Blue Light Checkpoint: How Blue Light Controls the Onset of Cell Division in Diatoms

Diatoms are tiny algae (see Figure) that are ubiquitous to aquatic environments, from backyard ponds to the open ocean. There are over 200,000 diatom species, which together carry out roughly one-fifth of the world's photosynthesis (Armbrust, 2009). Diatoms often live under variable conditions, which require them to adapt to rapid, intense changes in water temperature, nutrient availability, and light intensity. These fluctuations have a dramatic effect on the physiology and viability of these tiny organisms. While diatoms encounter many unpredictable conditions, there are also some constants in their lives. For example, diatoms are exposed to diurnal changes in light intensity. Because water selectively absorbs light of longer wavelengths, diatoms often encounter only blue light (450 to 500 nm) below the water's surface (Ragni and D’Alcala, 2007). Diatoms use photoreceptors such as aureochromes (Takahashi et al., 2007) to detect blue light. Centric diatom collected from Patagonia during the Tara Oceans expedition in 2011. (Photo by Christian Sardet.) Diatoms have developed mechanisms to adapt to and take advantage of diurnal fluctuations in blue light. Blue light controls many aspects of diatom physiology, not the least of which is the tightly regulated process of cell division. The presence of different cell cycle checkpoints ensures that genetic information is inherited correctly by inhibiting the replication and distribution of incomplete or damaged chromosomes to daughter cells. The major cell cycle checkpoints occur during the onset of DNA replication (G1-to-S transition) and mitosis (G2-to-M transition). While the onset of the cell cycle in diatoms is known to be dependent on light, little is known about how light perception is connected to cell cycle activation and progression. Huysman et al. (pages 215–228) help uncover the signaling cascade that controls the G1-to-S checkpoint in the cell cycle of the marine diatom Phaeodactylum tricornutum. When dark-arrested diatoms were exposed to light, diatom-specific cyclin2 (dsCYC2) transcript levels reached a peak within 10 to 15 min, long before the onset of cell division, followed by a translational peak 30 to 60 min after light exposure. This suggests that dsCYC2 may play a role in reactivating cell division upon illumination. The authors then used a yeast two-hybrid assay to show that dsCYC2 binds to the cyclin-dependent kinase CDKA1. Then, using a yeast complementation assay, they showed that dsCYC2 can complement G1 cyclin-deficient yeast. Also, P. tricornutum dsCYC2 knockdown lines showed a significant increase in generation time compared with wild-type cells, indicating that dsCYC2 is crucial for proper cell cycle progression. Moreover, silencing dsCYC2 decreased the rate of cell division in diatoms exposed to light-dark cycles, but not to constant light. Finally, dsCYC2 expression increased in response to blue light but not red light. The authors then searched for transcription factors that bind to and regulate the dsCYC2 promoter by performing a genome-wide yeast one-hybrid cDNA library screen. The screen yielded two putative bZIP transcription factors, namely, the classical bZIP transcription factor bZIP10 and, intriguingly, AUREOCHROME1a. Retransformation of AUREO1a and bZIP10 into the Y1H reporter strain confirmed their binding to the dsCYC2 promoter. Indeed, when genes encoding AUREO1a and bZIP10 were transiently expressed in tobacco (Nicotiana tabacum) protoplast cells, they functioned synergistically to activate the dsCYC2 promoter. Therefore, bZIP10 and the blue light receptor AUREO1a are involved in the blue light–dependent transcription of a cyclin gene that regulates the onset of the cell cycle in diatoms after a period of darkness. The light-dependent progression of the cell cycle may occur via a similar pathway in other organisms as well. Studying the tiny, adaptable diatom will no doubt shed light on many more basic questions in biology.