Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis

© 2023 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Main Authors: Fernández-Nicolas, Ana, Machaj, Gabriela, Ventós-Alfonso, Alba, Pagone, Viviana, Toshinori Minemura, Ohde, Takahiro, Daimon, Takaaki, Ylla, Guillem, Bellés, Xavier
Other Authors: Agencia Estatal de Investigación (España)
Format: artículo biblioteca
Language:English
Published: National Academy of Sciences (U.S.) 2023-02-06
Subjects:E93, Insect metamorphosis, Embryogenesis, Complex life cycles,
Online Access:http://hdl.handle.net/10261/348661
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id dig-ibe-es-10261-348661
record_format koha
institution IBE ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-ibe-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del IBE España
language English
topic E93
Insect metamorphosis
Embryogenesis
Complex life cycles
E93
Insect metamorphosis
Embryogenesis
Complex life cycles
spellingShingle E93
Insect metamorphosis
Embryogenesis
Complex life cycles
E93
Insect metamorphosis
Embryogenesis
Complex life cycles
Fernández-Nicolas, Ana
Machaj, Gabriela
Ventós-Alfonso, Alba
Pagone, Viviana
Toshinori Minemura
Ohde, Takahiro
Daimon, Takaaki
Ylla, Guillem
Bellés, Xavier
Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis
description © 2023 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
author2 Agencia Estatal de Investigación (España)
author_facet Agencia Estatal de Investigación (España)
Fernández-Nicolas, Ana
Machaj, Gabriela
Ventós-Alfonso, Alba
Pagone, Viviana
Toshinori Minemura
Ohde, Takahiro
Daimon, Takaaki
Ylla, Guillem
Bellés, Xavier
format artículo
topic_facet E93
Insect metamorphosis
Embryogenesis
Complex life cycles
author Fernández-Nicolas, Ana
Machaj, Gabriela
Ventós-Alfonso, Alba
Pagone, Viviana
Toshinori Minemura
Ohde, Takahiro
Daimon, Takaaki
Ylla, Guillem
Bellés, Xavier
author_sort Fernández-Nicolas, Ana
title Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis
title_short Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis
title_full Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis
title_fullStr Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis
title_full_unstemmed Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis
title_sort reduction of embryonic e93 expression as a hypothetical driver of the evolution of insect metamorphosis
publisher National Academy of Sciences (U.S.)
publishDate 2023-02-06
url http://hdl.handle.net/10261/348661
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spelling dig-ibe-es-10261-3486612024-02-28T13:05:32Z Reduction of embryonic E93 expression as a hypothetical driver of the evolution of insect metamorphosis Fernández-Nicolas, Ana Machaj, Gabriela Ventós-Alfonso, Alba Pagone, Viviana Toshinori Minemura Ohde, Takahiro Daimon, Takaaki Ylla, Guillem Bellés, Xavier Agencia Estatal de Investigación (España) Ministerio de Ciencia, Innovación y Universidades (España) Ministerio de Economía y Competitividad (España) Generalitat de Catalunya European Commission Ministry of Education, Culture, Sports, Science and Technology (Japan) Jagiellonian University in Kraków Fernández-Nicolas, Ana [0000-0002-4570-1893] Ventós-Alfonso, Alba [0000-0002-1386-505X] Pagone, Viviana [0000-0002-8725-629X] Ylla, Guillem [0000-0003-4540-0131] Bellés, Xavier [0000-0002-1566-303X] E93 Insect metamorphosis Embryogenesis Complex life cycles © 2023 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). The early embryo of the cockroach Blattella germanica exhibits high E93 expression. In general, E93 triggers adult morphogenesis during postembryonic development. Here we show that E93 is also crucial in early embryogenesis in the cockroach, as a significant number of E93-depleted embryos are unable to develop the germ band under maternal RNAi treatment targeting E93. Moreover, transcriptomic analysis indicates that E93 depletion results in important gene expression changes in the early embryo, and many of the differentially expressed genes are involved in development. Then, using public databases, we gathered E93 expression data in embryo and preadult stages, finding that embryonic expression of E93 is high in hemimetabolan species (whose juveniles, or nymphs, are similar to the adult) and low in holometabolans (whose juveniles, or larvae, are different from the adult). E93 expression is also low in Thysanoptera and in Hemiptera Sternorrhyncha, hemimetabolans with postembryonic quiescent stages, as well as in Odonata, the nymph of which is very different from the adult. In ametabolans, such as the Zygentoma Thermobia domestica, E93 transcript levels are very high in the early embryo, whereas during postembryonic development they are medium and relatively constant. We propose the hypothesis that during evolution, a reduction of E93 expression in the embryo of hemimetabolans facilitated the larval development and the emergence of holometaboly. Independent decreases of E93 transcripts in the embryo of Odonata, Thysanoptera, and different groups of Hemiptera Sternorrhyncha would have allowed the development of modified juvenile stages adapted to specific ecophysiological conditions. The work was supported by the Spanish Agencia Estatal de Investigación (grant number PID2019-104483 GB-I00/funded by MCIN/AEI/10.13039/501100011033; CGL2015‐64727‐P; and CGL2012‐36251, to X.B.), the Catalan Government (2017 SGR 1030, to X.B.), and the European Fund for Economic and Regional Development (FEDER funds, to X.B.), as well as the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grants-in-Aid for Scientific Research, KAKENHI, numbers 20H02999 and 17H03943, to T.D.) and JSPS Bilateral Joint Research Projects (JPJSBP120209917, to T.D.). Part of this research has been financed (to G.Y.) by the Faculty of Biochemistry, Biophysics and Biotechnology at Jagiellonian University (Poland), under the Strategic Programme Excellence Initiative. Peer reviewed 2024-02-28T13:05:31Z 2024-02-28T13:05:31Z 2023-02-06 artículo Proceedings of the National Academy of Sciences of the United States of America 120(7): e2216640120 (2023) 0027-8424 http://hdl.handle.net/10261/348661 10.1073/pnas.2216640120 1091-6490 en #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-104483GB-I00/ES/EL TERCER RECEPTOR DE INSULINA DE LAS CUCARACHAS/ info:eu-repo/grantAgreement/MINECO//CGL2015‐64727‐P info:eu-repo/grantAgreement/MINECO//CGL2012‐36251 Publisher's version https://doi.org/10.1073/pnas.2216640120 Sí open application/pdf National Academy of Sciences (U.S.)

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