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Comparative study on the mRNA expression of Pinus massoniana infected by Bursaphelenchus xylophilus

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Abstract

Pine wilt disease (PWD) is a devastating disease affecting the growth of Pinus massoniana, often leading to withering and death. To reveal the changes involved during disease progression, we investigated the mRNA expression profile of P. massoniana infested by Bursaphelenchus xylophilus. The infestation resulted in the downregulation of genes involved in interactions with pathogenic pathways such as disease resistance gene, CC-NBS-LRR resistance-like protein, and the gene encoding a putative nematode resistance protein. Increased infestation pressure (number of nematodes inoculated) caused a continuous decline in the gene expression of stem samples. An infestation of P. massoniana also resulted in a pathway enrichment of genes involved in phenylpropanoid metabolism and flavonoid biosynthesis, which in turn reduced the levels of total phenols and total flavonoids. A downregulation of auxin responsive family protein was observed in infested samples, which resulted in a suppression of plant growth. Thus, upon B. xylophilus infestation, a downregulation of genes associated with the recognition of pathogens, PWD resistance, and growth regulation was observed in P. massoniana, together with a decrease in the levels of phytoalexin-like secondary substances, all of which resulted in withering and ultimately death of P. massoniana.

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References

  • Cai D, Kleine M, Kifle S, Harloff HJ, Sandal NN, Marcker KA, Klein-Lankhorst RM, Salentijn EMJ, Lange W, Stiekema WJ, Wyss U, Grundler FMW, Jung C (1997) Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832–834

    Article  CAS  Google Scholar 

  • Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  CAS  Google Scholar 

  • Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284

    Article  CAS  Google Scholar 

  • Fukuda K (1997) Physiological process of the symptom development and resistance mechanism in pine wilt disease. J For Res 2:171–181

    Article  Google Scholar 

  • Futai K (2013) Pine wood nematode, Bursaphelenchus xylophilus. Annu Rev Phytopathol 51:61–83

    Article  CAS  Google Scholar 

  • Gao L, Tu ZJ, Millett BP, Bradeen JM (2013) Insights into organ-specific pathogen defense responses in plants: RNA-seq analysis of potato tuber-Phytophthora infestans interactions. BMC Genom 14:340

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hanin M, Brini F, Ebel C, Toda Y, Takeda S, Masmoudi K (2011) Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal Behav 6:1503–1509

    Article  CAS  Google Scholar 

  • Hirao T, Fukatsu E, Watanabe A (2012) Characterization of resistance to pine wood nematode infection in Pinus thunbergii using suppression subtractive hybridization. BMC Plant Biol 12:13

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:480–484

    Article  Google Scholar 

  • Kortekamp A (2006) Expression analysis of defence-related genes in grapevine leaves after inoculation with a host and a non-host pathogen. Plant Physiol Biochem 44:58–67

    Article  CAS  Google Scholar 

  • Li G, Asiegbu FO (2004) Induction of Pinus sylvestris PsACRE, a homology of Avr9/Cf-9 rapidly elicited defense-related gene following infection with root rot fungus Heterobasidion annosum. Plant Sci 167:535–540

    Article  CAS  Google Scholar 

  • Liu Y, Wang L, Xing X, Sun L, Pan J, Kong X, Zhang M, Li D (2013) ZmLEA3, a multifunctional group 3 LEA protein from maize (Zea mays L.), is involved in biotic and abiotic stresses. Plant Cell Physiol 54:944–959

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • McLean MD, Hoover GJ, Bancroft B, Makhmoudova A, Clark SM, Welacky T, Simmonds DH, Shelp BJ (2007) Identification of the full-length Hs1pro−1 coding sequence and preliminary evaluation of soybean cyst nematode resistance in soybean transformed with Hs1pro−1 cDNA. Botany 85:437–441

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Park S, Han K-H (2003) An auxin-repressed gene (RpARP) from black locust (Robinia pseudoacacia) is posttranscriptionally regulated and negatively associated with shoot elongation. Tree Physiol 23:815–823

    Article  CAS  Google Scholar 

  • Petit P, Granier T, d’Estaintot BL, Manigand C, Bathany K, Schmitter JM, Lauvergeat V, Hamdi S, Gallois B (2007) Crystal structure of grape dihydroflavonol 4-reductase, a key enzyme in flavonoid biosynthesis. J Mol Biol 368:1345–1357

    Article  CAS  Google Scholar 

  • Tan S, Wu S (2012) Genome wide analysis of nucleotide-binding site disease resistance genes in Brachypodium distachyon. Comp Funct Genom 3:418208

    Google Scholar 

  • Tronchet M, Balague C, Kroj T, Jouanin L, Roby D (2010) Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis. Mol Plant Pathol 11:83–92

    Article  CAS  Google Scholar 

  • Westermann AJ, Gorski SA, Vogel J (2012) Dual RNA-seq of pathogen and host. Nat Rev Microbiol 10:618–630

    Article  CAS  Google Scholar 

  • Xie W, Huang A, Li H, Feng L, Zhang F, Guo W (2017) Identification and comparative analysis of microRNAs in Pinus massoniana infected by Bursaphelenchus xylophilus. Plant Growth Regul 83:223–232

    Article  CAS  Google Scholar 

  • Xu L, Liu ZY, Zhang K, Lu Q, Liang J, Zhang XY (2013) Characterization of the Pinus massoniana transcriptional response to Bursaphelenchus xylophilus infection using suppression subtractive hybridization. Int J Mol Sci 14:11356–11375

    Article  Google Scholar 

  • Zhao BG (2008) Pine wilt disease in China. In: Zhao BG, Futai K, Sutherland JR, Takeuchi Y (eds) Pine wilt disease. Springer, Tokyo, pp 18–25

    Chapter  Google Scholar 

  • Zheng HY, Xu M, Xu FY, Ye JR (2015) A comparative proteomics analysis of Pinus massoniana inoculated with Bursaphelenchus xylophilus. Pak J Bot 47:1271–1280

    CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Jinshan College, Fujian Agriculture and Forestry University, Fuzhou, China

    Wanfeng Xie & Wenshuo Guo

  2. Institute of Forestry Protection, Forestry College, Fujian Agriculture and Forestry University, Fuzhou, China

    Wanfeng Xie, Guanghong Liang, Aizhen Huang, Feiping Zhang & Wenshuo Guo

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  1. Wanfeng Xie
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  2. Guanghong Liang
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  3. Aizhen Huang
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  4. Feiping Zhang
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  5. Wenshuo Guo
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Corresponding authors

Correspondence to Feiping Zhang or Wenshuo Guo.

Additional information

Project funding: This work was financially supported by the National Key Research and Development Program (2017YFD0600105), the National Natural Science Foundation of China (Grant No. 31870641), the Research Foundation of Education Department of Fujian Province (No. JAT170882), Project of Financial Department of Fujian Province (Nos. K81139238 and K8911010) and the Special Fund for Forestry Research in the Public Interest of China (No. 201304401).

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Corresponding editor: Hu Yanbo.

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Xie, W., Liang, G., Huang, A. et al. Comparative study on the mRNA expression of Pinus massoniana infected by Bursaphelenchus xylophilus. J. For. Res. 31, 75–86 (2020). https://doi.org/10.1007/s11676-018-0824-1

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  • DOI: https://doi.org/10.1007/s11676-018-0824-1

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