TY - JOUR
T1 - Assessing the Response of Small RNA Populations to Allopolyploidy Using Resynthesized Brassica napus Allotetraploids
AU - Martinez Palacios, Paulina
AU - Jacquemot, Marie-Pierre
AU - Tapie, Marion
AU - Rousselet, Agnès
AU - Diop, Mamoudou
AU - Remoué, Carine
AU - Falque, Matthieu
AU - Lloyd, Andrew H
AU - Jenczewski, Eric
AU - Lassalle, Gilles
AU - Chévre, Anne-Marie
AU - Lelandais, Christine
AU - Crespi, Martin
AU - Brabant, Philippe
AU - Joets, Johann
AU - Alix, Karine
N1 - Funding Information:
We particularly thank Clémentine Vitte (CNRS, GQE-Le Moulon, Gif-sur-Yvette, France), Jérôme Gouzy (INRA, UMR LIPM, Toulouse, France), and Mark Tepfer (INRA, IJPB, Versailles, France) for valuable discussions. We thank Pierre Montalent (INRA, GQE-Le Moulon, Gif-sur-Yvette, France) for technical assistance with Galaxy. Three anonymous reviewers are also acknowledged for their helpful comments on the manuscript. P.M.P. was supported by a PhD fellowship from the French Ministère de l’Enseignement Supérieur et de la Recherche (MESR). Experiments dedicated to sRNA library construction and sequencing were funded by the Institut Fédératif de Recherche 87 “La plante et son environnement” (Gif-sur-Yvette, France) and the Direction Scientifique of AgroParisTech (Paris, France). This article is dedicated to the memory of our colleague Dr HervéThiellement.
Publisher Copyright:
© The Author(s) 2019.
PY - 2019/4/1
Y1 - 2019/4/1
N2 - Allopolyploidy, combining interspecific hybridization with whole genome duplication, has had significant impact on plant evolution. Its evolutionary success is related to the rapid and profound genome reorganizations that allow neoallopolyploids to form and adapt. Nevertheless, how neoallopolyploid genomes adapt to regulate their expression remains poorly understood. The hypothesis of a major role for small noncoding RNAs (sRNAs) in mediating the transcriptional response of neoallopolyploid genomes has progressively emerged. Generally, 21-nt sRNAs mediate posttranscriptional gene silencing by mRNA cleavage, whereas 24-nt sRNAs repress transcription (transcriptional gene silencing) through epigenetic modifications. Here, we characterize the global response of sRNAs to allopolyploidy in Brassica, using three independently resynthesized Brassica napus allotetraploids originating from crosses between diploid Brassica oleracea and Brassica rapa accessions, surveyed at two different generations in comparison with their diploid progenitors. Our results suggest an immediate but transient response of specific sRNA populations to allopolyploidy. These sRNA populations mainly target noncoding components of the genome but also target the transcriptional regulation of genes involved in response to stresses and in metabolism; this suggests a broad role in adapting to allopolyploidy. We finally identify the early accumulation of both 21- and 24-nt sRNAs involved in regulating the same targets, supporting a posttranscriptional gene silencing to transcriptional gene silencing shift at the first stages of the neoallopolyploid formation. We propose that reorganization of sRNA production is an early response to allopolyploidy in order to control the transcriptional reactivation of various noncoding elements and stress-related genes, thus ensuring genome stability during the first steps of neoallopolyploid formation.
AB - Allopolyploidy, combining interspecific hybridization with whole genome duplication, has had significant impact on plant evolution. Its evolutionary success is related to the rapid and profound genome reorganizations that allow neoallopolyploids to form and adapt. Nevertheless, how neoallopolyploid genomes adapt to regulate their expression remains poorly understood. The hypothesis of a major role for small noncoding RNAs (sRNAs) in mediating the transcriptional response of neoallopolyploid genomes has progressively emerged. Generally, 21-nt sRNAs mediate posttranscriptional gene silencing by mRNA cleavage, whereas 24-nt sRNAs repress transcription (transcriptional gene silencing) through epigenetic modifications. Here, we characterize the global response of sRNAs to allopolyploidy in Brassica, using three independently resynthesized Brassica napus allotetraploids originating from crosses between diploid Brassica oleracea and Brassica rapa accessions, surveyed at two different generations in comparison with their diploid progenitors. Our results suggest an immediate but transient response of specific sRNA populations to allopolyploidy. These sRNA populations mainly target noncoding components of the genome but also target the transcriptional regulation of genes involved in response to stresses and in metabolism; this suggests a broad role in adapting to allopolyploidy. We finally identify the early accumulation of both 21- and 24-nt sRNAs involved in regulating the same targets, supporting a posttranscriptional gene silencing to transcriptional gene silencing shift at the first stages of the neoallopolyploid formation. We propose that reorganization of sRNA production is an early response to allopolyploidy in order to control the transcriptional reactivation of various noncoding elements and stress-related genes, thus ensuring genome stability during the first steps of neoallopolyploid formation.
KW - Brassica napus/genetics
KW - DNA Transposable Elements
KW - Genetic Speciation
KW - RNA, Small Untranslated/metabolism
KW - Tetraploidy
KW - allopolyploidy
KW - small noncoding RNAs
KW - transposable elements
KW - Brassica
KW - resynthesized oilseed rapes
KW - regulation of gene expression
KW - Small noncoding RNAs
KW - Resynthesized oilseed rapes
KW - Regulation of gene expression
KW - Allopolyploidy
KW - Transposable elements
UR - http://www.scopus.com/inward/record.url?scp=85064226323&partnerID=8YFLogxK
U2 - 10.1093/molbev/msz007
DO - 10.1093/molbev/msz007
M3 - Article
C2 - 30657939
SN - 0737-4038
VL - 36
SP - 709
EP - 726
JO - Molecular Biology and Evolution
JF - Molecular Biology and Evolution
IS - 4
ER -