Maria Manuela Ribeiro Costa

University of Minho

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Rómulo Sobral

University of Minho

Helena Silva

University of Minho

Margarida Rocheta

University of Lisbon

Miguel Ramos

University of Lisbon

Jorge Cunha

Instituto Nacional de Investigação Agrária e Veterinária

João L. Coito

University of Lisbon

Sara Amâncio

University of Lisbon

Leonor Morais–Cecílio

University of Lisbon

Ana Teresa Alhinho

University of Minho

Enrico Coen

John Innes Centre

Cooperative Institutions

University of Lisbon

University of Minho

John Innes Centre

Universidade do Porto

Universidade Nova de Lisboa

Instituto de Biologia Experimental e Tecnológica

Universidade de São Paulo

Norwich Research Park

Centre National de la Recherche Scientifique

Instituto Nacional de Investigação Agrária e Veterinária

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Unravelling the role of DRIF transcription factors in Arabidopsis thaliana

Free Radical Biology and Medicine (2018)

Ana Maria Cunha Sara Laranjeira Shweta Singh João Raimundo Rómulo Sobral

Transcription

10.1016/j.freeradbiomed.2018.04.383

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Molecular control of dormancy transitions throughout the year in the monoecious cork oak

bioRxiv (Cold Spring Harbor Laboratory) (2024)

Helena Silva Rómulo Sobral Ana Teresa Alhinho Hugo Afonso Teresa Ribeiro

Abstract Bud dormancy plays a vital role in flowering regulation and fruit production, being highly regulated by endogenous and environmental cues. Deployment of epigenetic modifications and differential gene expression control bud dormancy/break cycles. Information on how these genetic and epigenetic mechanisms are regulated throughout the year is still scarce for temperate trees, such as Quercus suber . Here, the expression levels of QsCENL and QsDYL1 during different seasonal cycles of bud development suggest that QsCENL may be implicated in the establishment of growth cessation in Q. suber and that QsDYL1 is a good dormancy marker. Moreover, the analysis of the profiles of epigenetic marks and the expression of modifiers, in dormant versus non-dormant bud meristems, indicate that epigenetic regulation is implicated in how bud development progresses in Q. suber . The identification of bud specific mechanisms opens new possibilities to understand how trees respond to challenging environmental signals derived from climate change.

Plant reproductive morphology

Quercus suber

10.1101/2024.07.03.601814

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Genome‐wide identification, phylogeny, and gene duplication of the epigenetic regulators in Fagaceae

Physiologia Plantarum (2022)

Sofia Alves Ângelo Braga Denise Parreira Ana Teresa Alhinho Helena Silva

Epigenetic regulators are proteins involved in controlling gene expression. Information about the epigenetic regulators within the Fagaceae, a relevant family of trees and shrubs of the northern hemisphere ecosystems, is scarce. With the intent to characterize these proteins in Fagaceae, we searched for orthologs of DNA methyltransferases (DNMTs) and demethylases (DDMEs) and Histone modifiers involved in acetylation (HATs), deacetylation (HDACs), methylation (HMTs), and demethylation (HDMTs) in Fagus, Quercus, and Castanea genera. Blast searches were performed in the available genomes, and freely available RNA-seq data were used to de novo assemble transcriptomes. We identified homologs of seven DNMTs, three DDMEs, six HATs, 11 HDACs, 32 HMTs, and 21 HDMTs proteins. Protein analysis showed that most of them have the putative characteristic domains found in these protein families, which suggests their conserved function. Additionally, to elucidate the evolutionary history of these genes within Fagaceae, paralogs were identified, and phylogenetic analyses were performed with DNA and histone modifiers. We detected duplication events in all species analyzed with higher frequency in Quercus and Castanea and discuss the evidence of transposable elements adjacent to paralogs and their involvement in gene duplication. The knowledge gathered from this work is a steppingstone to upcoming studies concerning epigenetic regulation in this economically important family of Fagaceae.

10.1111/ppl.13788

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The regulation of flowering time by daylength in Arabidopsis.

PubMed (1998)

George Coupland M. Isabel Igeño R Law Simon Robert J. Schaffer Giovanni Murtas

We are studying several Arabidopsis mutants that show altered regulation of flowering time in response to daylength. One of the mutations we are studying, constans, delays flowering under long days but has no effect under short days. Analysis of the expression of the CONSTANS gene, and modification of its expression in transgenic plants, suggests that this gene promotes flowering in response to long days and that the delay in flowering that occurs in wild-type plants under short days is at least in part due to regulation of CONSTANS gene transcription. We describe genetic approaches that we are taking to identify genes that act in the same genetic pathway as CONSTANS, and in particular the relationship between CONSTANS and two other genes that we are studying. These are LATE ELONGATED HYPOCOTYL, for which we have a dominant mutant allele that causes late flowering, and EARLY SHORT DAYS 4, whose inactivation causes early flowering. In addition to their effects on flowering time, the over-expression of CONSTANS and the inactivation of EARLY SHORT DAYS 4 cause the Arabidopsis shoot to become determinate and therefore to terminate development prematurely. This phenotype is discussed in light of other genes that have previously been shown to be required to maintain indeterminate development of the shoot.

Wild type

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The gene mutated in ataxia-ocular apraxia 1 encodes the new HIT/Zn-finger protein aprataxin

Nature Genetics (2001)

Maria-Céu Moreira Clara Barbot Nobutada Tachi Naoki Kozuka Eiji Uchida

10.1038/ng1001-189

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Arabinogalactan proteins and pectin distribution during female gametogenesis inQuercus suberL.

Annals of Botany (2016)

Ana Lúcia Lopes Mário Costa Rómulo Sobral Maria Manuela Ribeiro Costa Isabel Amorim

Quercus suber L. (cork oak) is one of the most important monoecious tree species in semi-arid regions of Southern Europe, with a high ecological value and economic potential. However, as a result of its long reproductive cycle, complex reproductive biology and recalcitrant seeds, conventional breeding is demanding. In its complex reproductive biology, little is known about the most important changes that occur during female gametogenesis. Arabinogalactan proteins (AGPs) and pectins are the main components of plant cell walls and have been reported to perform common functions in cell differentiation and organogenesis of reproductive plant structures. AGPs have been shown to serve as important molecules in several steps of the reproductive process in plants, working as signalling molecules, associated with the sporophyte-gametophyte transition, and pectins have been implicated in pollen-pistil interactions before double fertilization. In this study, the distribution of AGP and pectin epitopes was assessed during female gametogenesis.Immunofluorescence labelling of female flower cells was performed with a set of monoclonal antibodies (mAbs) directed to the carbohydrate moiety of AGPs (JIM8 and JIM13) and pectic homogalacturonans (HGs) (mAbs JIM5 and JIM7).The selective labelling obtained with AGP and pectin mAbs JIM8, JIM13, JIM5 and JIM7 during Q. suber female gametogenesis shows that AGPs and pectic HG can work as markers for mapping gametophytic cell differentiation in this species. Pectic HG showed different distribution patterns, depending on their levels of methyl esterification. Methyl-esterified HGs showed a uniform distribution in the overall female flower cells before fertilization and a more specific pattern after fertilization. A low methyl-ester pectin distribution pattern during the different developmental stages appears to be related to the pathway that pollen tubes follow to reach the embryo sac. AGPs showed a more sparse distribution in early stages of development, but specific labelling is shown in the synergids and their filiform apparatus.The labelling obtained with anti-AGP and anti-pectin mAbs in Q. suber female flower cells showed a dynamic distribution of AGPs and pectic HGs, which may render these molecules useful molecular markers during female gametogenesis. Changes occurring during development will be determined in order to help describe cork oak ovule structural properties before and after fertilization, providing new insight to better understand Q. suber female gametogenesis.

Arabinogalactan

Quercus suber

Dichlorosilane

10.1093/aob/mcw019

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Flower development and sex specification in wild grapevine

BMC Genomics (2014)

Miguel Ramos João L. Coito Helena Silva Jorge Cunha Maria Manuela Ribeiro Costa

Wild plants of Vitis closely related to the cultivated grapevine (V. v. vinifera) are believed to have been first domesticated 10,000 years BC around the Caspian Sea. V. v. vinifera is hermaphrodite whereas V. v. sylvestris is a dioecious species. Male flowers show a reduced pistil without style or stigma and female flowers present reflexed stamens with infertile pollen. V. vinifera produce perfect flowers with all functional structures. The mechanism for flower sex determination and specification in grapevine is still unknown. To understand which genes are involved during the establishment of male, female and complete flowers, we analysed and compared the transcription profiles of four developmental stages of the three genders. We showed that sex determination is a late event during flower development and that the expression of genes from the ABCDE model is not directly correlated with the establishment of sexual dimorphism. We propose a temporal comprehensive model in which two mutations in two linked genes could be players in sex determination and indirectly establish the Vitis domestication process. Additionally, we also found clusters of genes differentially expressed between genders and between developmental stages that suggest a role involved in sex differentiation. Also, the detection of differentially transcribed regions that extended existing gene models (intergenic regions) between sexes suggests that they may account for some of the variation between the subspecies. There is no evidence of differences of expression levels in genes from the ABCDE model that could explain the shift from hermaphroditism to dioecy. We propose that sex specification occurs after floral organ identity has been established and therefore, sex determination genes might be having an effect downstream of the ABCDE model genes. For the first time a full transcriptomic analysis was performed in different flower developmental stages in the same individual. Our experimental approach enabled us to create a comprehensive catalogue of transcribed genes across developmental stages and genders that will contribute for future work in sex determination in seed plants.

Hermaphrodite

Sexual dimorphism

10.1186/1471-2164-15-1095

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Another Twist in the Tale: Intrafamilial Phenotypic Heterogeneity in ANO3‐Related Dystonia

Movement Disorders Clinical Practice (2021)

Vanessa Carvalho Joana Martins Filipe Correia Maria Manuela Ribeiro Costa João Massano

Mutations in the anoctamin 3 (ANO3) gene cause autosomal dominant craniocervical dystonia (DYT24), presenting from childhood to mid-life. However, in the past years, the clinical spectrum of this disorder has widened. We present a family with heterogeneous presentation, exemplifying phenotypic diversity in DYT24.The index case presented with myoclonic dystonia at age 10. His family history was remarkable for cervical dystonia with myoclonus in his grandfather, cervical and upper limb dystonia along with dopa-responsive parkinsonism in his father and lower-limb dystonia in his teenage sister. Magnetic resonance imaging and blood work-ups of all the affected family members were normal. The genetic panel for inherited forms of dystonia disclosed a point mutation c.1787C > A (p.Ser596Tyr) segregated in all affected family members.ANO3 mutations usually present with craniocervical dystonia and rarely generalized or leg dystonia. This family exemplifies the heterogeneous presentation of this disorder as well as a wide phenotypic variability within the same family.

Paroxysmal dyskinesia

Cervical dystonia

10.1002/mdc3.13209

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Evaluation of the presence of arabinogalactan proteins and pectins during Quercus suber male gametogenesis

Annals of Botany (2014)

Mário Costa Rómulo Sobral Maria Manuela Ribeiro Costa Isabel Amorim Sı́lvia Coimbra

Background and AimsQuercus suber (cork oak) is a dominant tree of the Fagaceae in forests of the south-west Iberian Peninsula. It is monoecious with a long progamic phase that provides a comprehensive system for comparative studies in development and sexual reproduction. In this study the distribution of arabinogalactan protein (AGPs) and pectin epitopes in anthers of Q. suber was assessed to map these hydroxyproline-rich glycoproteins and the galacturonate-rich acidic polysaccharides during pollen development. Methods Immunolocalization in male flowers was performed with a set of monoclonal antibodies directed against the carbohydrate moiety that recognizes AGPs and pectins. To identify AGP genes involved in cork oak male flower development, a search was conducted for annotated AGP genes in the available transcriptome data of the Cork Oak EST Consortium database (www.corkoakdb.org). Key Results Ubiquitous labelling in all cell types was obtained with anti-homogalacturan antibodies for methyl-esterified pectins. In contrast, the antibody that labelled non-methyl-esterified homogalacturans had a preferential presence in microsporocyte cells walls at the beginning of pollen development. Intense labelling was obtained with anti-AGP antibodies both in the tapetum and in the intine wall near the pollen apertures and later in the generative cell wall and vegetative cell. Evaluation of the putative AGPs highly expressed in the male gametophyte was achieved by quantitative RT-PCR analysis in male and female cork oak flowers. Conclusions Four putative AGP genes were identified that are preferentially expressed in the male flower compared with the female flower. The putative Arabidopsis thaliana orthologues of these genes are associated with preferential expression in pollen, suggesting that the AGPs probably play a significant role in cork oak reproduction.

Quercus suber

Tapetum

Arabinogalactan

10.1093/aob/mcu223

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Citations (33)

Cloning of a peroxidase enzyme involved in the biosynthesis of pharmaceutically active terpenoid indole alkaloids in Catharanthus roseus (L.) G. Don

Frédérique Hilliou Maria Manuela Ribeiro Costa Maria Inês Almeida Inês Lopes Cardoso Mark J. Leech

Catharanthus roseus

Cloning (programming)

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Citations (5)