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Defence on demand: mechanisms behind optimal defence patterns
Open accessAbstract
BACKGROUND: The optimal defence hypothesis (ODH) predicts that tissues that contribute most to a plant's fitness and have the highest probability of being attacked will be the parts best defended against biotic threats, including herbivores. In general, young sink tissues and reproductive structures show stronger induced defence responses after attack from pathogens and herbivores and contain higher basal levels of specialized defensive metabolites than other plant parts. However, the underlying physiological mechanisms responsible for these developmentally regulated defence patterns remain unknown. SCOPE: This review summarizes current knowledge about optimal defence patterns in above- and below-ground plant tissues, including information on basal and induced defence metabolite accumulation, defensive structures and their regulation by jasmonic acid (JA). Physiological regulations underlying developmental differences of tissues with contrasting defence patterns are highlighted, with a special focus on the role of classical plant growth hormones, including auxins, cytokinins, gibberellins and brassinosteroids, and their interactions with the JA pathway. By synthesizing recent findings about the dual roles of these growth hormones in plant development and defence responses, this review aims to provide a framework for new discoveries on the molecular basis of patterns predicted by the ODH. CONCLUSIONS: Almost four decades after its formulation, we are just beginning to understand the underlying molecular mechanisms responsible for the patterns of defence allocation predicted by the ODH. A requirement for future advances will be to understand how developmental and defence processes are integrated.
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“A drop in secondary metabolite levels, as is often observed a few weeks after germination or at the onset of flowering, for instance (Meldau et al., 2012;Barton and Boege, 2017), may reflect an increased need of primary metabolites and nutrients rather than a drop in herbivore pressure.”
From Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy (2020) · cites this paper as Meldau et al., 2012
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“(3) Indirect interactions: CKs might influence herbivory-inducible defense responses indirectly, by up- or down-regulating other hormonal pathways, such as auxins and gibberellins, which subsequently leads to changes in JA sensitivity (Meldau et al., 2012).”
BackgroundSelf-citationCoppede, J. D. S., Pina, E. S., Paz, T. A., Fachin, A. L., Marins, M., Bertoni, B. W., França, S. D. C., & Pereira, A. M. S. (2014) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-014-0459-7 · Cited by 27
“It is generally accepted that young leaves and roots produce higher amounts of secondary metabolites in comparison with their older counterparts for the purpose of protection (Meldau et al. 2012).”
Brütting, C., Schäfer, M., Vaňková, R., Gase, K., Baldwin, I., & Meldau, S. (2017) · The Plant Journal · doi:10.1111/tpj.13316 · Cited by 28
Self-citationNiches and routes of transmission of Xanthomonas citri pv. fuscans to bean seeds
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Root Microbiome Assemblage is Modulated by Plant Host Factors
Lakshmanan, V. (2015) · Advances in botanical research · doi:10.1016/bs.abr.2015.09.004 · Cited by 36
Differences in resource use lead to coexistence of seed-transmitted microbial populations
Torres-Cortés, G., Garcia, B. J., Compant, S., Rezki, S., Jones, P., Préveaux, A., Briand, M., Roulet, A., Bouchez, O., Jacobson, D. A., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-42865-9 · Cited by 26
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Direct and indirect resistance of sugarcane to Diatraea saccharalis induced by jasmonic acid
Sanches, P., Santos, F., Peñaflor, M. G. V., & Bento, J. (2017) · Bulletin of entomological research · doi:10.1017/s0007485317000372 · Cited by 23
“JA, the main phytohormone responsible for signal-transduction pathways in plants damaged by chewing insects (Wasternack & Hause, 2013), and its catabolites (methyl jasmonate [MeJA], cis-jasmone) have been widely studied as elicitors in plants, against not only insect pests but also pathogen infections (Antico et al.,…”
BackgroundTerrasson, E., Darrasse, A., Righetti, K., Buitink, J., Lalanne, D., Vu, B. L., Pelletier, S., Bolingue, W., Jacques, M., & Leprince, O. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv167 · Cited by 23
“Accordingly, young or reproductive organs are expected to exhibit higher basal levels or stronger induced defence responses than other plant structures (Meldau et al., 2012; Neilson et al., 2013).”
BackgroundBaldwin, I., & Meldau, S. (2013) · Plant Signalling & Behavior · doi:10.4161/psb.24410 · Cited by 23
Self-citationTsunoda, T., Großer, K., & Dam, N. M. (2018) · Functional Ecology · doi:10.1111/1365-2435.13147 · Cited by 22
“Despite the ecological relevance of root herbivory, research on optimal defence patterns in root systems is still in its infancy (Meldau et al., 2012; Robert et al., 2012; Tsunoda, Krosse, et al., 2017).”
BackgroundSchimmel, B. C., Ataíde, L. M. S., & Kant, M. (2017) · Plant Signalling & Behavior · doi:10.1080/15592324.2017.1370526 · Cited by 20
“differ significantly in magnitude and/or in the timing of induction across plant age, developmental stage and tissue type, as well as across abiotic conditions.(1,2,5) Heterogeneity in defensive responses is an important aspect of plant-herbivore interac-”
BackgroundWang, Y., Carrillo, J., Siemann, E., Wheeler, G., Zhu, L., Gu, X., & Ding, J.-Q. (2013) · Annals of Botany · doi:10.1093/aob/mct129 · Cited by 20
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“Analyzing tissue-specific metabolomes is also critical to test ecological theories of plant investments into metabolic defenses such as the optimal defense theory that predicts greater metabolic defense accumulation in developmental stages/tissues with higher organismic-level fitness contribution and/or greater predat…”
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“While providing protection in agricultural systems 58 and potentially playing an important role in the evolution and optimization of host resistance [9], 59”
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“…than deploying defense mechanisms uniformly across different tissues, plants prioritize protecting the tissues that contribute more to a plant’s future fitness, such as young sink tissues and reproductive structures (optimal defense hypothesis, ODH) (Meldau et al., 2012; Meldau and Baldwin, 2013).”
BackgroundBoaro, C. S. F., Vieira, M. A. R., Campos, F. G., Ferreira, G., De‐la‐Cruz‐Chacón, I., & Marques, M. O. M. (2019) · Springer eBooks · doi:10.1007/978-3-030-16546-8_2 · Cited by 18
Herbivore-Induced Defenses in Rice and Their Potential Application in Rice Planthopper Management
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“Moreover, calcium flux, protein kinase (such as CDPK and MAPK) cascades, and JA-, SA-, ethylene-, and H2O2-mediated signaling pathways have been confirmed to play a central role in shaping the specificity of herbivore-induced plant defense responses (Wu et al. 2007; Howe and Jander 2008; Wu and Baldwin 2010; Heinrich…”
Backgroundde Leone, M. J., Hernando, C. E., Mora‐García, S., & Yanovsky, M. J. (2020) · Transcription · doi:10.1080/21541264.2020.1820300 · Cited by 20
“This hypothesis establishes that plants preferentially assign resources to the defense of tissues that are either more likely to be attacked or more valuable, resulting in tissue-specific “defense on demand” through the integration of developmental and defense signaling pathways [90,91].”
BackgroundFRS7 and FRS12 recruit NINJA to regulate expression of glucosinolate biosynthesis genes
Fernández‐Calvo, P., Iñigo, S., Glauser, G., Bossche, R. V., Tang, M., Li, B., Clercq, R. D., Durand, A. N., Eeckhout, D., Gevaert, K., et al. (2020) · New Phytologist · doi:10.1111/nph.16586 · Cited by 33
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Do phytoliths play an antiherbivory role in southwest Asian Asteraceae species and to what extent
Katz, O., Lev-Yadun, S., & Bar, P. (2014) · doi:10.1016/j.flora.2014.03.010 · Cited by 18
Plant biology: Electric defence
Christmann, A., & Grill, E. (2013) · Nature · doi:10.1038/500404a · Cited by 18
TOR coordinates Cytokinin and Gibberellin signals mediating development and defense
Marash, I., Gupta, R., Anand, G., Leibman-Markus, M., Lindner, N., Israeli, A., Nir, D., Avni, A., & Bar, M. (2023) · bioRxiv · doi:10.1101/2022.03.07.483332 · Cited by 17
“When pathogens attack, CK increases and GA decreases (Meldau et al., 2012; Gupta et al 2020), and TOR becomes less active (Margalha et al., 2019), promoting disease resistance.”
BackgroundHol, W., Raaijmakers, C., Mons, I., Meyer, K. M., & van Dam, N. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.00111 · Cited by 17
Mertens, D., Bouwmeester, K., & Poelman, E. (2021) · Ecology Letters · doi:10.1111/ele.13852 · Cited by 16
“Plants evolved inducible defences that are activated upon recognition of attack to save metabolic costs associated with production and maintenance of defence when herbivores are absent (Meldau et al., 2012).”
BackgroundSarika, G., Amruta, N., Kandikattu, H. K., Basavaraju, G. V., Suma, H. K., Manjunath, B. L., & Sravani, C. (2019) · South African Journal of Botany · doi:10.1016/j.sajb.2019.02.003 · Cited by 17
Optimal chemical defence allocation in roots: where, why and how?
Touw, A., & Dam, N. M. (2023) · Phytochemistry Reviews · doi:10.1007/s11101-023-09872-1 · Cited by 15
“In Brassicaceae, induced responses in the root system are most robust in the most valuable root class (Tsunoda et al. 2018), similar to above-ground tissues (reviewed in Meldau et al. 2012).”
InfluentialZhao, Y., Chen, Z.-Y., Chen, J.-X., Chen, B., Tang, W., Chen, X.-D., Lai, Z., & Guo, R.-F. (2021) · BMC Plant Biology · doi:10.1186/s12870-021-03168-2 · Cited by 15
“The distribution of GS over different parts follows optimal defense theory which allows plants to allocate defense compounds preferentially to the valuable plant parts which are also attractive to potential attackers [38].”
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“Ecological theory predicts ontogenetic and tissue-specific variation in the concentration of plant secondary metabolites, primarily in the context of herbivore resistance (Barton & Boege, 2017; McKey, 1974; Meldau et al., 2012; Pavia et al., 2002; Schuman & Baldwin, 2016; van Dam, 2009).”
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“Tissue specificity in metabolism in response to herbivory is thought to be mediated, in part, by tissue-specific deviations in jasmonate signaling [42].”
BackgroundSelf-citationJasmonates in Plant Growth and Stress Responses
Wasternack, C. (2014) · Springer eBooks · doi:10.1007/978-1-4939-0491-4_8 · Cited by 16
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“Therefore, the comparatively low amount of beneficial secondary metabolites, particularly in the shoots of immature plants, was clearly reflected in our experiment on the detection of SM, indicating that young plants have an increased requirement for primary metabolites and nutrients [33,34].”
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“that organisms put more resources into protecting their most valuable tissues to increase fitness [26].”
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Metadata
- Authors
- Meldau, S., Erb, M., & Baldwin, I. T.
- Affiliations
- Max Planck Society (DE)
- Corresponding author
- Meldau, Stefan
- Venue
- Annals of Botany
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-09-28
- Volume
- 110
- Issue
- 8
- Pages
- 1503-1514
- ISSN
- 0305-7364 (ISSN-L)
- 1095-8290
- PMC
- PMC3503495
- OpenAlex
- W2072280600
- Cited by
- 197
- References
- 0
- Citations by year
- 2026: 11 · 2025: 5 · 2024: 18 · 2023: 17 · 2022: 12 · 2021: 18 · 2020: 16 · 2019: 10 · 2018: 10 · 2017: 12 · 2016: 15 · 2015: 17 · 2014: 18 · 2013: 17
- FWCI
- 1.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Annals of Botany (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- BORIS (University Library Bern) (submittedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Open Access CRIS of the University of Bern
- Topics
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
- Keywords
- induced defense, jasmonic acid, plant hormones, auxin, cytokinins, gibberellin, brassinosteroids, sink tissues, herbivory, plant development, plant-pathogen interaction, plant-herbivore interactions
- MeSH terms
- Plant Diseases, Plant Growth Regulators, Plants, Signal Transduction, Plant Components, Aerial, Plant Immunity, Herbivory, Plant Development
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