Antiphase Light and Temperature Cycles Affect PHYTOCHROME B-Controlled Ethylene Sensitivity and Biosynthesis, Limiting Leaf Movement and Growth of Arabidopsis

Abstract

In the natural environment, days are generally warmer than the night, resulting in a positive day/night temperature difference (+DIF). Plants have adapted to these conditions, and when exposed to antiphase light and temperature cycles (cold photoperiod/ warm night [2DIF]), most species exhibit reduced elongation growth. To study the physiological mechanism of how light and temperature cycles affect plant growth, we used infrared imaging to dissect growth dynamics under +DIF and 2DIF in the model plant Arabidopsis (Arabidopsis thaliana). We found that 2DIF altered leaf growth patterns, decreasing the amplitude and delaying the phase of leaf movement. Ethylene application restored leaf growth in 2DIF conditions, and constitutive ethylene signaling mutants maintain robust leaf movement amplitudes under 2DIF, indicating that ethylene signaling becomes limiting under these conditions. In response to 2DIF, the phase of ethylene emission advanced 2 h, but total ethylene emission was not reduced. However, expression analysis on members of the 1-aminocyclopropane-1-carboxylic acid (ACC) synthase ethylene biosynthesis gene family showed that ACS2 activity is specifically suppressed in the petiole region under 2DIF conditions. Indeed, petioles of plants under 2DIF had reduced ACC content, and application of ACC to the petiole restored leaf growth patterns. Moreover, acs2 mutants displayed reduced leaf movement under +DIF, similar to wild-type plants under 2DIF. In addition, we demonstrate that the photoreceptor PHYTOCHROME B restricts ethylene biosynthesis and constrains the 2DIF-induced phase shift in rhythmic growth. Our findings provide a mechanistic insight into how fluctuating temperature cycles regulate plant growth.

Thermoperiodic Control of Hypocotyl Elongation Depends on Auxin-Induced Ethylene Signaling That Controls Downstream PHYTOCHROME INTERACTING FACTOR3 Activity

“…7, C and D). As shown before, phyB-9 showed a strong elongation response under both +DIF and 2DIF (Bours et al, 2013), and the treatment with AVG indicated a stronger contribution of ethylene to the elongation response under +DIF than under 2DIF (Fig. 7, C and D).…”

“…1, D-F). Previously, we showed that 2DIF reduces ethylene sensitivity in Arabidopsis seedlings (Bours et al, 2013). Because of the light-dependent role of ethylene in hypocotyl elongation (Smalle et al, 1997; Figure 1.…”

“…Therefore, 2DIF is frequently applied in greenhouses to reduce elongation (Myster and Moe, 1995). In Arabidopsis (Arabidopsis thaliana), 2DIF inhibits inflorescence stem and leaf elongation, and a 10°C 2DIF results in up to a 40% decrease of final leaf length compared with 10°C +DIF (Thingnaes et al, 2003;Bours et al, 2013). Although economically important in horticulture, a full mechanistic understanding of how 2DIF specifically affects elongation is still lacking.…”

Ethylene Signaling Influences Light-Regulated Development in Pea

“…In either case, these results suggest that growth changes in response to quality of light may also reflect adjustment of ethylene production, which was also reported in tobacco (Nicotiana tabacum) and Sorghum bicolor (Finlayson et al, 1999;Pierik et al, 2004). Although there is also evidence in the literature to suggest that light may influence ethylene sensitivity (Bours et al, 2013), the fact that blocking ethylene biosynthesis can rescue phyA phyB internode-length phenotypes in mature plants under white light (Foo et al, 2006) suggests that the effects of light on ethylene production may dominate in this system.…”

Genome-Wide Association Mapping and Genomic Prediction Elucidate the Genetic Architecture of Morphological Traits in Arabidopsis

“…ACS11 expression was high in petioles and ethylene nullified the differences in the PL/LL between two distinct haplotypes. From previous studies, it is known that ethylene can significantly influence PL and angle under different conditions and that ACS enzymes affect ethylene production (Tsuchisaka et al, 2009;van Zanten et al, 2009;Bours et al, 2013). All ACS genes are expressed in petioles, but only ACS2, 8, and 11 are differentially expressed between petiole and leaf blade (Bours et al, 2013).…”