Abstract
The ‘adaptive host manipulation’ hypothesis predicts that parasites can enhance their transmission rates via manipulation of their host’s phenotype. For example, many plant pathogens alter the nutritional quality of their host for herbivores that serve as their vectors. However, herbivores, including non-vectors, might cause additional alterations in the plant phenotype. Here, we studied changes in the amino acid (AA) content in the phloem of chilli (Capsicum annuum) plants infected with Pepper golden mosaic virus (PepGMV) upon subsequent colonization with a non-vector, the phloem-feeding whitefly (Trialeurodes vaporariorum). Virus infection alone caused an almost 30-fold increase in overall phloem AAs, but colonization by T. vaporariorum completely reversed this effect. At the level of individual AAs, contents of proline, tyrosine, and valine increased, and histidine and alanine decreased in PepGMV -infected as compared to control plants, whereas colonization by T. vaporariorum caused decreased contents of proline, tyrosine, and valine, and increased contents of histidine and alanine. Overall, the colonization by the whitefly had much stronger effects on phloem AA composition than virus infection. We conclude that the phloem composition of a virus-infected host plant can rapidly change upon arrival of an herbivore and that these changes need to be monitored to predict the nutritional quality of the plant in the long run.
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References
Ángeles-López YI, Martínez-Gallardo NA, Ramírez-Romero R, López MG, Sánchez-Hernández C, Délano-Frier JP (2012) Cross-kingdom effects of plant-plant signaling via volatile organic compounds emitted by tomato (Solanum lycopersicum) plants infested by the greenhouse whitefly (Trialeurodes vaporariorum. J Chem Ecol 38:1376–1386
Carrillo-Tripp J, Lozoya-Gloria E, Rivera-Bustamante RF (2007) Symptom remission and specific resistance of pepper plants after infection by Pepper golden mosaic virus. Phytopathology 97:51–59.
Deeken R, Ache P, Kajahn I, Klinkenberg J, Bringmann G, Hedrich R (2008) Identification of Arabidopsis thaliana phloem RNAs provides a search criterion for phloem-based transcripts hidden in complex datasets of microarray experiments. Plant J 55:746–759
Garzón-Tiznado A, Torres-Pacheco I, Ascencio-Ibañez JT, Herrera-Estrella L, Rivera-Bustamante RF (1993) Inoculation of peppers with infectious clones of a new Geminivirus by a biolistic procedure. Phytopathology 83:514–521.
Jones DR (2003) Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109:195–219
Luan J-B, Yao D-M, Zhang T, Walling LL, Yang M, Wang Y-J, Liu S-S (2013) Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors. Ecol Lett 16:390–398
Mauck K, Bosque-Perez NA, Eigenbrode SD, De Moraes CM, Mescher MC (2012) Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses. Funct Ecol 26:1162–1175
Wang J, Bing X-L, Li M, Ye G-Y, Liu S-S (2012) Infection of tobacco plants by a begomovirus improves nutritional assimilation by a whitefly. Entomol Exp Appl 144:191–201
Weinersmith K, Faulkes Z (2014) Parasitic manipulation of hosts’ phenotype, or how to make a zombie - an introduction to the symposium. Integrat Compar. Biol 54:93–100
Yang J-W, Yi H-S, Kim H, Lee B, Lee S, Ghim S-Y, Ryu C-M (2011) Whitefly infestation of pepper plants elicits defence responses against bacterial pathogens in leaves and roots and changes the below-ground microflora. J Ecol 99:46–56
Zhao S, Guo Y, Sheng Q, Shyr Y (2014) Advanced heat map and clustering analysis using heatmap3. BioMed Res Int. doi:10.1155/2014/986048
Acknowledgments
We thank Dr. Guadalupe Peña Chora (Universidad Autónoma del Estado de Morelos) for donating the whiteflies, two anonymous referees for highly constructive comments on an earlier version of our manuscript, and CONACyT de México for financial support (grants no. 130656 and 172607 to MH, grant no. 239819 to YIAL).
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Ángeles-López, Y.I., Rivera-Bustamante, R.F. & Heil, M. Colonization by Phloem-Feeding Herbivore Overrides Effects of Plant Virus on Amino Acid Composition in Phloem of Chili Plants. J Chem Ecol 42, 985–988 (2016). https://doi.org/10.1007/s10886-016-0747-2
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DOI: https://doi.org/10.1007/s10886-016-0747-2