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Transcriptome analysis reveals diversified adaptation of Stipa purpurea along a drought gradient on the Tibetan Plateau

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Abstract

Natural selection drives species adaptations to biotic and abiotic stresses. Species distributed along a moisture gradient, such as Stipa purpurea, a dominant grass in alpine arid and semi-arid meadows on the Tibetan Plateau, provide an opportunity to evaluate the effects of long-term adaptation to differing degrees of drought stress on gene expression. However, the genetic basis of this divergence remains largely unknown. Next-generation sequencing technologies have provided important genome-wide insights on the evolution of organisms for which genomic information is lacking. To understand how S. purpurea responds to drought stress, we selected five populations distributed along the degressive rainfall line on the northwestern Tibetan Plateau that currently present evolutionary acclimation to localized drought pressure at the physiological and biochemical levels and compared their transcriptome responses. In addition, we performed de novo assembly of the S. purpurea transcriptome using short read sequencing technology and successfully assembled 84,298 unigenes from approximately 51 million sequencing reads. We quantified gene expression level to compare their transcriptome responses using mRNA-Seq and identified differentially expressed transcripts that are involved in primary and secondary plant metabolism, plant hormone synthesis, defense responses, and cell wall synthesis. Furthermore, physiological and biochemical evidence supports that abscisic acid (ABA) accumulation and cell wall strengthening derived from the differential transcripts contribute to the tolerance of S. purpurea to drought stress. The mechanisms by which S. purpurea adapts to drought stress provide new insight into how plants ecologically adapt and evolve.

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References

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995

    CAS  PubMed  Google Scholar 

  • Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681

    Article  CAS  PubMed  Google Scholar 

  • Bai XG, Todd CD, Desikan R, Yang Y, Hu X (2012) N-3-Oxo-decanoyl-l-homoserine-lactone activates auxin-induced adventitious root formation via hydrogen peroxide- and nitric oxide-dependent cyclic GMP signaling in mung bean. Plant Physiol 158:725–736

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  PubMed Central  PubMed  Google Scholar 

  • Borghi L, Gutzat R, Fütterer J, Laizet YH, Hennig L et al (2010) Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22:1792–1811

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    Article  CAS  PubMed  Google Scholar 

  • Chang DHS, Gauch HG (1986) Multivariate analysis of plant communities and environmental factors in Ngari, Tibet. Ecol 67:1568–1575

    Article  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • Chelaifa H, Mahé F, Ainouche M (2010) Transcriptome divergence between the hexaploid salt-marsh sister species Spartina maritima and Spartina alterniflora (Poaceae). Mol Ecol 19:2050–2063

    Article  CAS  PubMed  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinforma 21:3674–3676

    Article  CAS  Google Scholar 

  • Costa P, Bahrman N, Frigerio JM et al (1998) Water-deficit-responsive proteins in maritime pine. Plant Mol Biol 38:587–596

    Article  CAS  PubMed  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ekblom R, Galindo J (2011) Applications of next generation sequencing in molecular ecology of non-model organisms. Hered 107:1–15

    Article  CAS  Google Scholar 

  • Fordyce JA (2006) The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. J Exp Biol 209:2377–2383

    Article  PubMed  Google Scholar 

  • Gong ZJ, Wu YQ, Miao J, Duan Y, Jiang YL et al (2013) Global transcriptome analysis of orange wheat blossom midge, Sitodiplosis mosellana (Gehin) (Diptera: Cecidomyiidae) to identify candidate transcripts regulating diapause. PLoS One 8:e71564

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gou XH, Chen FH, Yang MX, Jacoby G, Peng J et al (2006) A comparison of tree-ring records and glacier variations over the past 700 years, northeastern Tibetan Plateau. Ann Glaciol 43:86–90

    Article  Google Scholar 

  • Gou XH, Chen FH, Jacoby G, Cook E, Yang M et al (2007) Rapid tree growth with respect to the last 400 years in response to climate warming, northeastern Tibetan Plateau. Int J Climatol 27:1497–1503

    Article  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA et al (2011) Full-length transcriptome assembly from mRNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Greive CM, Grattan SR (1983) Rapid assay for determination of water-soluble quaternary amino compounds. Plant Soil 70:303–307

    Article  Google Scholar 

  • Gulati J, Baldwin IT, Gaquerel E (2014) The roots of plant defenses: integrative multivariate analyses uncover dynamic behaviors of gene and metabolic networks of roots elicited by leaf herbivory. Plant J 77:880–892

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Jiang S, Kumar S, Eu YJ, Jami SK, Stasolla C et al (2012) The Arabidopsis mutant, fy-1, has an ABA-insensitive germination phenotype. J Exp Bot 63:2693–2703

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jones MM, Turner NC (1978) Osmotic adjustment in leaves of sorghum in response to water deficits. Plant Physiol 61:122–126

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Klein JA, Harte J, Zhao XQ (2004) Experimental warming causes large and rapid species loss, dampened by simulated grazing, on the Tibetan Plateau. Ecol Lett 7:1170–1179

    Article  Google Scholar 

  • Li WH, Zhou XM (1998) Ecosystems of Qinghai-Xizang (Tibetan) Plateau and approach for their sustainable management. Guangdong Science and Technology Press, Guangzhou, pp 56–101

    Google Scholar 

  • Li R, Yu C, Li Y, Lam TW, Yiu SM et al (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinforma 25:1966–1967

    Article  CAS  Google Scholar 

  • Li R, Zhu H, Ruan J, Fang X, Shi Z et al (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu WS, Dong M, Song ZP, Wei W (2009) Genetic diversity pattern of Stipa purpurea populations in the hinterland of Qinghai-Tibet Plateau. Ann Appl Biol 154:57–65

    Article  CAS  Google Scholar 

  • Luo T, Li W, Zhu H (2002) Estimated biomass and productivity of natural vegetation on the Tibetan Plateau. Ecol Appl 12:980–997

    Article  Google Scholar 

  • Malenke JR, Milash B, Miller AW, Dearing MD (2013) Transcriptome sequencing and microarray development for the woodrat (Neotoma spp.): custom genetic tools for exploring herbivore ecology. Mol Ecol Resour 13:674–687

    Article  CAS  PubMed  Google Scholar 

  • Mann IK, Wegrzyn JL, Rajora OP (2013) Generation, functional annotation and comparative analysis of black spruce ESTs: an important conifer genomic resource. BMC Genom 14:702

    Article  CAS  Google Scholar 

  • Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18:1509–1517

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Miura K, Okamoto H, Okuma E, Shiba H, Kamada H et al (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J 73:91–104

    Article  CAS  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Ness RW, Siol M, Barrett SC (2011) De novo sequence assembly and characterization of the floral transcriptome in cross- and self-fertilizing plants. BMC Genom 12:298

    Article  CAS  Google Scholar 

  • Nicotra AB, Davidson A (2010) Adaptive phenotypic plasticity and plant water use. Funct Plant Biol 37:117–127

    Article  Google Scholar 

  • Ozsolak F, Milos PM (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12:87–98

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pertea G, Huang X, Liang F, Antonescu V, Sultana R et al (2003) TIGR Gene Indices Clustering Tools (TGICL): a software system for fast clustering of large EST datasets. Bioinforma 19:651–652

    Article  CAS  Google Scholar 

  • Ranocha P, Chabannes M, Chamayou S et al (2002) Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiol 129:145–155

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saldanha AJ (2004) Java treeview-extensible visualization of microarray data. Bioinforma 20:3246–3248

    Article  CAS  Google Scholar 

  • Sánchez FJ, Manzanares M, de Andres EF, Tenorio JL, Ayerbe L (1998) Turgor maintenance, osmotic adjustment and soluble sugar and proline accumulation in 49 pea cultivars in response to water stress. Field Crop Res 59:225–235

    Article  Google Scholar 

  • Senthil-Kumar M, Hema R, Suryachandra TR, Ramegowda HV, Gopalakrishna R et al (2010) Functional characterization of three water deficit stress-induced genes in tobacco and Arabidopsis: an approach based on gene down regulation. Plant Physiol Biochem 48:35–44

    Article  CAS  PubMed  Google Scholar 

  • Sheidai M, Attaei S (2005) Meiotic studies of some Stipa (Poaceae) species and populations in Iran. Cytologia 70:23–31

    Article  Google Scholar 

  • Shen CM, Liu KB, Morrill C, Overpeck JT, Peng J et al (2008) Ecotone shift and major droughts during the mid-late Holocene in the central Tibetan Plateau. Ecol 89:1079–1088

    Article  Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tang F, Barbacioru C, Wang Y, Nordman E, Lee C et al (2009) mRNA-Seq whole transcriptome analysis of a single cell. Nat Methods 6:377–382

    Article  CAS  PubMed  Google Scholar 

  • Vincent D, Lapierre C, Pollet B, Cornic G, Negroni L et al (2005) Water deficits affect caffeate O-methyltransferase, lignification, and related enzymes in maize leaves. A proteomic investigation. Plant Physiol 137:949–960

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang JT (1988) The steppes and deserts of the Xizang plateau. Tibet Vegetatio 75:135–142

    Google Scholar 

  • Wang LY, Abbott RJ, Zheng W, Chen P, Wang Y et al (2009) History and evolution of alpine plants endemic to the Qinghai-Tibetan Plateau: Aconitum gymnandrum (Ranunculaceae). Mol Ecol 18:709–721

    Article  PubMed  Google Scholar 

  • Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Zhu JK (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J et al (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yue PP, Lu XF, Ye RR, Zhang CX, Yang SB et al (2011) Distribution of Stipa purpurea steppe in the Northeastern Qinghai-Xizang Plateau. China Russ J Ecol+ 42:50–56

    Article  CAS  Google Scholar 

  • Zhang J, Wang JT, Chen W (1988) Vegetation of Xizang (Tibet). Science Press, Beijing

    Google Scholar 

  • Zhang JH, Jia WS, Yang JC, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119

    Article  Google Scholar 

  • Zhang X, Zhou J, Han Z, Shang Q, Wang ZG et al (2012) Active methyl cycle and transfer related gene expression in response to drought stress in rice leaves. Rice Sci 19:86–93

    Article  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zou XK, Zhai PM, Zhang Q (2005) Variations in droughts over China: 1951–2003. Geophys Res Lett 32:2–5

    Google Scholar 

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Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (NSFC) (No. 41271058), the Major State Basic Research Development Program of China (No. 2010CB951704).

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Authors and Affiliations

  1. Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming, 650204, China

    Yunqiang Yang, Xiong Li, Xiangxiang Kong, Lan Ma, Xiangyang Hu & Yongping Yang

  2. The Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan, 650201, China

    Yunqiang Yang, Xiong Li, Xiangxiang Kong, Lan Ma, Xiangyang Hu & Yongping Yang

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    Xiong Li & Lan Ma

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  1. Yunqiang Yang
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  2. Xiong Li
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  3. Xiangxiang Kong
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  4. Lan Ma
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  5. Xiangyang Hu
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  6. Yongping Yang
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Correspondence to Yongping Yang.

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Fig. S1

Search of unigenes against the nr database. (A) E-value distribution of BLAST hits for each unique sequence with a cut-off E-value of 1.0E-5. (B) Species distribution is shown as a percentage of the total homologous sequences with an E-value of at least 1.0E-5. (GIF 80 kb)

High Resolution Image (TIFF 527 kb)

Fig. S2

COG functional classifications of unigene sequences from the S. purpurea transcriptome data. (GIF 92 kb)

High Resolution Image (TIFF 2417 kb)

Fig. S3

Classification of RNA-seq raw reads. (GIF 45 kb)

High Resolution Image (TIFF 697 kb)

Figure S4

Distribution of gene coverage in the five S. purpurea populations. Gene coverage was the percentage of a gene covered by reads (the number of bases covered by unique mapping reads/the total number of bases in that gene). (GIF 101 kb)

High Resolution Image (TIFF 1273 kb)

Table S1

Primers used for the semi-quantitative PCR analysis. (PDF 28 kb)

Table S2

Principal components analysis of the contribution of differential climate factors in the field experiments. (PDF 55 kb)

Table S3

Length distribution of assembled contigs and unigenes. (PDF 7 kb)

Table S4

Summary of the unigene BLAST results. (PDF 37 kb)

Table S5

Functional annotation of unigene in S. purpurea. (XLS 28354 kb)

Table S6

Top 30 up- and down-regulated genes in S. purpurea. (PDF 31 kb)

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Yang, Y., Li, X., Kong, X. et al. Transcriptome analysis reveals diversified adaptation of Stipa purpurea along a drought gradient on the Tibetan Plateau. Funct Integr Genomics 15, 295–307 (2015). https://doi.org/10.1007/s10142-014-0419-7

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  • DOI: https://doi.org/10.1007/s10142-014-0419-7

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