Skip to main content
SpringerLink
Log in

Genome-wide analysis of lncRNAs in Paulownia tomentosa infected with phytoplasmas

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Paulownia witches’ broom is arisen from the invasion of an obligatory parasitic bacteria-phytoplasma, which can result in huge economic losses of Paulownia trees. The mechanism of the occurrence of this disease has been studied extensively. However, its pathogenesis is still poorly understood. Here, whole transcriptome strand-specific RNA sequencing was performed to identify long noncoding RNAs (lncRNAs) that referred to phytoplasma infection in Paulownia. In all, 2725 lncRNAs were identified and 748 of them were considered to be differentially expressed. KEGG pathway analysis showed the predicted target genes of these 748 lncRNAs participated mainly in lignin biosynthesis pathway, plant–pathogen interaction pathway and plant hormone signal transduction pathway, which indicated that lncRNAs may be closely related to the occurrence of witches’ broom. The results provide new perspective into the function of lncRNAs in Paulownia and potentially in other trees in answering phytoplasma invasion.

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ates S, Ni YA, Tozluoglu M (2008) A Characterization and evaluation of Paulownia elongata as a raw material for paper production. Afr J Biotechnol 7(22):4153–4158

    CAS  Google Scholar 

  • Ben AB, Wirth S, Merchan F et al (2008) Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res 19(1):57–69

    Article  Google Scholar 

  • Bernstein E, Allis CD (2005) RNA meets chromatin. Gene Dev 19(14):1635–1655

    Article  CAS  PubMed  Google Scholar 

  • Boerner S, McGinnis KM (2012) Computational identification and functional predictions of long noncoding RNA in Zea mays. PLoS One 7(8):e43047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boller T (2005) Peptide signalling in plant development and self/nonself perception. Curr Opin Cell Biol 17(2):116–122

    Article  CAS  PubMed  Google Scholar 

  • Brosnan CA, Voinnet O (2009) The long and the short of noncoding RNAs. Curr Opin Cell Biol 21(3):416–425

    Article  CAS  PubMed  Google Scholar 

  • Cabili MN, Trapnell C, Goff L et al (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Gene Dev 25(18):1915–1927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao X, Fan G, Deng M et al (2014a) Identification of genes related to Paulownia witches’ broom by AFLP and MSAP. Int J Mol Sci 15(8):14669–14683

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao X, Fan G, Deng M et al (2014b) Morphological changes of Paulownia seedlings infected phytoplasmas reveal the genes associated with witches’ broom through AFLP and MSAP. PLoS One 9(11):e112533

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao X, Fan G, Dong Y et al (2017) Proteome profiling of Paulownia seedlings infected with phytoplasma. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00342

    Google Scholar 

  • Chen J, Quan M, Zhang D (2015) Genome-wide identification of novel long non-coding RNAs in Populus tomentosa tension wood, opposite wood and normal wood xylem by RNA-seq. Planta 241(1):125–143

    Article  CAS  PubMed  Google Scholar 

  • Csorba T, Questa JI, Sun Q et al (2014) Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proc Natl Acad Sci 111(45):16160–16165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ćurković PM (2008) Auxin-treatment induces recovery of phytoplasma-infected periwinkle. J Appl Microbiol 105(6):1826–1834

    Article  Google Scholar 

  • Dixon RA, Achnine L, Kota P (2002) The phenylpropanoid pathway and plant defence-a genomics perspective. Mol Plant Pathol 3(5):371–390

    Article  CAS  PubMed  Google Scholar 

  • Doi Y, Ternaka M, Yora K (1967) Mycoplasma or PLT-group-like microorganisms found in the phloem elements of plants infected with mulberry dwarf, potato witches’ broom, aster yellows and Paulownia witches’ broom. Jpn J Phytopathol 33(4):259–266

    Article  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  CAS  PubMed  Google Scholar 

  • Fan G, Dong Y, Deng M et al (2014) Plant-pathogen interaction, circadian rhythm, and hormone-related gene expression provide indicators of phytoplasma infection in Paulownia fortunei. Int J Mol Sci 15(12):23141–23162

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan G, Cao X, Niu S et al (2015a) Transcriptome, microRNA, and degradome analyses of the gene expression of Paulownia with phytoplamsa. BMC Gen 16(1):896

    Article  Google Scholar 

  • Fan G, Cao X, Zhao Z et al (2015b) Transcriptome analysis of the genes related to the morphological changes of Paulownia tomentosa plantlets infected with phytoplasma. Acta Physiol Plant 37(10):202

    Article  Google Scholar 

  • Fan G, Xu E, Deng M et al (2015c) Phenylpropanoid metabolism, hormone biosynthesis and signal transduction-related genes play crucial roles in the resistance of Paulownia fortunei to paulownia witches’ broom phytoplasma infection. Genes Genom 37(11):913–929

    Article  CAS  Google Scholar 

  • Fan G, Cao Y, Deng M et al (2017) Identification and dynamic expression profiling of microRNAs and target genes of Paulownia tomentosa in response to Paulownia witches’ broom disease. Acta Physiol Plant 39(1):28

    Article  Google Scholar 

  • Gai Y, Han X, Li Y et al (2014) Metabolomic analysis reveals the potential metabolites and pathogenesis involved in mulberry yellow dwarf disease. Plant, Cell Environ 37(6):1474–1490

    Article  CAS  Google Scholar 

  • Gundersen DE, Lee IM (1996) Ultrasensitive detection of phytoplasmas by nested-PCR assays using two universal primer pairs. Phytopathol mediterr 35(3):144–151

    CAS  Google Scholar 

  • Hisami Y, Tomomi S, Kazunoir T et al (2001) The arabidopsis AHK4 histidine Kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42(9):1017–1023

    Article  Google Scholar 

  • Hu WJ, Kawaoka A, Tsai CJ et al (1998) Compartmentalized expression of two structurally and functionally distinct 4-coumarate:CoA ligase genes in aspen (Populus tremuloides). PNAS 95(9):5407–5412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia H, Osak M, Bogu GK (2010) Genome-wide computational identification and manual annotation of human long noncoding RNA genes. RNA 16(8):1478–1487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jone P (2001) Phytoplasma plant pathogens. In: Waller (ed) Plant Pathologists Pocketbook, 3rd end. CAB international, Harpenden, Hertfordshire, pp. 126–129

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329

    Article  CAS  PubMed  Google Scholar 

  • Kapranov P, Cheng J, Dike S et al (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316(5830):1484–1488

    Article  CAS  PubMed  Google Scholar 

  • Kong L, Zhang Y, Ye ZQ et al (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35(suppl 2):345–349

    Article  Google Scholar 

  • Kornblihtt AR (2014) A long noncoding way to alternative splicing in plant development. Dev Cell 368(30):117–119

    Article  Google Scholar 

  • Kunze G, Zipfel C, Robatzek S et al (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16(12):3496–3507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J (2013) Analysis of Alternative splicing in whole transcriptome and its regulator SR protein under drought stress in seed of Zea mays. Dissertation, Zhengzhou University

  • Li J, Wu B, Xu J et al (2013) Genome-wide identification and characterization of long intergenic non-coding RNAs in Ganoderma lucidum. PLoS One 9(6):e99442

    Article  Google Scholar 

  • Li J, Zhou B, Zhu Q et al (2017) Noncoding and coding transcriptome analysis reveals the regulation roles of long noncoding RNAs in fruit development of hot pepper (Capsicum annuum L.). Plant Growth Regul 83(1):141–156

    Article  CAS  Google Scholar 

  • Liu J, Jung C, Xu J et al (2012) Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24(11):4333–4345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu R, Dong Y, Fan G et al (2013) Discovery of genes related to witches broom disease in Paulownia tomentosa × Paulownia fortunei by a de Novo assembled transcriptome. PLoS ONE 8(11):e80238

    Article  PubMed  PubMed Central  Google Scholar 

  • Lucia FD, Dean C (2010) Long non-coding RNAs and chromatin regulation. Curr Opin Plant Biol 14(2):168–173

    Article  PubMed  Google Scholar 

  • Lukiw WJ, Handley P, Wong L (1992) BC200 RNA in normal human neocortex, non-Alzheimer dementia (NAD), and senile dementia of the Alzheimer type (AD). Neurochem Res 17(6):591–597

    Article  CAS  PubMed  Google Scholar 

  • Marquez Y, Brown JWS, Simpson C et al (2012) Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 22(6):1184–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mastrangelo AM, Marone D, Laidò G et al (2012) Alternative splicing: enhancing ability to cope with stress via transcriptome plasticity. Plant Sci 185–186(4):40–49

    Article  PubMed  Google Scholar 

  • Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10(3):155–159

    Article  CAS  PubMed  Google Scholar 

  • Mishina TE, Zeier J (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50(3):500–513

    Article  CAS  PubMed  Google Scholar 

  • Mohammadin S, Edger PP, Pires JC et al (2015) Positionally-conserved but sequence-diverged: identification of long non-coding RNAs in the Brassicaceae and Cleomaceae. BMC Plant Biol 15(1):217

    Article  PubMed  PubMed Central  Google Scholar 

  • Morin RD, O’Connor MD, Griffith M et al (2008) Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 18(4):610–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113(7):935–944

    Article  CAS  PubMed  Google Scholar 

  • Mou H, Lu J, Zhu S et al (2013) Transcriptomic analysis of paulownia infected by paulownia witches’-broom phytoplasma. PLoS One 8(10):e77217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muthusamy M, Uma S, Backiyarani S et al (2015) Genome-wide screening for novel, drought stress-responsive long non-coding RNAs in drought-stressed leaf transcriptome of drought-tolerant and -susceptible banana (Musa spp.) cultivars using Illumina high-throughput sequencing. Plant Biotechnol Rep 9(5):279–286

    Article  Google Scholar 

  • Namba S (2002) Molecular biological studies on phytoplasmas. J Gen Plant Pathol 68(3):257–259

    Article  CAS  Google Scholar 

  • Nawrocki EP, Kolbe DL, Eddy SR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25(10):1335–1337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman S, Bennett K, Wu Y (1998) Performance of maize, beans and ginger as in Paulownia plantations in China. Agroforestry Syst 39(1):23–30

    Article  Google Scholar 

  • Niu S, Fan G, Deng M et al (2016) Discovery of microRNAs and transcript targets related to witches’ broom disease in Paulownia fortunei by high-throughput sequencing and degradome approach. Mol Genet Genom 291(1):181–191

    Article  CAS  Google Scholar 

  • Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136(4):629–641

    Article  CAS  PubMed  Google Scholar 

  • Rinn JL, Chang HY (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81:145–166

    Article  CAS  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101

    Article  CAS  PubMed  Google Scholar 

  • Sugio A, Hogenhout SA (2012) The genome biology of phytoplasma: modulators of plants and insects. Curr Opin Microbiol 15(3):247–254

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Miwa K, Ishikawa K et al (2001) The Arabidopsis sensor His-kinase, AHk4, can respond to cytokinins. Plant Cell Physiol 42(2):107–113

    Article  CAS  PubMed  Google Scholar 

  • Swiezewski S, Liu F, Magusin A et al (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462(7274):799–802

    Article  CAS  PubMed  Google Scholar 

  • Szcześniak MW, Rosikiewicz W, Makałowska I (2015) CANTATAdb: a collection of plant long non-coding RNAs. Plant Cell Physiol 57(1):e8

    Article  PubMed  PubMed Central  Google Scholar 

  • Tian J, Song Y, Du Q et al (2016) Population genomic analysis of gibberellin-responsive long non-coding RNAs in Populus. J Exp Bot 67(8):2467–2482

    Article  CAS  PubMed  Google Scholar 

  • Trapnell C, Roberts A, Goff L et al (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang K, Chang H (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43(6):904–914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Zhang X, Liu JH (2015) Deep sequencing-based characterization of transcriptome of trifoliate orange (Poncirus trifoliata (L.) Raf.) in response to cold stress. BMC genomics 16(1):555

    Google Scholar 

  • Wang Z, Liu W, Fan G et al (2017) Quantitative proteome-level analysis of paulownia witches’ broom disease with methyl methane sulfonate assistance reveals diverse metabolic changes during the infection and recovery processes. Peer J. https://doi.org/10.7717/peerj.3495

    Google Scholar 

  • Weintraub P, Beanland L (2006) Insect vectors of phytoplasmas. Annu Rev Entomol 51(51):91–111

    Article  CAS  PubMed  Google Scholar 

  • Weintraub PG, Jones P (2010) Phytoplasmas: genomes. Plant Hosts and Vectors, Wallingford

    Google Scholar 

  • Wierzbicki AT (2012) The role of long non-coding RNA in transcriptional gene silencing. Curr Opin Plant Biol 15(5):517–522

    Article  CAS  PubMed  Google Scholar 

  • Xin M, Wang Y, Yao Y et al (2011) Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol 11(1):61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon JH, Abdelmohsen K, Gorospe M (2013) Posttranscriptional gene regulation by long noncoding RNA. J Mol Biol 425(19):3723–3730

    Article  CAS  PubMed  Google Scholar 

  • Yue H, Wu Y, Shi Y et al (2008) First report of paulownia witches’broom phytoplasma in China. Plant Dis 92(7):1134

    Article  Google Scholar 

  • Zhang Y, Liao J, Li Z et al (2014) Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Gen biol 15(12):512

    Article  Google Scholar 

  • Zhu Y, Chen L, Zhang C et al (2017) Global transcriptome analysis reveals extensive gene remodeling, alternative splicing and differential transcription profiles in non-seed vascular plant Selaginella moellendorffii. BMC Gen 18(1):1042

    Article  Google Scholar 

Download references

Acknowledgements

This study was funded by the Key Science and Technology Program of Henan Province of China (152107000097) and by the Distinguished Talents Foundation of Henan Province of China (174200510001).

Author information

Authors and Affiliations

  1. Institute of Paulownia, Henan Agricultural University, Zhengzhou, Henan, 450002, People’s Republic of China

    Yabing Cao, Guoqiang Fan & Yanpeng Dong

  2. College of Forestry, Henan Agricultural University, Zhengzhou, Henan, 450002, People’s Republic of China

    Guoqiang Fan & Yanpeng Dong

  3. Henan Academy of Forestry, Zhengzhou, Henan, 450002, People’s Republic of China

    Xiaoqiao Zhai

Authors
  1. Yabing Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guoqiang Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaoqiao Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanpeng Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guoqiang Fan.

Ethics declarations

Conflict of interest

No conflict interests exist in this research.

Additional information

Communicated by E. Kuzniak-Gebarowska.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1 Primers used for real-time quantitative PCR (XLSX 10 kb)

Changes of morphology in Paulownia witches’ broom seedlings (TIFF 1751 kb)

11738_2018_2627_MOESM3_ESM.tif

Online Resource 3 Detection of phytoplasma 16S rRNA in the phytoplasma-infected seedlings M. Marker; 1. Phytoplasma-infected seedlings; 2. Healthy seedlings; 3. ddH2O (TIFF 631 kb)

11738_2018_2627_MOESM4_ESM.tif

Correlation coefficients of the expression of duplicate samples X-axis represents the logarithmic value of PT expression, while Y-axis represents the logarithmic value of the corresponding duplicate sample (TIFF 319 kb)

Sequences of identified lncRNAs (XLSX 1426 kb)

Online Resource 6 The conservation of P. tomentosa lncRNAs (XLSX 40 kb)

Online Resource 7 Classification of predicted lncRNAs into different ncRNA families (XLSX 35 kb)

Online Resource 8 LncRNAs identified in P. tomentosa (XLSX 108 kb)

Online Resource 9 Phytoplasma-responsive lncRNAs (XLSX 83 kb)

Online Resource 10 The target genes of the phytoplasma-responsive lncRNAs (XLSX 149 kb)

Online Resource 11 The differentially expressed target genes of the phytoplasma-responsive lncRNAs (XLSX 80 kb)

11738_2018_2627_MOESM12_ESM.xlsx

Online Resource 12 KEGG analysis of the differentially expressed target genes of the phytoplasma-responsive lncRNAs (XLSX 13 kb)

Online Resource 13 Detailed information of Alternative splicing events in PT and PTI (XLSX 4249 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cao, Y., Fan, G., Zhai, X. et al. Genome-wide analysis of lncRNAs in Paulownia tomentosa infected with phytoplasmas. Acta Physiol Plant 40, 49 (2018). https://doi.org/10.1007/s11738-018-2627-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-018-2627-6

Keywords

Search

Navigation