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Tags:
Life sciences,
Epigenetics,
Genetics,
Plant reproduction
Publications
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Hornslien, Karina Stensland; Myking, Ida Velle; Bjerkan, Katrine Nergård; Krabberød, Anders Kristian; Miller, Jason Rafe & Grini, Paul
(2026).
Parent-of-origin specific allelic expression in outbreeding Arabidopsis arenosa identifies antagonistic parental enrichment in protein degradation pathways.
New Phytologist.
ISSN 0028-646X.
doi:
10.1111/nph.71551.
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Bramsiepe, Jonathan; Krabberød, Anders Kristian; Bjerkan, Katrine Nergård; Alling, Renate; Nielsen, Ida & Hornslien, Karina Stensland
[Show all 9 contributors for this article]
(2023).
Structural evidence for MADS-box type I family expansion seen in new assemblies of Arabidopsis arenosa and A. lyrata.
The Plant Journal.
ISSN 0960-7412.
116(3),
p. 942–961.
doi:
10.1111/tpj.16401.
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SUMMARY Arabidopsis thaliana diverged from A. arenosa and A. lyrata at least 6 million years ago. The three species differ by genome‐wide polymorphisms and morphological traits. The species are to a high degree reproductively isolated, but hybridization barriers are incomplete. A special type of hybridization barrier is based on the triploid endosperm of the seed, where embryo lethality is caused by endosperm failure to support the developing embryo. The MADS‐box type I family of transcription factors is specifically expressed in the endosperm and has been proposed to play a role in endosperm‐based hybridization barriers. The gene family is well known for its high evolutionary duplication rate, as well as being regulated by genomic imprinting. Here we address MADS‐box type I gene family evolution and the role of type I genes in the context of hybridization. Using two de‐novo assembled and annotated chromosome‐level genomes of A. arenosa and A. lyrata ssp. petraea we analyzed the MADS‐box type I gene family in Arabidopsis to predict orthologs, copy number, and structural genomic variation related to the type I loci. Our findings were compared to gene expression profiles sampled before and after the transition to endosperm cellularization in order to investigate the involvement of MADS‐box type I loci in endosperm‐based hybridization barriers. We observed substantial differences in type‐I expression in the endosperm of A. arenosa and A. lyrata ssp. petraea , suggesting a genetic cause for the endosperm‐based hybridization barrier between A. arenosa and A. lyrata ssp. petraea .
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Zhang, Yupeng; Viejo, Marcos; Yakovlev, Igor; Tengs, Torstein; Krokene, Paal & Hytönen, Timo
[Show all 8 contributors for this article]
(2023).
Major transcriptomic differences are induced by warmer temperature conditions experienced during asexual and sexual reproduction in Fragaria vesca ecotypes.
Frontiers in Plant Science.
14,
p. 1–16.
doi:
10.3389/fpls.2023.1213311.
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A major challenge for plants in a rapidly changing climate is to adapt to rising temperatures. Some plants adapt to temperature conditions by generating an epigenetic memory that can be transmitted both meiotically and mitotically. Such epigenetic memories may increase phenotypic variation to global warming and provide time for adaptation to occur through classical genetic selection. The goal of this study was to understand how warmer temperature conditions experienced during sexual and asexual reproduction affect the transcriptomes of different strawberry (Fragaria vesca) ecotypes. We let four European F. vesca ecotypes reproduce at two contrasting temperatures (18 and 28°C), either asexually through stolon formation for several generations, or sexually by seeds (achenes). We then analyzed the transcriptome of unfolding leaves, with emphasis on differential expression of genes belonging to the epigenetic machinery. For asexually reproduced plants we found a general transcriptomic response to temperature conditions but for sexually reproduced plants we found less significant responses. We predicted several splicing isoforms for important genes (e.g. a SOC1, LHY, and SVP homolog), and found significantly more differentially presented splicing event variants following asexual vs. sexual reproduction. This difference could be due to the stochastic character of recombination during meiosis or to differential creation or erasure of epigenetic marks during embryogenesis and seed development. Strikingly, very few differentially expressed genes were shared between ecotypes, perhaps because ecotypes differ greatly both genetically and epigenetically. Genes related to the epigenetic machinery were predominantly upregulated at 28°C during asexual reproduction but downregulated after sexual reproduction, indicating that temperature-induced change affects the epigenetic machinery differently during the two types of reproduction.
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Zhang, Yupeng; Toivainen, Tuomas; Mackenzie, Kathryn; Yakovlev, Igor; Krokene, Paal & Hytönen, Timo
[Show all 8 contributors for this article]
(2023).
Methylome, transcriptome, and phenotype changes induced by temperature conditions experienced during sexual reproduction in Fragaria vesca.
Physiologia Plantarum : An International Journal for Plant Biology.
ISSN 0031-9317.
175(4).
doi:
10.1111/ppl.13963.
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Temperature conditions experienced during embryogenesis and seed development may induce epigenetic changes that increase phenotypic variation in plants. Here we investigate if embryogenesis and seed development at two different temperatures (28 vs. 18°C) result in lasting phenotypic effects and DNA methylation changes in woodland strawberry (Fragaria vesca). Using five European ecotypes from Spain (ES12), Iceland (ICE2), Italy (IT4), and Norway (NOR2 and NOR29), we found statistically significant differences between plants from seeds produced at 18 or 28°C in three of four phenotypic features investigated under common garden conditions. This indicates the establishment of a temperature-induced epigenetic memory-like response during embryogenesis and seed development. The memory effect was significant in two ecotypes: in NOR2 flowering time, number of growth points and petiole length were affected, and in ES12 number of growth points was affected. This indicates that genetic differences between ecotypes in their epigenetic machinery, or other allelic differences, impact this type of plasticity. We observed statistically significant differences between ecotypes in DNA methylation marks in repetitive elements, pseudogenes, and genic elements. Leaf transcriptomes were also affected by embryonic temperature in an ecotype-specific manner. Although we observed significant and lasting phenotypic change in at least some ecotypes, there was considerable variation in DNA methylation between individual plants within each temperature treatment. This within-treatment variability in DNA methylation marks in F. vesca progeny may partly be a result of allelic redistribution from recombination during meiosis and subsequent epigenetic reprogramming during embryogenesis.
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Bjerkan, Katrine Nergård; Alling, Renate; Myking, Ida Velle; Brysting, Anne Krag & Grini, Paul
(2023).
Genetic and environmental manipulation of Arabidopsis hybridization barriers uncovers antagonistic functions in endosperm cellularization.
Frontiers in Plant Science.
14,
p. 1–16.
doi:
10.3389/fpls.2023.1229060.
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Speciation involves reproductive isolation, which can occur by hybridization barriers acting in the endosperm of the developing seed. The nuclear endosperm is a nutrient sink, accumulating sugars from surrounding tissues, and undergoes coordinated cellularization, switching to serve as a nutrient source for the developing embryo. Tight regulation of cellularization is therefore vital for seed and embryonic development. Here we show that hybrid seeds from crosses between Arabidopsis thaliana as maternal contributor and A. arenosa or A. lyrata as pollen donors result in an endosperm based post-zygotic hybridization barrier that gives rise to a reduced seed germination rate. Hybrid seeds display opposite endosperm cellularization phenotypes, with late cellularization in crosses with A. arenosa and early cellularization in crosses with A. lyrata . Stage specific endosperm reporters display temporally ectopic expression in developing hybrid endosperm, in accordance with the early and late cellularization phenotypes, confirming a disturbance of the source-sink endosperm phase change. We demonstrate that the hybrid barrier is under the influence of abiotic factors, and show that a temperature gradient leads to diametrically opposed cellularization phenotype responses in hybrid endosperm with A. arenosa or A. lyrata as pollen donors. Furthermore, different A. thaliana accession genotypes also enhance or diminish seed viability in the two hybrid cross-types, emphasizing that both genetic and environmental cues control the hybridization barrier. We have identified an A. thaliana MADS-BOX type I family single locus that is required for diametrically opposed cellularization phenotype responses in hybrid endosperm. Loss of AGAMOUS-LIKE 35 significantly affects the germination rate of hybrid seeds in opposite directions when transmitted through the A. thaliana endosperm, and is suggested to be a locus that promotes cellularization as part of an endosperm based mechanism involved in post-zygotic hybrid barriers. The role of temperature in hybrid speciation and the identification of distinct loci in control of hybrid failure have great potential to aid the introduction of advantageous traits in breeding research and to support models to predict hybrid admixture in a changing global climate.
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Zhang, Yupeng; Fan, Guangxun; Toivainen, Tuomas; Tengs, Torstein; Yakovlev, Igor & Krokene, Paal
[Show all 9 contributors for this article]
(2023).
Warmer temperature during asexual reproduction induce methylome, transcriptomic, and lasting phenotypic changes in Fragaria vesca ecotypes.
Horticulture Research.
ISSN 2662-6810.
10(9),
p. 1–15.
doi:
10.1093/hr/uhad156.
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Plants must adapt with increasing speed to global warming to maintain their fitness. One rapid adaptation mechanism is epigenetic memory, which may provide organisms sufficient time to adapt to climate change. We studied how the perennial Fragaria vesca adapted to warmer temperatures (28°C vs. 18°C) over three asexual generations. Differences in flowering time, stolon number, and petiole length were induced by warmer temperature in one or more ecotypes after three asexual generations and persisted in a common garden environment. Induced methylome changes differed between the four ecotypes from Norway, Iceland, Italy, and Spain, but shared methylome responses were also identified. Most differentially methylated regions (DMRs) occurred in the CHG context, and most CHG and CHH DMRs were hypermethylated at the warmer temperature. In eight CHG DMR peaks, a highly similar methylation pattern could be observed between ecotypes. On average, 13% of the differentially methylated genes between ecotypes also showed a temperature-induced change in gene expression. We observed ecotype-specific methylation and expression patterns for genes related to gibberellin metabolism, flowering time, and epigenetic mechanisms. Furthermore, we observed a negative correlation with gene expression when repetitive elements were found near (±2 kb) or inside genes. In conclusion, lasting phenotypic changes indicative of an epigenetic memory were induced by warmer temperature and were accompanied by changes in DNA methylation patterns. Both shared methylation patterns and transcriptome differences between F. vesca accessions were observed, indicating that DNA methylation may be involved in both general and ecotype-specific phenotypic variation.
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Ekelenburg, Yuri Stephan van; Hornslien, Karina Stensland; Hautegem, Tom Van; Fendrych, Matyáš; Isterdael, Gert Van & Bjerkan, Katrine Nergård
[Show all 9 contributors for this article]
(2022).
Spatial and temporal regulation of parent-of-origin allelic expression in the endosperm.
Plant Physiology.
ISSN 0032-0889.
191(2),
p. 986–1001.
doi:
10.1093/plphys/kiac520.
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Genomic imprinting promotes differential expression of parental alleles in the endosperm of flowering plants and is regulated by epigenetic modification such as DNA methylation and histone tail modifications in chromatin. After fertilization, the endosperm develops through a syncytial stage before it cellularizes and becomes a nutrient source for the growing embryo. Regional compartmentalization has been shown both in early and late endosperm development, and different transcriptional domains suggest divergent spatial and temporal regional functions. The analysis of the role of parent-of-origin allelic expression in the endosperm as a whole and the investigation of domain-specific functions have been hampered by the inaccessibility of the tissue for high-throughput transcriptome analyses and contamination from surrounding tissue. Here, we used fluorescence-activated nuclear sorting (FANS) of nuclear targeted GFP fluorescent genetic markers to capture parental-specific allelic expression from different developmental stages and specific endosperm domains. This approach allowed us to successfully identify differential genomic imprinting with temporal and spatial resolution. We used a systematic approach to report temporal regulation of imprinted genes in the endosperm, as well as region-specific imprinting in endosperm domains. Analysis of our data identified loci that are spatially differentially imprinted in one domain of the endosperm, while biparentally expressed in other domains. These findings suggest that the regulation of genomic imprinting is dynamic and challenge the canonical mechanisms for genomic imprinting.
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Davik, Jahn; Wilson, Robert Charles; Njah, Relindis Ghai; Grini, Paul Eivind; Randall, Stephen K. & Alsheikh, Muath K
[Show all 7 contributors for this article]
(2021).
Genetic mapping and identification of a QTL determining tolerance to freezing stress in Fragaria vesca L.
PLOS ONE.
16(5).
doi:
10.1371/journal.pone.0248089.
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Extreme cold and frost cause significant stress to plants which can potentially be lethal. Low temperature freezing stress can cause significant and irreversible damage to plant cells and can induce physiological and metabolic changes that impact on growth and development. Low temperatures cause physiological responses including winter dormancy and autumn cold hardening in strawberry (Fragaria) species, and some diploid F. vesca accessions have been shown to have adapted to low-temperature stresses. To study the genetics of freezing tolerance, a F. vesca mapping population of 143 seedlings segregating for differential responses to freezing stress was raised. The progeny was mapped using ‘Genotyping-by-Sequencing’ and a linkage map of 2,918 markers at 851 loci was resolved. The mapping population was phenotyped for freezing tolerance response under controlled and replicated laboratory conditions and subsequent quantitative trait loci analysis using interval mapping revealed a single significant quantitative trait locus on Fvb2 in the physical interval 10.6 Mb and 15.73 Mb on the F. vesca v4.0 genome sequence. This physical interval contained 896 predicted genes, several of which had putative roles associated with tolerance to abiotic stresses including freezing. Differential expression analysis of the 896 QTL-associated gene predictions in the leaves and crowns from ‘Alta’ and ‘NCGR1363’ parental genotypes revealed genotype-specific changes in transcript accumulation in response to low temperature treatment as well as expression differences between genotypes prior to treatment for many of the genes. The putative roles, and significant interparental differential expression levels of several of the genes reported here identified them as good candidates for the control of the effects of freezing tolerance at the QTL identified in this investigation and the possible role of these candidate genes in response to freezing stress is discussed.
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Hubin, Aliaksandr; Storvik, Geir Olve; Grini, Paul Eivind & Butenko, Melinka Alonso
(2020).
A Bayesian binomial regression model with latent gaussian processes for modelling DNA methylation.
Austrian Journal of Statistics.
ISSN 1026-597X.
49(4),
p. 46–56.
doi:
10.17713/ajs.v49i4.1124.
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Epigenetic observations are represented by the total number of reads from a given pool of cells and the number of methylated reads, making it reasonable to model this data by a binomial distribution. There are numerous factors that can influence the probability of success in a particular region. Moreover, there is a strong spatial (alongside the genome) dependence of these probabilities. We incorporate dependence on the covariates and the spatial dependence of the methylation probability for observations from a pool of cells by means of a binomial regression model with a latent Gaussian field and a logit link function. We apply a Bayesian approach including prior specifications on model configurations. We run a mode jumping Markov chain Monte Carlo algorithm (MJMCMC) across different choices of covariates in order to obtain the joint posterior distribution of parameters and models. This also allows finding the best set of covariates to model methylation probability within the genomic region of interest and individual marginal inclusion probabilities of the covariates.
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Hornslien, Karina Stensland; Miller, Jason Rafe & Grini, Paul Eivind
(2019).
Regulation of Parent-of-Origin Allelic Expression in the Endosperm.
Plant Physiology.
ISSN 0032-0889.
180(3),
p. 1498–1519.
doi:
10.1104/pp.19.00320.
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Hubin, Aliaksandr; Storvik, Geir Olve; Grini, Paul Eivind & Butenko, Melinka Alonso
(2019).
Bayesian binomial regression model with a latent Gaussian field for analysis of epigenetic data.
In Kharin, Y & Filzmoser, Peter (Ed.),
Proceedings of Computer Data Analysis and Modeling: Stochastics and Data Science 2019.
Belarusian State University Press.
ISSN 9789855668115.
p. 167–171.
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Bjerkan, Katrine; Hornslien, Karina Stensland; Johannessen, Ida Marie; Krabberød, Anders Kristian; Ekelenburg, Yuri Stephan van & Kalantarian, Maryam
[Show all 11 contributors for this article]
(2019).
Genetic variation and temperature affects hybrid barriers during interspecific hybridization.
The Plant Journal.
ISSN 0960-7412.
101,
p. 122–140.
doi:
10.1111/tpj.14523.
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Genomic imprinting regulates parent‐specific transcript dosage during seed development and is mainly confined to the endosperm. Elucidation of the function of many imprinted genes has been hampered by the lack of corresponding mutant phenotypes, and the role of imprinting is mainly associated with genome dosage regulation or allocation of resources. Disruption of imprinted genes has also been suggested to mediate endosperm‐based post‐zygotic hybrid barriers depending on genetic variation and gene dosage. Here, we have analyzed the conservation of a clade from the MADS‐box type I class transcription factors in the closely related species Arabidopsis arenosa, A. lyrata, and A. thaliana, and show that AGL36‐like genes are imprinted and maternally expressed in seeds of Arabidopsis species and in hybrid seeds between outbreeding species. In hybridizations between outbreeding and inbreeding species the paternally silenced allele of the AGL36‐like gene is reactivated in the hybrid, demonstrating that also maternally expressed imprinted genes are perturbed during hybridization and that such effects on imprinted genes are specific to the species combination. Furthermore, we also demonstrate a quantitative effect of genetic diversity and temperature on the strength of the post‐zygotic hybridization barrier. Markedly, a small decrease in temperature during seed development increases the survival of hybrid F1 seeds, suggesting that abiotic and genetic parameters play important roles in post‐zygotic species barriers, pointing at evolutionary scenarios favoring such effects.
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Bråte, Jon; Neumann, Ralf Stefan; Fromm, Bastian; Haraldsen, Arthur Alexander Blørstad; Tarver, James E. & Suga, Hiroshi
[Show all 11 contributors for this article]
(2018).
Unicellular origin of the animal microRNA machinery.
Current Biology.
ISSN 0960-9822.
28(20),
p. 3288–3295.e5.
doi:
10.1016/j.cub.2018.08.018.
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The emergence of multicellular animals was associated with an increase in phenotypic complexity and with the acquisition of spatial cell differentiation and embryonic development. Paradoxically, this phenotypic transition was not paralleled by major changes in the underlying developmental toolkit and regulatory networks. In fact, most of these systems are ancient, established already in the unicellular ancestors of animals [1, 2, 3, 4, 5]. In contrast, the Microprocessor protein machinery, which is essential for microRNA (miRNA) biogenesis in animals, as well as the miRNA genes themselves produced by this Microprocessor, have not been identified outside of the animal kingdom [6]. Hence, the Microprocessor, with the key proteins Pasha and Drosha, is regarded as an animal innovation [7, 8, 9]. Here, we challenge this evolutionary scenario by investigating unicellular sister lineages of animals through genomic and transcriptomic analyses. We identify in Ichthyosporea both Drosha and Pasha (DGCR8 in vertebrates), indicating that the Microprocessor complex evolved long before the last common ancestor of animals, consistent with a pre-metazoan origin of most of the animal developmental gene elements. Through small RNA sequencing, we also discovered expressed bona fide miRNA genes in several species of the ichthyosporeans harboring the Microprocessor. A deep, pre-metazoan origin of the Microprocessor and miRNAs comply with a view that the origin of multicellular animals was not directly linked to the innovation of these key regulatory components.
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Glöckle, Barbara; Urban, W.; Nagahara, Shiori; Andersen, Ellen Dehnes; Higashiyama, Tetsuya & Grini, Paul Eivind
[Show all 7 contributors for this article]
(2018).
Pollen differentiation as well as pollen tube guidance and discharge are independent of the presence of gametes.
Development.
ISSN 0950-1991.
145(1),
p. 1–8.
doi:
10.1242/dev.152645.
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After meiosis, an unequal cell division generates the male gamete lineage in flowering plants. The generative cell will undergo a second division, giving rise to the two gametes, i.e. the sperm cells. The other cell will develop into the vegetative cell that plays a crucial role in pollen tube formation and sperm delivery. Recently, the vegetative cell has been suggested to be important for programming of the chromatin state in sperm cells and/or the resulting fertilization products. Blocking the initial unequal division genetically, we first highlight that the default differentiation state after male meiosis is a vegetative fate, which is consistent with earlier work. We find that uni-nucleated mutant microspores differentiated as wild-type vegetative cells, including chromatin remodeling and the transcriptional activation of transposable elements. Moreover, live-cell imaging revealed that this vegetative cell is sufficient for the correct guidance of the pollen tube to the female gametes. Hence, we conclude that vegetative cell differentiation and function does not depend on the formation or presence of the actual gametes but rather on external signals or a cell-autonomous pace keeper.
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Lafon-Placette, Clément; Johannessen, Ida Marie; Hornslien, Karina Stensland; Ali, Mohammad F.; Bjerkan, Katrine & Bramsiepe, Jonathan
[Show all 11 contributors for this article]
(2017).
Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe.
Proceedings of the National Academy of Sciences of the United States of America (PNAS).
ISSN 0027-8424.
114(6),
p. E1027–E1035.
doi:
10.1073/pnas.1615123114.
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Oh, Sung-Aeong; Jeon, Jien; Park, Hyo-Jin; Grini, Paul Eivind; Twell, David & Park, Soon Ki
(2016).
Analysis of gemini pollen 3 mutant suggests a broad function of AUGMIN in microtubule organization during sexual reproduction in Arabidopsis.
The Plant Journal.
ISSN 0960-7412.
87(2),
p. 188–201.
doi:
10.1111/tpj.13192.
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Gregis, Veronica; Andrès, Fernandio; Sessa, Alice; Guerra, Rosalinda F; Simonini, Sara & Mateos, Julieta L
[Show all 15 contributors for this article]
(2013).
Identification of pathways directly regulated by SHORT VEGETATIVE PHASE during vegetative and reproductive development in Arabidopsis.
Genome Biology.
ISSN 1465-6906.
14(6).
doi:
10.1186/gb-2013-14-6-r56.
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Background MADS-domain transcription factors play important roles during plant development. The Arabidopsis MADS-box gene SHORT VEGETATIVE PHASE (SVP) is a key regulator of two developmental phases. It functions as a repressor of the floral transition during the vegetative phase and later it contributes to the specification of floral meristems. How these distinct activities are conferred by a single transcription factor is unclear, but interactions with other MADS domain proteins which specify binding to different genomic regions is likely one mechanism. Results To compare the genome-wide DNA binding profile of SVP during vegetative and reproductive development we performed ChIP-seq analyses. These ChIP-seq data were combined with tiling array expression analysis, induction experiments and qRT-PCR to identify biologically relevant binding sites. In addition, we compared genome-wide target genes of SVP with those published for the MADS domain transcription factors FLC and AP1, which interact with SVP during the vegetative and reproductive phases, respectively. Conclusions Our analyses resulted in the identification of pathways that are regulated by SVP including those controlling meristem development during vegetative growth and flower development whereas floral transition pathways and hormonal signaling were regulated predominantly during the vegetative phase. Thus, SVP regulates many developmental pathways, some of which are common to both of its developmental roles whereas others are specific to only one of them.
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Bjerkan, Katrine & Grini, Paul Eivind
(2013).
The Arabidopsis DDB1 interacting protein WDR55 is required for vegetative development.
Plant Signalling & Behavior.
ISSN 1559-2316.
8(9).
doi:
10.4161/psb.25347.
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Meza, Trine Johansen; Moen, Marivi; Vågbø, Cathrine Broberg; Krokan, Hans Einar; Klungland, Arne & Grini, Paul Eivind
[Show all 7 contributors for this article]
(2012).
The DNA dioxygenase ALKBH2 protects Arabidopsis thaliana against methylation damage.
Nucleic Acids Research (NAR).
ISSN 0305-1048.
40(14),
p. 6620–6631.
doi:
10.1093/nar/gks327.
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The Escherichia coli AlkB protein (EcAlkB) is a DNA repair enzyme which reverses methylation damage such as 1-methyladenine (1-meA) and 3-methylcytosine (3-meC). The mammalian AlkB homologues ALKBH2 and ALKBH3 display EcAlkB-like repair activity in vitro , but their substrate specificities are different, and ALKBH2 is the main DNA repair enzyme for 1-meA in vivo . The genome of the model plant Arabidopsis thaliana encodes several AlkB homologues, including the yet uncharacterized protein AT2G22260, which displays sequence similarity to both ALKBH2 and ALKBH3. We have here characterized protein AT2G22260, by us denoted ALKBH2, as both our functional studies and bioinformatics analysis suggest it to be an orthologue of mammalian ALKBH2. The Arabidopsis ALKBH2 protein displayed in vitro repair activities towards methyl and etheno adducts in DNA, and was able to complement corresponding repair deficiencies of the E. coli alkB mutant. Interestingly, alkbh2 knock-out plants were sensitive to the methylating agent methylmethanesulphonate (MMS), and seedlings from these plants developed abnormally when grown in the presence of MMS. The present study establishes ALKBH2 as an important enzyme for protecting Arabidopsis against methylation damage in DNA, and suggests its homologues in other plants to have a similar function.
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Bjerkan, Katrine; Jung-Romeo, S; Jurgens, G; Genschik, P & Grini, Paul Eivind
(2012).
Arabidopsis WD REPEAT DOMAIN55 Interacts with DNA DAMAGED BINDING PROTEIN1 and Is Required for Apical Patterning in the Embryo.
The Plant Cell.
ISSN 1040-4651.
24(3),
p. 1013–1033.
doi:
10.1105/tpc.111.089425.
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Shirzadi, Reza; Andersen, Ellen Dehnes; Bjerkan, Katrine; Gloeckle, Barbara M; Heese, Maren & Ungru, Alexander
[Show all 11 contributors for this article]
(2011).
Genome-Wide Transcript Profiling of Endosperm without Paternal Contribution Identifies Parent-of-Origin-Dependent Regulation of AGAMOUS-LIKE36.
PLoS Genetics.
ISSN 1553-7390.
7(2).
doi:
10.1371/journal.pgen.1001303.
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Seed development in angiosperms is dependent on the interplay among different transcriptional programs operating in the embryo, the endosperm, and the maternally-derived seed coat. In angiosperms, the embryo and the endosperm are products of double fertilization during which the two pollen sperm cells fuse with the egg cell and the central cell of the female gametophyte. In Arabidopsis, analyses of mutants in the cell-cycle regulator CYCLIN DEPENDENT KINASE A;1 (CKDA;1) have revealed the importance of a paternal genome for the effective development of the endosperm and ultimately the seed. Here we have exploited cdka;1 fertilization as a novel tool for the identification of seed regulators and factors involved in parent-of-origin–specific regulation during seed development. We have generated genome-wide transcription profiles of cdka;1 fertilized seeds and identified approximately 600 genes that are downregulated in the absence of a paternal genome. Among those, AGAMOUS-LIKE (AGL) genes encoding Type-I MADS-box transcription factors were significantly overrepresented. Here, AGL36 was chosen for an in-depth study and shown to be imprinted. We demonstrate that AGL36 parent-of-origin–dependent expression is controlled by the activity of METHYLTRANSFERASE1 (MET1) maintenance DNA methyltransferase and DEMETER (DME) DNA glycosylase. Interestingly, our data also show that the active maternal allele of AGL36 is regulated throughout endosperm development by components of the FIS Polycomb Repressive Complex 2 (PRC2), revealing a new type of dual epigenetic regulation in seeds.
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Leihne, VIbeke; Kirpekar, F; Vågbø, Cathrine Broberg; Born, Erwin Van den; Krokan, Hans Einar & Grini, Paul Eivind
[Show all 8 contributors for this article]
(2011).
Roles of Trm9-and ALKBH8-like proteins in the formation of modified wobble uridines in Arabidopsis tRNA.
Nucleic Acids Research (NAR).
ISSN 0305-1048.
39(17),
p. 7688–7701.
doi:
10.1093/nar/gkr406.
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Uridine at the wobble position of tRNA is usually modified, and modification is required for accurate and efficient protein translation. In eukaryotes, wobble uridines are modified into 5-methoxycarbonylmethyluridine (mcm 5 U), 5-carbamoylmethyluridine (ncm 5 U) or derivatives thereof. Here, we demonstrate, both by in vitro and in vivo studies, that the Arabidopsis thaliana methyltransferase AT1G31600, denoted by us AtTRM9, is responsible for the final step in mcm 5 U formation, thus representing a functional homologue of the Saccharomyces cerevisiae Trm9 protein. We also show that the enzymatic activity of AtTRM9 depends on either one of two closely related proteins, AtTRM112a and AtTRM112b. Moreover, we demonstrate that AT1G36310, denoted AtALKBH8, is required for hydroxylation of mcm 5 U to ( S ) - mchm 5 U in tRNA GlyUCC , and has a function similar to the mammalian dioxygenase ALKBH8. Interestingly, atalkbh8 mutant plants displayed strongly increased levels of mcm 5 U, and also of mcm 5 Um, its 2′- O -ribose methylated derivative. This suggests that accumulated mcm 5 U is prone to further ribose methylation by a non-specialized mechanism, and may challenge the notion that the existence of mcm 5 U- and mcm 5 Um-containing forms of the selenocysteine-specific tRNA Sec in mammals reflects an important regulatory process. The present study reveals a role in for several hitherto uncharacterized Arabidopsis proteins in the formation of modified wobble uridines.
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Masiero, S; Colombo, L; Grini, Paul Eivind; Schnittger, A & Kater, MM
(2011).
The Emerging Importance of Type I MADS Box Transcription Factors for Plant Reproduction.
The Plant Cell.
ISSN 1040-4651.
23(3),
p. 865–872.
doi:
10.1105/tpc.110.081737.
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Nowack, MK; Ungru, Alexander; Bjerkan, Katrine; Grini, Paul Eivind & Schnittger, Arp
(2010).
Reproductive cross-talk: seed development in flowering plants.
Biochemical Society Transactions.
ISSN 0300-5127.
38,
p. 604–612.
doi:
10.1042/BST0380604.
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Berger, Frederick; Grini, Paul Eivind & Schnittger, Arp
(2006).
Endosperm: an integrator of seed growth and development.
Current opinion in plant biology.
ISSN 1369-5266.
9,
p. 664–670.
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Nowack, MK; Grini, Paul Eivind; Jakoby, MJ; Lafos, M; Koncz, C & Schnittger, A
(2006).
A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis.
Nature Genetics.
ISSN 1061-4036.
38.
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Stangeland, Biljana; Nestestog, Ragnhild; Grini, Paul; Skrbo, Nirma; Berg, Anita & Salehian, Zhian
[Show all 8 contributors for this article]
(2005).
Molecular analysis of Arabidopsis endosperm and embryo promoter trap lines: reporter-gene expression can result from T-DNA insertions in antisense orientation, in introns and in intergenic regions, in addition to sense insertion at the 5' end of genes.
Journal of Experimental Botany.
ISSN 0022-0957.
419(Sep;56),
p. 2495–505.
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Random insertions of promoterless reporter genes in genomes are a common tool for identifying marker lines with tissue-specific expression patterns. Such lines are assumed to reflect the activity of endogenous promoters and should facilitate the cloning of genes expressed in the corresponding tissues. To identify genes active in seed organs, plant DNA flanking T-DNA insertions (T-DNAs) have been cloned in 16 Arabidopsis thaliana GUS-reporter lines. T-DNAs were found in proximal promoter regions, 5' UTR or intron with GUS in the same (sense) orientation as the tagged gene, but contrary to expectations also in inverted orientation in the 5' end of genes or in intergenic regions. RT-PCR, northern analysis, and data on expression patterns of tagged genes, compared with the expression pattern of the reporter lines, suggest that the expression pattern of a reporter gene will reflect the pattern of a tagged gene when inserted in sense orientation in the 5' UTR or intron. When inserted in the promoter region, the reporter-gene expression patterns may be restricted compared with the endogenous gene. Among the trapped genes, the previously described nitrate transporter gene AtNRT1.1, the cyclophilin gene ROC3, and the histone deacetylase gene AtHD2C were found. Reporter-gene expression when positioned in antisense orientation, for example, in the SLEEPY1 gene, is indicative of antisense expression of the tagged gene. For T-DNAs found in intergenic regions, it is suggested that the reporter gene is transcribed from cryptic promoters or promoters of as yet unannotated genes.
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Stangeland, Biljana; Nestestog, Ragnhild; Grini, Paul Eivind; Skrbo-Larssen, Nirma; Berg, Anita & Salehian, Zhian
[Show all 8 contributors for this article]
(2005).
Molecular analysis of Arabidopsis endosperm and embryo promoter trap lines: reporter-gene expression can result from T-DNA insertions in antisense orientation, in introns and in intergenic regions, in addition to sense insertion at the 5' end of genes.
Journal of Experimental Botany.
ISSN 0022-0957.
56(419),
p. 2495–2505.
doi:
10.1093/jxb/eri242.
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Haslekås, Camilla; Viken, Marte K.; Grini, Paul Eivind; Nygaard, Vigdis; Nordgard, Silje H. & Meza, Trine Johansen
[Show all 7 contributors for this article]
(2003).
Seed 1-Cys peroxiredoxin antioxidants are not involved in dormancy, but contribute to inhibition of germination during stress.
Plant Physiology.
ISSN 0032-0889.
133,
p. 1148–1157.
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Butenko, Melinka Alonso; Patterson, Sara E.; Grini, Paul Eivind; Stenvik, Grethe-Elisabeth; Amundsen, Svanstrøm Silja & Mandal, Abul
[Show all 7 contributors for this article]
(2003).
INFLORESCENCE DEFICIENT IN ABSCISSION Controls Floral Organ Abscission in Arabidopsis and Identifies a Novel Family of Putative Ligands in Plants.
The Plant Cell.
ISSN 1040-4651.
15,
p. 2296–2307.
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Kirik, V.; Grini, Paul Eivind; Mathur, J.; Klinkhammer, I.; Adler, K. & Bechtold, N.
[Show all 9 contributors for this article]
(2002).
The Arabidopsis TUBULIN-FOLDING COFACTOR A gene is involved in the control of the alpha/beta-tubulin monomer balance.
The Plant Cell.
ISSN 1040-4651.
p. 2265–2276.
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The control of the stoichiometric balance of alpha- and beta-tubulin is important during microtubule biogenesis. This process involves several tubulin-folding cofactors (TFCs), of which only TFC A is not essential in mammalian in vitro systems or in vivo in yeast. Here, we show that the TFC A gene is important in vivo in plants. The Arabidopsis gene KIESEL (KIS) shows sequence similarity to the TFC A gene. Expression of the mouse TFC A gene under the control of the 35S promoter rescues the kis mutation, indicating that KIS is the Arabidopsis ortholog of TFC A. kis plants exhibit a range of defects similar to the phenotypes associated with impaired microtubule function: plants are reduced in size and show meiotic defects, cell division is impaired, and trichomes are bulged and less branched. Microtubule density was indistinguishable from that of the wild type, but microtubule organization was affected in trichomes and hypocotyl cells of dark-grown kis plants. The kis phenotype was rescued by overexpression of an alpha-tubulin, indicating that KIS is involved in the control of the correct balance of alpha- and beta-tubulin monomers.
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Kirik, V.; Mathur, J.; Grini, Paul Eivind; Klinkhammer, I.; Adler, K. & Bechtold, N.
[Show all 9 contributors for this article]
(2002).
Functional analysis of the tubulin-folding cofactor C in Arabidopsis thaliana.
Current Biology.
ISSN 0960-9822.
12(17),
p. 1519–1523.
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The biogenesis of microtubules comprises several steps, including the correct folding of alpha- and beta-tubulin and heterodimer formation. In vitro studies and the genetic analysis in yeast revealed that, after translation, alpha- and beta-tubulin are processed by several chaperonins and microtubule-folding cofactors (TFCs) to produce assembly-competent alpha-/beta-tubulin heterodimers. One of the TFCs, TFC-C, does not exist in yeast, and a potential function of TFC-C is thus based only on the biochemical analysis. In this study and in a very recently published study by Steinborn and coworkers, the analysis of the Arabidopsis porcino (por) mutant has shown that TFC-C is important for microtubule function in vivo. The predicted POR protein shares weak amino acid similarity with the human TFC-C (hTFC-C). Our finding that hTFC-C under the control of the ubiquitously expressed 35S promoter can rescue the por mutant phenotype shows that the POR gene encodes the Arabidopsis ortholog of hTFC-C. The analysis of plants carrying a GFP:POR fusion construct showed that POR protein is localized in the cytoplasm and is not associated with microtubules. While, in por mutants, microtubule density was indistinguishable from wild-type, their organization was affected.
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Grini, Paul Eivind; Jürgens, Gerd & Hülskamp, Martin
(2002).
Embryo and Endosperm Development Is Disrupted in the Female Gametophytic capulet Mutants of Arabidopsis.
Genetics.
ISSN 0016-6731.
162(4),
p. 1911–1925.
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The female gametophyte of higher plants gives rise, by double fertilization, to the diploid embryo and triploid endosperm, which develop in concert to produce the mature seed. What roles gametophytic maternal factors play in this process is not clear. The female-gametophytic effects on embryo and endosperm development in the Arabidopsis mea, fis, and fie mutants appear to be due to gametic imprinting that can be suppressed by METHYL TRANSFERASE1 antisense (MET1 a/s) transgene expression or by mutation of the DECREASE IN DNA METHYLATION1 (DDM1) gene. Here we describe two novel gametophytic maternal-effect mutants, capulet1 (cap1) and capulet2 (cap2). In the cap1 mutant, both embryo and endosperm development are arrested at early stages. In the cap2 mutant, endosperm development is blocked at very early stages, whereas embryos can develop to the early heart stage. The cap mutant phenotypes were not rescued by wild-type pollen nor by pollen from tetraploid plants. Furthermore, removal of silencing barriers from the paternal genome by MET1 a/s transgene expression or by the ddm1 mutation also failed to restore seed development in the cap mutants. Neither cap1 nor cap2 displayed autonomous seed development, in contrast to mea, fis, and fie mutants. In addition, cap2 was epistatic to fis1 in both autonomous endosperm and sexual development. Finally, both cap1 and cap2 mutant endosperms, like wild-type endosperms, expressed the paternally inactive endosperm-specific FIS2 promoter GUS fusion transgene only when the transgene was introduced via the embryo sac, indicating that imprinting was not affected. Our results suggest that the CAP genes represent novel maternal functions supplied by the female gametophyte that are required for embryo and endosperm development.
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Alling, Renate; Brysting, Anne Krag; Grini, Paul; Bjerkan, Katrine & Myking, Ida Velle
(2022).
Environmental and genetic factors affecting endosperm based post-zygotic hybridization barriers.
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Proper development of the triploid endosperm is vital for seed viability. During the early stages of development, the endosperm works as a nutrient sink, accumulating sugars from the surrounding tissues. During this developmental phase, endosperm division is devoid of cytokinesis, resulting in a syncytium. After sufficient accumulation of nutrients, the endosperm nuclei undergo cellularization, switching to serve as a nutrient source for the embryo. Tight regulation of cellularization is therefore vital for embryo development. Crosses between Arabidopsis thaliana as maternal contributor and A. arenosa as pollen donor cause late cellularization and reduced germination rate in hybrid seeds. Here we show the opposite cellularization phenotype in hybrid seeds when using A. lyrata as pollen donor also resulting in low germination rate. Stage specific endosperm reporters display ectopic expression in developing hybrid endosperm confirming disturbance of the source-sink endosperm phase change. We also observe accession genotype as well as single loci effects on the severity of the barrier. Interestingly, we found that temperature can alleviate this hybridization barrier in opposite directions depending on whether the hybrid seed exhibit early or late endosperm cellularization. We postulate that temperature dependency might be a general mechanism affecting endosperm-based hybridization barriers.
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Grini, Paul Eivind; Miller, Jason Rafe & Hornslien, Karina Stensland
(2019).
Imprinting revisited: Genetic and phenotypic routes to postzygotic hybrid barriers and bridges.
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Hubin, Aliaksandr; Storvik, Geir Olve; Grini, Paul Eivind & Butenko, Melinka Alonso
(2019).
Bayesian binomial regression model with a latent Gaussian field for analysis of epigenetic data.
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Kenich, Håkon Muland; Bjerkan, Katrine; Bramsiepe, Jonathan; Grini, Paul Eivind & Brysting, Anne Krag
(2019).
An investigation of potential hybridisation barriers in Cochlearia / Scurvygrasses.
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Zhang, Yupeng; Fan, Guangxun; Toivainen, Tuomas; Yakovlev, Igor; Hytönen, Timo & Krokene, Paal
[Show all 8 contributors for this article]
(2018).
BEYOND THE GENOME: EPIGENETICS OF CLIMATIC ADAPTATION IN PLANTS.
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Climate change is one of the greatest challenges for the biosphere. As sessile organisms, plants must adapt quickly to keep pace with the rapidly changing climatic conditions. Epigenetic memory is one mechanism which would provide sufficient plasticity under rapid climate change and enable long-lived organisms to survive long enough to adapt by classical genetic selection. In Norway spruce, the timing of bud burst and bud set are regulated by an epigenetic memory established by the temperature sum endured during embryogenesis. The resulting epitypes display a life-long shift in seasonal timing of the bud phenology, a trait previously presumed to be under strict classical selection and highly heritable. However, Norway spruce is a difficult plant to study because it has a very long generation time and an extensive genome size. We therefore seek to find a suitable perennial model plant to study the phenomenon of epigenetic climatic memory. Woodland strawberry (Fragaria vesca) may be an ideal model to research the role of epigenetic memory on plant phenology. Fragaria vesca is a perennial plant with a small well-characterized genome, a short sexual reproduction cycle and can also propagate asexually trough clonal daughter plants formed by stolons. We will explore whether the temperature sum experienced during sexual and asexual reproduction impact on the phenology of Fragaria vesca and use this as a model to decipher the molecular mechanism underlying epigenetic memory in plants.
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Grini, Paul Eivind; Ekelenburg, Yuri Stephan van; Bjerkan, Katrine & Nowack, Moritz K.
(2018).
Analysis of Domain Specific Genomic Imprinting in the Arabidopsis Endosperm.
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Grini, Paul Eivind; Ekelenburg, Yuri Stephan van & Guiterrez-Marcos, Jose
(2018).
CAPULET2 controls endosperm development in a parent-of-origin dependent manner.
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Grini, Paul Eivind; Hornslien, Karina Stensland & Miller, Jason Rafe
(2018).
Imprinting Revisited: Regulation of Parent-of-Origin Allelic Expression in Arabidopsis thaliana endosperm.
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Johannessen, Ida Marie; Hornslien, Karina Stensland; Krabberød, Anders Kristian; Bramsiepe, Jonathan; Brysting, Anne Krag & Grini, Paul Eivind
(2018).
The Genetic Basis of Post-Zygotic Hybridization Barriers Between Arabidopsis lyrata and A. arenosa.
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Grini, Paul Eivind
(2018).
Imprinting Revisited: Regulation of Parent-of-Origin Allelic Expression in Arabidopsis thaliana Endosperm.
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Hubin, Aliaksandr; Storvik, Geir Olve & Grini, Paul Eivind
(2017).
Variable selection in binomial regression with latent Gaussian field models for analysis of
epigenetic data.
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Johannessen, Ida Marie; Hornslien, Karina Stensland; Krabberød, Anders Kristian; Bramsiepe, Jonathan; Brysting, Anne Krag & Grini, Paul Eivind
(2017).
The genetic basis of post-zygotic hybridization barriers between Arabidopsis lyrata and A. arenosa.
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Brysting, Anne Krag & Grini, Paul Eivind
(2017).
The molecular basis of postzygotic hybridization barriers in plants.
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Haraldsen, Arthur Alexander Blørstad; Bråte, Jon; Neumann, Ralf Stefan; Fromm, Bastian; Grini, Paul Eivind & Shalchian-Tabrizi, Kamran
(2016).
Pre-metazoan origin of animal microRNAs.
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Aalen, Reidunn B.; Grini, Paul Eivind; Thorstensen, Tage; Alm, Vibeke; Vizcay-Barrena, Gema & Windju, Susanne S.
[Show all 7 contributors for this article]
(2009).
The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis.
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SET-domain proteins add methyl groups to lysine (K) residues of histone tails, which may function as marks activating or repressing transcription. The ASH1 HOMOLOG 2 (ASHH2) protein of Arabidopsis thaliana groups with Drosophila ASH1, a positive maintainer of gene expression, and yeast Set2, a histone H3K36 methyltransferase, and has been implicated as a histone H3K4 or H3K36 methyltransferase. ashh2 mutants display pleiotropic developmental defects, including early flowering. Here we focus on the role of ASHH2 in plant reproduction, of homeotic changes in floral organ identity and specific effects on the development of the reproductive organs. On the female side, close to 80% of the mature ovules lack embryo sac. On the male side, anthers frequently develop without pollen sacs and where present show specific defects in the tapetum layer. As a result, the number of functional pollen per anther was reduced by up to ~90%. Transcriptional profiling identified more than 600 down-regulated genes in ashh2 mutant inflorescences, including genes involved in determination of floral organ identity, embryo sac development and anther/pollen development. Currently, there is a discrepancy in the literature on the primary substrate of ASHH2 methylation. We observed a reduction of H3K36 trimethylation (me3) but not H3K4me3 or H3K36me2 in chromatin from selected down-regulated genes. Thus, our analysis strongly suggests that ASHH2 works via H3K36 trimethylation in the regulation of genes essential in reproductive development.
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Aalen, Reidunn B.; Grini, Paul Eivind; Thorstensen, Tage & Alm, Vibeke
(2009).
The ASHH2 histone 3 lysine methyltransferase is required for ovule and anther development in Arabidopsis thaliana.
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SET-domain proteins are methyltransferases that add methyl groups to lysine (K) residues of histone tails, which function as marks activating or repressing transcription. SET-domain proteins can be divided into evolutionarily conserved classes in animals and plants. Mutation of the ASH1 HOMOLOG 2 (ASHH2) gene of the model plant Arabidopsis has severe pleiotropic effects on growth, development and fertility, in that it results in homoetic changes of floral organ identity, affects male and female gametogenesis, and especially the development of the reproductive organs. On the female side, close to 80 percent of the mature ovules lack embryo sac. On the male side, anthers in part develop without pollen sacs (locules) and in developed locules the tapetum layer, which provides material to the pollen wall, is distorted. Together this results in a more that 75 percent reduction in mature functional pollen grains. Transcriptional profiling was used to identify changes in gene expression in ashh2 mutant inflorescences. Genes involved in determination of floral organ identity, embryo sac development and anther/pollen development were found down-regulated. On such genes ChIP detected reduction of H3K36me3 but not H3K4me3 or H3K36me2. Our study indicates that ASHH2 is a major global H3K36 trimethyltransferase in Arabidopsis.
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Aalen, Reidunn B.; Grini, Paul Eivind; Thorstensen, Tage; Alm, Vibeke; Vizcay-Barrena, Gema & Windju, Susanne S.
[Show all 7 contributors for this article]
(2009).
The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis.
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The more than 30 SET-domain proteins of Arabidopsis can be classified in evolutionarily conserved subgroups that methylate different lysine residues on histone tails (1).The ASH1 HOMOLOG 2 (ASHH2) protein is similar to the Drosophila transcriptional activator ASH1, and the histone H3K36 methyltransferase Set2 from yeast. ashh2 mutants display pleiotropic developmental defects, including early flowering (2,3). We have focused on the role of ASHH2 in plant reproduction, of homeotic changes in floral organ identity and specific effects on the development of the reproductive organs. On the female side, close to 80% of the mature ovules lack embryo sac. On the male side, anthers frequently develop without pollen sacs and where present show specific defects in the tapetum layer, reducing the number of functional pollen per anther by up to ~90%. Transcriptional profiling identified more than 600 down-regulated genes in ashh2 mutant inflorescences, including genes involved in determination of floral organ identity, embryo sac development and anther/pollen development. We observed a reduction of H3K36 trimethylation (me3) but not H3K4me3 or H3K36me2 in chromatin of such genes. Thus, our analysis strongly suggests that ASHH2 works via H3K36 trimethylation in the regulation of genes essential in reproductive development.
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Aalen, Reidunn B.; Thorstensen, Tage; Alm, Vibeke & Grini, Paul Eivind
(2007).
Chromatin modification in Arabidopsis: SET-domain proteins with localization in euchromatin or the nucleolus and identification of a novel histone methyltransferase specificity.
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Thorstensen, Tage; Grini, Paul Eivind; Alm, Vibeke; Butenko, Melinka Alonso; Rosenhave, E. Maryann & Aalen, Reidunn
(2004).
Identification of new gene families and their function using bioinformatics tools and reverse genetics.
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Grini, Paul Eivind; Skrbo, Nirma; Stangeland, Biljana & Aalen, Reidunn
(2003).
Genetic and molecular analysis of gametophytic maternal effect mutants in Arabidopsis.
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Thorstensen, Tage; Grini, Paul Eivind; Mercy, Inderjit Singh & Aalen, Reidunn
(2003).
A SET-domain encoding gene possibly involved in embryo development in Arabidopsis thaliana.
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Grini, Paul Eivind; Skrbo, Nirma; Stangeland, Biljana; Hülskamp, Martin; Jürgens, Gerd & Aalen, Reidunn
(2003).
Genetic and molecular analysis of gametophytic maternal effect mutants in Arabidopsis.
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Skrbo, Nirma; Grini, Paul Eivind & Aalen, Reidunn
(2003).
Towards molecular cloning of the capulet2 gametophyte maternal-effect mutant in Arabidopsis thaliana.
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Skrbo, Nirma; Grini, Paul Eivind; Jürgens, Gerd; Hülskamp, Martin & Aalen, Reidunn
(2003).
Towards molecular cloning of the capulet2 gametophytic maternal-efect mutant in Arabidopsis thaliana.
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Published
Nov. 4, 2010 2:39 PM
- Last modified
Oct. 29, 2024 9:56 AM
