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Phylogenomic Analysis of Transcriptomic Sequences Of Acta Oceanol. Sin., 2014, Vol. 33, No. 2, P. 86–93 DOI: 10.1007/s13131-014-0444-3 http://www.hyxb.org.cn E-mail: [email protected] Phylogenomic analysis of transcriptomic sequences of mitochondria and chloroplasts for marine red algae (Rhodophyta) in China JIA Shangang1,3†, WANG Xumin1,3†, QIAN Hao2, LI Tianyong2, SUN Jing1,3,4, WANG Liang1,3,4, YU Jun1,3, LI Xingang1,3, YIN Jinlong1, LIU Tao2*, WU Shuangxiu1,3* 1 CAS Key Laboratory of Genome Sciences and Information, Beijing Key Laboratory of Genome and Precision Medicine Technologies, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, China 2 College of Marine Life Science, Ocean University of China, Qingdao 266003, China 3 Beijing Key Laboratory of Functional Genomics for Dao-di Herbs, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, China 4 University of Chinese Academy of Sciences, Beijing 100049, China Received 22 March 2013; accepted 2013 ©The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2014 Abstract The chloroplast and mitochondrion of red algae (Phylum Rhodophyta) may have originated from different endosymbiosis. In this study, we carried out phylogenomic analysis to distinguish their evolutionary lin- eages by using red algal RNA-seq datasets of the 1 000 Plants (1KP) Project and publicly available complete genomes of mitochondria and chloroplasts of Rhodophyta. We have found that red algae were divided into three clades of orders, Florideophyceae, Bangiophyceae and Cyanidiophyceae. Taxonomy resolution for Class Florideophyceae showed that Order Gigartinales was close to Order Halymeniales, while Order Graci- lariales was in a clade of Order Ceramials. We confirmed Prionitis divaricata (Family Halymeniaceae) was closely related to the clade of Order Gracilariales, rather than to genus Grateloupia of Order Halymeniales as reported before. Furthermore, we found both mitochondrial and chloroplastic genes in Rhodophyta under negative selection (Ka/Ks < 1), suggesting that red algae, as one primitive group of eukaryotic algae, might share joint evolutionary history with these two organelles for a long time, although we identified some dif- ferences in their phylogenetic trees. Our analysis provided the basic phylogenetic relationships of red algae, and demonstrated their potential ability to study endosymbiotic events. Key words: red algae, Rhodophyta, phylogenetic trees, mitochondrion, chloroplast Citation: Jia Shangang, Wang Xumin, Qian Hao, Li Tianyong, Sun Jing, Wang Liang, Yu Jun, Li Xingang, Yin Jinlong, Liu Tao, Wu Shuangxiu. 2014. Phylogenomic analysis of transcriptomic sequences of mitochondria and chloroplasts for marine red algae (Rho- dophyta) in China. Acta Oceanologica Sinica, 33(2): 86–93, doi: 10.1007/s13131-014-0444-3 1 Introduction Some missing genes had relocated to the nucleus, and many Red algae (Rhodophyta) are a distinct eukaryotic lineage genes were lost eventually (Martin et al., 1998). In subsequent which lacks chlorophyll b/c, centrioles and flagella in all life endosymbiosis, also called second or third endosymbiosis, eu- stages, but contains allophycocyanin, phycocyanin and phyco- karyotic hosts engulfed red algae or green algae, so that their erythrin in the form of phycobilisomes on unstacked thylakoids plastids finally contained three or four bounding membranes (Kawai et al., 2007). They are a morphologically diverse group (Green, 2011). In contrast, eukaryotes acquired algal mitochon- that consists of 6 000 unicellular and multicellular species in at dria long before the establishment of plastids. It was suggested least 12 orders (Burger and Nedelcu, 2012). For a long time, it is that mitochondria originated from an α-proteobacterial ances- believed that red algae diverged early from the primary endo- tor (Gray et al., 2001), and co-evolved together with their host, symbiosis. The ancient red algae share a common plastid with which means mitochondrial DNA probably could predict the the ancient green algae (Cavalier-Smith, 1998). evolutionary history of nuclear genome as a whole (Burger and Based on the primary endosymbiosis theory, the origin of Nedelcu, 2012). Although similar evolutionary events may be plastids would be derived from cyanobacterium-like prokary- shared in one single algal group, algal phylogenies based on otes (Rodríguez-Ezpeleta et al., 2005), leading to the origins of genes of plastid and mitochondrion may not be identical due three major host lineages: green algae and land plants, red algae to their potential differences in evolutionary history. Such dif- and glaucophytes (Moreira et al., 2000; McFadden, 2001). The ferences reflect the distinct endosymbiotic events of these two primary endosymbiosis resulted into the substantial reduc- organelles. For example, we had suggested that in the phyloge- tion of plastid genomes which have two bounding membranes. netic trees built with algal ESTs and genomes of mitochondria Foundation item: The National Natural Science Foundation of China under contract Nos 31140070, 31271397 and 41206116; the algal transcrip- tome sequencing was supported by 1KP Project (www.onekp.com). *Corresponding author, E-mail: [email protected], [email protected] †Contributed equally. JIA Shangang et al. Acta Oceanol. Sin., 2014, Vol. 33, No. 2, P. 86–93 87 and chloroplasts, Ulva prolifera was placed in a sister position major marine red algae, especially at the molecular genetic to Ulva linza and shared a similar chloroplast origin with Pseu- level. dendoclonium akinetum (Jia et al., 2011). Furthermore, chloroplastic and mitochondrial origins are 2 Materials and methods mostly determined based on the shared conserved regions or genes in the algal genomes, DNA or protein sequences. Protein 2.1 Sequence datasets from 1kp Project sequences are more preferred because they are more conserved The assembled transcriptomic sequencing datasets were than DNA. Many genes can be used to have a close look at al- downloaded from the website of 1KP Project, including 22 algal gal phylogenies, such as small subunit (SSU) (Tan and Druehl, species of Phylum Rhodophyta (Table 1). In total, 476 583 455 1994) and large subunit (LSU) of rDNA (Phillips et al., 2008) in base pairs as a candidate database were used to search for or- nucleus, rbcL, psaA and psbA (Cho et al., 2004) in plastids, and thologs in phylogenetic analysis. Cytochrome c (Danne et al., 2012) in mitochondria. Meanwhile Up to date, ten red algal species' complete mitochondrial the available whole-genome data have been valuable resources genomes have been sequenced, belonging to five distinct in algal research, especially phylogenomic analysis which is al- Rhodophyte orders, which are Cyanidiales, Gigartinales, Plo- ways performed for phylogenetic relationships. Phylogenomics camiales, Gracilariales and Bangiales. In contrast, only Order was first introduced in 1998 (Eisen, 1998), and widely accepted Gracilariales, Cyanidiales, and Bangiales have complete chloro- for phylogenetic inference. It is noted that the concatenated plastic genomes sequenced in five species. The gene numbers genes provide more comprehensive information than a single range 22–33 for mitochondria and 196–208 for plastids (Table one, and expressed-sequence-tags (ESTs) and genomes from 2). These complete genome sequences are available in NCBI. mitochondria and plastids can be used to construct phyloge- netic trees (Hallstrom and Janke, 2009). 2.2 Construction of phylogenetic trees In this study, as part of the 1 000 Plants (1KP) Project (http:// We collected all protein sequences of ten mitochondrial www.onekp.com/) which covers more than 1 000 different spe- genomes and five chloroplastic ones (including the out- cies of plants by generating large scale gene sequence informa- group species, Cyanophora paradoxa of Phylum Glauophyta, tion, we focused on 22 Chinese marine red alga species, includ- NC_001675.1) from NCBI website as references. Considering ing 21 species of class Florideophyceae and one species of class possible horizontal gene transfer or gene exchanges between Bangiophyceae. Based on the expressed gene orthologs from nucleus and organelles, we identified 18 typical genes shared the 1KP Project database and the publicly available complete by ten complete mitochondrial genomes and 139 genes shared red algal genomes of mitochondria and chloroplasts in NCBI, by five chloroplastic genomes in order to exclude potential we conducted a phylogenomic analysis, and our results showed nucleus originated genes. Using these typical and shared refer- that they are useful for development and utilization of Chinese ence genes, we performed local TBLASTN search against the as- Table 1. The 22 red algal species information with assembled contigs based on RNA-seq datasets Order Family Species Contig# Tot/Mb Avg/bp Lon/bp Ceramiales Dasyaceae Heterosiphonia pulchra 39 345 23.4 595 18 563 Ceramiaceae Ceramium kondoi 22 997 18.2 790 15 965 Rhodomelaceae Polysiphonia japonica 24 377 18.0 739 11 665 Symphyocladia latiuscul 37 839 18.5 490 15 887 Gigartinales Dumontiaceae Dumontia simplex 18 665 18.4 987 14 732 Endocladiaceae Gloiopeltis furcata 20 184 19.5 965 18 192 Gigartinaceae Chondrus crispus 25 526 20.3 797 16 329 Mazzaella japonica 26 703 21.2 795 18 268 Phyllophoraceae Gymnogongrus ftabelliformis 21 986 25.5 1 161 19 290 Solieriaceae Kappaphycus alvarezii 54 852 26.3 480 8 409 Eucheuma denticulatum 25 025 22.1 885 16 577 Betaphycus gelatinae 24 161 23.1 955 16 487 Gracilariales Gracilariaceae Gracilaria asiatica
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