ORIGINAL ARTICLE
Effect of disease prevalence and growth stage on symptom severity in the Turnip mosaic virus – Arabidopsis thaliana pathosystem
More details
Hide details
1
Instituto de Biología Integrativa de Sistemas (I2SysBio), CSIC-Universitat de València, CL. Catedrático Agustín Escardino Belloch 9, Paterna, 46980 València, Spain
2
Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
Submission date: 2023-02-23
Acceptance date: 2023-04-23
Online publication date: 2023-08-02
Corresponding author
Santiago F. Elena
Instituto de Biología Integrativa de Sistemas (I2SysBio), CSIC-Universitat de València, CL.
Catedrático Agustín Escardino Belloch 9, Paterna, 46980 València, Spain
Journal of Plant Protection Research 2023;63(3):297-305
HIGHLIGHTS
- Plants use chemical cues to communicate their infection status.
- High disease prevalence reduces the development of symptoms among receiver plants.
- The protective community effect is stronger for juvenile plants.
- JA is a candidate for volatile chemical messenger in the TuMV - A. thaliana pathosystem.
- Root communication also contributes to minimize the impact of infection in receiver plants.
KEYWORDS
TOPICS
ABSTRACT
In response to stresses, plants are capable of communicating their physiological status to
other individuals in the community using several chemical cues. Nearby receivers then adjust
their own homeostasis to increase resilience. The majority of studies to date have concentrated
on the communication of abiotic stressors (e.g., salinity or drought) or herbivory.
Less attention has been paid to the role of communication during microbial infections and
almost nothing has focused on viruses. Here we investigated the effect that the prevalence
of a turnip mosaic virus in a community of Arabidopsis thaliana has on the severity of
symptoms developed in a group of receivers. First, we looked at the influence of two factors
on the kinetics of symptom progression in the receivers, namely the prevalence of infection
among emitters and the growth stage of the receiver plants at inoculation. We found that
young receiver plants developed milder symptoms than older ones, and that high infection
prevalence resulted in slower disease progression in receivers. Second, we tested the possibility
that jasmonates could act as chemical signaling cues. To do this, we examined the
kinetics of symptom progression in jasmonate-insensitive and wild-type plants. The results
showed that the protective effect vanished in the mutant plants. Third, we investigated the
possibility that root communication could also be relevant. We found that the kinetics of
symptom progression across receivers was further slowed down in an age-dependent manner
when plants were planted in the same pot. Together, these preliminary findings point to
a potential function for disease prevalence in plant communities in regulating the severity
of symptoms, this effect being mediated by some volatile organic compounds.
RESPONSIBLE EDITOR
Natasza Borodynko-Filas
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
REFERENCES (48)
1.
Babikova Z., Gilbert L., Bruce T.J., Bikett M., Caulfield J.C., Woodcock C., Pickett J.A., Johnson D. 2013. Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecology Letters 16 (7): 835–843. DOI:
https://doi.org/10.1111/ele.12....
2.
Baldwin I.T., Schultz J.C. 1983. Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 221 (4607): 277–279. DOI: https:/doi.org/10.1126/science.221.4607.277.
3.
Betti F., Ladera-Carmona M.J., Weits D.A., Ferri G., Iacopino S., Novi G., Svezia B., Kunkowska A.B., Santaniello A., Piaggesi A., Loreti E., Perata P. 2021. Exogenous miRNA induces post-transcriptional gene silencing in plants. Nature Plants 7 (11): 1379–1388. DOI:
https://doi.org/10.1038/s41477....
4.
Bitas V., Kim H.S., Bennett J.W., Kang S. 2013. Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Molecular Plant-Microbe Interactions 26 (8): 835–843. DOI:
https://doi.org/10.1094/MPMI-1....
5.
Boyes D.C., Zayed A.M., Ascenzi R., McCaskill A.J., Hoffman N.E., Davis K.R., Görlach J. 2001. Growth stagebased phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13 (7): 1499–1510. DOI:
https://doi.org/10.1105/tpc.01....
6.
Brosset A., Blande J.D. 2022. Volatile-mediated plant-plant interactions: volatile organic compounds as modulators of receiver plant defence, growth, and reproduction. Journal of Experimental Botany 73 (2): 511–528. DOI:
https://doi.org/10.1093/jxb/er....
7.
Butković A., González R., Rivarez M.P.S., Elena S.F. 2021. A genome-wide association study identifies Arabidopsis thaliana genes that contribute to differences in the outcome of infection with two turnip mosaic potyvirus strains that differ in their evolutionary history and degree of host specialization. Virus Evolution 7 (2): veab063. DOI:
https://doi.org/10.1093/ve/vea....
8.
Chen C.C., Chao C.H., Chen C.C., Yeh S.D., Tsai H.T., Chang C.A. 2003. Identification of turnip mosaic virus isolates causing yellow stripe and spot on calla lily. Plant Disease 87 (8): 901–905. DOI:
https://doi.org/PDIS.2003.87.8....
9.
Cohen J. 1973. Eta-squared and partial eta-squared in fixed factor ANOVA designs. Educational and Phsychological Measurement 33 (1): 107–112. DOI:
https://doi.org/10.1177/001316....
10.
Corrêa R.L., Sanz-Carbonell A., Kogej Z., Müller S.Y., Ambrós S., López-Gomollón S., Gómez G., Baulcombe D.C., Elena S.F. 2020. Viral fitness determines the magnitude of transcriptomic and epigenomic reprograming of defense responses. Molecular Biology and Evolution 13 (7): 1866–1881. DOI:
https://doi.org/10.1093/molbev....
11.
Craufurd P.Q., Wheeler T.R. 2009. Climate change and the flowering time of annual crops. Journal of Experimental Botany 60 (9): 2529–2539. DOI:
https://doi.org/10.1093/jxb/er....
12.
Dolch R., Tscharntke T. 2000. Defoliation of alders (Alnus glutinosa) affects herbivory by leaf beetles on undamaged neighbours. Oecologia 125 (4): 504–511. DOI:
https://doi.org/10.1007/s00442....
13.
Falik O., Mauda S., Novoplansky A. 2023. The ecological implications of interplant drought cuing. Journal of Ecology 111 (1): 23–32. DOI:
https://doi.org/10.1111/1365-2....
14.
Gao S., Dai X., Wang L., Perra N., Wang Z. 2022. Epidemic spreading in metapopulation networks coupled with awareness propagation. IEEE Transactions on Cybernetics : 1–13. DOI:
https://doi.org/10.1109/TCYB.2....
15.
García-Ruiz H., Murphy J.F. 2001. Age-related resistance in bell pepper to cucumber mosaic virus. Annals of Applied Biology 139 (3): 307–317. DOI:
https://doi.org/10.1111/j.1744....
16.
Ghosh S., Didi-Cohen S., Cna’ani A., Kontsedalov S., Lebedev G., Tzin V., Ghanim M. 2022. Comparative analysis of volatiles emitted from tomato and pepper plants in response to infection by two whitefly-transmitted persistent viruses. Insects 13 (9): 840. DOI:
https://doi.org/10.3390/insect....
18.
Glazebrook J. 2005. Contrasting mechanisms of deffense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43: 205–227. DOI:
https://doi.org/10.1146/annure....
19.
González R., Butković A., Elena S.F. 2019. Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus. Virus Evolution 5 (2): vez024.DOI:
https://doi.org/10.1093/ve/vez....
20.
Granell C., Gómez S., Arenas A. 2013. Dynamical interplay between awareness and epidemic spreading in multiplex networks. Physical Review Letters 111 (12): 128701. DOI:
https://doi.org/10.1103/PhysRe....
22.
Hammerbacher A., Coutinho T.A., Gershenzon J. 2019. Roles of plant volatiles in defence against microbial pathogens and microbial exploitation of volatiles. Plant Cell and Environment 42 (10): 2827–2843. DOI:
https://doi.org/10.1111/pce.13....
24.
Huang Y., Hong H., Xu M., Yan J., Dai J., Wu J., Feng Z., Zhu M., Zhang Z., Yuan X., Ding X., Tao X. 2020. Developmentally regulated Arabidopsis thaliana susceptibility to tomato spotted wilt virus infection. Molecular Plant Pathology 21 (7): 985–998. DOI:
https://doi.org/10.1111/mpp.12....
25.
Islam W., Naveed H., Zaynab M., Huang Z., Chen H.Y.H. 2019. Plant defense against virus diseases; growth hormones in highlights. Plant Signaling & Behavior 14 (6): e15967189. DOI:
https://doi.org/10.1080/155923....
26.
Kus J.V., Zaton K., Sarkar R., Cameron R.K. 2002. Age-related resistance in Arabidopsis is a developmentally regulated defense response to Pseudomonas syringae. Plant Cell 14 (2): 479–490. DOI:
https://doi.org/10.1105/tpc.01....
27.
Laurie-Berry N., Joardar V., Street I.H., Kunkel B.N. 2006. The Arabidopsis thaliana jasmonate insensitive 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Molecular Plant Microbe Interactions 19 (7): 789–800. DOI:
https://doi.org/10.1094/MPMI-1....
28.
Lee K., Seo P.J. 2014. Airborne signals from salt-stressed Arabidopsis plants trigger salinity tolerance in neighboring plants. Plant Signaling and Behavior 9 (1): e28392. DOI:
https://doi.org/10.4161/psb.28....
29.
Levy D., Lapidot M. 2008. Effect of plant age at inoculation on expression of gene resistance to tomato yellow leaf curl virus. Archives of Virology 153 (1): 171–179. DOI:
https://doi.org/10.1007/s00705....
30.
Li T., Xiao Y. 2021. Linking the disease transmission to information dissemination dynamics: an insight from a multi-scale model study. Journal of Theoretical Biology 526: 110796. DOI:
https://doi.org/10.1016/j.jtbi....
32.
Melero I., González R., Elena S.F. 2023. Host developmental stages shape the evolution of a plant RNA virus. Philosophical Transactions of the Royal Society B, Biological Sciences 378 (1873): 20220005. DOI
https://doi.org/10.1098/rstb.2....
33.
Moreira X., Granjel R.R., de la Fuente M., Fernández-Conradi P., Pasch V., Soengas P., Turlings T.C.J., Vázquez-González C., Abdala-Roberts L., Rasmann S. 2020. Plant Cell and Environment 44 (4): 1192–1201. DOI:
https://doi.org/10.1111/pce.13....
34.
Navarro R., Ambrós S., Butković A., Carrasco J.L., González R., Martínez F., Wu B., Elena S.F. 2022. Defects in plant immunity modulate the rates and patterns of RNA virus evolution. Virus Evolution 8 (2): veac059. DOI:
https://doi.org/10.1093/ve/vea....
36.
Nickstadt A., Thomma B.P.H.J., Feussner I., Kangasjärvi J., Zeier J, Loeffler C., Scheel D., Berger S. 2004. The Jasmonateinsensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Molecular Plant Pathology 5 (5): 425–434. DOI:
https://doi.org/10.1111/J.1364....
37.
Peñuelas J, Llusià J. 2004. Plant VOC emissions: making use of the unavoidable. Trends in Ecology and Evolution 19 (8): 402–404. DOI:
https://doi.org/10.1016/j.tree....
38.
Riedlmeier M., Ghirardo A., Wening M., Knappe C., Koch K., Georgii E., Dey S., Parker J.E., Schnitzler J.P., Vlot A.C. 2017. Monoterpens support systemic acquired resistance within and between plants. Plant Cell 29 (6): 1440–1459. DOI:
https://doi.org/10.1105/tpc.16....
39.
Santonja M., Bousquet-Mélou A., Greff S., Ormeño E., Fernandez C. 2019. Allelopathic effects of volatile organic compounds released from Pinus halepensis needles and roots. Ecology and Evolution 9 (14): 8201–8213. DOI:
https://doi.org/10.1002/ece3.5....
40.
Scatà M., Di Stefano A., Liò P., La Corte A. 2016. The impact of heterogeneity and awareness in modeling epidemic spreading on multiplex networks. Scientific Reports 6: 37105. DOI:
https://doi.org/10.1038/srep37....
41.
Shulaev V., Silverman P., Raskin I. 1997. Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385 (6618): 718–721. DOI:
https://doi.org/10.1038/385718....
42.
Tamogami S., Rakwal R., Agrawal G.K. 2008. Interplant communication: airborne methyl jasmonate is essentially converted into JA and JA-Ile activating jasmonate signaling pathway and VOCs emission. Biochemical and Biophysical Research Communications 376 (4): 723–727. DOI:
https://doi.org/10.1016/j.bbrc....
43.
Tun W., Yoon J., Jeon J.S., An G. 2021. Influence of climate change on flowering time. Journal of Plant Biology 64 (3): 193–203. DOI:
https://doi.org/10.1007/s12374....
44.
Ueda H., Kikuta Y., Matsuda K. 2012. Plant communication: mediated by individual or blended VOCs? Plant Signaling and Behavior 7 (2): 222–226. DOI:
https://doi.org/10.4161/psb.18....
45.
Wang Z., Andrews M.A., Wu Z.X., Wang L., Bauch C.T. 2015. Coupled disease-behavior dynamics on complex networks: a review. Physics of Life Reviews 15: 1–29. DOI:
https://doi.org/10.1016/j.plre....
46.
Wang N.Q., Kong C.H., Wang P., Meiners S.J. 2020. Root exudate signals in plant-plant interactions. Plant Cell and Environment 44 (4): 1044–1058. DOI:
https://doi.org/10.1111/pce.13....
48.
Wolf A.A., Zavaleta E.S., Selmants P.C. 2017. Flowering phenology shits in response to biodiversity loss. Proceedings of the National Academy of the USA 114 (13): 3463–3468. DOI:
https://doi.org/10.1073/pnas.1....