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Version 3.24
Publication Type J
Authors Yang, YC; Yang, SH; Li, JF; Deng, YF; Zhang, Z; Xu, SH; Guo, WX; Zhong, CR; Zhou, RC; Shi, SH
Author Full Name Yang, Yuchen; Yang, Shuhuan; Li, Jianfang; Deng, Yunfei; Zhang, Zhang; Xu, Shaohua; Guo, Wuxia; Zhong, Cairong; Zhou, Renchao; Shi, Suhua
Title Transcriptome analysis of the Holly mangrove Acanthus ilicifolius and its terrestrial relative, Acanthus leucostachyus, provides insights into adaptation to intertidal zones
Language English
Document Type Article
Author Keywords Abiotic stress; Adaptation; Mangroves; Comparative transcriptome
Abstract Background: Acanthus is a unique genus consisting of both true mangrove and terrestrial species; thus, it represents an ideal system for studying the origin and adaptive evolution of mangrove plants to intertidal environments. However, little is known regarding the two respects of mangrove species in Acanthus. In this study, we sequenced the transcriptomes of the pooled roots and leaves tissues for a mangrove species, Acanthus ilicifolius, and its terrestrial congener, A. leucostachyus, to illustrate the origin of the mangrove species in this genus and their adaptive evolution to harsh habitats. Results: We obtained 73,039 and 69,580 contigs with N50 values of 741 and 1557 bp for A. ilicifolius and A. leucostachyus, respectively. Phylogenetic analyses based on four nuclear segments and three chloroplast fragments revealed that mangroves and terrestrial species in Acanthus fell into different clades, indicating a single origin of the mangrove species in Acanthus. Based on 6634 orthologs, A. ilicifolius and A. leucostachyus were found to be highly divergent, with a peak of synonymous substitution rate (Ks) distribution of 0.145 and an estimated divergence time of approximately 16.8 million years ago (MYA). The transgression in the Early to Middle Miocene may be the major reason for the entry of the mangrove lineage of Acanthus into intertidal environments. Gene ontology (GO) classifications of the full transcriptomes did not show any apparent differences between A. ilicifolius and A. leucostachyus, suggesting the absence of gene components specific to the mangrove transcriptomes. A total of 99 genes in A. ilicifolius were identified with signals of positive selection. Twenty-three of the 99 positively selected genes (PSGs) were found to be involved in salt, heat and ultraviolet stress tolerance, seed germination and embryo development under periodic inundation. These stress-tolerance related PSGs may be crucial for the adaptation of the mangrove species in this genus to stressful marine environments and may contribute to speciation in Acanthus. Conclusions: We characterized the transcriptomes of one mangrove species of Acanthus, A. ilicifolius, and its terrestrial relative, A. leucostachyus, and provided insights into the origin of the mangrove Acanthus species and their adaptive evolution to abiotic stresses in intertidal environments.
Author Address [Yang, Yuchen; Yang, Shuhuan; Li, Jianfang; Zhang, Zhang; Xu, Shaohua; Guo, Wuxia; Zhou, Renchao; Shi, Suhua] Sun Yat Sen Univ, State Key Lab Biocontrol, Guangzhou 510275, Guangdong, Peoples R China; [Yang, Yuchen; Yang, Shuhuan; Li, Jianfang; Zhang, Zhang; Xu, Shaohua; Guo, Wuxia; Zhou, Renchao; Shi, Suhua] Sun Yat Sen Univ, Guangdong Prov Key Lab Plant Resources, Guangzhou 510275, Guangdong, Peoples R China; [Deng, Yunfei] Chinese Acad Sci, Key Lab Plant Resource Conservat & Sustainable Ut, South China Bot Garden, Guangzhou 510650, Guangdong, Peoples R China; [Zhong, Cairong] Hainan Dongzhai Harbor Natl Nat Reserve, Haikou 571129, Peoples R China
Reprint Address Zhou, RC (reprint author), Sun Yat Sen Univ, State Key Lab Biocontrol, Guangzhou 510275, Guangdong, Peoples R China.
E-mail Address zhrench@mail.sysu.edu.cn; lssssh@mail.sysu.edu.cn
Funding Agency and Grant Number National Natural Science Foundation of China [91331202, 41130208, 41276107, 31170213, 91231106]; State Key Laboratory of Biocontrol [13A03, 12 K04, 2011 K01]; Scientific Research Foundation for Returned Overseas Chinese Scholars, State Education Ministry; Chang Hungta Science Foundation of Sun Yat-sen University
Funding Text This study was supported by grants from the National Natural Science Foundation of China (Grant Nos. 91331202, 41130208, 41276107, 31170213, and 91231106), the State Key Laboratory of Biocontrol (Grant Nos. 13A03, 12 K04, and 2011 K01), the Scientific Research Foundation for Returned Overseas Chinese Scholars, State Education Ministry, and the Chang Hungta Science Foundation of Sun Yat-sen University.
Cited References Allan WL, 2008, J EXP BOT, V59, P2555, DOI 10.1093/jxb/ern122; Coyne JA, 2004, AM NAT; Ashburner M, 2000, NAT GENET, V25, P25; BALL MC, 1995, FUNCT ECOL, V9, P77, DOI 10.2307/2390093; Bell CD, 2010, AM J BOT, V97, P1296, DOI 10.3732/ajb.0900346; Breitkreuz KE, 2003, J BIOL CHEM, V278, P41552, DOI 10.1074/jbc.M305717200; Bremer K, 2004, SYST BIOL, V53, P496, DOI 10.1080/10635150490445913; Broin M, 2003, PLANT PHYSIOL, V132, P1335, DOI 10.1104/pp.103.021626; Chen SF, 2011, MAR GENOM, V4, P129, DOI 10.1016/j.margen.2011.03.005; Conesa A, 2008, INT J PLANT GENOMICS, V2008, P12, DOI [10.1155/2008/619832, DOI 10.1155/2008/619832]; Cox MP, 2010, BMC BIOINFORMATICS, V11, DOI 10.1186/1471-2105-11-485; Dassanayake M, 2009, NEW PHYTOL, V183, P764, DOI 10.1111/j.1469-8137.2009.02913.x; Datta Paramita Nandy, 2003, Acta Botanica Croatica, V62, P37; DERUITER H, 1983, PLANT PHYSIOL, V73, P525, DOI 10.1104/pp.73.3.525; Dixon DP, 2005, PLANT PHYSIOL, V138, P2233, DOI 10.1104/pp.104.058917; Duke NC, 1998, GLOBAL ECOL BIOGEOGR, V7, P27, DOI 10.2307/2997695; Duke NC, 1992, COASTAL ESTUARINE ST, P63; Duke NC, 2006, AUSTR MANGROVES AUTH; Ezawa S, 2009, PLANT SCI, V176, P272, DOI 10.1016/j.plantsci.2008.11.005; Fischer S, 2011, CURR PROTOC BIOINFOR, V12, P1, DOI DOI 10.1002/0471250953.BI0612S35; Fu LM, 2012, BIOINFORMATICS, V28, P3150, DOI 10.1093/bioinformatics/bts565; Fu XH, 2005, PLANT SCI, V169, P147, DOI 10.1016/j.plantsci.2005.03.009; Fu XinHui, 2004, Plant Molecular Biology Reporter, V22, P197, DOI 10.1007/BF02772728; Grabherr MG, 2011, NAT BIOTECHNOL, V29, P644, DOI 10.1038/nbt.1883; Hsia MM, 2010, J BIOL CHEM, V285, P37070, DOI 10.1074/jbc.M110.168021; Hu J., 2011, FLORA CHINA, V19, P369; Kanehisa M, 2012, NUCLEIC ACIDS RES, V40, P109, DOI DOI 10.1093/NAR/GKR988; KIMURA M, 1980, J MOL EVOL, V16, P111, DOI 10.1007/BF01731581; Kipp E, 2013, RES PLANT SCI, V1, P20; Kleine T, 2012, FRONT PLANT SCI, V3, DOI 10.3389/fpls.2012.00233; Langmead B, 2012, NAT METHODS, V9, P357, DOI [10.1038/nmeth.1923, 10.1038/NMETH.1923]; Larkin MA, 2007, BIOINFORMATICS, V23, P2947, DOI 10.1093/bioinformatics/btm404; Li H, 2009, BIOINFORMATICS, V25, P2078, DOI 10.1093/bioinformatics/btp352; LI WH, 1985, MOL BIOL EVOL, V2, P150; Liang S, 2012, PLOS ONE, V7, DOI 10.1371/journal.pone.0036499; Martinez-Millan M, 2010, BOT REV, V76, P83, DOI 10.1007/s12229-010-9040-1; McCarthy FM, 2006, BMC GENOMICS, V7, DOI 10.1186/1471-2164-7-229; McDade LA, 1999, AM J BOT, V86, P70, DOI 10.2307/2656956; Miller KG, 2005, SCIENCE, V310, P1293, DOI 10.1126/science.1116412; Miyama M, 2008, PLANT MOL BIOL, V68, P119, DOI 10.1007/s11103-008-9356-y; Nguyen PD, 2007, TREES-STRUCT FUNCT, V21, P515, DOI 10.1007/s00468-007-0144-0; Nguyen PD, 2006, TREE GENET GENOMES, V2, P196, DOI 10.1007/s11295-006-0044-2; Ni DA, 2009, NEW PHYTOL, V184, P1469; Ni DA, 2009, NEW PHYTOL, V184, P311, DOI 10.1111/j.1469-8137.2009.02961.x; Parida AK, 2004, Z NATURFORSCH C, V59, P408; Parida AK, 2010, TREES-STRUCT FUNCT, V24, P199, DOI 10.1007/s00468-010-0417-x; Percival M., 1975, FLORISTICS ECOLOGY M; Pertea G, 2003, BIOINFORMATICS, V19, P651, DOI 10.1093/bioinformatics/btg034; Pih KT, 1999, MOL CELLS, V9, P84; Pompella A, 2003, BIOCHEM PHARMACOL, V66, P1499, DOI 10.1016/S0006-2952(03)00504-5; Posada D, 2004, SYST BIOL, V53, P793, DOI 10.1080/10635150490522304; Raffaele S, 2013, FRONT PLANT SCI, V4, DOI 10.3389/fpls.2013.00098; Rey P, 1998, PLANT J, V13, P97, DOI 10.1046/j.1365-313X.1998.00015.x; Rey P, 2005, PLANT J, V41, P31, DOI 10.1111/j.1365-313X.2004.02271.x; Ricklefs RE, 2006, AM NAT, V168, P805, DOI 10.1086/508711; Rieseberg LH, 2007, SCIENCE, V317, P910, DOI 10.1126/science.1137729; Rieseberg LH, 2010, ANN BOT-LONDON, V106, P439, DOI 10.1093/aob/mcq126; Schaferhoff B, 2010, BMC EVOL BIOL, V10, DOI 10.1186/1471-2148-10-352; Shi S, 2005, MOL PHYLOGENET EVOL, V34, P1055; Shi SH, 2005, MOL PHYLOGENET EVOL, V34, P159, DOI 10.1016/j.ympev.2004.09.002; Siol M, 2010, NEW PHYTOL, V188, P313, DOI 10.1111/j.1469-8137.2010.03401.x; Sorrell DA, 2003, PLANTA, V218, P50, DOI 10.1007/s00425-003-1083-7; Stranska Jana, 2008, Plant Signal Behav, V3, P929; Suyama M, 2006, NUCLEIC ACIDS RES, V34, pW609, DOI 10.1093/nar/gkl315; Swofford DL., 2001, PAUP PHYLOGENETIC AN; Taji T, 2004, PLANT PHYSIOL, V135, P1697, DOI 10.1104/pp.104.039909; Tamura K, 2011, MOL BIOL EVOL, V28, P2731, DOI 10.1093/molbev/msr121; Thompson JD, 1997, NUCLEIC ACIDS RES, V25, P4876, DOI 10.1093/nar/25.24.4876; Tomlinson P, 1986, CAMBRIDGE TROPICAL B; Trapnell C, 2012, NAT PROTOC, V7, P562, DOI 10.1038/nprot.2012.016; Trapnell C, 2010, NAT BIOTECHNOL, V28, P511, DOI 10.1038/nbt.1621; Tripp EA, 2014, SYST BIOL, V63, P660, DOI 10.1093/sysbio/syu029; Tzafrir I, 2004, PLANT PHYSIOL, V135, P1206, DOI 10.1104/pp.104.045179; Wu CI, 2001, J EVOLUTION BIOL, V14, P851, DOI 10.1046/j.1420-9101.2001.00335.x; Yang ZH, 2000, MOL BIOL EVOL, V17, P32; Yang ZH, 2002, MOL BIOL EVOL, V19, P908; Yang ZH, 2007, MOL BIOL EVOL, V24, P1586, DOI 10.1093/molbev/msm088; Ye J, 2006, NUCLEIC ACIDS RES, V34, pW293, DOI 10.1093/nar/gkl1031; Zhang J, 2014, BMC GENOMICS, V15, DOI 10.1186/1471-2164-15-337; Zhang JZ, 2005, MOL BIOL EVOL, V22, P2472, DOI 10.1093/molbev/msi237; GUAN W, 2011, CHINESE J ECOL, V10, P009; Zhang Zhang, 2006, Genomics Proteomics & Bioinformatics, V4, P259, DOI 10.1016/S1672-0229(07)60007-2; Zhang Z, 2012, BIOCHEM BIOPH RES CO, V419, P779, DOI 10.1016/j.bbrc.2012.02.101; Zhou HP, 2012, PLANT CELL, V24, P5106, DOI 10.1105/tpc.112.106393; Zhou RC, 2007, MOL BIOL EVOL, V24, P2746, DOI 10.1093/molbev/msm209
Cited Reference Count 85
Times Cited 1
Total Times Cited Count (WoS, BCI, and CSCD) 1
Publisher City LONDON
ISSN 1471-2164
29-Character Source Abbreviation BMC GENOMICS
ISO Source Abbreviation BMC Genomics
Publication Date AUG 14
Year Published 2015
Volume 16
Article Number 605
Digital Object Identifier (DOI) 10.1186/s12864-015-1813-9
Page Count 12
Web of Science Category Biotechnology & Applied Microbiology; Genetics & Heredity
Subject Category Biotechnology & Applied Microbiology; Genetics & Heredity
Document Delivery Number CO9VW
Unique Article Identifier WOS:000359525300001
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