Fitness consequences of a clock pollinator filter in Nicotiana attenuata flowers in nature

Abstract

Summary Nicotiana attenuata flowers, diurnally open, emit scents and move vertically to interact with nocturnal hawkmoth and day‐active hummingbird pollinators. To examine the fitness consequences of these floral rhythms, we conducted pollination trials in the plant's native habitat with phase‐shifted flowers of plants silenced in circadian clock genes. The results revealed that some pollination benefits observed under glasshouse conditions were not reproduced under natural field conditions. Floral arrhythmicity increased pollination success by hummingbirds, while reducing those by hawkmoths in the field. Thus, floral circadian rhythms may influence a plant's fitness by filtering pollinators leading to altered seed set from outcrossed pollen.

Circadian Rhythms in Plants

“…It would be interesting to assess crop cultivars with known clock gene variants under different nutrient and environmental stresses to get a fuller picture of the role of the clock in response to different environmental challenges. A relatively unexplored area for future research is how clock-regulated processes in plants affect and are affected by clockregulated processes in other organisms during plant-pathogen, plant-pollinator, and plantmicrobiome interactions, and what the implications are for adaptation and domestication (Hevia et al 2015;Yon et al 2017;Fenske et al 2018;Hubbard et al 2018). It is clear that the plant circadian clock has a central role to play in adapting crops to the ever-changing environment; however, there remains a great deal we do not yet know about circadian clocks in different plant species and their roles in distinct environments.…”

Herbivory elicits changes in green leaf volatile production via jasmonate signaling and the circadian clock

“…Plant metabolism is synchronized with environmental rhythms (Wijnen & Young, ) and around 30% of expressed genes in A. thaliana have circadian patterns of transcript accumulation (Covington, Maloof, Straume, Kay, & Harmer, ; Harmer et al, ; Pan et al, ). The circadian clock can increase plant Darwinian fitness by coordinating plant metabolism with environmental factors, for example, light/dark cycles (Dodd et al, ), herbivory (Goodspeed, Chehab, Min‐Venditti, Braam, & Covington, ), and pollination (Atamian et al, ; Yon, Kessler, Joo, Kim, & Baldwin, ). Emission of GLVs is strongly affected by the timing of herbivore attack (Joo et al, ).…”

Circadian Regulation of the Plant Transcriptome Under Natural Conditions

“…The N. attenuata circadian oscillator also appears to contribute to the rate of flower opening and flower angle (Yon et al, 2016). Although circadian regulation modified flower selection by moths under laboratory conditions (Yon et al, 2016), these findings did not extrapolate with statistical significance to field conditions (Yon et al, 2017b). This illustrates how roles for circadian regulation can differ between field and laboratory conditions, and the need to extrapolate cautiously from the laboratory to field.…”

“…Translation of laboratory research concerning circadian rhythms into information of agricultural benefit requires an understanding of circadian regulation in crops under both artificial and natural environments. Understanding circadian regulation in crops provides opportunities to alter the latitudinal range of cultivation (Müller et al, 2015; Nakamichi, 2015), intercept developmental and signaling processes including photoperiodism (Turner et al, 2005; Nakamichi, 2015) and stress responses (Fowler et al, 2005; Bieniawska et al, 2008; Nakamichi et al, 2009; Seo et al, 2012; Nakamichi et al, 2016), manipulate plant defences or pollination biology (Roden and Ingle, 2009; Goodspeed et al, 2012; Yon et al, 2017a; Yon et al, 2017b), and fuse chemical biology and circadian biology to develop and optimize agrochemical use (Belbin et al, 2019; Uehara et al, 2019). On the other hand, plant breeding that causes inadvertent alterations in circadian clock function could have deleterious consequences for crop performance.…”