The embryonic transcriptome of Parhyale hawaiensis reveals different dynamics of microRNAs and mRNAs during the maternal-zygotic transition

Abstract

Parhyale hawaiensis has emerged as the crustacean model of choice due to its tractability, ease of imaging, sequenced genome, and development of CRISPR/Cas9 genome editing tools. However, transcriptomic datasets spanning embryonic development are lacking, and there is almost no annotation of non-protein-coding RNAs, including microRNAs. We have sequenced microRNAs, together with mRNAs and long non-coding RNAs, in Parhyale using paired size-selected RNA-seq libraries at seven time-points covering important transitions in embryonic development. Focussing on microRNAs, we annotate 175 loci in Parhyale, 88 of which have no known homologs. We use these data to annotate the microRNAome of 37 crustacean genomes, and suggest a core crustacean microRNA set of around 61 sequence families. We examine the dynamic expression of microRNAs and mRNAs during the maternal-zygotic transition. Our data suggest that zygotic genome activation occurs in two waves in Parhyale with microRNAs transcribed almost exclusively in the second wave. Contrary to findings in other arthropods, we do not predict a general role for microRNAs in clearing maternal transcripts. These data significantly expand the available transcriptomics resources for Parhyale, and facilitate its use as a model organism for the study of small RNAs in processes ranging from embryonic development to regeneration.

The transcriptional landscape of the giant freshwater prawn: Embryonic development and early sexual differentiation mechanisms

“…Prior to the maternal-to-zygotic transition, the embryo genome is not transcribed, and all the RNA is of maternal origin. This time window of the maternal-to-zygotic transition is in accordance with the expression pattern of g25172 and g32461, the homologs of Zelda, the activator of the zygotic genome during the maternal-to-zygotic transition in Drosophila, and with findings in Parhyale hawaiensis, in which only maternal RNA is found in eight-cell embryos (0-9 hours post fertilization), whereas in 32-cell embryos (9.5-12 hours post fertilization) zygotic RNA is already being transcribed (54).…”

“…Nonetheless, many of the genes that were upregulated in males only on day 1 were on the Z chromosome, which has two copies in males and neo-females (ZZ) and one copy in females. Although we cannot rule out the possibility that most of the transcriptional differences between the sexes occur transiently on day 1, i.e., early in embryonic development, it is more likely that day-1 embryos have not yet undergone the maternal-to-zygotic transition, which is conserved in metazoans ( 53 ), including crustaceans ( 54 ). Thus, day-1 embryos possibly contain a larger quantity of maternal RNA, and thus the differences between the sexes may be attributed to maternal RNA, which is transcribed from neo-females (mature ZZ females) or from mature WW females.…”

Molecular Approaches Detect Early Signals of Programmed Cell Death in Hippolyte inermis Leach

“…Taking into account that several crustaceans are employed for evolutionary developmental studies because of their unique physiologic properties [ 49 , 50 , 51 , 52 ], the results obtained are suitable for application in investigations on other protandric species. For example, Parhyale hawaiensis is a well-known amphipod for which an extensive toolbox for genetic manipulation is available [ 53 , 54 , 55 , 56 ] and several pandalid and hippolytid decapods exhibit interesting patterns of sex reversal, in addition to the other families of crustaceans containing hermaphroditic species. However, despite the availability of several model organisms, genetic variations of key cellular processes and their functional consequences have received less attention [ 16 ].…”