Research in Plant Metabolites

Research in Plant Metabolites

Network topology reveals metabolic resilience of resistant wheat to WSMV under heat stress

Document Type : Original Article

Authors
Farideh Farahbakhsh 1
Habiballah Hamzeh zarghani 2
Zahra Amjadi 3
Mohsen Yassaei 4
Victor Rodriguez grana 5
1 Assistant Professor, Plant Protection Research Department, Fars Agricultural and Natural Resources and Education Center, Agricultural Research, Education, and Extension Organization (AREEO), Darab, Iran.
2 Associate Professor, Plant Protection Department, College of Agriculture, Shiraz University, Shiraz, Iran
3 Plant Protection Department, College of Agriculture, Shiraz University, Shiraz, Iran
4 Agricultural and Horticultural Research Department.Fars Agricultural & Natural Resources Research & Education Center, Shiraz, Iran
5 Group of Genetics, Breeding, and Biochemistry of Brassicas, Misión Biológica de Galicia (MBG-CSIC), Pontevedra, Spain.
10.22034/jrpsm.2025.538860.1085
Abstract
Wheat streak mosaic virus (WMV) from the Potyviridae family is one of the most important viruses infecting wheat in the world and Iran. In this study, metabolic network analysis related to LC-qTOF-MS analysis was investigated in the resistant cultivar Cross Adl 24 hours after inoculation at both optimal (20°C) and high (32°C) temperatures using Metaboanalyst 6.0 software. By measuring the network parameters, it was determined that there were relatively different systemic metabolic responses in the resistant cultivar infected with WSMV at optimal and high temperatures. At optimal temperature, an increase in the expression of nucleotides such as adenine, guanine, and sphingolipids (sphinginine) were observed, which play a role in antiviral defense through the induction of programmed cell death in the accumulation of ROS. On the other hand, a decrease in aromatic amino acids (phenylalanine and tryptophan) was observed, which probably directs carbon sources towards defense pathways. Under high temperature stress, a decrease in number of compounds such as choline (cell membrane destruction at high temperature) and 2-aminobenzoic acid (as virus inhibitor) and an increase in the amino acids proline (increasing plant tolerance to high temperature) and arginine (increasing defense based on RNA silencing and synthesis of proteins related to host stress) occurred. This study showed that resistance to WSMV is the result of precise coordination of multidimensional metabolic networks to combat multiple simultaneous stresses such as pathogens and high temperature. The findings can be used to develop cultivars with sustainable resistance to biotic and abiotic stresses under climate change conditions.
Keywords
Abiotic stress
Biotic stress
Metabolomics
Network analysis
Budzinski, I.G.F., de Moraes, F.E., Cataldi, T.R., Franceschini, L.M., & Labate, C.A. (2019). Network
analyses and data integration of proteomics and metabolomics from leaves of two contrasting varieties of
sugarcane in response to drought. Frontiers in plant science, 10, 1524.
Castro, M.S., & Fontes, W. (2005). Plant defense and antimicrobial peptides. Protein and Peptide letters,
12(1), 11-16.
Chong, J., Soufan, O., Li, C., Caraus, I., Li, S., Bourque, G., Wishart, D.S., & Xia, J. (2018).
MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic acids
research, 46(W1), W486-W494.
Dai, J.M., Zhang, J.D., Liu, X., Zhang, L.F., Wang, J., Xu, Y., Yang, G.Y., Li, J., Chen, M.L. & Hu, Q.F. (2025). Gene editing, metabolomics, network pharmacology strategies to explore terpenoid content and antiTMV activity in NtSPS1 knockout Nicotiana tabacum. Scientific Reports, 15(1), 14581.
Farahbakhsh, F., Hamzehzarghani, H., Massah, A., Tortosa, M., Yassaie, M., & Rodriguez, V.M. (2019).
Comparative metabolomics of temperature sensitive resistance to wheat streak mosaic virus (WSMV) in resistant
and susceptible wheat cultivars. Journal of plant physiology, 237, 30-42.
Graybosch, R. A., Peterson, C. J., Baenziger, P. S., Baltensperger, D. D., Nelson, L. A., Jin, Y., Kolmer,
J., Seabourn, B., French, R., Hein, G., Martin, T. J., Beecher, B., Schwarzacher, T., & Heslop-Harrison, P.
(2009). Registration of ‘Mace’ hard red winter wheat. Journal of Plant Registrations, 3:51–56.
Hassani, F., & Assad, M.T. (2004). Inheritance and allelism of Wheat streak mosaic virus resistance in two
Iranian wheat lines. Euphytica, 140, 213-216.
Hochberg, U., Degu, A., Rachmilevitch, S., Cramer, G.R., & Fait, A. (2013). Water deficit effects on the
molecular processes, physiology and quality of grapevine. In IX International Symposium on Grapevine
Physiology and Biotechnology 1157 (pp. 239-254).
Hu, H., Jia, Y., Hao, Z., Ma, G., Xie, Y., Wang, C., & Ma, D. (2023). Lipidomics-based insights into the
physiological mechanism of wheat in response to heat stress. Plant Physiology and Biochemistry, 205, 108190.
Jiang, T., Hao, T., Chen, W., Li, C., Pang, S., Fu, C., Cheng, J., Zhang, C., Ghorbanpour, M., & Miao,
S. (2025). Reprogrammed plant metabolism during viral infections: mechanisms, pathways and implications.
Molecular Plant Pathology, 26(2):e70066. https://doi.org/10.1111/mpp.70066
Kavi Kishor, P. B., Suravajhala, P., Rathnagiri, P., & Sreenivasulu, N. (2022). Intriguing role of proline
in redox potential conferring high temperature stress tolerance. Frontiers in Plant Science, 13, 867531.
Lehr, P., Hernández-Montes, E., Ludwig-Müller, J., Keller, M., & Zörb, C. (2022). Abscisic acid and
proline are not equivalent markers for heat, drought and combined stress in grapevines. Australian Journal of
Grape and Wine Research 28, 119–130. https://doi.org/10.1111/ajgw.12523.
Liu, G., Ji, Y., Bhuiyan, N.H., Pilot, G., Selvaraj, G., Zou, J., & Wei, Y. (2010). Amino acid homeostasis
modulates salicylic acid–associated redox status and defense responses in Arabidopsis. The Plant Cell, 22(11),
3845-3863.
Liu, Z., You, J., Zhao, P., Wang, X., Sun, S., Wang, X., Gu, S., & Xu, Q. (2025). Metabolomics Profiling
and Advanced Methodologies for Wheat Stress Research. Metabolites, 15(2), 123.
López-Gresa, M.P., Lisón, P., Kim, H.K., Choi, Y.H., Verpoorte, R., Rodrigo, I., Conejero, V., & Bellés,
J.M., (2012). Metabolic fingerprinting of tomato mosaic virus infected Solanum lycopersicum. Journal of plant
physiology, 169(16), 1586-1596.
Mauck, K.E. (2016). Variation in virus effects on host plant phenotypes and insect vector behavior: what can
it teach us about virus evolution?. Current Opinion in Virology 21: 114-123.
Nachappa, P., Haley, S., & Pearce, S. (2021). Resistance to the wheat curl mite and mite-transmitted viruses:
Challenges and future directions. Current Opinion in Insect Science, 45, 21-27.
Nunna, H., Palmer, N.A., Sarath, G., Wegulo, S.N., & Tatineni, S. (2025). Synergistic interaction between
wheat streak mosaic virus and Triticum mosaic virus modulates wheat transcriptome to favor disease
severity. Frontiers in Plant Science, 15, 1504482.
Pang, Z., Lu, Y., Zhou, G., Hui, F., Xu, L., Viau, C., & Xia, J. (2024). MetaboAnalyst 6.0: towards a
unified platform for metabolomics data processing, analysis and interpretation. Nucleic acids research, 52(W1),
W398-W406
Ployet, R., Feng, K., Zhang, J., Baxter, I., Glasgow, D.C., Andrews, H.B., Rodriguez, M., Chen, J.G.,
Tuskan, G.A., Tschaplinski, T.J., & Weston, D.J. (2024). Elemental profiling and genome-wide association
studies reveal genomic variants modulating ionomic composition in Populus trichocarpa leaves. Frontiers in Plant
Science, 15, 1450646.
Sade, D., Shriki, O., Cuadros-Inostroza, A., Tohge, T., Semel, Y., Haviv, Y., Willmitzer, L., Fernie, A.R.,
Czosnek, H. & Brotman, Y. (2015). Comparative metabolomics and transcriptomics of plant response to Tomato
yellow leaf curl virus infection in resistant and susceptible tomato cultivars. Metabolomics, 11(1), 81-97.
Salam, U., Ullah, S., Tang, Z.H., Elateeq, A.A., Khan, Y., Khan, J., Khan, A., & Ali, S. (2023). Plant
metabolomics: an overview of the role of primary and secondary metabolites against different environmental
stress factors. Life, 13(3), 706.
Sanchez, D.H., Pieckenstain, F.L., Escaray, F., Erban, A., Kraemer, U.T.E., Udvardi, M.K., & Kopka,
J. (2011). Comparative ionomics and metabolomics in extremophile and glycophytic Lotus species under salt
stress challenge the metabolic pre‐adaptation hypothesis. Plant, Cell & Environment, 34(4), 605-617.
Schubert, J., Ziegler, A., Rabenstein, F. (2015). First detection of wheat streak mosaic virus in Germany:
molecular and biological characteristics. Archives of virology, 160(7), 1761-1766.
Singh, D.P., Maurya, S., Yerasu, S.R., Bisen, M.S., Farag, M.A., Prabha, R., Shukla, R., Chaturvedi,
K.K., Farooqi, M.S., Srivastava, S., Rai, A., Sarma, B.K., Rai, N., & Behera, T.K. (2023). Metabolomics of
early blight (Alternaria solani) susceptible tomato (Solanum lycopersicum) unfolds key biomarker metabolites
and involved metabolic pathways. Scientific Reports 13, 21023. https://doi.org/10.1038/s41598-023-48269-0
Singh, K., Wegulo, S.N., Skoracka, A., & Kundu, J.K. (2018). Wheat streak mosaic virus: a century old
virus with rising importance worldwide. Molecular Plant Pathology, 19(9), 2193-2206.
Song, J., Xi, X., Qian, X., Li, J., Tao, Y., Li, L., & Zhou, G. (2024). Revealing the microbial composition
changes and relationship with Fusarium caused by rot disease in the Crocus sativus L. Annals of
Microbiology, 74(1), 24.
Soylu, I., Lakshman, D.K., Tatineni, S., Galvez, L.C., & Mitra, A. (2024). Differential regulation of
miRNAs involved in the susceptible and resistance responses of wheat cultivars to wheat streak mosaic virus and
Triticum mosaic virus. BMC genomics, 25(1), 221
Takahashi, Y., Berberich, T., Kanzaki, H., Matsumura, H., Saitoh, H., Kusano, T., & Terauchi, R.
(2009). Unraveling the roles of sphingolipids in plant innate immunity. Plant Signaling & Behavior, 4, 536–
538.
Toubiana, D., Batushansky, A., Tzfadia, O., Scossa, F., Khan, A., Barak, S., Zamir, D., Fernie, A.R.,
Nikoloski, Z., & Fait, A. (2015). Combined correlation‐based network and mQTL analyses efficiently identified
loci for branched‐chain amino acid, serine to threonine, and proline metabolism in tomato seeds. The Plant
Journal, 81(1), 121-133.
Tortosa, M., Cartea, M.E., Rodríguez, V.M., & Velasco, P. (2018). Unraveling the metabolic response of
Brassica oleracea exposed to Xanthomonas campestris pv. campestris. Journal of the Science of Food and
Agriculture, 98(10), pp.3675-3683.
Yang, S.Y., Park, M.R., Kim, I.S., Kim, Y.C., Yang, J.W., & Ryu, C.M. (2011). 2-Aminobenzoic acid
of Bacillus sp. BS107 as an ISR determinant against Pectobacterium carotovorum subsp. carotovotrum SCC1 in
tobacco. European Journal of Plant Pathology, 129, 371–378.
Yassaie, M., Masumi, M., Amin, H., & Izadpanah, K. (2002). Evaluation of wheat streak mosaic virus
response in commercial and native wheat ancestors. In: Proceedings of the 15th Iranian Congress of Plant
Pathology, 52p, University of Razi, Kermanshah, Iran.
Zhang, G., Martin, T. J., Fritz, A. K., Miller, R., Chen, M. S., Bowden, R. L., et al. (2015). Registration
of ‘Oakley CL' wheat. Journal of Plant Registrations, 9, 190–195.
Zhu, Q., Ahmad, A., Shi, C., Tang, Q., Liu, C., Ouyang, B., Deng, Y., Li, F. & Cao, X. (2024). Protein
arginine methyltransferase 6 mediates antiviral immunity in plants. Cell Host & Microbe, 32(9), 1566-1578.
Zhu, X., Gao, P., Zhao, S., Luo, X., Li, L., & Peng, G. (2025). Metabolomic Profiling Identifies Key
Metabolites and Defense Pathways in Rlm1-Mediated Blackleg Resistance in Canola. International Journal of
Molecular Sciences, 26(12), 5627.
Zinati, Z., Assad, M. T., Masumi, M., Alemzadeh, A., Razi, H., & Izadpanah, K. (2012). The effect of
high temperature treatment on Wheat streak mosaic virus resistance and certain resistance-related chemicals in
bread wheat. Iranian Journal of Virology, 6, 27-35.