Skip to main content

Advertisement

Log in

Comparative transcriptome analysis and identification of candidate adaptive evolution genes of Miscanthus lutarioriparius and Miscanthus sacchariflorus

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

Miscanthus species are perennial C4 grasses that are considered promising energy crops because of their high biomass yields, excellent adaptability and low management costs. Miscanthus lutarioriparius and Miscanthus sacchariflorus are closely related subspecies that are distributed in different habitats. However, there are only a few reports on the mechanisms by which Miscanthus adapts to different environments. Here, comparative transcriptomic and morphological analyses were used to study the evolutionary adaptation of M. lutarioriparius and M. sacchariflorus to different habitats. In total, among 7586 identified orthologs, 2060 orthologs involved in phenylpropanoid biosynthesis and plant hormones were differentially expressed between the two species. Through an analysis of the Ka/Ks ratios of the orthologs, we estimated that the divergence time between the two species was approximately 4.37 Mya. In addition, 37 candidate positively selected orthologs (PSGs) that played important roles in the adaptation of these species to different habitats were identified. Then, the expression levels of 20 PSGs in response to flooding and drought stress were analyzed, and the analysis revealed significant changes in their expression levels. These results facilitate our understanding of the evolutionary adaptation to habitats and the speciation of M. lutarioriparius and M. sacchariflorus. We hypothesise that lignin synthesis genes are the main cause of the morphological differences between the two species. In summary, the plant nonspecific phospholipase C gene family and the receptor-like protein kinase gene family played important roles in the evolution of these two species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Availability of data and material

The sequencing raw data from 6 RNA-Seq libraries were deposited on the Sequence Read Archive from NCBI under SRA accession: SRP158951 and SRP190160. Data are available here:

References

  • Altenhoff AM, Dessimoz C (2009) Phylogenetic and functional assessment of orthologs inference projects and methods. PLoS Comput Biol 5:e1000262

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ayadi M, Hanana M, Kharrat N, Merchaoui H, Marzoug RB, Lauvergeat V, Rebai A, Mzid R (2016) The wrky transcription factor family in citrus: Valuable and useful candidate genes for citrus breeding. Appl Biochem Biotechnol 180:516–543

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Yin Y (2017) Wrky transcription factors are involved in brassinosteroid signaling and mediate the crosstalk between plant growth and drought tolerance. Plant Signal Behav 12:e1365212

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen X, Li C, Wang H, Guo Z (2019) Wrky transcription factors: evolution, binding, and action. Phytopathol Res 1:1–5

    Article  CAS  Google Scholar 

  • Cheng J, Fan H, Li L, Hu B, Liu H, Liu Z (2018) Genome-wide identification and expression analyses of rpp13-like genes in barley. BioChip J 12:102–113

    Article  CAS  Google Scholar 

  • Clifton-Brown J, Hastings A, Mos M, McCalmont JP et al (2017) Progress in upscalingmiscanthusbiomass production for the european bio-economy with seed-based hybrids. GCB Bioenergy 9:6–17

    Article  CAS  Google Scholar 

  • Dohleman FG, Heaton EA, Leakey AD, Long SP (2009) Doe’s greater leaf-level photosynthesis explain the larger solar energy conversion efficiency of miscanthus relative to switchgrass? Plant Cell Environ 32:1525–1537

    Article  CAS  PubMed  Google Scholar 

  • El-Esawi MA, Al-Ghamdi AA, Ali HM, Ahmad M (2019) Overexpression of atwrky30 transcription factor enhances heat and drought stress tolerance in wheat (triticum aestivum l.). Genes 10:163

    Article  CAS  PubMed Central  Google Scholar 

  • Elmer KR, Fan S, Gunter HM et al (2010) Rapid evolution and selection inferred from the transcriptomes of sympatric crater lake cichlid fishes. Mol Ecol 19:197–211

    Article  CAS  PubMed  Google Scholar 

  • Gao F, Yang F, Zhou H, Sun Q, Zhang Y, Brown MA (2014) Evaluation of processing technology for triarrhena sacchariflora (maxim.) nakai for ethanol production. PloS one 9:e114399

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gao F, Wang N, Li H et al (2016) Identification of drought-responsive microRNAs and their targets in Ammopiptanthus mongolicus by using high-throughput sequencing. Sci Rep 6:34601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao F, Li H, Xiao Z, Wei C, Feng J, Zhou Y (2017) De novo transcriptome analysis of ammopiptanthus nanus and its comparative analysis with a. Mongolicus Trees 32:287–300

    Article  CAS  Google Scholar 

  • Grabherr MG, Haas BJ et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta P, Nutan KK, Singla-Pareek SL, Pareek A (2017) Abiotic stresses cause differential regulation of alternative splice forms of gata transcription factor in rice. Front Plant Sci 8:1944

    Article  PubMed  PubMed Central  Google Scholar 

  • He GH, Xu JY, Wang YX, Liu JM, Li PS, Chen M, Ma YZ, Xu ZS (2016) Drought-responsive wrky transcription factor genes tawrky1 and tawrky33 from wheat confer drought and/or heat resistance in arabidopsis. BMC Plant Biol 16:116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heaton EA, Dohleman FG, Long SP (2008) Meeting us biofuel goals with less land: the potential of miscanthus. Glob Change Biol 14:2000–2014

    Article  Google Scholar 

  • Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. ISMB 99:138–148

    Google Scholar 

  • Jia Y, Liu ML, Yue M, Zhao Z, Zhao GF, Li ZH (2017) Comparative transcriptome analysis reveals adaptive evolution of notopterygium incisum and notopterygium franchetii, two high-alpine herbal species endemic to china. Molecules 22:1158

    Article  PubMed Central  CAS  Google Scholar 

  • Krckova Z, Brouzdova J, Danek M, Kocourkova D, Rainteau D, Ruelland E, Valentova O, Pejchar P, Martinec J (2015) Arabidopsis non-specific phospholipase c1: characterization and its involvement in response to heat stress. Front Plant Sci 6:928

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee WC, Kuan WC (2015) Miscanthus as cellulosic biomass for bioethanol production. Biotechnol J 10:840–854

    Article  CAS  PubMed  Google Scholar 

  • Lehti-Shiu MD, Shiu SH (2012) Diversity, classification and function of the plant protein kinase superfamily. Philos Trans R Soc Lond B Biol Sci 367:2619–2639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levy ED, Michnick SW, Landry CR (2012) Protein abundance is key to distinguish promiscuous from functional phosphorylation based on evolutionary information. Philos Trans R Soc Lond B Biol Sci 367:2594–2606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323

    Article  CAS  Google Scholar 

  • Li L, Stoeckert CJ, Roos DS (2003) OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genom Res 13:2178–2189

    Article  CAS  Google Scholar 

  • Li X, Liao H, Fan C, Hu H, Li Y, Li J, Yi Z, Cai X, Peng L, Tu Y (2016) Distinct geographical distribution of the miscanthus accessions with varied biomass enzymatic saccharification. PloS one 11:e0160026

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li X, Salman A, Guo C, Yu J, Cao S, Gao X, Li W, Li H, Guo Y (2018) Identification and characterization of lrr-rlk family genes in potato reveal their involvement in peptide signaling of cell fate decisions and biotic/abiotic stress responses. Cells 7:120

    Article  CAS  PubMed Central  Google Scholar 

  • Li SS, Zhou HF, Chen WL, Yan J, Cai Z, Wei RX, Chen CH, Han B, Li JQ, Sang T, Ge S (2019) Population genetics and evolutionary history of miscanthus species in china. J Syst Evol 57:530–542

    Article  Google Scholar 

  • Liu X, Song Y, Xing F, Wang N, Wen F, Zhu C (2016) Ghwrky25, a group i wrky gene from cotton, confers differential tolerance to abiotic and biotic stresses in transgenic nicotiana benthamiana. Protoplasma 253:1265–1281

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Peatman E, Tang H, Lewis J, Liu Z (2012) Profiling of gene duplication patterns of sequenced teleost genomes evidence for rapid lineage-specific genome expansion mediated by recent tandem duplications. BMC Genomics 13:1–10

    Article  CAS  Google Scholar 

  • Nabholz B, Sarah G, Sabot F, Ruiz M, Adam H, Nidelet S, Ghesquiere A, Santoni S, David J, Glemin S (2014) Transcriptome population genomics reveals severe bottleneck and domestication cost in the african rice (oryza glaberrima). Mol Ecol 23:2210–2227

    Article  CAS  PubMed  Google Scholar 

  • Niu CF, Wei W, Zhou QY, Tian AG, Hao YJ, Zhang WK, Ma B, Lin Q, Zhang ZB, Zhang JS, Chen SY (2012) Wheat wrky genes tawrky2 and tawrky19 regulate abiotic stress tolerance in transgenic arabidopsis plants. Plant Cell Environ 35:1156–1170

    Article  CAS  PubMed  Google Scholar 

  • Peret B, Middleton AM, French AP, Larrieu A, Bishopp A, Njo M, Wells DM, Porco S, Mellor N, Band LR, Casimiro I, Kleine-Vehn J, Vanneste S, Sairanen I, Mallet R, Sandberg G, Ljung K, Beeckman T, Benkova E, Friml J, Kramer E, King JR, De Smet I, Pridmore T, Owen M, Bennett MJ (2013) Sequential induction of auxin efflux and influx carriers regulates lateral root emergence. Mol Syst Biol 9:699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters C, Kim SC, Devaiah S, Li M, Wang X (2014) Non-specific phospholipase c5 and diacylglycerol promote lateral root development under mild salt stress in Arabidopsis. Plant Cell Environ 37:2002–2013

    Article  CAS  PubMed  Google Scholar 

  • Pokotylo I, Pejchar P, Potocky M, Kocourkova D, Krckova Z, Ruelland E, Kravets V, Martinec J (2013) The plant non-specific phospholipase c gene family. Novel competitors in lipid signalling. Prog Lipid Res 52:62–79

    Article  CAS  PubMed  Google Scholar 

  • Rahi ML, Mather PB, Ezaz T, Hurwood DA (2019) The molecular basis of freshwater adaptation in prawns: Insights from comparative transcriptomics of three macrobrachium species. Genome Biol Evol 11:1002–1018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson MD et al (2010) edgeR: a Bioconductorpackage for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–14

    Article  CAS  PubMed  Google Scholar 

  • Schuler MA, Duan H, Bilgin M, Ali S (2006) Arabidopsis cytochrome p450s through the looking glass: a window on plant biochemistry. Phytochem Rev 5:205–237

    Article  CAS  Google Scholar 

  • Sharma R, Singh G, Bhattacharya S, Singh A (2018) Comparative transcriptome meta-analysis of arabidopsis thaliana under drought and cold stress. PloS one 13:e0203266

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shen X, Wan S, Colin C, Tada R, Shi X, Pei W, Li A (2018) Increased seasonality and aridity drove the C4 plant expansion in Central Asia since the Miocene-Pliocene boundary. Earth Planet Sci Lett 502:74–83

    Article  CAS  Google Scholar 

  • Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6:196–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song Z, Xu Q, Lin C, Tao C, Zhu C, Xing S, Fan Y, Liu W, Yan J, Li J, Sang T (2017) Transcriptomic characterization of candidate genes responsive to salt tolerance of Miscanthus energy crops. GCB Bioenergy 9:1222–1237

    Article  CAS  Google Scholar 

  • Song H, Sun W, Yang G, Sun J (2018) Wrky transcription factors in legumes. BMC Plant Biol 18:243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sorensen I, Domozych D, Willats WG (2010) How have plant cell walls evolved? Plant Physiol 153:366–372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stroud JT, Losos JB (2016) Ecological opportunity and adaptive radiation. Annu Rev Ecol Evol Syst 47:507–532

    Article  Google Scholar 

  • Sun Q, Lin Q, Yi Z-L, Yang Z-R, Zhou F-S (2010) A taxonomic revision of miscanthussl (poaceae) from china. Bot J Linn Soc 164:178–220

    Article  Google Scholar 

  • Tao SQ, Cao B, Tian CM, Liang YM (2017) Comparative transcriptome analysis and identification of candidate effectors in two related rust species (gymnosporangium yamadae and gymnosporangium asiaticum). BMC Genomics 18:651

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Timotijevic GS, Milisavljevic M, Radovic SR, Konstantinovic MM, Maksimovic VR (2010) Ubiquitous aspartic proteinase as an actor in the stress response in buckwheat. J Plant Physiol 167:61–68

    Article  CAS  PubMed  Google Scholar 

  • Turupcu A, Almohamed W, Oostenbrink C, Seifert GJ (2018) A speculation on the tandem fasciclin 1 repeat of fla4 proteins in angiosperms. Plant Signal Behav 13:e1507403

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang J, Li C, Yao X, Liu S, Zhang P, Chen K (2017a) The antarctic moss leucine-rich repeat receptor-like kinase (pnlrr-rlk2) functions in salinity and drought stress adaptation. Polar Biol 41:353–364

    Article  Google Scholar 

  • Wang J, Chen Z, Jin S, Hu Z, Huang Y, Diao Y (2017b) Development and characterization of simple sequence repeat (SSR) markers based on a full-length cDNA library of Napier Grass (Pennisetum purpureum Schum). Genes Genomics 39(12):1297–1305

    Article  CAS  Google Scholar 

  • Wang Z, Hong X, Hu K, Wang Y, Wang X, Du S, Li Y, Hu D, Cheng K, An B, Li Y (2017c) Impaired magnesium protoporphyrin ix methyltransferase (chlm) impedes chlorophyll synthesis and plant growth in rice. Front Plant Sci 8:1694

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang L, Yao L, Hao X, Li N, Qian W, Yue C, Ding C, Zeng J, Yang Y, Wang X (2018) Tea plant sweet transporters: Expression profiling, sugar transport, and the involvement of cssweet16 in modifying cold tolerance in Arabidopsis. Plant Mol Biol 96:577–592

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Sun H, Sheng J, Jin S, Zhou F, Hu Z, Diao Y (2019) Transcriptome, physiological and biochemical analysis of Triarrhena sacchariflora in response to flooding stress. BMC Genet 20(1):88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weng JK, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187:273–285

    Article  CAS  PubMed  Google Scholar 

  • Xiao YG, Sun QB, Kang XJ, Chen CB, Ni M (2016) Short hypocotyl under blue1 or haiku2 mixepression alters canola and Arabidopsis seed development. New Phytol 209:636–649

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Xing S, Zhu C, Liu W, Fan Y, Wang Q, Song Z, Yang W, Luo F, Shang F, Kang L, Chen W, Yan J, Li J, Sang T (2015) Population transcriptomics reveals a potentially positive role of expression diversity in adaptation. J Integr Plant Biol 57:284–299

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Zhu C, Fan Y, Song Z, Xing S, Liu W, Yan J, Sang T (2016) Population transcriptomics uncovers the regulation of gene expression variation in adaptation to changing environment. Sci Rep 6:25536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu G, Li M, Zhang H, Chen Q, Jin L, Zheng Q, Liu P, Cao P, Chen X, Zhai N, Zhou H (2018) Ntrlk5, a novel rlk-like protein kinase from nitotiana tobacum, positively regulates drought tolerance in transgenic Arabidopsis. Biochem Biophys Res Commun 503:1235–1240

    Article  CAS  PubMed  Google Scholar 

  • Xue H, Seifert GJ (2015) Fasciclin like arabinogalactan protein 4 and respiratory burst oxidase homolog d and f independently modulate abscisic acid signaling. Plant Signal Behav 10:e989064

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yao K, Wu Y (2016) Phosphofructokinase and glucose-6-phosphate dehydrogenase in response to drought and bicarbonate stress at transcriptional and functional levels in mulberry. Russ J Plant Physiol 63:235–242

    Article  CAS  Google Scholar 

  • Yi L, Chen C, Yin S, Li H, Li Z, Wang B, King GJ, Wang J, Liu K (2018) Sequence variation and functional analysis of a frigida orthologue (bnaa3.Fri) in brassica napus. BMC plant biology 18:32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J (2006) KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genom Proteom Bioinform 4:259–263

    Article  CAS  Google Scholar 

  • Zhao YJ, Liu XY, Guo R, Hu KR, Cao Y, Dai F (2019) Comparative genomics and transcriptomics analysis reveals evolution patterns of selection in the salix phylogeny. BMC Genomics 20:253

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (No. 31571740), Anhui University of Science and Technology launched a research fund to attract talents (No:13200389).

Funding

This work was financially supported by the National Natural Science Foundation of China (No. 31571740), and the Anhui University of Science and Technology launched a research fund to attract talents (13200389).

Author information

Authors and Affiliations

Authors

Contributions

Jia Wang performed and analyzed the experiments, and wrote the manuscript; Jianyong Zhu and Jiajing Sheng contributed experiments materials and provided assistance to the experiments. Ying Diao and Zhongli Hu offered scientific advice, guided the experiments and revised the manuscript. All authors read and approved the final manuscript revision.

Corresponding author

Correspondence to Ying Diao.

Ethics declarations

Conflict of interest

The authors declare that the submitted work was not performed in the presence of any personal, professional or financial relationships that could be constructed as a conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, J., Sheng, J., Zhu, J. et al. Comparative transcriptome analysis and identification of candidate adaptive evolution genes of Miscanthus lutarioriparius and Miscanthus sacchariflorus. Physiol Mol Biol Plants 27, 1499–1512 (2021). https://doi.org/10.1007/s12298-021-01030-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-021-01030-1

Keywords

Navigation