Evolutionary change from induced to constitutive expression of an indirect plant resistance

Abstract

Induced plant resistance traits are expressed in response to attack and occur throughout the plant kingdom1,2. Despite their general occurrence, the evolution of such resistances has rarely been investigated3. Here we report that extrafloral nectar, a usually inducible trait, is constitutively secreted by Central American Acacia species that are obligately inhabited by ants. Extrafloral nectar is secreted as an indirect resistance4, attracting ants that defend plants against herbivores5. Leaf damage induces extrafloral nectar secretion in several plant species6,7,8; among these are various Acacia species and other Fabaceae investigated here. In contrast, Acacia species obligately inhabited by symbiotic ants9 nourish these ants by secreting extrafloral nectar constitutively at high rates that are not affected by leaf damage. The phylogeny of the genus Acacia and closely related genera indicate that the inducibility of extrafloral nectar is the plesiomorphic or ‘original’ state, whereas the constitutive extrafloral nectar flow is derived within Acacia. A constitutive resistance trait has evolved from an inducible one, obviously in response to particular functional demands.

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Figure 1: Extrafloral nectar secretion in response to different treatments.
Figure 2: Endogenous concentrations of jasmonic acid.
Figure 3: Extrafloral nectar secretion rates after inhibition of jasmonic acid synthesis.
Figure 4: Phylogenetic relationships.

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Acknowledgements

We thank D. Davidson, J. Gershenzon, I. Baldwin, G. Stone, C. Kost and G. Pohnert for critically reading earlier versions of the manuscript, K. Heil and B. Baumann for help with field work, A. Kreiner and F. Thiele for taking care of greenhouse plant, and M. Sousa for species determination. Financial support by the Deutsche Forschungsgesellschaft and the Max-Planck-Society is acknowledged.

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Correspondence to Martin Heil.

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Supplementary information

Supplementary Discussion

This discussion provides an overview on the available information concerning phylogenetic relations within the genus Acacia and among the genus Acacia and related genera. It places the phylogenetic analysis presented here in a broader context. Supplementary references are also included. (DOC 45 kb)

Supplementary Figure 1

Results of a phylogenetic analysis of published trnK intron data combined with those of species investigated here: inducible and non-inducible Acacia species belong to the monophyletic subgenus Acacia, while the (inducible) non-Acacias appear in neighboring groups. This confirms the ancestral state of inducible EFN secretion. (DOC 46 kb)

Supplementary Figure 2

The position of the species investigated here in a broader phylogenetic context: species with inducible EFN secretion appear in different parts of the phylogenetic tree, while species exhibiting constitutive EFN flow form one single clade, further supporting the derived state of this character. (DOC 34 kb)

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Heil, M., Greiner, S., Meimberg, H. et al. Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430, 205–208 (2004). https://doi.org/10.1038/nature02703

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