Abstract
The photosynthetic capacity of mature leaves increases after several days' exposure to constant or intermittent episodes of high light (HL) and is manifested primarily as changes in chloroplast physiology. How this chloroplast-level acclimation to HL is initiated and controlled is unknown. From expanded Arabidopsis leaves, we determined HL-dependent changes in transcript abundance of 3844 genes in a 0-6h time-series transcriptomics experiment. It was hypothesized that among such genes were those that contribute to the initiation of HL acclimation. By focusing on differentially expressed transcription (co-)factor genes and applying dynamic statistical modelling to the temporal transcriptomics data, a regulatory network of 47 predominantly photoreceptor-regulated transcription (co-)factor genes was inferred. The most connected gene in this network was B-BOX DOMAIN CONTAINING PROTEIN32 (BBX32). Plants overexpressing BBX32 were strongly impaired in acclimation to HL and displayed perturbed expression of photosynthesis-associated genes under LL and after exposure to HL. These observations led to demonstrating that as well as regulation of chloroplast-level acclimation by BBX32, CRYPTOCHROME1, LONG HYPOCOTYL5, CONSTITUTIVELY PHOTOMORPHOGENIC1 and SUPPRESSOR OF PHYA-105 are important. In addition, the BBX32-centric gene regulatory network provides a view of the transcriptional control of acclimation in mature leaves distinct from other photoreceptor-regulated processes, such as seedling photomorphogenesis.
Highlights
Our plan was to subject groups of time-resolved differentially expressed genes (DEGs) to Variational Bayesian State Space Modelling (VBSSM; see Experimental procedures), which requires highly resolved time-series data (Beal et al, 2005; Bechtold et al, 2016; Penfold and BuchananWollaston, 2014; Penfold and Wild, 2011)
To determine DEGs that showed a significant difference between high light (HL)-exposed leaves and the LL controls over all or part of the time period, a Gaussian process two-sample test (GP2S; Stegle et al, 2010) was applied and 4069 probes were selected with a Bayes factor score >10, which corresponded to 3844 DEGs (Data S1)
We suggest that COP1 and SUPPRESSOR OF PHYA-105 (SPA) genes act together to suppress HL acclimation under LL by enabling the ubiquitin-mediated degradation of HY5 and coupling photosynthetic capacity to the prevailing photosynthetically active photon flux densities (PPFDs)
Summary
The exposure of plants to increased light intensities can lead to the development of enhanced photosynthetic capacity [here defined as high-light (HL) acclimation], is an important determinant of plant fitness or crop yield, is under genetic as well as environmental control and includes changes in the expression of many genes (Athanasiou et al, 2010; Eberhard et al, 2008; Murchie and Horton, 1997; Murchie et al, 2005; Oguchi et al, 2003; van Rooijen et al, 2015; Schottler and Toth, 2014; VialetChabrand et al, 2017; Walters et al, 1999). Diameter in minor veins and thickness of the lamina (Adams et al, 2014; Oguchi et al, 2003; Terashima et al., 2011; Vialet-Chabrand et al, 2017) This developmental acclimation includes changes to chloroplast physiology such as adjustments to the composition of reaction centres and light harvesting antennae (Drozak and Romanowska, 2006; Murchie and Horton, 1997; Murchie et al, 2005; Vialet-Chabrand et al, 2017; Walters et al, 1999). It was proposed that a PHYTOCHROMEA (PHYA), PHYB, and CRYPTOCHROME1 (CRY1) photoreceptor driven CONSTI-
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