Tissue-Specific Emission of (E)-α-Bergamotene Helps Resolve the Dilemma When Pollinators Are Also Herbivores

Zhou, Wenwu; Kügler, Anke; McGale, Erica; Haverkamp, Alexander; Knaden, Markus; Guo, Han; Beran, Franziska; Yon, Felipe; Li, Ran; Lackus, Nathalie D.; Köllner, Tobias G.; Bing, Julia; Schuman, Meredith C.; Hansson, Bill S.; Kessler, Danny; Baldwin, Ian Thomas; Xu, Shuqing

doi:10.1016/j.cub.2017.03.017

Cited by 61 publications

(112 citation statements)

References 14 publications

(27 reference statements)

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“…The emission of αbergamotene, in particular, was highly correlated with β-trans-bergamotene. Tissue-specific emission of (E)-α-bergamotene in Nicotiana attenuata was found to mediate both defence and reproduction by attracting predators during the day and pollinators (Manduca sexta moths) at night (Halitschke, Stenberg, Kessler, Kessler, & Baldwin, 2008;Kessler & Baldwin, 2001;Zhou et al, 2015). Although M. guttatus emitted both of these compounds (especially α-bergamotene)…”

Section: Discussionmentioning

confidence: 99%

A key floral scent component (β‐trans‐bergamotene) drives pollinator preferences independently of pollen rewards in seep monkeyflower

et al. 2018

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Floral odours play an important role in attracting insect pollinators. Because pollinators visit flowers to obtain pollen and nectar rewards, they should prefer floral odour profiles associated with the highest‐rewarding flowers (honest signals). In previous work, bumblebees exhibited a preference for flowers from outbred over inbred Mimulus guttatus plants. Pollen is the only floral reward in M. guttatus, and pollen viability (a reliable indicator of protein content) is reduced in inbred plants. Yet, differences in pollen viability did not explain the observed preferences. In this study, we examined the floral volatile profiles of inbred and outbred M. guttatus to identify inbreeding effects and associations between volatile compounds and the number of viable pollen grains per flower, designated “PRQ” (pollen reward quality). We also conducted pairwise choice tests with Bombus impatiens to evaluate the ability of bees to discriminate between odours of rewarding and non‐rewarding flowers and to determine whether bumblebee preferences are explained by differences in the floral odours of inbred and outbred plants. Inbred plants exhibited reduced emission of β‐trans‐bergamotene, the second‐most abundant compound in the volatile blend of outbred plants. Furthermore, pollen and fertile anthers emitted nonadecane. Six other compounds in the floral blend were positively correlated with PRQ. There was no overlap between compounds affected by inbreeding and compounds associated with PRQ. Even when given prior experience foraging on M. guttatus, bumblebees did not distinguish between the floral odours of rewarding and non‐rewarding outbred plants. However, they preferred floral odours from non‐rewarding outbred plants over rewarding inbred plants. Bumblebees without prior experience of flowers preferred volatile blends with higher versus lower amounts of β‐trans‐bergamotene. Taken together, these results suggest that the volatile emissions of M. guttatus provide reliable indicators of pollen rewards (potential honest signals), but that the preference of bumblebees for outbred plants is not driven by these cues but rather by a sensory bias for β‐trans‐bergamotene. This may represent a subtle form of deceit‐pollination that allows plants to attract pollinators while minimizing investment in costly rewards. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13246/suppinfo is available for this article.

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Section: Discussionmentioning

confidence: 99%

A key floral scent component (β‐trans‐bergamotene) drives pollinator preferences independently of pollen rewards in seep monkeyflower

et al. 2018

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“…1E). Although floral (E)-α-bergamotene is unlikely to function as an indirect defense as it does in leaves, it plays a role in attracting and guiding the behavior of pollinators in N. attenuata (70,71). Interestingly, (E)-α-bergamotene also has been shown to have a repellent role against a nectar thief (Solenopsis xyloni ants) (70).…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, (E)-α-bergamotene also has been shown to have a repellent role against a nectar thief (Solenopsis xyloni ants) (70). Given that (E)-α-bergamotene is largely produced in the corolla tube (71), it might also have a defensive function in repelling other nectar robbers, such as carpenter bees (Xylocopa spp. ), which commonly rob the nectar of flowers in N. attenuata's natural habitat (67).…”

Section: Discussionmentioning

confidence: 99%

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

Wang

et al. 2017

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

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Optimal defense (OD) theory predicts that within a plant, tissues are defended in proportion to their fitness value and risk of predation. The fitness value of leaves varies greatly and leaves are protected by jasmonate (JA)-inducible defenses. Flowers are vehicles of Darwinian fitness in flowering plants and are attacked by herbivores and pathogens, but how they are defended is rarely investigated. We used Nicotiana attenuata, an ecological model plant with well-characterized herbivore interactions to characterize defense responses in flowers. Early floral stages constitutively accumulate greater amounts of two well-characterized defensive compounds, the volatile (E)-α-bergamotene and trypsin proteinase inhibitors (TPIs), which are also found in herbivore-induced leaves. Plants rendered deficient in JA biosynthesis or perception by RNA interference had significantly attenuated floral accumulations of defensive compounds known to be regulated by JA in leaves. By RNA-seq, we found a JAZ gene, NaJAZi, specifically expressed in early-stage floral tissues. Gene silencing revealed that NaJAZi functions as a flower-specific jasmonate repressor that regulates JAs, (E)-α-bergamotene, TPIs, and a defensin. Flowers silenced in NaJAZi are more resistant to tobacco budworm attack, a florivore. When the defensin was ectopically expressed in leaves, performance of Manduca sexta larvae, a folivore, decreased. NaJAZi physically interacts with a newly identified NINJA-like protein, but not the canonical NINJA. This NINJA-like recruits the corepressor TOPLESS that contributes to the suppressive function of NaJAZi on floral defenses. This study uncovers the defensive function of JA signaling in flowers, which includes components that tailor JA signaling to provide flower-specific defense

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“…Population geneticists have long utilized the genetic variance derived from natural populations to query the genetic architecture underlying traits of interest. Recently, the allelic diversity in the genome of two natural accessions collected from Utah and Arizona (Glawe et al ., ; Wu et al ., ) has been utilized to create an advanced intercross recombinant inbred line (AI‐RIL) population to identify genetic components of indirect defense (Zhou et al ., ) and arbuscular mycorrhizal interactions (Wang et al ., ). This AI‐RIL approach has recently been extended by creating a 26‐parent Multiparent Advanced Generation Inter‐Cross (MAGIC) population which we describe in the next section.…”

Section: Natural Variation In Ja Signaling In N Attenuata Populationsmentioning

confidence: 99%

Using natural variation to achieve a whole‐plant functional understanding of the responses mediated by jasmonate signaling

Ray

Halitschke

et al. 2019

The Plant Journal

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Summary The dramatic advances in our understanding of the molecular biology and biochemistry of jasmonate (JA) signaling have been the subject of several excellent recent reviews that have highlighted the phytohormonal function of this signaling pathway. Here, we focus on the responses mediated by JA signaling which have consequences for a plant's Darwinian fitness, i.e. the organism‐level function of JA signaling. The most diverse module in the signaling cascade, the JAZ proteins, and their interactions with other proteins and transcription factors, allow this canonical signaling cascade to mediate a bewildering array of traits in different tissues at different times; the functional coherence of these diverse responses are best appreciated in an organismal/ecological context. From published work, it appears that jasmonates can function as the ‘Swiss Army knife’ of plant signaling, mediating many different biotic and abiotic stress and developmental responses that allow plants to contextualize their responses to their frequently changing local environments and optimize their fitness. We propose that a deeper analysis of the natural variation in both within‐plant and within‐population JA signaling components is a profitable means of attaining a coherent whole‐plant functional perspective of this signaling cascade, and provide examples of this approach from the Nicotiana attenuata system.

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Tissue-Specific Emission of (E)-α-Bergamotene Helps Resolve the Dilemma When Pollinators Are Also Herbivores

Cited by 61 publications

References 14 publications

A key floral scent component (β‐trans‐bergamotene) drives pollinator preferences independently of pollen rewards in seep monkeyflower

A key floral scent component (β‐trans‐bergamotene) drives pollinator preferences independently of pollen rewards in seep monkeyflower

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

Using natural variation to achieve a whole‐plant functional understanding of the responses mediated by jasmonate signaling

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