Please wait a minute...
Journal of Integrative Agriculture  2023, Vol. 22 Issue (8): 2426-2440    DOI: 10.1016/j.jia.2023.02.032
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
Characterization of volatile organic compounds in grafted tomato plants upon potyvirus necrotic infection
Roberta SPANÒ1, Mariarosaria MASTROCHIRICO1, Francesco LONGOBARDI2#, Salvatore#br# CERVELLIERI3, Vincenzo LIPPOLIS3, Tiziana MASCIA1#

1 Department of Soil, Plant and Food Sciences, University of Bari “Aldo Moro”, Via Amendola 165/A, Bari 70126, Italy

2 Department of Chemistry, University of Bari “Aldo Moro”, Via Orabona 4, Bari 70126, Italy

3 National Research Council (CNR), Institute of Sciences of Food Production (ISPA), Via Amendola 122/O, Bari 70126, Italy

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  

A headspace solid-phase microextraction-gas chromatography-mass spectrometry (HS-SPME/GC-MS) method was used to study the volatile organic compounds (VOCs) associated with the differential immune response of tomato plants infected with the recombinant strain of potato virus Y (PVYC-to), necrogenic to tomato.  Analysis was carried out in UC82 (UC), a virus susceptible tomato variety, comparing the same UC plants grafted or not onto a virus tolerant tomato ecotype, Manduria (Ma); the three types of samples used for the GC-MS analysis were mock-inoculated UC/Ma plants, UC/Ma+PVYC-to and UC+PVYC-to plants; the VOCs obtained were 111.  Results from symptomatic PVYC-to-infected UC plants showed a VOCs composition enriched in alcohols, fatty acid derivates, benzenoids, and salicylic acid derivatives, while in mock-inoculated UC/Ma plants VOCs were mainly characterized by methyl ester compounds.  The VOC profile was in line with RNAseq data analyses, denoting that PVYC-to viral RNA accumulation and disease symptoms induce the specific transcriptional activation of genes involved in VOCs biosynthesis.  Furthermore, principal component analysis highlighted that VOCs of PVYC-to-infected and mock-inoculated grafted plants were much closer each other than that of symptomatic PVYC-to-infected non-grafted UC plants.  These results suggest that VOCs profiles of tomato plants are related to the viral RNA accumulation, disease intensity and graft-derived tolerance to PVYC-to infection.

Keywords:  tomato        potyvirus        VOCs        defense        grafted plants  
Received: 01 September 2022   Accepted: 26 January 2023
Fund: 

This study was carried out within the Agritech National Research Center, Italy, and received funding from the European Union NextGenerationEU (PIANO NAZIONALE DI RIPRESA E RESILIENZA (PNRR) – MISSIONE 4 COMPONENTE 2, INVESTIMENTO 1.4 – D.D. 1032 17/06/2022, CN00000022). 

About author:  Roberta SPANÒ, E-mail: roberta.spano@uniba.it; #Correspondence Francesco LONGOBARDI, Tel: +39-0805442042, E-mail: francesco.longobardi@uniba.it; Tiziana MASCIA, Tel: +39-0805442913, E-mail: tiziana.mascia@uniba.it

Cite this article: 

Roberta SPANÒ, Mariarosaria MASTROCHIRICO, Francesco LONGOBARDI, Salvatore CERVELLIERI, Vincenzo LIPPOLIS, Tiziana MASCIA. 2023. Characterization of volatile organic compounds in grafted tomato plants upon potyvirus necrotic infection. Journal of Integrative Agriculture, 22(8): 2426-2440.

Ament K, Krasikov V, Allmann S, Rep M, Takken F L W, Schuurink R C. 2010. Methyl salicylate production in tomato affects biotic interactions. The Plant Journal, 62, 124–134.

Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology, 11, R106.

Battaglia D, Bossi S, Cascone P, Digilio M C, Prieto J D, Fanti P, Guerrieri E, Iodice L, Lingua G, Lorito M, Maffei M E, Massa N, Ruocco M, Sasso R, Trotta V. 2013. Tomato below ground–above ground interactions: Trichoderma longibrachiatum affects the performance of Macrosiphum euphorbiae and its natural antagonists. Molecular Plant-Microbe Interactions, 26, 1249–1256.

Beck J J, Merrill G B, Higbee B S, Light D M, Gee W S. 2009. In situ seasonal study of the volatile production of almonds (Prunus dulcis) var. ‘Nonpareil’ and relationship to navel orangeworm. Journal of Agricultural and Food Chemistry, 57(9), 3749–3753.

Beck J J, Smith L, Merrill G B. 2008. In situ volatile collection, analysis, and comparison of three Centaurea species and their relationship to biocontrol with herbivorous insects. Journal of Agricultural and Food Chemistry, 56(8), 2759–2764.

Bellés J M, Pilar López-Gresa M, Fayos J, Pallás V, Rodrigo I, Conejero V. 2008. Induction of cinnamate 4-hydroxylase and phenylpropanoids in virus-infected cucumber and melon plants. Plant Science, 174(5), 524–533.

Carr J P, Murphy A M, Tungadi T, Yoon J-Y. 2019. Plant defense signals: Players and pawns in plant-virus-vector interactions. Plant Science, 279, 87–95.

Croft K P C, Juttner F, Slusarenko A J. 1993. Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiology, 101(1), 13–24.

De Vos M, Jander G. 2010. Volatile communication in plant–aphid interactions. Current Opinion in Plant Biology, 13(4), 366–371.

Deng H, Zhang Y, Reuss L, Suh J H, Yu Q, Liang G, Wang Y, Gmitter Jr F G. 2021 Comparative leaf volatile profiles of two contrasting mandarin cultivars against candidatus liberibacter asiaticus infection illustrate huanglongbing tolerance mechanisms. Journal of Agricultural and Food Chemistry, 69(37), 10869–10884.

Dicke M, Baldwin I T. 2010. The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science, 15(3), 167–175.

Dong X, Sun L, Maker G, Ren Y, Yu X. 2022. Ozone treatment increases the release of voc from barley, which modifies seed germination. Journal of Agricultural and Food Chemistry, 70(10), 3127–3135.

Eigenbrode S D, Bosque-Pérez N A, Davis T S. 2018. Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annual Review of Entomology, 63, 169–191.

Erb M, Meldau S, Howe G A. 2012. Role of phytohormones in insect-specific plant reactions. Trends in Plant Science, 17(5), 250–259.

Gadhave K R, Gautam S, Rasmussen D A, Srinivasan R. 2020. Aphid transmission of Potyvirus: the largest plant-infecting RNA virus genus. Viruses, 12(7), 773.

Gaion L A, Braz L T, Carvalho R F. 2018. Grafting in vegetable crops: A great technique for Agriculture. International Journal of Vegetable Science, 24, 85–102.

Gargallo-Garriga A, Sardans J, Pérez-Trujillo M, Rivas-Ubach A, Oravec M, Vecerova K, Urban O, Jentsch A, Kreyling J, Beierkuhnlein C, Parella T, Peñuelas J. 2014. Opposite metabolic responses of shoots and roots to drought. Scientific Reports, 4(1), 1–17.

Groen S C, Jiang S, Murphy A M, Cunniffe N J, Westwood J H, Davey M P, Bruce T J A, Caulfield J C, Furzer O J, Reed A, Robinson S I, Miller E, Davis C N, Pickett J A, Whitney H M; Glover B J, Carr J P. 2016. Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts? PLOS Pathogens, 12(8), e1005790.

Heiden A C, Kobel K, Langebartels C, Schuh-Thomas G, Wildt J. 2003. Emissions of oxygenated volatile organic compounds from plants part i: emissions from lipoxygenase activity. Journal of Atmospheric Chemistry, 45(2), 143–172.

Howe G A, Jander G. 2018. Plant Immunity to Insect Herbivores. Annual Review of Plant Biology, 59, 41–66.

Hull R. 2014. In: Hull R ed., Plant Virology, 5th edn, Academic Press, London, UK.

Kim D, Langmead B, Salzberg S L. 2015. HISAT: a fast spliced aligner with low memory requirements. Nature Methods, 12, 357–360.

Knudsen G K, Norli H R, Tasin M. 2017. The ratio between field attractive and background volatiles encodes host-plant recognition in a specialist moth. Frontiers in Plant Science, 8, 2206.

Kørner J, Pitzalis N, Peña E J, Erhardt M, Vazquez F, Heinlein M. 2018. Crosstalk between PTGS and TGS pathways in natural antiviral immunityand disease recovery. Nature Plants, 4, 157–164.

Kumar S, Bharti N, Saravaiya S N. 2018. Vegetable grafting: a surgical approach to combat biotic and abiotic stresses: A review. Agricultural Reviews, 39(1), 1–11.

Langmead B, Trapnell C, Pop M, Salzberg S L. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, 1–10.

Lin Y, Huang J, Akutse K, Hou Y. 2022. Phytopathogens increase the preference of insect vectors to volatiles emitted by healthy host plants. Journal of Agricultural and Food Chemistry, 70(16), 5262–5269.

López-Berenguer C, Donaire L, González-Ibeas D, Gómez-Aix C, Truniger V, Pechar G S, Aranda M A. 2021. Virus-infected melon plants emit volatiles that induce gene deregulation in neighboring healthy plants. Phytopathology, 111(5), 862–869.

Mariutto M, Duby F, Adam A, Bureau C, Fauconnier M-L, Ongena M, Thonart P, Dommes J. 2011. The elicitation of a systemic resistance by Pseudomonas putida BTP1 in tomato involves the stimulation of two lipoxygenase isoforms. BMC Plant Biology, 11(1), 1–15.

Mascia T, Finetti-Sialer M M, Cillo F, Gallitelli D. 2010a, Biological and molecular characterization of a recombinant isolate of Potato virus Y associated with a tomato necrotic disease occurring in Italy. Journal of Plant Pathology, 9, 131–138.

Mascia T, Santovito E, Gallitelli D, Cillo F. 2010b Evaluation of reference genes for quantitative reverse‐transcription polymerase chain reaction normalization in infected tomato plants. Molecular Plant Pathology, 11(6), 805–816.

Mauck K E, Bosque-Pérez N A, Eigenbrode S D, De Moraes C, Mescher M C. 2012.Transmission mechanisms shape pathogen effects on host–vector interactions: evidence from plant viruses. Functional Ecology, 26(5), 1162–1175.

Minutillo S A, Mascia T, Gallitelli D. 2012. A DNA probe mix for the multiplex detection of ten artichoke viruses. European Journal of Plant Pathology, 134(3), 459–465.

Mudge K, Janick J, Scofield S, Goldschmidt E E. 2009. A History of Grafting, In: J. Janick ed., Horticultural Reviews. John Wiley & Sons, Inc., NY, USA, 35, 437–93.

Niinemets U, Kännaste A, Copolovici L. 2013. Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage. Frontiers in Plant Science, 4, 262.

Prost I, Dhondt S, Rothe G, Vicente J, Rodriguez M J, Kift N, Carbonne F, Griffiths G, Esquerré-Tugayé M-T, Rosahl S, Castresana C, Hamberg M, Fournier J. 2005. Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiology, 139(4), 1902–1913.

Scholthof K B G, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P, Hemenway C, Foster G D. 2011. Top 10 plant viruses in molecular plant pathology. Molecular Plant Pathology, 12, 938–954.

Sharma R, Zhou M, Hunter M D, Fan X. 2019. Rapid in situ analysis of plant emission for disease diagnosis using a portable gas chromatography device. Journal of Agricultural and Food Chemistry, 67(26), 7530–7537.

Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J. 2006a. Changing green leaf volatile biosynthesis in plants: An approach for improving plant resistance against both herbivores and pathogens. Proceedings of the National Academy of Sciences of the United States of America, 103(45), 16672–16676.

Shiojiri K, Ozawa R, Matsui K, Kishimoto K, Kugimiya S, Takabayashi J. 2006b. Role of the lipoxygenase/lyase pathway of host-food plants in the host searching behaviour of two parasitoid species, Cotesia glomerata and Cotesia plutellae. Journal of Chemical Ecology, 32, 969–979.

Spanò R, Ferrara M, Gallitelli D, Mascia T. 2020a. The Role of grafting in the resistance of tomato to viruse. Plants, 9(8), 1042–1062.

Spanò R, Ferrara M, Montemurro C, Mulè G, Gallitelli D, Mascia T. 2020b. Grafting alters tomato transcriptome and enhances tolerance to an airborne virus infection. Scientific Reports, 10(1), 1–13.

Spanò R, Mascia T, Kormelink R, Gallitelli D. 2015. Grafting on a non-transgenic tolerant tomato variety confers resistance to the infection of a Sw5- breaking strain of tomato spotted wilt virus via RNA silencing. PLOS ONE, 10(10), e0141319.

Wei J, Yan L, Ren QIN, Li C, Ge F, Kang L E. 2013. Antagonism between herbivore-induced plant volatiles and trichomes affects tritrophic interactions. Plant, Cell & Environment, 36(2), 315–327.

Wylie S J, Adams M, Chalam C, Kreuze J, López-Moya J J, Ohshima K, Praveen S, Rabenstein F, Stenger D, Wang A, Zerbini F M, Ictv Report Consortium. 2017. ICTV Virus Taxonomy Profile: Potyviridae. Journal of General Virology, 98(3),352–354.

Zellner B D, Bicchi C, Dugo P, Rubiolo P, Dugo G, Mondello L. 2008. Linear retention indices in gas chromatographic analysis: a review. Flavour and Fragrance Journal, 23, 297–314.

[1] XIAO Yang-yang, QIAN Jia-jia, HOU Xing-liang, ZENG Lan-ting, LIU Xu, MEI Guo-guo, LIAO Yin-yin.

Diurnal emission of herbivore-induced (Z)-3-hexenyl acetate and allo-ocimene activates sweet potato defense responses to sweet potato weevils [J]. >Journal of Integrative Agriculture, 2023, 22(6): 1782-1796.

[2] ZHAO Ting-ting, WANG Zi-yu, BAO Yu-fang, ZHANG Xiao-chun, YANG Huan-huan, ZHANG Dong-ye, JIANG Jing-bin, ZHANG He, LI Jing-fu, CHEN Qing-shan, XU Xiang-yang. Downregulation of SL-ZH13 transcription factor gene expression decreases drought tolerance of tomato[J]. >Journal of Integrative Agriculture, 2019, 18(7): 1579-1586.
[3] HAN Xue-yuan, MAO Lin-chun, LU Wen-jing, TAO Xiao-ya, WEI Xiao-peng, LUO Zi-sheng. Abscisic acid induces differential expression of genes involved in wound-induced suberization in postharvest tomato fruit[J]. >Journal of Integrative Agriculture, 2018, 17(12): 2670-2682.
No Suggested Reading articles found!