Processing bodies control the selective translation for optimal development of Arabidopsis young seedlings

Abstract

Significance Photomorphogenic development allows young plant seedlings to acquire photosynthetic activities and growth competitiveness when they emerge from soil. More than 1,000 mRNAs are translationally inert in dark-grown seedlings but quickly engage in translation when seedlings are first exposed to light signals. However, why some mRNAs undergo selective translation, how the selective translation is regulated, and why it is important remain unknown. Our work fills in this missing gap by demonstrating that processing bodies function as mRNA reservoirs in dark-grown seedlings. Photoreceptors negate the function of a negative regulator CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1), thereby reducing the accumulation of processing bodies in light-grown seedlings to release thousands of mRNAs for translation, which explains in part the light-enhanced global translation in photomorphogenic seedlings. Germinated plant seeds buried in soil undergo skotomorphogenic development before emergence to reach the light environment. Young seedlings transitioning from dark to light undergo photomorphogenic development. During photomorphogenesis, light alters the transcriptome and enhances the translation of thousands of mRNAs during the dark-to-light transition in Arabidopsis young seedlings. About 1,500 of these mRNAs have comparable abundance before and after light treatment, which implies widespread translational repression in dark-grown seedlings. Processing bodies (p-bodies), the cytoplasmic granules found in diverse organisms, can balance the storage, degradation, and translation of mRNAs. However, the function of p-bodies in translation control remains largely unknown in plants. Here we found that an Arabidopsis mutant defective in p-body formation (Decapping 5; dcp5-1) showed reduced fitness under both dark and light conditions. Comparative transcriptome and translatome analyses of wild-type and dcp5-1 seedlings revealed that p-bodies can attenuate the premature translation of specific mRNAs in the dark, including those encoding enzymes for protochlorophyllide synthesis and PIN-LIKES3 for auxin-dependent apical hook opening. When the seedlings protrude from soil, light perception by photoreceptors triggers a reduced accumulation of p-bodies to release the translationally stalled mRNAs for active translation of mRNAs encoding proteins needed for photomorphogenesis. Our data support a key role for p-bodies in translation repression, an essential mechanism for proper skotomorphogenesis and timely photomorphogenesis in seedlings.