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Plant Molecular Biology Reporter

, Volume 37, Issue 5–6, pp 413–420 | Cite as

Genome-Wide Analysis of Alternative Splicing in Zea mays during Maize Iranian Mosaic Virus Infection

  • Abozar GhorbaniEmail author
  • Ahmad Tahmasebi
  • Keramatollah Izadpanah
  • Alireza Afsharifar
  • Ralf G. Dietzgen
Original Paper
  • 72 Downloads

Abstract

Maize Iranian mosaic virus (MIMV) infects several gramineous plants and is an economically important nucleorhabdovirus in Iran. Maize responds to MIMV infection at the transcriptional level. Alternative splicing (AS) is a mechanism that generates multiple mRNAs from a single pre-mRNA, often encoding protein isoforms with functional differences. We carried out genome-wide analysis of AS responses to MIMV in maize seedlings and identified genes involved in this molecular response. The AS events we investigated included skipped exons, alternative 3′ splice site, alternative 5′ splice site, mutually exclusive exons, and retained introns. In total 10,881 maize genes showed AS, of which 601 genes were involved in response to MIMV-infection and 186 were found only in uninfected maize. AS was identified in some of the genes that are involved in disease resistance or pathogenicity pathways. We demonstrated that in MIMV-infects maize, host genes that are involved in symptom development, virus multiplication, resistance to pathogens and host-pathogen interaction are affected by AS mechanism. Gene network analysis showed that ten genes represent the hubs for the protein network in maize and that they are involved in response to pathogen attack and include 26S proteasome, 14–3-3-like protein A, Rop family, mitogen-activated protein kinase, ubiquitin and serine/threonine-protein kinases. In conclusion, we showed that AS occurs as a transcriptional regulatory mechanism in maize response to MIMV infection and we identified genes that have the key roles in pathogenicity pathways that were differentially spliced in infected seedlings.

Keywords

Alternative splicing Maize Nucleorhabdovirus Protein network Response to pathogens 

Notes

Acknowledgements

AG was supported by a fellowship from Shiraz University and Iran National Foundation of Elites. Supported also by the Queensland Department of Agriculture and Fisheries and the University of Queensland through the Queensland Alliance for Agriculture and Food Innovation.

Compliance with Ethical Standards

The manuscript has not been submitted in other Journal. This research was financial supported by Shiraz University, Iran. AG, AT, KI, RD and AA designed the study; AG performed the experiments, AG and AT analyzed the data, AG drafted the manuscript, all authors edited and approved the final version of the manuscripts.

Supplementary material

11105_2019_1169_MOESM1_ESM.xlsx (45 kb)
Supplementary table 1 Complete list of genes that were affected by alternative splicing events in MIMV-infected maize. Gene ontology terms for molecular function (F), biological processes (P) and cellular component (C) are shown. (XLSX 45 kb)
11105_2019_1169_Fig4_ESM.png (1 mb)
Supplementary figure 1

Venn diagram showing the number and percentage of genes that were affected by AS events in MIMV-infection and uninfected maize. (PNG 1056 kb)

11105_2019_1169_MOESM2_ESM.tif (24.5 mb)
High Resolution Image (TIF 25065 kb)

References

  1. An C, Gao Y, Li J, Liu X, Gao F, Gao H (2017) Alternative splicing affects the targeting sequence of peroxisome proteins in Arabidopsis. Plant Cell Rep 36:1027–1036PubMedCrossRefPubMedCentralGoogle Scholar
  2. Barbazuk WB, Fu Y, McGinnis KM (2008) Genome-wide analyses of alternative splicing in plants: opportunities and challenges. Genome Res 18:1381–1392PubMedCrossRefPubMedCentralGoogle Scholar
  3. Bazzini AA, Manacorda CA, Tohge T, Conti G, Rodriguez MC, Nunes-Nesi A, Villanueva S, Fernie AR, Carrari F, Asurmendi S (2011) Metabolic and miRNA profiling of TMV infected plants reveals biphasic temporal changes. PLoS One 6:e28466PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bolser DM, Staines DM, Perry E, Kersey PJ (2017) Ensembl plants: integrating tools for visualizing, mining, and analyzing plant genomic data. In: Plant Genomics Databases. Springer, Berlin, pp 1–31Google Scholar
  5. Calil IP, Fontes EP (2016) Plant immunity against viruses: antiviral immune receptors in focus. Ann Bot 119:711–723PubMedCentralPubMedGoogle Scholar
  6. Chen Q, Han Y, Liu H, Wang X, Sun J, Zhao B, Li W, Tian J, Liang Y, Yan J (2018) Genome-wide association analyses reveal the importance of alternative splicing in diversifying gene function and regulating phenotypic variation in maize. Plant Cell 30:1404–1423PubMedPubMedCentralCrossRefGoogle Scholar
  7. Chin C-H, Chen S-H, Wu H-H, Ho C-W, Ko M-T, Lin C-Y (2014) cytoHubba: identifying hub objects and sub-networks from complex interactome. BMC Syst Biol 8:S11PubMedPubMedCentralCrossRefGoogle Scholar
  8. Converse R, Martin R (1990) Enzyme-linked immunosorbent assay (ELISA). In: Serological methods for detection and identification of viral and bacterial plant pathogens, pp 179–196Google Scholar
  9. Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong W-K, Mockler TC (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20:45–58PubMedPubMedCentralCrossRefGoogle Scholar
  10. Gassmann W (2008) Alternative splicing in plant defense. Nuclear pre-mRNA processing in plants. Springer, Berlin, pp 219–233CrossRefGoogle Scholar
  11. Ghorbani A, Izadpanah K, Dietzgen RG (2018a) Changes in maize transcriptome in response to maize Iranian mosaic virus infection. PLoS One 13:e0194592PubMedPubMedCentralCrossRefGoogle Scholar
  12. Ghorbani A, Izadpanah K, Dietzgen RG (2018b) Completed sequence and corrected annotation of the genome of maize Iranian mosaic virus. Arch Virol 163:767–770PubMedCrossRefPubMedCentralGoogle Scholar
  13. Ghorbani A, Izadpanah K, Dietzgen RG (2018c) Gene expression and population polymorphism of maize Iranian mosaic virus in Zea mays, and intracellular localization and interactions of viral N, P, and M proteins in Nicotiana benthamiana. Virus Genes 54:290–296PubMedCrossRefPubMedCentralGoogle Scholar
  14. Ghorbani A, Izadpanah K, Peters JR, Dietzgen RG, Mitter N (2018d) Detection and profiling of circular RNAs in uninfected and maize Iranian mosaic virus-infected maize. Plant Sci 274:402–409PubMedCrossRefPubMedCentralGoogle Scholar
  15. Izadpanah K (1989) Purification and serology of the Iranian maize mosaic rhabdovirus. J Phytopathol 126:43–50CrossRefGoogle Scholar
  16. Izadpanah K, Ahmadi A, Parvin S, Jafari S (1983) Transmission, particle size and additional hosts of the rhabdovirus causing maize mosaic in shiraz, Iran 1. J Phytopathol 107:283–288CrossRefGoogle Scholar
  17. Kachroo A, Kachroo P (2009) Fatty acid-derived signals in plant defense. Annu Rev Phytopathol 47:153–176PubMedCrossRefGoogle Scholar
  18. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36PubMedPubMedCentralCrossRefGoogle Scholar
  19. Kogovšek P, Pompe-Novak M, Petek M, Fragner L, Weckwerth W, Gruden K (2016) Primary metabolism, phenylpropanoids and antioxidant pathways are regulated in potato as a response to potato virus Y infection. PLoS One 11:e0146135PubMedPubMedCentralCrossRefGoogle Scholar
  20. Laloum T, Martín G, Duque P (2017) Alternative splicing control of abiotic stress responses. Trends Plant Sci 23:140–150PubMedCrossRefGoogle Scholar
  21. Li L, Howe GA (2001) Alternative splicing of prosystemin pre-mRNA produces two isoforms that are active as signals in the wound response pathway. Plant Mol Biol 46:409–419PubMedCrossRefGoogle Scholar
  22. Liu Z, Qin J, Tian X, Xu S, Wang Y, Li H, Wang X, Peng H, Yao Y, Hu Z (2018) Global profiling of alternative splicing landscape responsive to drought, heat and their combination in wheat (Triticum aestivum L.). Plant Biotechnol J 16:714–726PubMedCrossRefGoogle Scholar
  23. López-Gresa MP, Lisón P, Kim HK, Choi YH, Verpoorte R, Rodrigo I, Conejero V, Bellés JM (2012) Metabolic fingerprinting of tomato mosaic virus infected Solanum lycopersicum. J Plant Physiol 169:1586–1596PubMedCrossRefGoogle Scholar
  24. Marquez Y, Brown JW, Simpson CG, Barta A, Kalyna M (2012) Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Research:gr:134106.134111Google Scholar
  25. Massah A, Izadpanah K, Lesemann D (2005) Relationship of Iranian maize mosaic virus with insect vector and plant cells. Iranian J Plant Pathol 41:151–159Google Scholar
  26. Massah A, Izadpanah K, Afsharifar A, Winter S (2008) Analysis of nucleotide sequence of Iranian maize mosaic virus confirms its identity as a distinct nucleorhabdovirus. Arch Virol 153:1041–1047PubMedCrossRefGoogle Scholar
  27. Mei W, Liu S, Schnable JC, Yeh C-T, Springer NM, Schnable PS, Barbazuk WB (2017) A comprehensive analysis of alternative splicing in paleopolyploid maize. Front Plant Sci 8:694PubMedPubMedCentralCrossRefGoogle Scholar
  28. Nilsen TW, Graveley BR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463:457–463PubMedPubMedCentralCrossRefGoogle Scholar
  29. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40:1413–1415PubMedCrossRefGoogle Scholar
  30. Richardson DN, Rogers MF, Labadorf A, Ben-Hur A, Guo H, Paterson AH, Reddy AS (2011) Comparative analysis of serine/arginine-rich proteins across 27 eukaryotes: insights into sub-family classification and extent of alternative splicing. PLoS One 6:e24542PubMedPubMedCentralCrossRefGoogle Scholar
  31. Salah Ud-Din A, Tikhomirova A, Roujeinikova A (2016) Structure and functional diversity of GCN5-related N-acetyltransferases (GNAT). Int J Mol Sci 17:1018PubMedCentralCrossRefGoogle Scholar
  32. Seifi HS, Van Bockhaven J, Angenon G, Höfte M (2013) Glutamate metabolism in plant disease and defense: friend or foe? Mol Plant-Microbe Interact 26:475–485PubMedCrossRefPubMedCentralGoogle Scholar
  33. Shang X, Cao Y, Ma L (2017) Alternative splicing in plant genes: a means of regulating the environmental fitness of plants. Int J Mol Sci 18:432PubMedCentralCrossRefGoogle Scholar
  34. Shen S, Park JW, Huang J, Dittmar KA, Lu Z-x, Zhou Q, Carstens RP, Xing Y (2012) MATS: a Bayesian framework for flexible detection of differential alternative splicing from RNA-Seq data. Nucleic Acids Res 40:e61–e61PubMedPubMedCentralCrossRefGoogle Scholar
  35. Shi J, Zhang M, Zhai W, Meng J, Gao H, Zhang W, Han R, Qi F (2018) Genome-wide analysis of nucleotide binding site-leucine-rich repeats (NBS-LRR) disease resistance genes in Gossypium hirsutum. Physiol Mol Plant Pathol 104:1–8CrossRefGoogle Scholar
  36. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319PubMedCrossRefPubMedCentralGoogle Scholar
  37. Song J, Liu H, Zhuang H, Zhao C, Xu Y, Wu S, Qi J, Li J, Hettenhausen C, Wu J (2017) Transcriptomics and alternative splicing analyses reveal large differences between maize lines B73 and Mo17 in response to aphid Rhopalosiphum padi infestation. Front Plant Sci 8:1738Google Scholar
  38. Strable J, Scanlon MJ (2009) Maize (Zea mays): a model organism for basic and applied research in plant biology. Cold Spring Harb Protoc 2009:pdb. emo132CrossRefGoogle Scholar
  39. Syed NH, Kalyna M, Marquez Y, Barta A, Brown JW (2012) Alternative splicing in plants–coming of age. Trends Plant Sci 17:616–623PubMedPubMedCentralCrossRefGoogle Scholar
  40. Thiel H, Hleibieh K, Gilmer D, Varrelmann M (2012) The P25 pathogenicity factor of beet necrotic yellow vein virus targets the sugar beet 26S proteasome involved in the induction of a hypersensitive resistance response via interaction with an F-box protein. Mol Plant-Microbe Interact 25:1058–1072PubMedCrossRefPubMedCentralGoogle Scholar
  41. Urbach JM, Ausubel FM (2017) The NBS-LRR architectures of plant R-proteins and metazoan NLRs evolved in independent events. Proc Natl Acad Sci 114:1063–1068PubMedCrossRefGoogle Scholar
  42. Wang B-B, Brendel V (2006) Genomewide comparative analysis of alternative splicing in plants. Proc Natl Acad Sci 103:7175–7180PubMedCrossRefGoogle Scholar
  43. Wang X, Goregaoker SP, Culver JN (2009) Interaction of the tobacco mosaic virus replicase protein with a NAC domain transcription factor is associated with the suppression of systemic host defenses. J Virol 83:9720–9730PubMedPubMedCentralCrossRefGoogle Scholar
  44. Zeier J (2013) New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant Cell Environ 36:2085–2103PubMedCrossRefGoogle Scholar
  45. Zheng Y, Wang Y, Ding B, Fei Z (2017) Comprehensive transcriptome analyses reveal that potato spindle tuber viroid triggers genome-wide changes in alternative splicing, inducible trans-acting activity of phasiRNAs and immune responses. Journal of Virology:JVI:00247–00217Google Scholar
  46. Zurbriggen MD, Carrillo N, Hajirezaei M-R (2010) ROS signaling in the hypersensitive response: when, where and what for? Plant Signal Behav 5:393–396PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Abozar Ghorbani
    • 1
    • 2
    Email author
  • Ahmad Tahmasebi
    • 3
  • Keramatollah Izadpanah
    • 1
  • Alireza Afsharifar
    • 1
  • Ralf G. Dietzgen
    • 2
  1. 1.Plant Virology Research Center, College of AgricultureShiraz UniversityShirazIran
  2. 2.Queensland Alliance for Agriculture and Food InnovationThe University of QueenslandSt. LuciaAustralia
  3. 3.Biotechnology Institute, College of AgricultureShiraz UniversityShirazIran

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