Why fruit rots: theoretical support for Janzen's theory of microbe–macrobe competition

Ruxton, Graeme D.; Wilkinson, David M.; Schaefer, H. Martin; Sherratt, Thomas N.

doi:10.1098/rspb.2013.3320

Cited by 34 publications

(28 citation statements)

References 21 publications

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“…Janzen 11 suggested that fruits infested by microbes are rarely eaten by vertebrates because microbes produce toxic compounds and reduce the nutritional value of infested fruit. Most empirical investigations of these cross-kingdom interactions 12–14 as well as recent theoretical evidence have supported Janzen’s famous prediction 15 , but see 16 . Nonetheless, there exist a handful of studies showing that frugivores prefer infested fruits 9, 17–19 .…”

Section: Introductionmentioning

confidence: 89%

Fungal infestation boosts fruit aroma and fruit removal by mammals and birds

Peris

Rodríguez

Peña

et al. 2017

Sci Rep

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For four decades, an influential hypothesis has posited that competition for food resources between microbes and vertebrates selects for microbes to alter these resources in ways that make them unpalatable to vertebrates. We chose an understudied cross kingdom interaction to experimentally evaluate the effect of fruit infection by fungi on both vertebrate (mammals and birds) fruit preferences and on ecologically relevant fruit traits (volatile compounds, toughness, etc). Our well-replicated field experiments revealed that, in contrast to previous studies, frugivorous mammals and birds consistently preferred infested over intact fruits. This was concordant with the higher level of attractive volatiles (esters, ethanol) in infested fruits. This investigation suggests that vertebrate frugivores, fleshy-fruited plants, and microbes form a tripartite interaction in which each part could interact positively with the other two (e.g. both orange seeds and fungal spores are likely dispersed by mammals). Such a mutualistic view of these complex interactions is opposed to the generalized idea of competition between frugivorous vertebrates and microorganisms. Thus, this research provides a new perspective on the widely accepted plant evolutionary dilemma to make fruits attractive to mutualistic frugivores while unattractive to presumed antagonistic microbes that constrain seed dispersal.

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Section: Introductionmentioning

confidence: 89%

Fungal infestation boosts fruit aroma and fruit removal by mammals and birds

Peris

Rodríguez

Peña

et al. 2017

Sci Rep

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“…This process occurs when fruit becomes infected by yeasts capable of producing ethanol via fermentation under anaerobic conditions (Levey, 2004). Ethanol production by yeasts increases their competiveness, as ethanol may deter frugivorous competitors (Dudley, 2004;Janzen, 1977;Ruxton et al, 2014). However, the negative relationship between sugar and ethanol content in fruit is quite weak, presumably because over-ripe or rotting fruit constitutes a heterogeneous milieu for micro-organisms.…”

Section: Introductionmentioning

confidence: 99%

Feeding on ripening and over-ripening fruit: interactions between sugar, ethanol and polyphenol contents in a tropical butterfly

Beaulieu

Franke

Fischer

2017

Journal of Experimental Biology

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In ripe fruit, energy mostly derives from sugar, while in over-ripe fruit, it also comes from ethanol. Such ripeness differences may alter the fitness benefits associated with frugivory if animals are unable to degrade ethanol when consuming over-ripe fruit. In the tropical butterfly Bicyclus anynana, we found that females consuming isocaloric solutions mimicking ripe (20% sucrose) and over-ripe fruit (10% sucrose, 7% ethanol) of the palm Astrocaryum standleyanum exhibited higher fecundity than females consuming a solution mimicking unripe fruit (10% sucrose). Moreover, relative to butterflies consuming a solution mimicking unripe fruit, survival was enhanced when butterflies consumed a solution mimicking either ripe fruit supplemented with polyphenols (fruit antioxidant compounds) or over-ripe fruit devoid of polyphenols. This suggests that (1) butterflies have evolved tolerance mechanisms to derive the same reproductive benefits from ethanol and sugar, and (2) polyphenols may regulate the allocation of sugar and ethanol to maintenance mechanisms. However, variation in fitness owing to the composition of feeding solutions was not paralleled by corresponding physiological changes (alcohol dehydrogenase activity, oxidative status) in butterflies. The fitness proxies and physiological parameters that we measured therefore appear to reflect distinct biological pathways. Overall, our results highlight that the energy content of fruit primarily affects the fecundity of B. anynana butterflies, while the effects of fruit consumption on survival are more complex and vary depending on ripening stage and polyphenol presence. The actual underlying physiological mechanisms linking fruit ripeness and fitness components remain to be clarified.

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“…() suggested that d ‐limonene was present in wild‐type orange fruit to promote infection by microorganisms that facilitated access to the fruit pulp by frugivores and thus aided seed dispersal. However, many vertebrates, including humans, are very sensitive to microbial spoilage of potential foods and find such spoilage highly aversive (Ruxton et al ., ). In this case, spoilt fruit might act to deter specific frugivores but attract others.…”

Section: Discussionmentioning

confidence: 97%

Genetic control of α‐farnesene production in apple fruit and its role in fungal pathogenesis

et al. 2019

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Terpenes are important compounds in plant trophic interactions. A meta-analysis of GC-MS data from a diverse range of apple (Malus 3 domestica) genotypes revealed that apple fruit produces a range of terpene volatiles, with the predominant terpene being the acyclic branched sesquiterpene (E,E)-a-farnesene. Four quantitative trait loci (QTLs) for a-farnesene production in ripe fruit were identified in a segregating 'Royal Gala' (RG) 3 'Granny Smith' (GS) population with one major QTL on linkage group 10 co-locating with the MdAFS1 (a-farnesene synthase-1) gene. Three of the four QTLs were derived from the GS parent, which was consistent with GC-MS analysis of headspace and solvent-extracted terpenes showing that cold-treated GS apples produced higher levels of (E,E)-a-farnesene than RG. Transgenic RG fruit downregulated for MdAFS1 expression produced significantly lower levels of (E,E)-a-farnesene. To evaluate the role of (E,E)-a-farnesene in fungal pathogenesis, MdAFS1 RNA interference transgenic fruit and RG controls were inoculated with three important apple post-harvest pathogens [Colletotrichum acutatum, Penicillium expansum and Neofabraea alba (synonym Phlyctema vagabunda)]. From results obtained over four seasons, we demonstrate that reduced (E,E)-a-farnesene is associated with decreased disease initiation rates of all three pathogens. In each case, the infection rate was significantly reduced 7 days post-inoculation, although the size of successful lesions was comparable with infections on control fruit. These results indicate that (E,E)-a-farnesene production is likely to be an important factor involved in fungal pathogenesis in apple fruit.

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Why fruit rots: theoretical support for Janzen's theory of microbe–macrobe competition

Cited by 34 publications

References 21 publications

Fungal infestation boosts fruit aroma and fruit removal by mammals and birds

Fungal infestation boosts fruit aroma and fruit removal by mammals and birds

Feeding on ripening and over-ripening fruit: interactions between sugar, ethanol and polyphenol contents in a tropical butterfly

Genetic control of α‐farnesene production in apple fruit and its role in fungal pathogenesis

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