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Gene expression changes in tomato during symptom development in response to leaf curl virus infection

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Abstract

During stress conditions, plant gene expression changes to cope up with the altered environment. The reprogramming of gene expression during viral infections is to be accounted towards host adaptation to the invading virus by developing defense mechanism. As a consequence of restructured gene expression, plant’s physiology gets affected and is evident in the form of symptoms. In the present study, Tomato leaf curl New Delhi virus (ToLCNDV) has been used as model system for the study of altered expression of genes in tomato during symptom development using microarray. Gene expression profiles were monitored in leaf tissues during symptom development in Solanum lycopersicum. To explore the differential expression analysis, tomato cDNA gene chip arrays have been used with 26,173 protein-coding genes. A total of 920 differentially expressed genes in response to ToLCNDV were identified in tomato. KEGG pathway analysis of these genes categorizes 652 differentially expressed genes into 77 known pathways, mostly related to increasing respiration rate, decreasing rate of photosynthesis, accumulation of soluble sugars/starch and results in elevated levels of amino acid synthesis. The possible role of these changes in altering host physiology, developed in the form of symptoms has been discussed.

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Abbreviations

ROS:

Reactive oxygen species

AOX:

Alternative oxidase

JA:

Jasmonic acid

SA:

Salicylic acid

ET:

Ethylene

References

  • Agudelo-Romero P, Carbonell P, de la Iglesia F, Carrera J, Rodrigo G, Jaramillo A, Perez-Amador MA, Elena SF (2008) Changes in the gene expression profile of Arabidopsis thaliana after infection with tobacco etch virus. Virol J 5:92

    Article  PubMed Central  PubMed  Google Scholar 

  • Amirsadeghi S, Robson CA, Vanlerberghe GC (2007) The role of the mitochondrion in plant responses to biotic stress. Physiol Plant 129:253–266

    Article  CAS  Google Scholar 

  • Arias MC, Luna C, Rodriguez M, Lenardon S, Taleisnik E (2005) Sunflower chlorotic mottle virus in compatible interactions with sunflower: ROS generation and antioxidant response. Eur J Plant Pathol 113:223–232

    Article  CAS  Google Scholar 

  • Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  PubMed  Google Scholar 

  • Babu M, Griffiths JS, Huang TS, Wang A (2008) Altered gene expression changes in Arabidopsis leaf tissues and protoplasts in response to plum pox virus infection. BMC Genomics 9:325

    Article  PubMed Central  PubMed  Google Scholar 

  • Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: relations between plant primary metabolism and plant-pathogen-interactions. J Exp Bot 58:4019–4026

    Article  CAS  PubMed  Google Scholar 

  • Bilgin D, Zavala J, Zhu J, Clough S, Ort D, DeLucia E (2010) Biotic stress globally down regulates photosynthesis genes. Plant Cell Environ 33:1597–1613

    Article  CAS  PubMed  Google Scholar 

  • Clarke S, Guy P, Burritt D, Jameson P (2002) Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment. Physiol Plant 114:157–164

    Article  CAS  PubMed  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinform 21:3674–3676

    Article  CAS  Google Scholar 

  • Culver JN, Padmanabhan MS (2007) Virus-induced disease: altering host physiology one interaction at a time. Annu Rev Phytopathol 45:221–43

    Article  CAS  PubMed  Google Scholar 

  • Del Río L, Pastori G, Palma J, Sandalio L, Sevilla F, Corpas F, Jiménez A, López-Huertas E, Hernández J (1998) The activated oxygen role of peroxisomes in senescence. Plant Physiol 116:1195–1200

  • Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1:316–323

    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  CAS  PubMed Central  PubMed  Google Scholar 

  • Espinoza C, Medina C, Somerville S, Arce-Johnson P (2007) Senescence-associated genes induced during compatible viral interactions with grapevine and Arabidopsis. J Exp Bot 58:3197–3212

    Article  CAS  PubMed  Google Scholar 

  • Golem S, Culver JN (2003) Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana. Mol Plant Microbe Interact 16:681–688

    Article  CAS  PubMed  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hanssen IM, Peter EH, Ballester AR, Hogewoning SW, Parra NO (2011) Differential tomato transcriptomic responses induced by pepino mosaic virus isolates with differential aggressiveness. Plant Physiol 156:301–318

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jia MA, Li Y, Lei L, Di D, Miao H, Fan Z (2012) Alteration of gene expression profile in maize infected with a double-stranded RNA fijivirus associated with symptom development. Mol Plant Pathol 13:251–262

    Article  CAS  PubMed  Google Scholar 

  • Jyothsna P, Haq QMI, Priyanka S, Sumiya KV, Shelly P, Ramaveer R, Rob W, Briddon WB, Malathi VG (2013) Infection of Tomato leaf curl New Delhi virus tomato leaf curl new Delhi virus (ToLCNDV), a bipartite begomovirus with betasatellites results in enhanced level of helper virus components and antagonistic interaction between DNA B and betasatellites. Appl Microbiol Biot 97(12):5457–5471

    Article  CAS  Google Scholar 

  • Kazan K, Manners JM (2009) Linking development to defense: auxin in plant–pathogen interactions. Trends Plant Sci 14(7):373–384

    Article  CAS  PubMed  Google Scholar 

  • Kyseláková H, Prokopová J, NauˇsNaus J, Novák O, Navrátil M, Safáˇrová D, Spundová M, Ilík P (2011) Photosynthetic alterations of pea leaves infected systemically by Pea enation mosaic virus: a coordinated decrease in efficiencies of CO2 assimilation and photosystem II photochemistry. Plant Physiol Biochem 49:1279–1289

    Article  PubMed  Google Scholar 

  • Lambers H (1982) Cyanide-resistant respiration: a non-phosphorylating electron pathway acting as an energy overflow. Physiol Plant 55:478–485

    Article  CAS  Google Scholar 

  • Lu J, Du ZX, Kong J, Chen LN, Qiu YH, Li GF, Meng XH, Zhu SF (2012) Transcriptome analysis of nicotiana tabacum infected by cucumber mosaic virus during systemic symptom development. PLoS One 7(8):e43447

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mandadi KK, Scholthof KBG (2012) Characterization of a viral synergism in the monocot brachypodium distachyon reveals distinctly altered host molecular processes associated with disease. Plant Physiol 160:1432–1452

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marathe R, Guan Z, Anandalakshmi R, Zhao H, Dinesh-Kumar SP (2004) Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Mol Biol 55:501–520

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwerab S, Gollerya M, Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18:2929–2945

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nooden LD (2004) Introduction. In: Nooden LD (ed). Plant Cell Death Processes. Elsevier, Amsterdam, pp 1–18

  • Padmanabhan MS, Shiferaw H, Culver JN (2006) The tobacco mosaic virus replicase protein disrupts the localization and function of interacting Aux/IAA proteins. Mol Plant-Microbe Interact 19:864–873

    Article  CAS  PubMed  Google Scholar 

  • Pallas V, García JA (2011) How do plant viruses induce disease? interactions and interference with host components. J Gen Virol 92:2691–2705

    Article  CAS  PubMed  Google Scholar 

  • Pieterse CM, Van Loon LC (1999) Salicylic acid-independent plant defense pathways. Trends Plant Sci 4(2):52–58

    Article  PubMed  Google Scholar 

  • Riedle-Bauer M (2000) Role of reactive oxygen species and antioxidant enzymes in systemic virus infections of plants. J Phytopathol 148:297–302

    Article  CAS  Google Scholar 

  • Schoelz JE, Harries PA, Nelson RS (2011) Intracellular transport of plant viruses: finding the door out of the cell. Mol Plant 4:813–831

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Trinidad J, Ascencio I, Rosangela S, Lee TJ, Chu TM, Russell DW, Cella R, Linda HB (2008) Global analysis of arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 148:1436–454

    Article  Google Scholar 

  • Whitham SA, Quan S, Chang HS, Cooper B, Estes B (2003) Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J 33:271–283

  • Yuan GS, Zhang ZM, Xiang K, Zhao MJ, Shen YO, Pan GT (2012) Large-scale identification of differentially expressed genes in maize inbreds susceptible and resistant to fusarium ear rot. Plant Omics J 5:471–475

    CAS  Google Scholar 

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Acknowledgments

This work was supported by ICAR funding under NPTC project on transgenic tomato. We are also thankful to Department of Biotechnology, Government of India for providing fellowship to Harpreet Kaur and C.B. Yadav.

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Correspondence to Shelly Praveen.

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Harpreet Kaur and Chandra Bhan Yadav contributed equally

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Kaur, H., Yadav, C.B., Alatar, A.A. et al. Gene expression changes in tomato during symptom development in response to leaf curl virus infection. J. Plant Biochem. Biotechnol. 24, 347–354 (2015). https://doi.org/10.1007/s13562-014-0280-8

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