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The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development

BACKGROUND: The Fertilization-related kinases (FRK) form a class that belongs to the MEKK subfamily of plant MAPKKKs. It was recently shown that FRK class kinases expanded during angiosperm evolution, reaching their maximum numbers in the lineage leading to solanaceous species and culminating in the...

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Autores principales: Daigle, Caroline, Mazin, Benjamin, Matton, Daniel P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6524262/
https://www.ncbi.nlm.nih.gov/pubmed/31096905
http://dx.doi.org/10.1186/s12870-019-1804-0
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author Daigle, Caroline
Mazin, Benjamin
Matton, Daniel P.
author_facet Daigle, Caroline
Mazin, Benjamin
Matton, Daniel P.
author_sort Daigle, Caroline
collection PubMed
description BACKGROUND: The Fertilization-related kinases (FRK) form a class that belongs to the MEKK subfamily of plant MAPKKKs. It was recently shown that FRK class kinases expanded during angiosperm evolution, reaching their maximum numbers in the lineage leading to solanaceous species and culminating in the Solanum genus where they account for more than 40% of the total MEKKs. The first members studied, ScFRK1 and ScFRK2 were shown to play a pivotal role in gametophyte development in the wild potato species Solanum chacoense. RESULTS: ScFRK3 is also involved in gametophyte development. ScFRK3 is expressed in developing pollen and young ovules, reaching its highest level immediately after meiosis and during the mitosis steps in both gametophytes. Hence, three independent lines of ScFRK3 RNAi mutant plants showed decreased number of seeds per fruit. We also observed an important number of degenerated embryo sac in mature ovary. Analysis of ovule development showed that most embryo sac did not enter mitosis I in ScFRK3 RNAi mutant plants. Severe lethality was also observed during male gametophyte development, pollen being arrested before mitosis I, as observed in the female gametophyte. Obvious defects in vegetative organs were not observed, emphasizing the reproductive roles of the FRK class kinases. To isolate MAP kinases acting downstream of ScFRK3, a de novo S. chacoense transcriptome from male and female reproductive organs was assembled. Of the five ScMKKs and 16 ScMPKs retrieved, only the ScMKK3 interacted with ScFRK3, while only the ScMPK13 interacted with ScMKK3, leading to an apparent single three-tiered canonical MAP kinase cascade combination involving ScFRK3-ScMKK3-ScMPK13. CONCLUSIONS: The ScFRK3 MAPKKK is involved in a signaling cascade that regulates both male and female gamete development, and most probably act upstream of ScMKK3 and ScMPK13. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1804-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-65242622019-05-24 The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development Daigle, Caroline Mazin, Benjamin Matton, Daniel P. BMC Plant Biol Research Article BACKGROUND: The Fertilization-related kinases (FRK) form a class that belongs to the MEKK subfamily of plant MAPKKKs. It was recently shown that FRK class kinases expanded during angiosperm evolution, reaching their maximum numbers in the lineage leading to solanaceous species and culminating in the Solanum genus where they account for more than 40% of the total MEKKs. The first members studied, ScFRK1 and ScFRK2 were shown to play a pivotal role in gametophyte development in the wild potato species Solanum chacoense. RESULTS: ScFRK3 is also involved in gametophyte development. ScFRK3 is expressed in developing pollen and young ovules, reaching its highest level immediately after meiosis and during the mitosis steps in both gametophytes. Hence, three independent lines of ScFRK3 RNAi mutant plants showed decreased number of seeds per fruit. We also observed an important number of degenerated embryo sac in mature ovary. Analysis of ovule development showed that most embryo sac did not enter mitosis I in ScFRK3 RNAi mutant plants. Severe lethality was also observed during male gametophyte development, pollen being arrested before mitosis I, as observed in the female gametophyte. Obvious defects in vegetative organs were not observed, emphasizing the reproductive roles of the FRK class kinases. To isolate MAP kinases acting downstream of ScFRK3, a de novo S. chacoense transcriptome from male and female reproductive organs was assembled. Of the five ScMKKs and 16 ScMPKs retrieved, only the ScMKK3 interacted with ScFRK3, while only the ScMPK13 interacted with ScMKK3, leading to an apparent single three-tiered canonical MAP kinase cascade combination involving ScFRK3-ScMKK3-ScMPK13. CONCLUSIONS: The ScFRK3 MAPKKK is involved in a signaling cascade that regulates both male and female gamete development, and most probably act upstream of ScMKK3 and ScMPK13. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1804-0) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-16 /pmc/articles/PMC6524262/ /pubmed/31096905 http://dx.doi.org/10.1186/s12870-019-1804-0 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Daigle, Caroline
Mazin, Benjamin
Matton, Daniel P.
The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development
title The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development
title_full The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development
title_fullStr The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development
title_full_unstemmed The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development
title_short The Solanum chacoense Fertilization-Related Kinase 3 (ScFRK3) is involved in male and female gametophyte development
title_sort solanum chacoense fertilization-related kinase 3 (scfrk3) is involved in male and female gametophyte development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6524262/
https://www.ncbi.nlm.nih.gov/pubmed/31096905
http://dx.doi.org/10.1186/s12870-019-1804-0
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