Circadian Rhythms Confer a Higher Level of Fitness to Arabidopsis Plants

Abstract

Circadian rhythms have been demonstrated in organisms across the taxonomic spectrum. In view of their widespread occurrence, the adaptive significance of these rhythms is of interest. We have previously shown that constitutive expression of the CCA1 (CIRCADIAN CLOCK ASSOCIATED 1) gene in Arabidopsis plants (CCA1-ox) results in loss of circadian rhythmicity. Here, we demonstrate that these CCA1-ox plants retain the ability to respond to diurnal changes in light. Thus, transcript levels of several circadian-regulated genes, as well as CCA1 itself and the closely related LHY, oscillate robustly if CCA1-ox plants are grown under diurnal conditions. However, in contrast with wild-type plants in which transcript levels change in anticipation of the dark/light transitions, the CCA1-ox plants have lost the ability to anticipate this daily change in their environment. We have used CCA1-ox lines to examine the effects of loss of circadian regulation on the fitness of an organism. CCA1-ox plants flowered later, especially under long-day conditions, and were less viable under very short-day conditions than their wild-type counterparts. In addition, we demonstrate that two other circadian rhythm mutants, LHY-ox and elf3, have low-viability phenotypes. Our findings demonstrate the adaptive advantage of circadian rhythms in Arabidopsis.First described in plants more than 270 years ago, circadian rhythms have been found in the vast majority of eukaryotes examined and in many prokaryotes. The basic mechanisms that are responsible for circadian rhythms are being elucidated in several model species. At the core of a circadian system is a molecular oscillator that generates a period of rhythmicity of about 24 h. The oscillator is self-sustaining, but it is influenced by environmental cues such as changes in light and temperature conditions (Dunlap, 1999). The oscillator controls a plethora of biological processes including nitrogen fixation in cyanobacteria (Johnson et al., 1996), scent emission in plants ( Kolosova et al., 2001), conidiation in Neurospora crassa. (Pittendrigh et al., 1959), olfactory responses of Drosophila melanogaster (Krishnan et al., 1999), luteinizing hormone levels in birds (Follett et al., 1974), and wheel running activity in hamsters (Mesocricetus auratus; Ralph and Menaker, 1988). The fact that circadian regulation is ubiquitous across the taxonomic spectrum and that its importance was even recognized in the Hebrew Bible (Ancoli-Israel, 2001) suggests that it is important for optimizing an organism's response to its environment and enhancing its fitness.The circadian clock plays a number of different roles. One is in the regulation of photoperiodism, which is the detection and response to changes in the duration of days and nights that enables organisms to adapt to seasonal changes in their environment (Thomas, 1998). Photoperiodism controls reproduction in many organisms, including flowering time in many plants ( Thomas and Vince-Prue, 1997). This photoperiodic response ensures that plants flower duri...

Biological Rhythms Workshop IA: Molecular Basis of Rhythms Generation

“…This correlation suggests the evolutionary importance of tightly regulating internal timing to match the surrounding environment. Additional evidence for the adaptive advantage of maintaining an endogenous timekeeper is seen in plants that overexpress the core clock component CCA1 or LHY; these plants no longer regulate transcription in an anticipatory manner of light-todark transitions (Green et al 2002). Consequently, these plants flower under long-day conditions later than their wild-type counterparts and are less viable under short-day conditions.…”

Organ specificity in the plant circadian system is explained by different light inputs to the shoot and root clocks

“…In Arabidopsis, expression of about one‐third of the genome is under circadian regulation (Michael & McClung, 2003; Covington et al ., 2008) and at the physiological level the circadian clock can control many plant processes, including photosynthesis, leaf movement, hormone responses, stem extension and stomatal opening (McClung, 2006; Harmer, 2009; Pruneda‐Paz & Kay, 2010). Appropriate circadian timing can confer a competitive advantage (Green et al ., 2002; Dodd et al ., 2005). …”

Quinone sensing by the circadian input kinase of the cyanobacterial circadian clock

“…This program of cellular metabolism allows organisms to anticipate predictable daily environmental changes, and it provides an adaptive advantage (2,3). The circadian mechanism has been studied extensively in eukaryotic models such as fruit flies, fungi, and mice (4).…”