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Evolutionary History of PEPC Genes in Green Plants: Implications for the 7 Q 5 Evolution of CAM in Orchids

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Evolutionary History of PEPC Genes in Green Plants: Implications for the 7 Q 5 Evolution of CAM in Orchids YMPEV 5323 No. of Pages 6, Model 5G 23 October 2015 Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx 1 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev 2 Short Communication 6 4 Evolutionary history of PEPC genes in green plants: Implications for the 7 q 5 evolution of CAM in orchids a,b,1 c,1 c a c,d,e,⇑ 8 Hua Deng , Liang-Sheng Zhang , Guo-Qiang Zhang , Bao-Qiang Zheng , Zhong-Jian Liu , a,⇑ 9 Yan Wang 10 a State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of State Forestry Administration, Research Institute of Forestry, Chinese 11 Academy of Forestry, Beijing 100091, China 12 b Research Institute of Forestry Policy and Information, Chinese Academy of Forestry, Beijing 100091, China 13 c Shenzhen Key Laboratory for Orchid Conservation and Utilization, The National Orchid Conservation Center of China and The Orchid Conservation and Research Center of 14 Shenzhen, Shenzhen, China 15 d The Center for Biotechnology and BioMedicine, Graduate School at Shenzhen, Tsinghua University, Shenzhen, China 16 e College of Forestry, South China Agricultural University, Guangzhou, China 1718 19 article info abstract 3421 22 Article history: The phosphoenolpyruvate carboxylase (PEPC) gene is the key enzyme in CAM and C4 photosynthesis. A 35 23 Received 14 November 2014 detailed phylogenetic analysis of the PEPC family was performed using sequences from 60 available pub- 36 24 Revised 7 October 2015 lished plant genomes, the Phalaenopsis equestris genome and RNA-Seq of 15 additional orchid species. The 37 25 Accepted 8 October 2015 PEPC family consists of three distinct subfamilies, PPC-1, PPC-2, and PPC-3, all of which share a recent 38 26 Available online xxxx common ancestor in chlorophyte algae. The eudicot PPC-1 lineage separated into two clades due to whole 39 genome duplication (WGD). Similarly, the monocot PPC-1 lineage also divided into PPC-1M1 and PPC- 40 27 Keywords: 1M2 through an ancient duplication event. The monocot CAM- or C -related PEPC originated from the 41 28 Crassulacean acid metabolism (CAM) 4 clade PPC-1M1. WGD may not be the major driver for the performance of CAM function by PEPC, 42 29 Orchidaceae 30 Phosphoenolpyruvate carboxylase (PEPC) although it increased the number of copies of the PEPC gene. CAM may have evolved early in monocots, 43 31 Phylogeny as the CAM-related PEPC of orchids originated from the monocot ancient duplication, and the earliest 44 32 RNA-Seq sequences CAM-related PEPC may have evolved immediately after the diversification of monocots, with CAM devel- 45 33 oping prior to C4. Our results represent the most complete evolutionary history of PEPC genes in green 46 plants to date and particularly elucidate the origin of PEPC in orchids. 47 Ó 2015 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license 48 (http://creativecommons.org/licenses/by-nc-nd/4.0/). 49 50 51 52 53 1. Introduction Silvera et al., 2010a). In the Orchidaceae, 50% of species were antic- 60 ipated to be CAM plants (Smith and Winter, 1996). 61 54 C4 photosynthesis has evolved independently more than 62 Phosphoenolpyruvate carboxylase (PEPC; EC 4.1.1.31) plays a 62 55 times, including 7500 species in 19 families or 3% of flowering key role in the carbon metabolism of C4 and crassulacean acid 63 56 plant species (Sage et al., 2011), whereas CAM has arisen multiple metabolism (CAM) plants (Masumoto et al., 2010) and markedly 64 57 times in 35 plant families and is present in 30,000 species, improves photosynthetic efficiency and water use efficiency 65 58 comprising 6% of plant species from the Lycophyta, Pterophyta, (Driever and Kromdijk, 2013). PEPC is widely present in all photo- 66 59 Gnetophyta, and Anthophyta divisions (Keeley and Rundel, 2003; synthetic organisms (Izui et al., 2004). In addition to photosyn- 67 thetic function, housekeeping isoforms of PEPC also play 68 essential metabolic roles in non-photosynthetic functions (Fan 69 Abbreviations: CAM, crassulacean acid metabolism; ML, maximum likelihood; et al., 2013; O’Leary et al., 2011). Consistent with its diverse roles 70 NJ, neighbor-joining; PEPC, phosphoenolpyruvate carboxylase; WGD, whole and origin, plant PEPC can be divided into two types: plant-type 71 genome duplication. q 72 This paper was edited by the Associate Editor Elizabeth Zimmer. PEPC (PPC-1) and bacterial-type PEPC (PPC-2). Although the PEPC ⇑ Corresponding authors at: Shenzhen Key Laboratory for Orchid Conservation involved in the CAM pathway has shown high sequence identity 73 and Utilization, The National Orchid Conservation Center of China and The Orchid to its counterpart in C4 photosynthesis, these genes are completely 74 Conservation and Research Center of Shenzhen, Shenzhen, China (Z.-J. Liu). different (Christin et al., 2014). 75 E-mail addresses: [email protected] (Z.-J. Liu), [email protected] Understanding the origin and function of PEPC has both funda- 76 (Y. Wang). mental and bioengineering importance, as it may help in identify- 77 1 These authors contributed equally to this work. http://dx.doi.org/10.1016/j.ympev.2015.10.007 1055-7903/Ó 2015 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article in press as: Deng, H., et al. Evolutionary history of PEPC genes in green plants: Implications for the evolution of CAM in orchids. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.10.007 YMPEV 5323 No. of Pages 6, Model 5G 23 October 2015 2 H. Deng et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx 78 ing certain gene lineages suitable for the evolution of C4 and CAM After local searches were performed in the proteome datasets with 137 79 plants and in detecting specific amino acids essential for enzymatic the PEPC domain (PF00311) (Finn et al., 2014), the resulting 138 80 characteristics of photosynthetic PEPC and therefore in applying sequences were manually adjusted in multiple sequence align- 139 81 the C4 and CAM pathways in crops and fuel plants. The evolution- ments to delete obvious errors. Multiple sequence alignment was 140 82 ary history of the PEPC gene family, however, remains poorly performed in MUSCLE using the default parameters (Edgar, 2004). 141 83 understood in green plants, especially in the CAM plants, such as 84 orchids. In this work, a detailed phylogenetic analysis of the PEPC 2.4. Phylogenetic reconstruction and synteny analysis 142 85 family was performed, using Phalaenopsis equestris genome 86 sequences (Cai et al., 2015) and the RNA-Seq sequences of 15 other The phylogenetic trees of PEPC were reconstructed using the 143 87 orchid species, in combination with available genome sequences, neighbor-joining (NJ) and maximum likelihood (ML) methods. 144 88 to outline the evolutionary history of PEPC and to identify suitable Using the ‘pairwise deletion’ option and the ‘Poisson correction’ 145 model, we constructed NJ trees with MEGA, with a bootstrap test 146 89 lineages for the evolution of C4 and CAM plants. Our comparative 90 analyses help to elucidate the history of photosynthetic PEPC of 1000 replicates. ML trees were constructed using FastTree 147 91 and, in particular, shed light on the origin of PEPC in orchids. (http://www.microbesonline.org/fasttree) with the approximate 148 likelihood ratio test (aLRT) method. Synteny was detected using 149 92 2. Materials and methods the Plant Genome Duplication Database (Tang et al., 2008). 150 93 2.1. RNA extraction and transcriptome sequencing 3. Results and discussion 151 94 Total RNA was extracted from Dendrobium catenatum and Pha- 3.1. The evolutionary history of PEPC genes in green plants 152 95 laenopsis equestris tissue samples from the National Orchid Conser- 96 vation Center of China (NOCC) using the Sigma SpectrumTM Plant We constructed a phylogenetic tree of PEPC family members 153 97 Total RNA Kit. To identify the number of PEPC genes present in using genomic sequences of representative species (Fig. S1). The 154 98 D. catenatum, different tissues and timings were sampled, includ- tree shows that the PEPC gene family can be divided into three lin- 155 99 ing leaves (one was sampled at dawn, 6:30 a.m. and another at eages: PPC-1 (plant-type PEPC), PPC-2 (bacterial-type PEPC) and 156 100 dusk, 6:30 p.m.), stem, root (one sample of just the green tips with- PPC-3. To comprehensively understand the origin of PEPC, we 157 101 out velamen, another of the root with velamen), blossom-bud, and added the recently sequenced genome of Klebsormidium flaccidum 158 102 lip (modified petal). The P. equestris samples were taken from leaf, to the dataset. As the terrestrial algae closest to land plants, the 159 103 stem, root, and flower. Except for the leaves of D. catenatum, all charophytic alga Klebsormidium is important for finding the origins 160 104 other samples were collected in daytime. The transcriptome library of the CO2-concentrating mechanism and PEPC in aquatic algae and 161 105 construction and sequencing were performed at BGI and followed land plants. Our phylogenetic tree indicates that the PEPC of Kleb- 162 106 the protocols in Peng’s paper (Peng et al., 2012b). sormidium fills the major phylogenetic gap between PPC-1 and 163 PPC-2, as it is located between Chlorophyta and land plants. We 164 107 2.2. Data sources also found another class of PEPC in Klebsormidium and retrieved 165 its homologs from NCBI GenBank (http://www.ncbi.nlm.nih.gov/).
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