RNA-Seq revealed that infection with white tip nematodes could downregulate rice photosynthetic genes

  • Hong-Le Wang
  • Si-Hua Yang
  • Mei Lv
  • Shan-Wen Ding
  • Jun-Yi Li
  • Chun-Ling Xu
  • Hui XieEmail author
Original Article


White-tip nematode, Aphelenchoides besseyi is a kind of widely distributed migratory parasitic nematode that can infect plant shoots. Transcriptome sequencing of plant parasitic nematodes and their host plants is helpful for understanding their interaction relationship. This study first reported expression patterns of defense-related genes in rice, and rice transcriptomes at different periods after infection with A. besseyi. The result showed that the defense response pathways of rice changed obviously in the early stage of A. besseyi infection, including upregulated salicylic acid and jasmonate pathways and a downregulated ethylene pathway. Transcriptome analysis results suggested that A. besseyi infection was associated with the downregulation of multiple genes related to photosynthesis with possible suppression of the photosynthetic activity. It suggested that the photosynthesis system of rice could be suppressed by infections of migratory nematodes, including A. besseyi and Hirschmanniella oryzae, but was stimulated by that of a sedentary nematode, Meloidogyne graminicola, by comparing our study with the reported transcriptome. OS09G0417800 (OsWRKY62) might play an important role in the interaction of migratory nematodes and rice. It also indicated that the infection strategy of both A. besseyi and the reported migratory nematode H. oryzae was similar to that of the fungal pathogen Magnaporthe grisea. These results provided an interesting starting point to elucidate the mechanism of the interaction between rice and A. besseyi, as well as the host and migratory plant nematodes.


Aphelenchoides besseyi Rice Plant defense response RNA-Seq Photosynthesis 


Authors’ contributions

HX and HLW designed the experiments; HLW, SHY, ML, SWD, and JYL performed the experiments; HLW, SWD, JYL, and CLX analyzed the data; HLW, HX, and CLX wrote the manuscript. All authors read and approved the final version of the manuscript.

Funding information

This work was funded by National Natural Science Foundation of China (No.31871939 and 31371920) and Doctoral innovative talents (domestic training) Cultivation Project of South China Agricultural University in 2019 (No. CX2019N048).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval and consent to participate

Animals were treated in strict accordance with the Animal Ethics Procedures and Guidelines of the People’s Republic of China. All animal procedures were approved by the Animal Ethics Committee of the South China Agricultural University.

Supplementary material

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  1. Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EGJ, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC, Caillaud MC, Coutinho PM, Dasilva C, Luca FD, Deau F, Esquibet M, Flutre T, Goldstone JV, Hamamouch N, Hewezi T, Jaillon O, Jubin C, Leonetti P, Magliano M, Maier TR, Markov GV, McVeigh P, Pesole G, Poulain J, Robinson-Rechavi M, Sallet E, Se’gurens B, Steinbach D, Tytgat T, Ugarte E, Ghelder CV, Veronico P, Baum TJ, Blaxter M, Bleve-Zacheo T, Davis EL, Ewbank JJ, Favery B, Grenier E, Henrissat B, Jones JT, Laudet V, Maule AG, Quesneville H, Rosso MN, Schiex T, Smant G, Weissenbach J, Wincker P (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26Google Scholar
  2. Akker SED, Lilley CJ, Canchin EGJ, Rancurel C, Cock PJA, Urwin PE, Jones JT (2014) The transcriptome of Nacobbus aberrans reveals insights into the evolution of sedentary endoparasitism in plant-parasitic nematodes. Genome Biol Evol 6(9):2181–2194CrossRefGoogle Scholar
  3. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106CrossRefPubMedPubMedCentralGoogle Scholar
  4. Anders S, Pyl PT, Huber W (2015) HTSeq. a Python framework to work with high-throughput sequencing data. Bioinformatics 31(2):166–169CrossRefGoogle Scholar
  5. Bagnaresi P, Sala T, Irdani T, Scotto C, Lamontanara A, Beretta M, Rotino GL, Sestili S, Cattivelli L, Sabatini E (2013) Solanum torvum responses to the root-knot nematode Meloidogyne incognita. BMC Genomics 14:540PubMedPubMedCentralCrossRefGoogle Scholar
  6. Barnes SN, Wram CL, Mitchum MG, Baum TJ (2018) The plant-parasitic cyst nematode effector GLAND4 is a DNA-binding protein. Mol Plant Pathol 19(10):2263–2276PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bauters L, Haegeman A, Kyndt T, Gheysen G (2014) Analysis of the transcriptome of Hirschmanniella oryzae to explore potential survival strategies and host–nematode interactions. Mol Plant Pathol 15(4):352–363PubMedCrossRefGoogle Scholar
  8. Berger S, Sinha AK et al (2007) Plant physiology meets phytopathology: plant primary metabolism and plant–pathogen interactions. J Exp Bot 58(15/16):4019–4026PubMedCrossRefGoogle Scholar
  9. Bolton MD (2009) Primary metabolism and plant defense—fuel for the fire. Mol Plant-Microbe Interact 22:487–497PubMedCrossRefGoogle Scholar
  10. Cheng X, Xiang Y, Xie H, Xu CL, Xie TF, Zhang C, Li Y (2013) Molecular characterization and functions of fatty acid and retinoid binding protein gene (Ab-far-1) in Aphelenchoides besseyi. PLoS One 8:e66011PubMedPubMedCentralCrossRefGoogle Scholar
  11. Chen CJ, Xia R, Chen H, He YH (2018) TBtools, a toolkit for biologists integrating various HTS-data handling tools with a user-friendly interface. bioRix.
  12. De Torres Zabala M, Littlejohn G, Jayaraman S, Studholme D, Bailey T, Lawson T, Tillich M, Licht D, Bölter B, Delfino L, Truman W, Mansfield J, Smirnoff N, Grant M (2015) Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nat Plants 1:15074PubMedCrossRefGoogle Scholar
  13. Göhre V, Jones AME, Sklenář J, Robatzek S, Weber APM (2012) Molecular crosstalk between PAMP-triggered immunity and photosynthesis. MPMI 25(8)PubMedCrossRefGoogle Scholar
  14. Haegeman A, Joseph S, Gheysen G (2011) Analysis of the transcriptome of root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Mol Biochem Parasitol 178:7–14PubMedCrossRefGoogle Scholar
  15. Haegeman A, Bauters L, Kyndt T, Rahman MM, Gheysen G (2013) Identification of candidate effector genes in the transcriptome of the rice root knot nematode Meloidogyne graminicola. Mol Plant Pathol 14(4):379–390PubMedCrossRefPubMedCentralGoogle Scholar
  16. Jacob J, Mitreva M, Vanholme B, Gheysen G (2008) Exploring the transcriptome of the burrowing nematode Radopholus similis. Mol Gen Genomics 280:1–17CrossRefGoogle Scholar
  17. Jiang J, Ma S, Ye N, Jiang M, Cao J, Zhang J (2017) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59:86–101PubMedCrossRefPubMedCentralGoogle Scholar
  18. Jimmy JL, Babu S (2015) Role of OsWRKY transcription factors in rice disease resistance. Trop Plant Pathol 40:355–361CrossRefGoogle Scholar
  19. Karmakar S, Molla KA, Chanda PK, Sarkar SN, Datta SK, Datta K (2016) Green tissue-specific co-expression of chitinase and oxalate oxidase 4 genes in rice for enhanced resistance against sheath blight. Planta 243:115–130PubMedCrossRefGoogle Scholar
  20. Karssen G, Groza M (2018) First report of the plant-parasitic nematode Aphelenchoides besseyi (Nematoda: Aphelenchoididae) on rice in Romania. Bull OEPP/EPPO Bull 48(2):254–255CrossRefGoogle Scholar
  21. Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4)PubMedPubMedCentralCrossRefGoogle Scholar
  22. Kong LA, Wu DQ, Huang WK, Peng H, Wang GF, Cui JK, Liu SM, Li ZG, Yang J, Peng DL (2015) Large-scale identification of wheat genes resistant to cereal cyst nematode Heterodera avenae using comparative transcriptomic analysis. BMC Genomics 16:801PubMedPubMedCentralCrossRefGoogle Scholar
  23. Kyndt T, Denil S, Haegeman A, Trooskens G, Bauters L, Van CW, De MT, Gheysen G (2012a) Transcriptional reprogramming by root knot and migratory nematode infection in rice. New Phytol 196(2012a):887–900PubMedCrossRefGoogle Scholar
  24. Kyndt T, Hofte M, Gheysen L (2012b) Comparing the defence-related gene expression changes upon migratory and sedentary nematode attack in rice. Plant Biol:73–82Google Scholar
  25. Lilley CJ, Kyndt T, Gheysen G (2011) Nematode resistant GM crops in industrialised and developing countries. In: Jones JT, Gheysen G, Fenoll C (eds) Genomics and molecular genetics of plant–nematode interactions. Springer, Heidelberg López-Martínez, N., Colinas-L 517–541Google Scholar
  26. Lin MS, Ding XF, Wang ZM, Zhou FM, Lin N (2004) Description of Aphelenchoides besseyi from abnormal rice with ‘small grains and erect panicles’ symptom in China. Rice Sci 12(4):289–294Google Scholar
  27. Liu B, Li JF, Ao Y, Wang J, Wang HB (2012) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24(8):3406–3419PubMedPubMedCentralCrossRefGoogle Scholar
  28. Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21(19):3787–3793CrossRefGoogle Scholar
  29. Mota APZ, Vidigal B, Danchin EGJ, Togawa RC, Leal-Bertioli SCM, Bertioli DJ, Araujo ACG, Brasileiro ACM, Guimaraes PM (2018) Comparative root transcriptome of wild Arachis reveals NBS-LRR genes related to nematode resistance. BMC Plant Biol 18:159PubMedPubMedCentralCrossRefGoogle Scholar
  30. Nahar K, Kyndt T, Vleesschauwer DD, Höfte M, Gheysen G (2011) The Jasmonate pathway is a key player in systematically induced defense against root nematodes in rice. Plant Physiol 157:305–316PubMedPubMedCentralCrossRefGoogle Scholar
  31. Peng Y, Bartley LE, Chen XW, Dardick C, Chern M, Ruan R (2008) OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in Rice. Mol Plant 3(1):446–458CrossRefGoogle Scholar
  32. Petitot AS, Dereeper A, Agbessi M, Da CS (2016) Dual RNA-Seq reveals Meloidogyne graminicola transcriptome and candidate effectors during the interaction with rice plants. Mol Plant Pathol 17(6):860–874PubMedPubMedCentralCrossRefGoogle Scholar
  33. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:36CrossRefGoogle Scholar
  34. Santos CS, Pinheiro M, Silva AI, Egas C, Vasconcelos MW (2012) Searching for resistance genes to Bursaphelenchus xylophilus using high throughput screening. BMC Genomics 13:599PubMedPubMedCentralCrossRefGoogle Scholar
  35. Swiecicka M, Filipecki M, Lont D, Van VJ, Goverse A, Bakker J, Helder J (2009) Dynamics in the tomato root transcriptome on infection with the potato cyst nematode Globodera rostochiensis. Mol Plant Pathol 10(4):487–500PubMedPubMedCentralCrossRefGoogle Scholar
  36. Szakasits D, Heinen P, Wieczorek K, Hofmann J, Wagner F, Kreil DP (2009) The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant J 57:771–784PubMedCrossRefGoogle Scholar
  37. Tariq R, Wang CL, Qin TF, Xu F, Tang Y, Gao Y, Ji Z, Zhao K (2018) Comparative transcriptome profiling of rice near-isogenic line carrying Xa23 under infection of Xanthomonas oryzae pv. Oryzae. Int J Mol Sci 19:717PubMedCentralCrossRefPubMedGoogle Scholar
  38. Thim O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37(6):914–939CrossRefGoogle Scholar
  39. Thorpe P, Mantelin S, Cock PJA, Blok VC, Coke MC, Akker SEV, Guzeeva DE, Lilley CJ, Smant G, Reid AJ, Wright KM, Urwin PE (2014) Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida. BMC Genomics 15:923PubMedPubMedCentralCrossRefGoogle Scholar
  40. Toufexi A, Duggan C, Pandey WP, Savage Z, Segretin ME, Yuen LH, Gaboriau D, Leary A, Khandare V, Ward AD, Botchway SW, Bateman BC, Pan I, Schattat MH, Sparkes I, Bozkurt T (2019). Chloroplasts navigate towards the pathogen interface to counteract infection by the Irish potato famine pathogen. BioRxiv.
  41. Trapnell CL, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2014) Differential gene and transcript expression analysis of RNA-Seq experiments with TopHat and cufflinks. Nat Protoc 2513Google Scholar
  42. Vo KTX, Kim CY, Hoang TV, Lee SK, Shirsekar G, Seo YS, Lee SW, Wang GL, Jeon JS (2018) OsWRKY67 plays a positive role in basal and XA21-mediated resistance in rice. Front Plant Sci 8:2220PubMedPubMedCentralCrossRefGoogle Scholar
  43. Wang F, Li DL, Wang ZY, Dong A, Liu L, Wang B, Chen Q, Liu X (2014) Transcriptomic analysis of the rice white tip nematode, Aphelenchoides besseyi (Nematoda: Aphelenchoididae). PLoS One 9(3):1–10Google Scholar
  44. Wang DW, Peng XF, Xie H, Xu CL, Cheng DQ, Li JY, Wu WJ, Wang K (2016) Arabidopsis thaliana as a suitable model host to research on interactions between plant and foliar nematodes, parasites of plant shoot. Sci Rep 6:38286PubMedPubMedCentralCrossRefGoogle Scholar
  45. Wang DW, Xu CL, Ding SW, Huang X, Cheng X, Zhang C, Chen C, Xie H (2018) Identification and function of FAR protein family genes from a transcriptome analysis of Aphelenchoides besseyi. Bioinformatics:1–8Google Scholar
  46. Wei T, Qu B, Li JB, Zhao Y, Guo D, Zhu Y, Chen Z, Gu H, Li C, Qin G, Qu LJ (2013) Transcriptional profiling of Rice early response to Magnaporthe oryzae identified OsWRKYs as important regulators in rice blast resistance. PLoS One 8(3):e59720PubMedPubMedCentralCrossRefGoogle Scholar
  47. Wuriyanghan H, Chen LJ, Dong Y, Lei G, Jia FX, Zhang JS, Chen SY (2007) Rice receptor-like kinase OsSI-RLK2 inhibits internode elongation. Chin Sci Bull 19(52):2657–2663CrossRefGoogle Scholar
  48. Young MD, Wakefiled MJ, Smyth GK, Oshlack A (2010) Method gene ontology analysis for RNA-Seq: accounting for selection bias. Genome Biol 11:R14PubMedPubMedCentralCrossRefGoogle Scholar
  49. Zhang H, Huan XF, Xu HC (2014) Changes of photosynthesis and antioxidant enzyme activities at different stage naturally infected by Bursaphelenchus xylophilus. J Environ Entomol 36(2):139–144 (In Chinese)Google Scholar
  50. Zhu Q, Zhang XL, Nadir S, Doku HA, Chen LJ, Li DX (2018) Cloning and overexpression strain construction of a LysM domain-containing gene OsEMSA1 in Rice. Mol Plant Breed (In Chinese) 1(16):22–30. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratory of Plant Nematology and Research Center of Nematodes of Plant Quarantine, Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, College of AgricultureSouth China Agricultural UniversityGuangzhouPeople’s Republic of China

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