNA sequences used in this study and their GenBank accession numbers Family Taxon 18S 26S rbcL matK rps4 cp16S coxI atp1 Araucariaceae Agathis alba EU164976b) EU165000b) EU164984b) EU164995b) EU165030b) EU164989b) EU165023b) EU165017b) Araucariaceae Agathis dammara EU164977b) EU165001b) U96477 EU164996b) EU165031b) EU164987b) EU165024b) EU165016b) Araucariaceae Agathis robusta EU164978b) EU165002b) AF249665 AF456371 EU165032b) EU164988b) EU165025b) EU165018b) Araucariaceae Araucaria araucana FJ179543 FJ179544 AF249664 AF456373 FJ179545 DQ629437 FJ179546 FJ179547 Araucariaceae Araucaria bidwillii EU164979b) EU165003b) ABU87751 EU164997b) EU165033b) EU164993b) EU165026b) EU165022b) Araucariaceae Araucaria angustifolia EU164980b) EU165004b) EU164985b) EU164998b) EU165034b) EU164994b)
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