Benefits of jasmonate-dependent defenses against vertebrate herbivores in nature

Machado, Ricardo A. R.; McClure, Mark S.; Hervé, Maxime; Baldwin, Ian Thomas; Erb, Matthias

doi:10.7554/elife.13720

Cited by 44 publications

(45 citation statements)

References 134 publications

(195 reference statements)

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“…This transcription factor may therefore represent a target for the integration of IAA and JA signaling. While IAA strongly potentiated the accumulation of stem phenolamides, it had little effect on the accumulation of other JA-dependent secondary metabolites, including nicotine and 7-hydroxygeranyllinalool diterpene glycosides (Machado et al, 2013(Machado et al, , 2016Paschold et al, 2007;Jimenez-Aleman et al, 2015). This result is consistent with earlier studies showing neutral to negative effects of auxin application on nicotine accumulation in Nicotiana spp.…”

Section: Discussionsupporting

confidence: 91%

“…The stems of N. attenuata are often attacked by herbivores, including stem borers (Diezel et al, 2011b;Lee et al, 2016), and are very important for plant fitness (Machado et al, 2016). We observed a strong up-regulation of defensive secondary metabolites in the stems in response to M. sexta attack (Fig.…”

Section: Iaa Specifically Potentiates the Herbivore-induced Accumulatmentioning

confidence: 63%

“…The stem of N. attenuata is vital for its reproduction and can be attacked by a wide variety of organisms, including vertebrates and invertebrate stem borers (Machado et al, 2016;Diezel et al, 2011b). We observed that real and simulated M. sexta attack induced anthocyanin accumulation in the stems, an effect that could not be reproduced by MeJA or IAA treatments alone, but by the combination of these two hormones.…”

Section: Discussionmentioning

confidence: 86%

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Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

et al. 2016

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Plant responses to herbivore attack are regulated by phytohormonal networks. To date, the role of the auxin indole-3-acetic acid (IAA) in this context is not well understood. We quantified and manipulated the spatiotemporal patterns of IAA accumulation in herbivore-attacked Nicotiana attenuata plants to unravel its role in the regulation of plant secondary metabolism. We found that IAA is strongly, rapidly, and specifically induced by herbivore attack. IAA is elicited by herbivore oral secretions and fatty acid conjugate elicitors and is accompanied by a rapid transcriptional increase of auxin biosynthetic YUCCA-like genes. IAA accumulation starts 30 to 60 s after local induction and peaks within 5 min after induction, thereby preceding the jasmonate (JA) burst. IAA accumulation does not require JA signaling and spreads rapidly from the wound site to systemic tissues. Complementation and transport inhibition experiments reveal that IAA is required for the herbivore-specific, JA-dependent accumulation of anthocyanins and phenolamides in the stems. In contrast, IAA does not affect the accumulation of nicotine or 7-hydroxygeranyllinalool diterpene glycosides in the same tissue. Taken together, our results uncover IAA as a rapid and specific signal that regulates a subset of systemic, JA-dependent secondary metabolites in herbivore-attacked plants.

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Section: Discussionsupporting

confidence: 91%

Section: Iaa Specifically Potentiates the Herbivore-induced Accumulatmentioning

confidence: 63%

Section: Discussionmentioning

confidence: 86%

See 1 more Smart Citation

Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

et al. 2016

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“…These results are consistent with the hypothesis that TEs, which have often been considered as "junk" DNA, can be important orchestrators of the gene expression remodeling that is required for the evolution of adaptive traits. Because native Nicotiana species do not survive in nature without the ability to produce large quantities of nicotine to ward off attackers (27), it might be that this junk has facilitated innovations essential for their survival.…”

Section: Resultsmentioning

confidence: 99%

Wild tobacco genomes reveal the evolution of nicotine biosynthesis

Brockmöller

Navarro‐Quezada

et al. 2017

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

160

100

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Nicotine, the signature alkaloid of Nicotiana species responsible for the addictive properties of human tobacco smoking, functions as a defensive neurotoxin against attacking herbivores. However, the evolution of the genetic features that contributed to the assembly of the nicotine biosynthetic pathway remains unknown. We sequenced and assembled genomes of two wild tobaccos, Nicotiana attenuata (2.5 Gb) and Nicotiana obtusifolia (1.5 Gb), two ecological models for investigating adaptive traits in nature. We show that after the Solanaceae whole-genome triplication event, a repertoire of rapidly expanding transposable elements (TEs) bloated these Nicotiana genomes, promoted expression divergences among duplicated genes, and contributed to the evolution of herbivoryinduced signaling and defenses, including nicotine biosynthesis. The biosynthetic machinery that allows for nicotine synthesis in the roots evolved from the stepwise duplications of two ancient primary metabolic pathways: the polyamine and nicotinamide adenine dinucleotide (NAD) pathways. In contrast to the duplication of the polyamine pathway that is shared among several solanaceous genera producing polyamine-derived tropane alkaloids, we found that lineage-specific duplications within the NAD pathway and the evolution of rootspecific expression of the duplicated Solanaceae-specific ethylene response factor that activates the expression of all nicotine biosynthetic genes resulted in the innovative and efficient production of nicotine in the genus Nicotiana. Transcription factor binding motifs derived from TEs may have contributed to the coexpression of nicotine biosynthetic pathway genes and coordinated the metabolic flux. Together, these results provide evidence that TEs and gene duplications facilitated the emergence of a key metabolic innovation relevant to plant fitness.Nicotiana genomes | genome-wide multiplications | transposable elements | nicotine biosynthesis | expression divergence

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“…The facilitation process reduces plant reproductive potential beyond the individual or combined effect of both stresses. Jasmonate signalling is a highly polymorphic trait in N. attenuata (D. Li, Baldwin, & Gaquerel, , ; Machado et al, ; Schuman, Heinzel, Gaquerel, Svatos, & Baldwin, ), which partially accounts for the asymmetric herbivore damage under natural conditions (Machado, McClure, et al, ; Kallenbach et al, ; Steppuhn, Schuman, & Baldwin, ). Our experiments suggest that nematode attack might exert selective pressure against jasmonate signalling and could therefore be one of the factors that favours polymorphisms in jasmonate signalling and jasmonate‐independent defensive mechanisms in nature (Machado et al, ; Machado, Zhou, et al, ).…”

Section: Discussionmentioning

confidence: 99%

Aboveground herbivory induced jasmonates disproportionately reduce plant reproductive potential by facilitating root nematode infestation

Machado

Arce

McClure

et al. 2018

Plant Cell & Environment

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Different plant feeders, including insects and parasitic nematodes, can influence each other by triggering systemic changes in their shared host plants. In most cases, however, the underlying mechanisms are unclear, and the consequences for plant fitness are not well understood. We studied the interaction between leaf feeding Manduca sexta caterpillars and root parasitic nematodes in Nicotiana attenuata. Simulated M. sexta attack increased the abundance of root parasitic nematodes in the field and facilitated Meloidogyne incognita reproduction in the glasshouse. Intact jasmonate biosynthesis was found to be required for both effects. Flower counts revealed that the jasmonate-dependent facilitation of nematode infestation following simulated leaf attack reduces the plant's reproductive potential to a greater degree than would be expected from the additive effects of the individual stresses. This work reveals that jasmonates mediate the interaction between a leaf herbivore and root parasitic nematodes and illustrates how plant-mediated interactions can alter plant's reproductive potential. The selection pressure resulting from the demonstrated fitness effects is likely to influence the evolution of plant defense traits in nature.

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Benefits of jasmonate-dependent defenses against vertebrate herbivores in nature

Cited by 44 publications

References 134 publications

Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

Wild tobacco genomes reveal the evolution of nicotine biosynthesis

Aboveground herbivory induced jasmonates disproportionately reduce plant reproductive potential by facilitating root nematode infestation

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