Ontogenetic switches from plant resistance to tolerance: minimizing costs with age?

Boege, Karina; Dirzo, Rodolfo; Siemens, David H.; Brown, P. D.

doi:10.1111/j.1461-0248.2006.01012.x

Cited by 119 publications

(119 citation statements)

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“…Resource allocation and spatiotemporal accumulation of defense-related metabolites vary within plant tissues and often reflect the degree and frequency of stresses that plants have to face during their development (Boege and Marquis, 2005;Boege et al, 2007). Therefore, we analyzed NaMYB8-dependent CP accumulation in plant ontogeny, namely at rosette, early elongated, elongated, flowering, and mature stages of the development, using 3-d W+OS-elicited (stressed) and unelicited (control) wild-type plants.…”

Section: Young Systemic Leaves Accumulate High Levels Of Cp After Simmentioning

confidence: 99%

R2R3-NaMYB8 Regulates the Accumulation of Phenylpropanoid-Polyamine Conjugates, Which Are Essential for Local and Systemic Defense against Insect Herbivores inNicotiana attenuata

et al. 2010

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Although phenylpropanoid-polyamine conjugates (PPCs) occur ubiquitously in plants, their biological roles remain largely unexplored. The two major PPCs of Nicotiana attenuata plants, caffeoylputrescine (CP) and dicaffeoylspermidine, increase dramatically in local and systemic tissues after herbivore attack and simulations thereof. We identified NaMYB8, a homolog of NtMYBJS1, which in BY-2 cells regulates PPC biosynthesis, and silenced its expression by RNA interference in N. attenuata (ir-MYB8), to understand the ecological role(s) of PPCs. The regulatory role of NaMYB8 in PPC biosynthesis was validated by a microarray analysis, which revealed that transcripts of several key biosynthetic genes in shikimate and polyamine metabolism accumulated in a NaMYB8-dependent manner. Wild-type N. attenuata plants typically contain high levels of PPCs in their reproductive tissues; however, NaMYB8-silenced plants that completely lacked CP and dicaffeoylspermidine showed no changes in reproductive parameters of the plants. In contrast, a defensive role for PPCs was clear; both specialist (Manduca sexta) and generalist (Spodoptera littoralis) caterpillars feeding on systemically preinduced young stem leaves performed significantly better on ir-MYB8 plants lacking PPCs compared with wild-type plants expressing high levels of PPCs. Moreover, the growth of M. sexta caterpillars was significantly reduced when neonates were fed ir-MYB8 leaves sprayed with synthetic CP, corroborating the role of PPCs as direct plant defense. The spatiotemporal accumulation and function of PPCs in N. attenuata are consistent with the predictions of the optimal defense theory: plants preferentially protect their most fitnessenhancing and vulnerable parts, young tissues and reproductive organs, to maximize their fitness.

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Section: Young Systemic Leaves Accumulate High Levels Of Cp After Simmentioning

confidence: 99%

R2R3-NaMYB8 Regulates the Accumulation of Phenylpropanoid-Polyamine Conjugates, Which Are Essential for Local and Systemic Defense against Insect Herbivores inNicotiana attenuata

et al. 2010

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“…A value of 0.5 indicates no preference. Significant preferences for damaged (PI \ 0.5) or undamaged (PI [ 0.5) plants are indicated with asterisks: ***P \ 0.001, **P \ 0.01, *P \ 0.05, one-sample t test (n = 17-20) mature trees (Boege et al 2007;Eichhorn et al 2010). Time lags in systemically induced resistance result from complex plant responses based on the detection of damage, production and allocation of signals (e.g.…”

Section: Temporal Aspect Of Induced Resistancementioning

confidence: 99%

Within-plant distribution of induced resistance in apple seedlings: rapid acropetal and delayed basipetal responses

Gutbrodt

Mody

Wittwer

et al. 2011

Planta

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Induction of plant resistance by herbivory is a complex process, which follows a temporal dynamic and varies spatially at the within-plant scale. This study aimed at improving the understanding of the induction process in terms of time scale and within-plant allocation, using apple tree seedlings (Malus 9 domestica) as plant model. Feeding preferences of a leaf-chewing insect (Spodoptera littoralis) for previously damaged and undamaged plants were assessed for six different time intervals with respect to the herbivore damage treatment and for three leaf positions. In addition, main secondary defense compounds were quantified and linked to herbivore feeding preferences. Significant herbivore preference for undamaged plants (induced resistance) was first observed 3 days after herbivore damage in the most apical leaf. Responses were delayed in the other leaf positions, and induced resistance decreased within 10 days after herbivore damage simultaneously in all tested leaf positions. Chemical analysis revealed higher concentrations of the flavonoid phloridzin in damaged plants as compared to undamaged plants. This indicates that herbivore preference for undamaged apple plants may be linked to phloridzin, which is the main secondary metabolite of apple leaves. The observed time course and distribution of resistance responses within plants contribute to the understanding of induction processes and patterns, and support the optimal defense theory stating young tissue to be prioritized. Moreover, induced resistance responses occurred also basipetally in leaves below the damage site, which suggests that signaling pathways involved in resistance responses are not unidirectional.

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“…Conflicting selection pressures during ontogeny are common and often arise because of trade-offs among traits (23,24). For example, growth rate has clear fitness benefits but also incurs intrinsic and extrinsic costs (23,25).…”

mentioning

confidence: 99%

Insect outbreak shifts the direction of selection from fast to slow growth rates in the long-lived conifer Pinus ponderosa

Mata

Hood

Sala

2017

Proc. Natl. Acad. Sci. U.S.A.

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Long generation times limit species' rapid evolution to changing environments. Trees provide critical global ecosystem services, but are under increasing risk of mortality because of climate changemediated disturbances, such as insect outbreaks. The extent to which disturbance changes the dynamics and strength of selection is unknown, but has important implications on the evolutionary potential of tree populations. Using a 40-y-old Pinus ponderosa genetic experiment, we provide rare evidence of context-dependent fluctuating selection on growth rates over time in a long-lived species. Fast growth was selected at juvenile stages, whereas slow growth was selected at mature stages under strong herbivory caused by a mountain pine beetle (Dendroctonus ponderosae) outbreak. Such opposing forces led to no net evolutionary response over time, thus providing a mechanism for the maintenance of genetic diversity on growth rates. Greater survival to mountain pine beetle attack in slow-growing families reflected, in part, a host-based life-history trade-off. Contrary to expectations, genetic effects on tree survival were greatest at the peak of the outbreak and pointed to complex defense responses. Our results suggest that selection forces in tree populations may be more relevant than previously thought, and have implications for tree population responses to future environments and for tree breeding programs.fluctuating selection | growth-survival trade-offs | selection response | Pinus ponderosa | Dendroctonus ponderosae U nderstanding the dynamics of selection over time is fundamental for understanding life-history evolution (1) and predicting evolutionary change under climate change (2, 3). To date, such understanding is based almost exclusively on data for relatively short-lived species (4, 5), but virtually nonexistent for long-lived organisms, such as trees (ref. 6; but see ref. 7). Trees and forests provide critical ecological and commercial services, including impacts on global carbon cycles, species diversity, water quality, and climate regulation (8). Recent forest mortality (9, 10) highlights the importance of understanding how climate change and climate change-driven disturbances may impact forests (11,12). Trees may live for hundreds of years and experience varying selection pressures associated with fluctuating climate (13), disturbance regimes (14), and biotic interactions (15), all of which may be magnified under climate change. The extent to which these events may change the strength and direction of selection and contribute to the maintenance of genetic diversity and evolutionary potential is unknown. Of special relevance are insect outbreaks, a biotic interaction expected to increase with climate change (16) but unaccounted for in models to predict the evolutionary potential of tree populations (17, 18).Mountain pine beetle (MPB; Dendroctonus ponderosae Hopkins) is a native, irruptive forest insect in western North America that uses numerous Pinus species as hosts. Via pheromone-mediated mass attacks that o...

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Ontogenetic switches from plant resistance to tolerance: minimizing costs with age?

Cited by 119 publications

References 71 publications

R2R3-NaMYB8 Regulates the Accumulation of Phenylpropanoid-Polyamine Conjugates, Which Are Essential for Local and Systemic Defense against Insect Herbivores inNicotiana attenuata

R2R3-NaMYB8 Regulates the Accumulation of Phenylpropanoid-Polyamine Conjugates, Which Are Essential for Local and Systemic Defense against Insect Herbivores inNicotiana attenuata

Within-plant distribution of induced resistance in apple seedlings: rapid acropetal and delayed basipetal responses

Insect outbreak shifts the direction of selection from fast to slow growth rates in the long-lived conifer Pinus ponderosa

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