PMID- 35289745
OWN - NLM
STAT- MEDLINE
DCOM- 20220517
LR  - 20220914
IS  - 2050-084X (Electronic)
IS  - 2050-084X (Linking)
VI  - 11
DP  - 2022 Mar 15
TI  - Functional characterization of a 'plant-like' HYL1 homolog in the cnidarian 
      Nematostella vectensis indicates a conserved involvement in microRNA biogenesis.
LID - 10.7554/eLife.69464 [doi]
LID - e69464
AB  - While the biogenesis of microRNAs (miRNAs) in both animals and plants depends on 
      the RNase III Dicer, its partner proteins are considered distinct for each 
      kingdom. Nevertheless, recent discovery of homologs of Hyponastic Leaves1 (HYL1), 
      a 'plant-specific' Dicer partner, in the metazoan phylum Cnidaria, challenges the 
      view that miRNAs evolved convergently in animals and plants. Here, we show that 
      the HYL1 homolog Hyl1-like a (Hyl1La) is crucial for development and miRNA 
      biogenesis in the cnidarian model Nematostella vectensis. Inhibition of Hyl1La by 
      morpholinos resulted in metamorphosis arrest in Nematostella embryos and a 
      significant reduction in levels of most miRNAs. Further, meta-analysis of 
      morphants of miRNA biogenesis components, like Dicer1, shows clustering of their 
      miRNA profiles with Hyl1La morphants. Strikingly, immunoprecipitation of Hyl1La 
      followed by quantitative PCR revealed that in contrast to the plant HYL1, Hyl1La 
      interacts only with precursor miRNAs and not with primary miRNAs. This was 
      complemented by an in vitro binding assay of Hyl1La to synthetic precursor miRNA. 
      Altogether, these results suggest that the last common ancestor of animals and 
      plants carried a HYL1 homolog that took essential part in miRNA biogenesis and 
      indicate early emergence of the miRNA system before plants and animals separated.
CI  - (c) 2022, Tripathi et al.
FAU - Tripathi, Abhinandan M
AU  - Tripathi AM
AD  - Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of 
      Life Sciences, Faculty of Science, The Hebrew University of Jerusalem, Jerusalem, 
      Israel.
FAU - Admoni, Yael
AU  - Admoni Y
AD  - Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of 
      Life Sciences, Faculty of Science, The Hebrew University of Jerusalem, Jerusalem, 
      Israel.
FAU - Fridrich, Arie
AU  - Fridrich A
AD  - Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of 
      Life Sciences, Faculty of Science, The Hebrew University of Jerusalem, Jerusalem, 
      Israel.
FAU - Lewandowska, Magda
AU  - Lewandowska M
AD  - Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of 
      Life Sciences, Faculty of Science, The Hebrew University of Jerusalem, Jerusalem, 
      Israel.
FAU - Surm, Joachim M
AU  - Surm JM
AD  - Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of 
      Life Sciences, Faculty of Science, The Hebrew University of Jerusalem, Jerusalem, 
      Israel.
FAU - Aharoni, Reuven
AU  - Aharoni R
AD  - Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of 
      Life Sciences, Faculty of Science, The Hebrew University of Jerusalem, Jerusalem, 
      Israel.
FAU - Moran, Yehu
AU  - Moran Y
AUID- ORCID: 0000-0001-9928-9294
AD  - Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of 
      Life Sciences, Faculty of Science, The Hebrew University of Jerusalem, Jerusalem, 
      Israel.
LA  - eng
PT  - Journal Article
PT  - Meta-Analysis
PT  - Research Support, Non-U.S. Gov't
DEP - 20220315
PL  - England
TA  - Elife
JT  - eLife
JID - 101579614
RN  - 0 (Arabidopsis Proteins)
RN  - 0 (HYL1 protein, Arabidopsis)
RN  - 0 (MicroRNAs)
RN  - 0 (RNA-Binding Proteins)
SB  - IM
MH  - Animals
MH  - *Arabidopsis/genetics
MH  - *Arabidopsis Proteins/metabolism
MH  - *MicroRNAs/genetics/metabolism
MH  - Plants/genetics
MH  - RNA-Binding Proteins/metabolism
MH  - *Sea Anemones/genetics/metabolism
PMC - PMC9098223
OAB - In both animals and plants, small molecules known as micro ribonucleic acids (or 
      miRNAs for short) control the amount of proteins cells make from instructions 
      encoded in their DNA. Cells make mature miRNA molecules by cutting and modifying 
      newly-made RNA molecules in two stages. Some of the components animals and plants 
      utilize to make and use miRNAs are similar, but most are completely different. 
      For example, in plants an enzyme known as Dicer cuts newly made RNAs into mature 
      miRNAs with the help of a protein called HYL1, whereas humans and other animals 
      do not have HYL1 and Dicer works with alternative partner proteins, instead. 
      Therefore, it is generally believed that miRNAs evolved separately in animals and 
      plants after they split from a common ancestor around 1.6 billion years ago. 
      Recent studies on sea anemones and other primitive animals challenge this idea. 
      Proteins similar to HYL1 in plants have been discovered in sea anemones and 
      sponges, and sea anemone miRNAs show several similarities to plant miRNAs 
      including their mode of action. However, it is not clear whether these HYL1-like 
      proteins work in the same way as their plant counterparts. Here, Tripathi, Admoni 
      et al. investigated the role of the HYL1-like protein in sea anemones. The 
      experiments found that this protein was essential for the sea anemones to make 
      miRNAs and to grow and develop properly. Unlike HYL1 in plants - which is 
      involved in both stages of processing newly-made miRNAs into mature miRNAs - the 
      sea anemone HYL1-like protein only helped in the second stage to make mature 
      miRNAs from intermediate molecules known as precursor miRNAs. These findings 
      demonstrate that some of the components plants use to make miRNAs also perform 
      similar roles in sea anemones. This suggests that the miRNA system evolved before 
      the ancestors of plants and animals separated from each other. Questions for 
      future studies will include investigating how plants and animals evolved 
      different miRNA machinery, and why sponges and jellyfish have HYL1-like proteins, 
      whereas humans and other more complex animals do not.
OABL- eng
OTO - NOTNLM
OT  - Cnidaria
OT  - HYL1
OT  - Nematostella vectensis
OT  - evolutionary biology
OT  - microRNA
OT  - small RNA biogenesis
COIS- AT, YA, AF, ML, JS, RA, YM No competing interests declared
EDAT- 2022/03/16 06:00
MHDA- 2022/05/18 06:00
PMCR- 2022/03/15
CRDT- 2022/03/15 12:20
PHST- 2021/04/15 00:00 [received]
PHST- 2022/03/14 00:00 [accepted]
PHST- 2022/03/16 06:00 [pubmed]
PHST- 2022/05/18 06:00 [medline]
PHST- 2022/03/15 12:20 [entrez]
PHST- 2022/03/15 00:00 [pmc-release]
AID - 69464 [pii]
AID - 10.7554/eLife.69464 [doi]
PST - epublish
SO  - Elife. 2022 Mar 15;11:e69464. doi: 10.7554/eLife.69464.