Only a Matter of Time: the Impact of Daily and Seasonal Rhythms on Phytochemicals

Phytochem Rev https://doi.org/10.1007/s11101-019-09617-z (0123456789().,-volV)(0123456789().,-volV) Only a matter of time: the impact of daily and seasonal rhythms on phytochemicals Donna J. Liebelt . Juliette T. Jordan . Colleen J. Doherty Received: 1 February 2019 / Accepted: 11 June 2019 Ó Springer Nature B.V. 2019 Abstract Plants regulate molecular bioactivity in Graphic abstract Temporal regulation of phyto- response to daily and seasonal environmental fluctu- chemical composition. The phytochemical composi- ations in temperature, light, humidity, and precipita- tion of a plant is under complex control, affected by tion. These rhythms interconnect, overlap, and both external environmental factors and endogenous feedback both into each other and into the plant’s circadian rhythms. The environmental factors that endogenous circadian clock. The resulting regulatory directly affect phytochemical profiles and concentra- network tightly ensures that the overall phytochemical tions themselves vary across time of day and time of composition is highly adaptive to the plant’s needs at year. These cyclic environmental factors also entrain any point in time. Temporally coordinated control of the endogenous circadian clock which imposes addi- primary and secondary metabolism ensures phyto- tional regulation on the production and processing of chemicals are in tune with the demands of the many phytochemicals. This concerted effort to ensure environment and the available resources. As a conse- phytochemicals are exquisitely in tune with the quence, phytochemical composition varies throughout demands of the environment results in fluctuating the day and year. This variation in phytochemical phytochemical composition. Variation in phytochem- abundance and composition across time can affect ical abundance and composition across time can affect experimental results and conclusions. Understanding experimental results and conclusions. Failing to how phytochemical composition varies across time is consider the factors of time of day and year can result critical for uncovering the underlying regulatory in misleading or inconsistent estimations of the connections and ultimately improving the quality of potency and composition of phytochemical extrac- phytochemical products. Herein, we review the mech- tions. Integrating temporal factors will improve our anisms underlying diel and seasonal variations in understanding of the underlying regulatory connec- phytochemical composition and provide examples of tions and ultimately improve the quality of phyto- temporal regulation of specific compounds within chemical products. phenol, terpenoid, and alkaloid phytochemical classes. D. J. Liebelt Á J. T. Jordan Á C. J. Doherty (&) Department of Molecular and Structural Biochemistry, North Carolina State University, Raleigh, NC, USA e-mail: [email protected] 123 Phytochem Rev Keywords Diel Á Time of day Á Temporal between tea leaves grown in the sun versus shade regulation Á Circadian rhythms Á Photoperiod (Ahmed et al. 2010) or harvested during the monsoon responses Á Environmental regulation Á Specialized season versus the dry spring (Ahmed et al. 2014). metabolites Á Phenols Á Flavonoids Á Terpenoids Á Therefore, understanding how environmental factors Alkaloids impact the phytochemical composition can have profound consequences in breeding and agricultural production of specialty crops. Variation in primary metabolism throughout dif- Introduction ferent times of day or seasons of the year is well- established (Farre´ and Weise 2012). However, com- The properties that determine the perceived value of a paratively little is known on the temporal regulation of plant as a source for phytochemicals depend on the specialized metabolites. Temporal changes in metabo- composition, relative concentration, and potency of lite concentrations can alter the efficacy of nutraceu- these bioactive molecules. All of these factors can ticals. Daily or seasonal changes in the metabolic vary as highly plastic plant biochemistry responds profile of a plant can alter the toxicity or potency. dynamically to the environment. Research on spe- Moreover, understanding the temporal variation in cialty crops producing phytochemicals has shown that specialized metabolites can improve selection and value-added phenotypes from aesthetics to flavor and breeding strategies, increasing the consistency of texture vary with environmental changes. In turn, phytochemical production and research. In this these variations can impact shelf life, food safety, and review, we focus on the impact of recurring daily health benefits that determine the value and drive the and seasonal cycles on phytochemical biochemistry. consumer perception of quality (Ahmed and Stepp We provide a general overview of the mechanisms that 2016). Risks for food waste and financial harm to can drive daily and seasonal variation in phytochem- producers and retailers are enhanced as devalued or ical levels and then provide specific examples of unaesthetic products are discarded (Buzby et al. 2014). compounds in various phytochemical classes that For example, consumers can taste the difference show daily and seasonal variation. Finally, we discuss 123 Phytochem Rev how current trends are changing these rhythmic and processing of specialized metabolites (Bla¨sing environmental patterns and how these changes may et al. 2005). Finally, the physiological and molecular impact phytochemical research and production. responses to abiotic and biotic stresses are ‘gated’ so In several plant species, the regulatory and biosyn- that the potential for response is maximal when the thetic genes of specialized metabolite pathways show stress stimulus is most likely to occur. circadian, diel, or photoperiod driven rhythmic transcript expression (Alabadı´ et al. 2002; Filichkin et al. Regulation of phytochemicals by changes in light 2011; Pavarini et al. 2012; Gyllenstrand et al. 2014; quality and temperature Soni et al. 2015; Fenske and Imaizumi 2016; Zeng et al. 2017; Greenham et al. 2017; Koda et al. 2017; For many phytochemicals, their accumulation levels Weiss et al. 2018; Yin et al. 2018; Yoshida and are directly affected by changes in light, temperature, Oyama-okubo 2018). The correlation between and water availability. As these environmental fea- changes in transcript and metabolite levels will depend tures vary both throughout the day and year, the on the environmental conditions and the specific impact of these environmental variables can result in pathway of interest. Therefore, in this review, where their altered accumulation depending on the time of possible, we focus on evidence of temporal variation day or year the plant is sampled. at the metabolite level. Light quality Daily cycles of environmental change drive The filtering effects of the atmosphere change as the variation in phytochemical production position of the sun in the sky changes throughout the and processing day and the year, altering the total light intensity. Additionally, since the atmospheric filtering is not Plants coordinate their molecular activities by time to consistent across all wavelengths, this change in the operate at optimum efficiency. Growth, stomatal angle of the sun also impacts the spectrum of light that opening, photosynthesis, metabolism, nutrient, and is available to plants. The accumulation of some water uptake are timed to coincide with the availabil- phytochemicals is directly impacted by changes in ity of resources; primarily light and water (Nozue and light quality, perhaps driving their daily and seasonal Maloof 2006; Harmer 2010). Throughout a 24 h variation in levels. period, there are changes in light intensity, light Blue light and other shorter wavelengths are quality, temperature, and humidity. These four factors strongly affected by Rayleigh scattering, resulting in have a direct impact on nutrient uptake and photosyn- a lower abundance of these wavelengths in winter as thesis and therefore impact the availability and well as dawn and dusk which leads to an increase in the distribution of carbon and nitrogen (Rufty et al. relative amount of the longer, red wavelengths. The 1989; Bla¨sing et al. 2005; Ruts et al. 2012). This ratio of the red to far-red wavelengths impacts cycling availability of carbon and nitrogen starting developmental transitions such as the transition to materials has consequences on the production and flowering. The mechanism for this sensitivity in processing of specialized metabolites. In addition to Arabidopsis is through the light-quality dependent modulating the availability of the building blocks switching of the phytochromes between active and necessary to generate specialized metabolites, these inactive states (Ulijasz and Vierstra 2011; Ushijima daily-changing environmental factors also directly et al. 2017; Sethe et al. 2017). The phytochromes in influence the pathways that regulate specialized Arabidopsis impact photosynthesis and primary meta- metabolites. Not only do temperature, humidity, light bolism (Yang et al. 2016a, b; Kreslavski et al. 2018). intensity, and quality directly influence specialized Loss of phytochromes alter the metabolic profiles with metabolite levels, these four factors also serve as cues increases in sugars and amino acids. These changes are to modulate the plant’s circadian clock so that it is in similar to those observed in plants under abiotic stress, sync with the local environment (McClung in particular, there is a large accumulation of proline 2006, 2008; Harmer 2010; Mwimba

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