Photoregulation of Chloroplast Gene Transcription in the Chromophytic Alga Heterosigma carterae

Abstract

Light acts as a complex regulator of cellular development and gene expression in photoautotrophs. Although light signals are highly effective in controlling cellular division and chloroplast biogenesis in the toxic marine alga Heterosigma carterae, their influence on gene expression has not been well characterized. To address this need cultures of H. carterae synchronized by an alternating light-dark regime were sampled through 12 h of light and 12 h of dark to characterize cell division, chloroplast complement, and chloroplast RNA abundance. These studies have identified a unimodal pattern of chloroplast transcriptional activity for a suite of cellular and photosynthetic genes. To determine the alga's response to a change in photoperiod, 12-h light/12-h dark-synchronized cultures were transferred to constant light and then periodically sampled. Although cellular and chloroplast division cycles remained synchronized in constant conditions for 24 h, the transcriptional apparatus responded by increasing ctRNA abundance within 45 min of the change in photoperiod. However, the ability of the alga to mount this rapid transcriptional response was limited to the first 2 h of the putative dark period. Thus, the chloroplast transcriptional apparatus of H. carterae may initiate a rapid, temporally gated response to a change in photoperiod that is independent of ongoing light-entrained cellular and chloroplast division cycles.

Genome-wide diel growth state transitions in the diatom Thalassiosira pseudonana

“…(RuBisCO), aldose-1-epimerase, and transketolase] and protein synthesis were up-regulated in apparent anticipation of the impending light phase (Fig. S6), in agreement with prior findings for genes encoding photosynthetic functions in algae (29)(30)(31)(32). This supports the theory that diatom gene regulation becomes entrained to anticipate the diurnal cycle such that the up-regulation of photosynthetic genes precedes the onset of light (33,34).…”

“…pseudonana appears to be broadly entrained to anticipate the diurnal cycle at the level of gene expression, as previously suggested (29,30). The shift from exponential growth to nutrientdepleted stationary phase attenuated many diel patterns of expression.…”

Identification and expression analysis of blue light receptor aureochrome in the harmful alga Heterosigma akashiwo (raphidophyceae)

“…This is consistent with the phylogenetic result that HaAUREOs were divided to different groups. In addition, it is common that organisms up-regulate the expression of important genes in anticipation of changes in environmental cues (Doran and Cattolico, 1997). For example, many plants start to synthesize photosynthetic proteins before sunrise (Ashworth et al, 2013;Lin, 2002).…”

“…In two raphidophytes H. akashiwo and Chattonella antiqua, Shikata et al (2015) observed that these species required (blue) light to regulate diurnal vertical migration (DVM), which plays an important role on HAB development and formation. Moreover, light signals are also highly effective in controlling cyst germination, cell survival and accumulation, and cellular division in H. akashiwo (Doran and Cattolico, 1997;Lee et al, 2012;Shikata et al, 2007). In other stramenopiles algae such as diatoms, xanthophytes, and phaeophytes, BL also promotes germination of resting cells, modifies their growth and behavior, and controls their cell division (Huysman et al, 2010;Ishikawa et al, 2012;Kataoka, 1990;Kropf, 1992;Mercado et al, 2004;Shikata et al, 2009Shikata et al, , 2015Takahashi et al, 2001).…”

Chloroplast His-to-Asp signal transduction: a potential mechanism for plastid gene regulation in Heterosigma akashiwo (Raphidophyceae)

“…These organelles are surrounded by four membranes, indicative of their serial endosymbiotic origin from a putative rhodophytic ancestor [14,17]. As an obligate autotroph, H. akashiwo is dependent on chloroplast function for survival and responds to changing environmental cues by rapidly altering transcript levels within the plastid [18,19]. Run-on analysis clearly demonstrates that the changes in mRNA abundance are largely due to transcript initiation [19].…”