Fluctuating Light Interacts with Time of Day and Leaf Development Stage to Reprogram Gene Expression

Abstract

Natural light environments are highly variable. Flexible adjustment between light energy utilization and photoprotection is therefore of vital importance for plant performance and fitness in the field. Short-term reactions to changing light intensity are triggered inside chloroplasts and leaves within seconds to minutes, whereas long-term adjustments proceed over hours and days, integrating multiple signals. While the mechanisms of long-term acclimation to light intensity have been studied by changing constant growth light intensity during the day, responses to fluctuating growth light intensity have rarely been inspected in detail. We performed transcriptome profiling in Arabidopsis (Arabidopsis thaliana) leaves to investigate long-term gene expression responses to fluctuating light (FL). In particular, we examined whether responses differ between young and mature leaves or between morning and the end of the day. Our results highlight global reprogramming of gene expression under FL, including that of genes related to photoprotection, photosynthesis, and photorespiration and to pigment, prenylquinone, and vitamin metabolism. The FL-induced changes in gene expression varied between young and mature leaves at the same time point and between the same leaves in the morning and at the end of the day, indicating interactions of FL acclimation with leaf development stage and time of day. Only 46 genes were up-or down-regulated in both young and mature leaves at both time points. Combined analyses of gene coexpression and cis-elements pointed to a role of the circadian clock and light in coordinating the acclimatory responses of functionally related genes. Our results also suggest a possible cross talk between FL acclimation and systemic acquired resistance-like gene expression in young leaves.Adjustments of photosynthetic light energy utilization and photoprotection to changing light intensity are triggered over different time scales. Rapid changes (seconds to minutes) are induced inside chloroplasts by reduction of electron transport chain or upon formation of a [H + ] gradient (DpH) across the thylakoid membrane. Short-term responses have been studied intensively to unveil various regulatory mechanisms involved therein. Reduction of the plastoquinone (PQ) pool by preferential excitation of PSII relative to PSI, for example, leads to activation of thylakoid protein kinase STN7, which phosphorylates PSII light-harvesting complex (LHC) to trigger its displacement from PSII to PSI in a process termed state transition (Bellafiore et al., 2005). Light-dependent acidification of thylakoid lumen protonates the PSBS protein to quickly induce thermal energy dissipation (or nonphotochemical quenching [NPQ]) and thus down-regulate PSII (Li et al., 2000). Lumen acidification also activates a xanthophyll-cycle enzyme, violaxanthin deepoxidase (VDE), to convert violaxanthin to antheraxanthin and zeaxanthin, which enhances NPQ (Niyogi et al., 1998). Furthermore, alternative electron (e 2 ) flows (e.g. waterwater cycle and cyclic e 2...

Fluctuating light experiments and semi-automated plant phenotyping enabled by self-built growth racks and simple upgrades to the IMAGING-PAM

“…To validate the script and to provide interested users with a training dataset, we recorded an eleven-day fluctuating light experiment using mostly genotypes recently tested in a five day long Dynamic Environmental Photosynthetic Imaging run (Höhner et al, 2019) (Figure 6). In line with earlier studies, we found that all genotypes were affected by fluctuating light (Vialet-Chabrand et al, 2017;Schneider et al, 2019). Leaf surface area in WT plants decreased by more than half.…”

Photosynthetic Acclimation to Fluctuating Irradiance in Plants

“…Nuclear gene expression reacts to irradiance in a highly dynamic way: hundreds of transcripts change within seconds-minutes after increases (Suzuki et al, 2015) and decreases (Crisp et al, 2017) in irradiance, suggesting that under a naturally fluctuating irradiance, gene expression will also be strongly affected. Indeed, a recent ground-breaking study (Schneider et al, 2019) has demonstrated the impact of fluctuating irradiance on gene expression in Arabidopsis. Short and strong light pulses, applied repeatedly for 3 d, caused a differential expression (DE) of ∼4000 genes, 75% of which were upregulated.…”

“…The molecular response to fluctuating irradiance goes far beyond that of photooxidative stress: the data by Schneider et al (2019) suggested that processes regulating plant growth are affected on many levels, and that the expression of the respective genes is further under strong circadian and developmental control. However, altered gene expression does not necessarily equate altered protein abundance.…”

Growth under Fluctuating Light Reveals Large Trait Variation in a Panel of Arabidopsis Accessions

“…Correlation analysis revealed a greater reduction in Φ PSII under FL the further north on the globe the accession had originated from (Figure 8). This finding could potentially be explained by the following factors, considering that the main phase of vegetative growth of most Arabidopsis accessions is in early spring: (i) lower temperatures with increasing latitude, thus, accessions from further north may have optimized their photosynthesis to lower temperatures than those in our experiment (16 • C night, 21 • C day); (ii) differences in day length, because changes in gene expression that drive acclimation in response to FL have been shown to intercept with the circadian clock [3]; and/ or (iii) light intensity and availability.…”

“…However, plant responses strongly depend on the environment that plants have acclimated to, as they adjust their metabolism to cope most efficiently with the prevailing condition. Several recent studies focused on the model plant Arabidopsis thaliana (hereafter: Arabidopsis) under dynamic light [1][2][3], but these were restricted to few accessions only and thus did not assess the effects of genetic factors. The study of a larger set of genotypes is warranted, also because photosynthesis shows great intraspecific variation in Arabidopsis [4,5], and variation on the genetic level has been shown to translate more strongly into phenotypic variation under fluctuating light regimes (FL; [6]).…”