Dr. Julie Ferreira de Carvalho
Evolutionary Biologist, Interested in Plant Speciation and Adaptation
Marie Curie Fellow INRAE Rennes, France – Joint Laboratory for Genetics, Environment and Plant protection (IGEPP).
Expertise in Transcriptomics, Comparative Epi/Genomics, Molecular Phylogeny and Bioinformatics.
UMR1349 IGEPP, INRAE – Agrocampus Ouest – Université Rennes1, Domaine de la Motte, BP 35327, 35653 Le Rheu Cedex, France
June 2018-present - Marie Curie post-doctoral fellow, Group Biodiversity and Polyploidy, INRAE IGEPP Rennes, France. Subject: Structural and functional dynamics of Brassica napus polyploid genome.
May 2017-May 2018 - Agreenskills+ post-doctoral fellow, Group Biodiversity and Polyploidy, INRA IGEPP Rennes, France. Subject: Immediate impact of polyploidy and of human selection on the evolutionary dynamic of Brassica napus.
Apr 2013-Apr 2017 - Post-doctoral fellow in the group of Dr. Koen Verhoeven, Netherlands Institute of Ecology, Wageningen (NL). Subject: (Epi)Genomic footprints associated with asexual evolution.
Oct 2009-Feb 2013 - PhD student/teaching assistant, UMR CNRS Ecobio, University of Rennes 1, France. Title: Genome evolution of polyploid Spartina species invading salt-marshes: contribution of Next-Generation Sequencing technologies. Supervised by Prof. Malika Ainouche.
In the era of Anthropocene and extreme human disturbances, one of the main challenges is to sustainably feed the world population. Crops are already disturbed by extreme temperature, lack of water and repeated hot waves as well as emerging pathogens. Thus, it is timely to develop novel varieties, more adapted to these environmental changes. In the last years, considerable advances have been undertaken to better comprehend the molecular mechanisms at the origin of speciation, human domestication and adaptation of plant species. However, more integrative and predictable models are essential to provide the scientific community, breeders and governmental agencies to tackle current issues.
For a decade, rapidly evolving sequencing technologies have helped to address major pending questions in evolutionary biology and agronomy. It is a unique tool to draw an integrative vision of the molecular mechanisms underlying phenotypic traits in every possible biological systems. My work is situated in the heart of this technological and societal context. I am interested in unravelling molecular processes (transcriptomic, genomic and epigenomic) and building an integrative understanding (from genes to eco-agrosystems) of the main molecular mechanisms involved in plant genome evolution and adaptation. These fundamental mechanisms can help us predict the faith of biodiversity in a changing environment and improve its management.
I. Consequences of Interspecific hybridization and Genome doubling on speciation and adaptive processes
Whole Genome Duplication (WGD) or Polyploidy has played a major role in shaping biodiversity and forming adapted plant species. Many of current important crops are polyploids or come from early rounds of hybridization and WGD events. I am interested in unravelling the molecular processes associated with these speciation and adaptive phenomena using comparative epi/genomic approaches.
Genome stabilization after allopolyploidy
Meiosis and fertility. In oilseed rape (Brassica napus), meiotic stability and high fertility are observed in natural form of the allopolyploid (created from the cross between turnip, B. rapa, and cabbage, B. oleracea, ca. 7500 years ago). However, when mimicking the speciation process in the lab, resynthesized lines of B. napus exhibit large number of multivalent chromosomes leading to unreduced gamete formation and low fertility. Using various resynthesized lines of B. napus and SNP array technology, I am investigating the links between homoeologous rearrangements, gene loss, multivalent apparition and low fertility. This research project will allow discovering the still unknown molecular processes at the origin of oilseed rape speciation and successful establishment (Ferreira de Carvalho et al. In prep).
Figure 1 : Schematic representation of oilseed rape speciation process
Cytonuclear interactions. After allopolyploidy, cytoplasmic incompatibilities can also arise as newly formed allopolyploid species confront biparental nuclear chromosomes with uniparentally inherited plastid genome. To avoid any deleterious effects of unequal genome inheritance, preferential utilization of the plastid donor over the other one has been hypothesized to occur in allopolyploids. I retrieved 110 genes implicated in nine plastid protein complexes. These genes in the young allopolyploid B. napus showed no subgenome expression biased or maternal homogenization via gene conversion despite presence of some non-synonymous substitutions between plastid genomes of parental progenitors. Instead, subgenome dominance was observed regardless of the maternal progenitor (Ferreira de Carvalho et al. 2019 Plant Journal).
Figure 2 : Position of nuclear genes involved in nine plastid protein complexes and their homoeologous and paralogous relationships in Brassica napus. The outer circle represents the 19 chromosomes of B. napus var. Darmor (from Chalhoub et al. 2014). Genes are then positioned on the chromosomes and possible events of gene conversion events are illustrated with the black dashed lines. Homoeologous relationships between nuclear gene copies from the A and C subgenomes are presented by solid colored lines. The dashed colored lines represent the paralogous relationships between redundant copies within a subgenome.
Molecular mechanisms underlying functionalization processes in polyploid species
As mentioned before, ancient and recent polyploidy events are recurrent within Angiosperms. Increase of duplicated gene copies can be a source of additional variability to successful establish in natural environments or selected for in response to stresses.
Gene loss and fractionation. Most of redundant gene copies return to single gene status. This process is not random. However, the rules steering this process and the evolutionary consequences are still unknown. Studying in parallel B. rapa and B. oleracea genomes that both have experienced the same WGD, we show that the same paleologous copies are retained in both species. Additionally, the ancestral function is maintained in those copies, making neo-functionalization processes quite scarce in Brassica species (Rousseau-Gueutin et al. In prep).
Gene expression dynamics. In addition to gene copy retention, we investigated gene expression dynamics and demonstrated that despite variation in gene expression between parental species, the subgenome coming from B. rapa is often upregulated compared to B. oleracea subgenome in the allopolyploid (Rousseau-Gueutin et al. In prep). Follow-up analyses are ongoing to investigate the probable causes of this subgenome dominance in Brassica polyploids. I also studied the faith of gene expression in other paleo- and allopolyploid models to detect genes involved in invasiveness and stress tolerance (in Spartina maritima S. alterniflora and S. anglica; Ferreira de Carvalho et al. 2013a Heredity, 2017 PSE, Alvarez et al. 2018 Molecular Ecology).
Epigenetic disruptions. Following allopolyploidy, epigenetic factors can also be disrupted and impact plant phenotypes. I previously looked at the repetitive compartment using shallow DNA sequencing in polyploid Spartina (Ferreira de Carvalho et al. 2013b Plant Molecular Biology) and currently investigate the impact of transposable elements on transcriptome evolution and phenotypic traits in Brassica. To that purpose, I use PacBio assembled genomes, resequencing strategies and RNA-Seq in resynthesized and natural populations of B. napus.
II. Adaptive consequences of epigenetic mechanisms in asexually reproducing species
Change in ploidy level is, in some cases, associated with a change in reproductive systems. For instance, common dandelions are diploid and reproduced sexually in the south of Europe whereas in the North East of Europe triploid apomictic populations are encountered (See Figure 3). This system offers the opportunity to (1) study the transition from sexuality to strict asexuality in various natural lineages and (2) the importance of transgenerational epigenetic mechanisms in plant adaptation. I developed the first reference transcriptome for the common triploid dandelion (Ferreira de Carvalho et al. 2016a BMC Genomics) and initiated the first reference genome using long reads for the sexual diploid common dandelion (In prep). Using RNA-Seq, I then investigated metabolic pathways showing signs of early divergence among allopatric populations of the same apomictic lineage. I demonstrated functional divergence regarding acyl-lipid and abscisic acid pathways. Finally, I identified mutation accumulation in SNPs as well as in Transposable elements that cannot simply be explained by genetic drift (Ferreira de Carvalho et al. 2016a BMC Genomics). Therefore, I investigated further the potential impact of Transposable elements in asexual plant adaptation. I identified young specific TE families that are functionally dynamic; some of these families are differentially transcribed between allopatric populations and are associated with differences in methylation levels. Therefore, some copies could be experiencing activity in asexual dandelion to provide genetic diversity that can then be selected upon. Interestingly, the flowering pathway and key regulator genes seem to be epigenetically regulated. As the same genotype can be found from Switzerland to Sweden where vernalization requirements differ tremendously, asexual populations seem to have diverged at the epigenetic level to adapt to contrasted environments. In parallel, I took part in various research projects on transgenerational epigenetic heritability in stress conditions (Morgado et al. 2017 in Molecular Biology and Evolution; Verhoeven et al. 2018 in New Phytologist).
Figure 3 : Distribution of the common dandelion in Europe. New asexual lineages arising from intraspecific crosses between diploid maternal donor and triploid paternal donor
Peer-reviewed publications (impact factor)
- Ferreira de Carvalho J., Lucas J., Deniot G., Falentin C., Filangi O., Gilet M., Legeai F., Lode M., Morice J., Trotoux G., Aury J-M., Barbe V., Keller J., Snowdon R., He Z., Denoeud F., Wincker P., Bancroft I., Chèvre A-M. and M. Rousseau-Gueutin (2019). Cytonuclear interactions remain stable during allopolyploid evolution despite repeated whole-genome duplications in Brassica. Accepted in The Plant Journal (IF=5.78)
- Alvarez M., Ferreira de Carvalho J., Salmon A., Ainouche M., Cavé-Radet A., El Amrani A., Foster T.E., Moyer S. and C.L. Richards (2018). Transcriptome response of the foundation plant Spartina alterniflora. To the Deepwater Horizon oil spill. Molecular Ecology 27(14):2986-3000 (IF=6.13)
- Verhoeven K.J.F, Verbon E., van Gurp T., Oplaat C., Ferreira de Carvalho J., Morse A., Stahl M., Macel M. and L. McIntyre (2018). Parental jasmonic acid treatment affects offspring transcriptomes and leaf chemical profiles in dandelion. New Phytologist 217(2):871-882 (IF=7.43)
- Ferreira de Carvalho J., Boutte J., Bourdau P., Chelaifa H., Ainouche K., Salmon A. and M. Ainouche (2017). Gene expression variation in natural populations of hexaploid (parents and hybrids) and allododecaploid Spartina species (Poaceae). Plant Systematics and Evolution 303(8):1061-79 (IF=1.45)
- Morgado L., Preite V., Oplaat C., Anava S., Ferreira de Carvalho J., Rechavi O., Johannes F., and K.J.F. Verhoeven (2017). Small RNAs reflect environment from grandparental generation in apomictic dandelions. Molecular Biology and Evolution 34(8):2035-40 (IF=10.22)
- Ferreira de Carvalho J., de Jager V., van Gurp T., Wagemaker N. and K.J.F. Verhoeven (2016). Recent and dynamic transposable elements contribute to genomic divergence under asexuality. BMC Genomics 17:884 (IF=3.73)
- Boutte J., Ferreira de Carvalho J., Ainouche M. and Salmon A. Reference transcriptomes and detection of duplicated copies in hexaploid parents, hybrids and allododecaploid Spartina species (Poaceae) (2016). Genome Biology and Evolution 8(9):3030-44 (IF=3.94)
- Huska D., Leitch I., Ferreira de Carvalho J., Leitch A., Salmon A., Ainouche M. and A. Kovarik (2016). Persistence, dispersal and genetic evolution of recently formed Spartina homoploid hybrids and allopolyploids in Southern England. Biological Invasions 18(8):2137-51 (IF=3.05)
- Ferreira de Carvalho J., Oplaat C., Pappas N., Derks M., de Ridder D. and K.J.F. Verhoeven (2016). Heritable gene expression differences between apomictic clone members in Taraxacum officinale: Insights into early stages of evolutionary divergence in asexual plants. BMC Genomics. 17: 203 (IF=3.73)
- Boutte J., Aliaga B., Lima O., Ferreira de Carvalho J., Ainouche A., Macas J., Rousseau-Gueutin M., Coriton O., Ainouche M. and A. Salmon (2015). Haplotype Detection from Next Generation Sequencing in High Ploidy-Level Species: 45S rDNA Gene Copies in the Hexaploid Spartina maritima. G3 6(1):29-40 (IF=2.74)
- Martin G., Rousseau-Gueutin M., Cordonnier S., Lima O., Michon-Coudouel S., Naquin D., Ferreira de Carvalho J., Ainouche M., Salmon A. and A. Ainouche (2014). The first complete chloroplast genome of Genistoid legume Lupinus lucteus: Evidence for a novel major lineage-specific rearrangement and new insights regarding plastome evolution in the legume family. Annals of Botany 113 (7): 1197-1210 (IF=3.65)
- Ferreira de Carvalho J., Poulain J., Da Silva C., Wincker P., Michon-Coudouel S., Dheilly A., Naquin D., Boutte J., Salmon A. and M. Ainouche (2013a). Transcriptome de novo assembly from Next-Generation Sequencing and comparative analyses in the hexaploid salt marsh species Spartina maritima and Spartina alterniflora (Poaceae). Heredity 110: 181-93 (IF=3.87)
- Ferreira de Carvalho J., Chelaifa H., Mangenot S., Couloux A., Wincker P., Bellec A., Fourment J., Berges H., Salmon A. and M. Aïnouche (2013b). Exploring the genome of the salt-marsh species Spartina maritima (Poaceae, Chloridoideae) through BAC End Sequence analysis. Plant Molecular Biology 83: 591-606 (IF=3.54)
- Rousseau-Gueutin M., Keller J., Ferreira de Carvalho J., Aïnouche A., and G. Martin (2018). The intertwined plastid and nuclear evolution in land plants. In: Soltis PS, Soltis DE (Eds) Chloroplasts - Physiology and Genetics, IntechOpen.
- Ainouche M., Chelaifa H., Ferreira de Carvalho J., Bellot S., Ainouche A. and A. Salmon (2012). Polyploid evolution in Spartina: dealing with highly redundant genomes. In: Soltis PS, Soltis DE (Eds) Polyploidy and Genome Evolution, Springer Berlin Heidelberg. pp 225-244
Publications in preparation
- Rousseau-Gueutin M., Ferreira de Carvalho J., Lucas J., Denoeud F., He Z., Boutte J., Deniot G., Falentin C., Filangi O., Gilet M., Legeai F., Lode M., Morice J., Trotoux G., Aury J-M., Barbe V., Snowdon R., Wincker P., Bancroft I. and A-M Chèvre. Structural and functional evolutionary dynamics of duplicated genes and genomes in nascent and natural B. napus.