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Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata.

ABSTRACT: Plant trypsin proteinase inhibitors (TPIs) are potent herbivore- and jasmonate (JA)-induced defenses, but support for the commonly invoked explanation for their inducible expression, namely their associated fitness costs, has been elusive. To determine whether the expression of TPIs incurs fitness costs, we expressed 175 bp of the seven-domain pi from Nicotiana attenuata in an antisense orientation in a TPI-producing genotype (WT) of N. attenuata to reduce TPI expression. Moreover, we expressed the full-length seven-domain pi in a sense orientation under control of a constitutive promoter to restore TPI activity in a natural genotype unable to produce TPIs because of a mutation in its endogenous pi gene. Lifetime reproductive output was determined from high and low TPI-producing plants of the same genetic background with and without JA elicitation and grown in the same pot to simulate natural competitive and nutrient regimes. Transformants with either low or no TPI activity grew faster and taller, flowered earlier, and produced more seed capsules (25-53%) than did neighboring TPI-producing genotypes, and JA elicitation increased TPI production and decreased seed capsule production further. Growth under high light levels only marginally reduced these fitness costs. Results were similar regardless of whether TPI activity was suppressed or restored by transformation: the larger the difference in TPI activity between neighbors, the larger the difference in seed capsule production (R(2) = 0.57). TPI production is costly for a plant's components of fitness when grown under realistic competitive regimes and is consistent with the hypothesis that inducibility evolved as a cost-saving mechanism.

SUBMITTER: Zavala JA

PROVIDER: S-EPMC341788 | biostudies-literature | 2004 Feb

REPOSITORIES: biostudies-literature

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Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata.

Zavala Jorge A JA Patankar Aparna G AG Gase Klaus K Baldwin Ian T IT

Proceedings of the National Academy of Sciences of the United States of America 20040202 6

Plant trypsin proteinase inhibitors (TPIs) are potent herbivore- and jasmonate (JA)-induced defenses, but support for the commonly invoked explanation for their inducible expression, namely their associated fitness costs, has been elusive. To determine whether the expression of TPIs incurs fitness costs, we expressed 175 bp of the seven-domain pi from Nicotiana attenuata in an antisense orientation in a TPI-producing genotype (WT) of N. attenuata to reduce TPI expression. Moreover, we expressed ...[more]

PMID: 14757829

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Project description:BackgroundInduced defense responses to herbivores are generally believed to have evolved as cost-saving strategies that defer the fitness costs of defense metabolism until these defenses are needed. The fitness costs of jasmonate (JA)-mediated defenses have been well documented. Those of the early signaling units mediating induced resistance to herbivores have yet to be examined. Early signaling components that mediate herbivore-induced defense responses in Nicotiana attenuata, have been well characterized and here we examine their growth and fitness costs during competition with conspecifics. Two mitogen-activated protein kinases (MAPKs), salicylic acid (SA)-induced protein kinase (SIPK) and wound-induced protein kinase (WIPK) are rapidly activated after perception of herbivory and both kinases regulate herbivory-induced JA levels and JA-mediated defense metabolite accumulations. Since JA-induced defenses result in resource-based trade-offs that compromise plant productivity, we evaluated if silencing SIPK (irSIPK) and WIPK (irWIPK) benefits the growth and fitness of plants competiting with wild type (WT) plants, as has been shown for plants silenced in JA-signaling by the reduction of Lipoxygenase 3 (LOX3) levels.ResultsAs expected, irWIPK and LOX3-silenced plants out-performed their competing WT plants. Surprisingly, irSIPK plants, which have the largest reductions in JA signaling, did not. Phytohormone profiling of leaves revealed that irSIPK plants accumulated higher levels of SA compared to WT. To test the hypothesis that these high levels of SA, and their presumed associated fitness costs of pathogen associated defenses in irSIPK plants had nullified the JA-deficiency-mediated growth benefits in these plants, we genetically reduced SA levels in irSIPK plants. Reducing SA levels partially recovered the biomass and fitness deficits of irSIPK plants. We also evaluated whether the increased fitness of plants with reduced SA or JA levels resulted from increased nitrogen or CO? assimilation rates, and found no evidence that greater intake of these fitness-limiting resources were responsible.ConclusionsSignaling mediated by WIPK, but not SIPK, is associated with large fitness costs in competing N. attenuata plants, demonstrating the contrasting roles that these two MAPKs play in regulating the plants' growth-defense balance. We discuss the role of SIPK as an important regulator of plant fitness, possibly by modulating SA-JA crosstalk as mediated through ethylene signaling.

Dataset Information

Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata.

Publications

Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata.

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