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Transcriptome comparison reveals the patterns of selection in domesticated and wild ramie (Boehmeria nivea L. Gaud)

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Abstract

Ramie is an old fiber crop, cultivated for thousands of years in China. The cultivar ramie evolved from the wild species Qingyezhuma (QYZM, Boehmeria nivea var. tenacissima). However, the mechanism of domestication of this old fiber crop is poorly understood. In order to characterize the selective pattern in ramie domestication, orthologous genes between the transcriptomes of domesticated ramie variety Zhongzhu 1 (ZZ1) and wild QYZM were assessed using bidirectional best-hit method and ratio of non-synonymous (Ka) to synonymous (Ks) nucleotide substitutions was estimated. Sequence comparison of 56,932 and 59,246 unigenes from the wild QYZM and domesticated ZZ1, respectively, helped identify 10,745 orthologous unigene pairs with a total orthologous length of 10.18 Mb. Among these unigenes, 85 and 13 genes were found to undergo significant purifying and positive selection, respectively. Most of the selected genes were homologs of those involved in abiotic stress tolerance or disease resistance in other plants, suggesting that abiotic and biotic stresses were important selective pressures in ramie domestication. Two genes probably related to the fiber yield of ramie were subjected to positive selection, which may be caused by human manipulation. Thus, our results show the pervasive effects of artificial and natural selections on the accelerated domestication of ramie from its wild relative.

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References

  • Ahuja SL (1988) Association and path-coefficient studies on vegetatively propagating and sexually reproducing parts in ramie (Boehmeria nivea L. Gaud.). Sex Plant Reprod 1:63–64

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Berkey R, Bendigeri D, Xiao S (2012) Sphingolipids and plant defense/disease: the “death” connection and beyond. Front Plant Sci 3:68

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boudsocq M, Lauriere C (2005) Osmotic signaling in plants: multiple pathways mediated by emerging kinase families. Plant Physiol 138:1185–1194

    CAS  PubMed Central  PubMed  Google Scholar 

  • Denancé N, Ranocha P, Oria N, Barlet X, Riviere M, Yadeta K, Hoffmann L, Perreau F, Clement G, Maia-Grondard A et al (2013) Arabidopsis wat1 (walls are thin1)-mediated resistance to the bacterial vascular pathogen, Ralstonia solanacearum, is accompanied by cross-regulation of salicylic acid and tryptophan metabolism. Plant J 73:225–239

    Google Scholar 

  • Deng G, Liu L, Zhong X, Lao C, Wang H, Wang B, Zhu C, Shah F, Peng D (2014) Comparative proteome analysis of the response of ramie under N, P and K deficiency. Planta 239:1175–1186

    CAS  PubMed  Google Scholar 

  • Doebley J, Gaut B, Smith B (2006) The molecular genetics of crop domestication. Cell 127:1309–1321

    CAS  PubMed  Google Scholar 

  • Doron-Faigenboim A, Stern A, Mayrose I, Bacharach E, Pupko T (2005) Selecton: a server for detecting evolutionary forces at a single amino-acid site. Bioinformatics 21:2101–2103

    CAS  PubMed  Google Scholar 

  • Fan C, Xing Y, Mao H, Lu T, Han B, Xu C, Li X, Zhang Q (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112:1164–1171

    CAS  PubMed  Google Scholar 

  • Frary A, Nesbitt T, Frary A, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert K et al (2000) fw2.2: A quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88

    CAS  PubMed  Google Scholar 

  • Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525

    CAS  PubMed  Google Scholar 

  • Gegas V, Nazari A, Griffiths S, Simmonds J, Fish L, Orford S, Sayers L, Doonan J, Snapea J (2010) A genetic framework for grain size and shape variation in wheat. Plant Cell 22:1046–1056

    CAS  PubMed Central  PubMed  Google Scholar 

  • Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gross BL, Olsen KM (2010) Genetic perspectives on crop domestication. Trends Plant Sci 15:529–537

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guo B, Chen X, Dang P, Scully B, Liang X, Holbrook CC, Yu J, Culbreath A (2008) Peanut gene expression profiling in developing seeds at different reproduction stages during Aspergillus parasiticus infection. BMC Dev Biol 8:12

    PubMed Central  PubMed  Google Scholar 

  • Guo B, Fedorova ND, Chen X, Wan CH, Wang W, Nierman WC, Bhatnagar D, Yu J (2011) Gene expression profiling and identification of resistance genes to Aspergillus flavus infection in peanut through EST and microarray strategies. Toxins 3:737–753

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hooley R (1994) Gibberellins: perception, transduction and responses. Plant Mol Biol 26:1529–1555

    CAS  PubMed  Google Scholar 

  • Huang X, Kurata N, Wei X, Wang Z, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W et al (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501

    CAS  PubMed  Google Scholar 

  • Hufford M, Xu X, Heerwaarden J, Pyhäjärvi T, Chia J, Cartwright R, Elshire R, Glaubitz J, Guill K, Kaeppler S et al (2012) Comparative population genomics of maize domestication and improvement. Nat Genet 44:808–811

    CAS  PubMed  Google Scholar 

  • Jia G, Huang X, Zhi H, Zhao Y, Zhao Q, Li W, Chai Y, Yang L, Liu K, Lu H et al (2013) A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nat Genet 45:957–961

    CAS  PubMed  Google Scholar 

  • Jiang YB, Jie YC (2005) Advances in research on the genetic relationships of Boehmeria in China. J Plant Genet Res 6:114–118

    Google Scholar 

  • Jonak C, Kiegerl S, Ligterink W, Barker P, Huskisson N, Hirt H (1996) Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci USA 93:11274–11279

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koenig D, Jiménez-Gómez J, Kimura S, Fulopa D, Chitwooda D, Headlanda L, Kumara R, Covingtona M, Devisettya U, Tata A et al (2013) Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proc Natl Acad Sci USA 110:E2655–E2662

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li HL (1970) The origin of cultivated plants in Southeast Asia. Econ Bot 24:3–19

    Google Scholar 

  • Li C, Zhou A, Sang T (2006) Rice domestication by reducing shattering. Science 311:1936–1939

    CAS  PubMed  Google Scholar 

  • Li D, Wang F, Liu B, Zhang Y, Huang L, Zhang H, Song F (2013) Ectopic expression of rice OsBIANK1, encoding an ankyrin repeat-containing protein, in Arabidopsis confers enhanced disease resistance to Botrytis cinerea and Pseudomonas syringae. J Phytopathol 161:27–34

    CAS  Google Scholar 

  • Liao L, Li T, Zhang J, Xu L, Deng H, Ha X (2014) The domestication and dispersal of the cultivated ramie (Boehmeria nivea (L.) Gaud. in Freyc.) determined by nuclear SSR marker analysis. Genet Resour Crop Evol 61:55–67

    Google Scholar 

  • Liu T, Zhu S, Tang Q, Chen P, Yu Y, Tang S (2013a) De novo assembly and characterization of transcriptome using Illumina paired-end sequencing and identification of CesA gene in ramie (Boehmeria nivea L. Gaud). BMC Genom 14:125

    CAS  Google Scholar 

  • Liu T, Zhu S, Tang Q, Yu Y, Tang S (2013b) Identification of drought stress-responsive transcription factors in ramie (Boehmeria nivea L. Gaud). BMC Plant Biol 13:130

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu T, Zhu S, Fu L, Yu Y, Tang Q, Tang S (2013c) Morphological and physiological changes of ramie (Boehmeria nivea L. Gaud) in response to drought stress and GA3 treatment. Rus J Plant Physiol 60:749–755

    CAS  Google Scholar 

  • Liu T, Tang S, Zhu S, Tang Q (2014) QTL mapping for fiber yield-related traits by constructing the first genetic linkage map in ramie (Boehmeria nivea L. Gaud). Mol Breed. doi:10.1007/s11032-014-0082-7

  • Lu L, Shao D, Qiu X, Sun L, Yan W, Zhou X, Yang L, He Y, Yu S, Xing Y (2013) Natural variation and artificial selection in four genes determine grain shape in rice. New Phytol 200:1269–1280

    CAS  PubMed  Google Scholar 

  • Mou S, Liu Z, Guan D, Qiu A, Lai Y, He S (2013) Functional analysis and expressional characterization of rice ankyrin repeat-containing protein, OsPIANK1, in basal defense against Magnaporthe oryzae attack. PLoS One 8:e59699

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nakayama H, Ogawa H, Takamori K, Iwabuchi K (2013) GSL-enriched membrane microdomains in innate immune responses. Arch Immunol Ther Exp 61:217–228

    CAS  Google Scholar 

  • Qi J, Liu X, Shen D, Miao H, Xie B, Li X, Zeng P, Wang S, Shang Y, Gu X et al (2013) A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat Genet 45:1510–1518

    CAS  PubMed  Google Scholar 

  • Ranocha P, Denancé N, Vanholme R, Freydier A, Martinez Y, Hoffmann L, Kohler L, Pouzet C, Renou J, Sundberg B et al (2010) Walls are thin 1 (WAT1), an Arabidopsis homolog of Medicago truncatula NODULIN21, is a tonoplast-localized protein required for secondary wall formation in fibers. Plant J 63:469–483

    CAS  PubMed  Google Scholar 

  • Sen T, Reddy HN (2011) Various industrial applications of hemp, kinaf, flax and ramie natural fibres. IJIMT 2:192–198

    Google Scholar 

  • Shou H, Bordallo P, Wang K (2004) Expression of the Nicotiana protein kinase (NPK1) enhanced drought tolerance in transgenic maize. J Exp Bot 55:1013–1019

    CAS  PubMed  Google Scholar 

  • Sun C, Li Y, Wu Q, Luo H, Sun Y, Song J, Lui EM, Chen S (2010) De novo sequencing and analysis of the American ginseng root transcriptome using a GS FLX Titanium platform to discover putative genes involved in ginsenoside biosynthesis. BMC Genom 11:262

    Google Scholar 

  • Tan L, Li X, Liu F, Sun X, Li C, Zhu Z, Fu Y, Cai H, Wang X, Xie D et al (2008) Control of a key transition from prostrate to erect growth in rice domestication. Nat Genet 40:1360–1364

    CAS  PubMed  Google Scholar 

  • Thomas SG, Phillips AL, Hedden P (1999) Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc Natl Acad Sci USA 96:4698–4703

    CAS  PubMed Central  PubMed  Google Scholar 

  • Umezawa T, Yoshida R, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:17306–17311

    CAS  PubMed Central  PubMed  Google Scholar 

  • Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotech 17:113–122

    CAS  PubMed  Google Scholar 

  • Vavilov NI (1992) Origin and geography of cultivated plants. Cambridge University Press, Cambridge

    Google Scholar 

  • Wang WT (1981a) Revisio Boehmeriae sinicae. Acta Botanica Yunnanica 3:307–328

    Google Scholar 

  • Wang WT (1981b) Revisio Boehmeriae sinicae (cont.). Acta Bot Yunnanica 3:401–416

    Google Scholar 

  • Wang Z, Fang B, Chen J, Zhang X, Luo Z, Huang L, Chen X, Li Y (2010) De novo assembly and characterization of root transcriptome using Illumina paired-end sequencing and development of cSSR markers in sweetpotato (Ipomoea batatas). BMC Genom 11:726

    CAS  Google Scholar 

  • Wu ZY, Raven PH, Hong DY (2003) Flora of China, volume 5: Ulmaceae through Basellaceae. Science Press, Beijing

    Google Scholar 

  • Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X et al (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767

    CAS  PubMed  Google Scholar 

  • Yan W, Liu H, Zhou X, Li Q, Zhang J, Lu L, Liu T, Liu H, Zhang C, Zhang Z et al (2013) Natural variation in Ghd7.1 plays an important role in grain yield and adaptation in rice. Cell Res 23:969–971

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang M, Leong H (2010) Bidirectional best hit r-window gene clusters. BMC Bioinform 11(Suppl 1):S63

    Google Scholar 

  • Zhu S, Tang S, Tang Q, Liu T (2014) Genome-wide transcriptional changes of ramie (Boehmeria nivea L.Gaud) in response to the infection of root-lesion nematode. PLoS One (in press)

  • Zuo K, Wang J, Wu W, Chai Y, Sun X, Tang K (2005) Identification and characterization of differentially expressed ESTs of Gossypium barbadense infected by Verticillium dahliae with suppression subtractive hybridization. Mol Biol 39:191–199

    CAS  Google Scholar 

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Acknowledgments

We acknowledge the Novogene Bioinformatics Institute for its assistance in original data processing and related bioinformatics analysis. This work was supported by grants from the National Natural Science Foundation of China (31101189) and National Modern Agro-industry Technology Research System (nycytx-19-E16).

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Correspondence to Touming Liu.

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Liu, T., Tang, S., Zhu, S. et al. Transcriptome comparison reveals the patterns of selection in domesticated and wild ramie (Boehmeria nivea L. Gaud). Plant Mol Biol 86, 85–92 (2014). https://doi.org/10.1007/s11103-014-0214-9

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