Circadian, Carbon, and Light Control of Expansion Growth and Leaf Movement

Abstract

We used Phytotyping 4D to investigate the contribution of clock and light signaling to the diurnal regulation of rosette expansion growth and leaf movement in Arabidopsis (Arabidopsis thaliana). Wild-type plants and clock mutants with a short (lhycca1) and long (prr7prr9) period were analyzed in a T24 cycle and in T-cycles that were closer to the mutants' period. Wild types also were analyzed in various photoperiods and after transfer to free-running light or darkness. Rosette expansion and leaf movement exhibited a circadian oscillation, with superimposed transients after dawn and dusk. Diurnal responses were modified in clock mutants. lhycca1 exhibited an inhibition of growth at the end of night and growth rose earlier after dawn, whereas prr7prr9 showed decreased growth for the first part of the light period. Some features were partly rescued by a matching T-cycle, like the inhibition in lhycca1 at the end of the night, indicating that it is due to premature exhaustion of starch. Other features were not rescued, revealing that the clock also regulates expansion growth more directly. Expansion growth was faster at night than in the daytime, whereas published work has shown that the synthesis of cellular components is faster in the day than at nighttime. This temporal uncoupling became larger in short photoperiods and may reflect the differing dependence of expansion and biosynthesis on energy, carbon, and water. While it has been proposed that leaf expansion and movement are causally linked, we did not observe a consistent temporal relationship between expansion and leaf movement.

Multiple circadian clock outputs regulate diel turnover of carbon and nitrogen reserves

“…Hydrolysis of sucrose to reducing sugars may have further functions in addition to increasing starch accumulation. The transient peak of reducing sugars at about ZT4 coincides with a maximum in the circadian oscillation in rosette expansion (Apelt et al, , ; Dornbusch, Michaud, Xenarios, & Fankhauser, ; Poiré et al, ). EC plays an important role in the circadian regulation of extension growth in hypocotyls (Nozue et al, ) and roots (Yazdanbakhsh et al, ).…”

“…Wild-type plants pace mobilization to about 24 hr after the previous dawn, with the result that starch is incompletely exhausted in a T-17 cycle and is prematurely exhausted in a T-28 cycle (Graf, Schlereth, Stitt, & Smith, 2010). Starch is exhausted prematurely in the short-period lhy cca1 mutant (Graf et al, 2010;Scialdone et al, 2013) resulting in an inhibition of growth before dawn that can be prevented by growing the mutant in a short T-cycle (Apelt et al, 2017;Graf et al, 2010) or by providing exogenous sugar (Yazdanbakhsh et al, 2011). This underlines the impor- Scialdone et al (2013) proposed that plants set an appropriate rate of starch mobilization at night by arithmetic division of the starch content by the remaining time to dawn.…”

Circadian Rhythms in Plants

“…New findings suggest that the circadian clock can regulate growth not only on a wholeplant or organ level but can differentially regulate growth in a subset of cells within a specific organ (Atamian et al 2016;Endo 2016;Apelt et al 2017;Ke et al 2018). The first written record of diel rhythms was the observation in the fourth century BC that a number of plants show daily rhythms in leaf movement (McClung, 2006).…”

“…However, most species lack pulvini and leaf movements are thought to rely on differential expansion of cells on the adaxial and abaxial sides of petioles (Polko et al 2012;Rauf et al 2013). Recently, this differential growth and leaf movement in Arabidopsis was found to depend on the PRR clock components, with a prr7prr9 double mutant displaying poor leaf movements compared with wild-type plants (Apelt et al 2017). These results suggest that the circadian clock can reg-ulate the differential expansion of specific cell layers to mediate leaf movement.…”

Nighttime gibberellin biosynthesis is influenced by fluctuating environmental conditions and contributes to growth adjustments of Arabidopsis leaves

“…However, size increases of plants do not necessarily follow carbon availability. Hypocotyl and leaf expansion rates have been shown to vary throughout the day, and these expansion patterns have been attributed to the circadian clock and light signalling (6)(7)(8). Interestingly, expansion and metabolic biosynthesis can be distinctly regulated.…”