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The (r)evolution of gene regulatory networks controlling Arabidopsis plant reproduction; a two decades history
Pajoro, A. ; Biewers, S. ; Dougali, E. ; Valentim, F.L. ; Mendes, M.A. ; Porri, A. ; Coupland, G. ; Peer, Y. Van de; Dijk, A.D.J. van; Colombo, L. ; Davies, B. ; Angenent, G.C. - \ 2014
Journal of Experimental Botany 65 (2014)17. - ISSN 0022-0957 - p. 4731 - 4745.
floral organ identity - flowering-locus-t - mads-box genes - chromatin immunoprecipitation chip - domain transcription factors - cell-fate determination - short-vegetative-phase - homeotic gene - circadian clock - target genes
Successful plant reproduction relies on the perfect orchestration of singular processes that culminate in the product of reproduction: the seed. The floral transition, floral organ development, and fertilization are well-studied processes and the genetic regulation of the various steps is being increasingly unveiled. Initially, based predominantly on genetic studies, the regulatory pathways were considered to be linear, but recent genome-wide analyses, using high-throughput technologies, have begun to reveal a different scenario. Complex gene regulatory networks underlie these processes, including transcription factors, microRNAs, movable factors, hormones, and chromatin-modifying proteins. Here we review recent progress in understanding the networks that control the major steps in plant reproduction, showing how new advances in experimental and computational technologies have been instrumental. As these recent discoveries were obtained using the model species Arabidopsis thaliana, we will restrict this review to regulatory networks in this important model species. However, more fragmentary information obtained from other species reveals that both the developmental processes and the underlying regulatory networks are largely conserved, making this review also of interest to those studying other plant species.
Research on floral timing by ambient temperature comes into blossom
Verhage, D.S.L. ; Angenent, G.C. ; Immink, R.G.H. - \ 2014
Trends in Plant Science 19 (2014)9. - ISSN 1360-1385 - p. 583 - 591.
flowering-locus-c - transcription factor pif4 - mads-box genes - arabidopsis-thaliana - negative regulator - membrane-fluidity - light quality - phytochrome-b - time - expression
The floral transition is an essential process in the life cycle of flower-bearing plants, because their reproductive success depends on it. To determine the right moment of flowering, plants respond to many environmental signals, including day length, light quality, and temperature. Small changes in ambient temperature also affect the flowering process, although our knowledge of the genetic and molecular mechanisms underlying this flowering pathway is limited. However, recent advances in Arabidopsis (Arabidopsis thaliana) have uncovered multiple molecular mechanisms controlling ambient temperature regulation of flowering, which modulate both repressing and activating factors of flowering time. At a time when temperatures are rising worldwide, understanding how plants integrate ambient temperature signals can be crucial for crop production.
Transfer of knowledge about flowering and vegetative propagation from model species to bulbous plants
Leeggangers, H.A.C.F. ; Moreno Pachón, N.M. ; Gude, H. ; Immink, G.H. - \ 2013
International Journal of Developmental Biology 57 (2013)6-8. - ISSN 0214-6282 - p. 611 - 620.
mads-box genes - axillary meristem formation - tulip tulipa-gesneriana - crocus-sativus l. - agrobacterium-mediated transformation - lily lilium-longiflorum - wild-type - heterotopic expression - arabidopsis-thaliana - stalk elongation
The extensive characterization of plant genes and genome sequences summed to the continuous development of biotechnology tools, has played a major role in understanding biological processes in plant model species. The challenge for the near future is to generate methods and pipelines for an efficient transfer of this knowledge to economically important crops and other plant species. In the case of flower bulbs, which are economically very important for the ornamental industry, flowering time control and vegetative propagation constitute the most relevant processes for agronomical improvements. Those processes have been reasonably studied in reference species, making them excellent candidates for translational investigations in bulbous plant species. The approaches that can be taken for the transfer of biological knowledge from model to non-model species can be roughly categorized as "bottom-up" or "top-down". The former approach usually goes from individual genes to systems, also known as a "gene-by-gene" approach. It assumes conservation of molecular pathways and therefore makes use of sequence homology searches to identify candidate genes. "Top-down" methodologies go from systems to genes, and are e.g. based on large scale transcriptome profiling via heterologous microarrays or RNA sequencing, followed by the identification of associations between phenotypes, genes, and gene expression patterns and levels. In this review, examples of the various knowledge-transfer approaches are provided and pros and cons are discussed. Due to the latest developments in transgenic research and next generation sequencing and the emerging of systems biology as a matured research field, transfer of knowledge concerning flowering time and vegetative propagation capacity in bulbous species are now within sight
The Tarenaya hassleriana Genome Provides Insight into Reproductive Trait and Genome Evolution of Crucifers
Cheng, S. ; Bergh, E. van den; Zeng, P. ; Zong, X. ; Hofberger, J. ; Bruijn, S.A. de; Bhide, A.S. ; Kuelahoglu, C. ; Bian, C. ; Chen, J. ; Fan, G. ; Kaufmann, K. ; Hall, J.C. ; Becker, A. ; Brautigam, A. ; Weber, A.P.M. ; Shi, C. ; Zheng, Z. ; Li, W. ; Lv, M. ; Tao, Y. ; Wang, M. ; Zou, H. ; Quan, Z. ; Hibberd, J.M. ; Zhang, G. ; Zhu, X. ; Schranz, M.E. - \ 2013
The Plant Cell 25 (2013)8. - ISSN 1040-4651 - p. 2813 - 2830.
real-time pcr - mads-box genes - arabidopsis-thaliana - self-incompatibility - corolla monosymmetry - expression patterns - protein-kinases - model-plant - rna-seq - sequence
The Brassicaceae, including Arabidopsis thaliana and Brassica crops, is unmatched among plants in its wealth of genomic and functional molecular data and has long served as a model for understanding gene, genome, and trait evolution. However, genome information from a phylogenetic outgroup that is essential for inferring directionality of evolutionary change has been lacking. We therefore sequenced the genome of the spider flower (Tarenaya hassleriana) from the Brassicaceae sister family, the Cleomaceae. By comparative analysis of the two lineages, we show that genome evolution following ancient polyploidy and gene duplication events affect reproductively important traits. We found an ancient genome triplication in Tarenaya (Th-a) that is independent of the Brassicaceae-specific duplication (At-a) and nested Brassica (Br-a) triplication. To showcase the potential of sister lineage genome analysis, we investigated the state of floral developmental genes and show Brassica retains twice as many floral MADS (for MINICHROMOSOME MAINTENANCE1, AGAMOUS, DEFICIENS and SERUM RESPONSE FACTOR) genes as Tarenaya that likely contribute to morphological diversity in Brassica. We also performed synteny analysis of gene families that confer self-incompatibility in Brassicaceae and found that the critical SERINE RECEPTOR KINASE receptor gene is derived from a lineage-specific tandem duplication. The T. hassleriana genome will facilitate future research toward elucidating the evolutionary history of Brassicaceae genomes.
Parthenocarpic potential in Capsicum annuum L. is enhanced by carpelloid structures and controlled by a single recessive gene
Tiwari, A. ; Vivian-Smith, A. ; Voorrips, R.E. ; Habets, M.E.J. ; Xue, L.B. ; Offringa, R. ; Heuvelink, E. - \ 2011
BMC Plant Biology 11 (2011). - ISSN 1471-2229 - 15 p.
mads-box genes - ovule development - fruit-development - sweet-pepper - arabidopsis - tomato - pollen - growth - flower - mutant
Background Parthenocarpy is a desirable trait in Capsicum annuum production because it improves fruit quality and results in a more regular fruit set. Previously, we identified several C. annuum genotypes that already show a certain level of parthenocarpy, and the seedless fruits obtained from these genotypes often contain carpel-like structures. In the Arabidopsis bel1 mutant ovule integuments are transformed into carpels, and we therefore carefully studied ovule development in C. annuum and correlated aberrant ovule development and carpelloid transformation with parthenocarpic fruit set. Results We identified several additional C. annuum genotypes with a certain level of parthenocarpy, and confirmed a positive correlation between parthenocarpic potential and the development of carpelloid structures. Investigations into the source of these carpel-like structures showed that while the majority of the ovules in C. annuum gynoecia are unitegmic and anatropous, several abnormal ovules were observed, abundant at the top and base of the placenta, with altered integument growth. Abnormal ovule primordia arose from the placenta and most likely transformed into carpelloid structures in analogy to the Arabidopsis bel1 mutant. When pollination was present fruit weight was positively correlated with seed number, but in the absence of seeds, fruit weight proportionally increased with the carpelloid mass and number. Capsicum genotypes with high parthenocarpic potential always showed stronger carpelloid development. The parthenocarpic potential appeared to be controlled by a single recessive gene, but no variation in coding sequence was observed in a candidate gene CaARF8. Conclusions Our results suggest that in the absence of fertilization most C. annuum genotypes, have parthenocarpic potential and carpelloid growth, which can substitute developing seeds in promoting fruit development.
A new member of the LIR gene family form perennial ryegrass is cold-resposive, and promotes vegetative growth in Arabidopsis
Ciannamea, S. ; Jensen, C.S. ; Agerskov, H. ; Petersen, K. ; Lenk, I. ; Didion, T. ; Immink, R.G.H. ; Angenent, G.C. ; Nielsen, K.K. - \ 2007
Plant Science 172 (2007)2. - ISSN 0168-9452 - p. 221 - 227.
mads-box genes - vernalization response - lolium-perenne - floral transition - flowering time - messenger-rnas - expression - thaliana - rice - tolerance
A cold-regulated gene Lolium perenne LIR1 (LpLIR1) was isolated from perennial ryegrass using a subtractive approach. The gene has strong homology to the Light Induced Rice1 (LIR1) gene and is regulated at the transcriptional level by cold, and by a diurnal rhythm. Expression of LpLIR1 in perennial ryegrass was upregulated by vernalization but did not follow a standard vernalization-responsive expression pattern. LpLIR1 expression was restricted to vegetative tissues and absent in apices during floral induction and in flowers. LpLIR1 mRNA levels displayed diurnal fluctuations, which peaked before dusk and declined during the night. Heterologous expression of LpLIR1 in Arabidopsis led to a significant increase in leaf formation under short days (SD) conditions but only when plants had received a preceding vernalization treatment. Furthermore, dissection of plant development under SD revealed a minor but significant delay of flowering in the transgenic lines compared to wildtype plants
Analysis of the SHP2 enhancer for the use of tissue specific activation tagging in Arabidopsis thaliana
Chalfun Junior, A. ; Mes, J.J. ; Busscher, M. ; Angenent, G.C. - \ 2006
Genetics and Molecular Biology 29 (2006)2. - ISSN 1415-4757 - p. 401 - 407.
mads-box genes - transformation - biosynthesis - growth - plants - fruit - transcription - regulator - sequences - promoter
Activation tagging is a powerful tool to identify new mutants and to obtain information about possible biological functions of the overexpressed genes. The quadruple cauliflower mosaic virus (CaMV) 35S enhancer fragment is a strong enhancer, which is most commonly used for this purpose. However, the constitutive nature of this enhancer may generate lethal mutations or aberrations in different plant organs by the same overexpressed gene. A tissue-specific activation tagging approach may overcome these drawbacks and may also lead more efficiently to the desired phenotype. For this reason the SHATTERPROOF2 (SHP2) promoter fragment was analysed for enhancer activity. The SHP2 gene is involved in dehiscence zone development and expressed during silique development. The aim of the experiments described here was to identify a dehiscence zone specific enhancer that could be used for tissue-specific activation tagging. The chosen SHP2 enhancer fragment was found to be expressed predominantly in the dehiscence zone and showed enhancer activity as well as ectopic expression activity. This activity was not influenced by its orientation towards the promoter and it was still functional at the largest tested distance of 2.0 kb. Based on these results, the SHP2 enhancer fragment can potentially be used in a tissue-specific activation tagging approach to identify new Arabidopsis mutants with an altered dehiscence zone formation.
Characterization of the vernalization response in Lolium perenne by a cDNA microarry approach
Ciannamea, S. ; Busscher-Lange, J. ; Folter, S. de; Angenent, G.C. ; Immink, R.G.H. - \ 2006
Plant and Cell Physiology 47 (2006)4. - ISSN 0032-0781 - p. 481 - 492.
mads-box genes - arabidopsis flowering time - freezing tolerance - transcription factors - reproductive growth - histone methylation - expression - thaliana - wheat - repressor
Many plant species including temperate grasses require vernalization in order to flower. Vernalization is the process of promotion of flowering after exposure to prolonged periods of cold. To investigate the vernalization response in monocots, the expression patterns of about 1,500 unique genes of Lolium perenne were analyzed by a cDNA microarray approach, at different time points after transfer of plants to low temperatures. Vernalization of L. perenne takes around 80 d and, therefore, the plants were incubated at low temperatures for at least 12 weeks. A total of 70 cold-responsive genes were identified that are either up- or down-regulated with a minimal 2-fold difference compared with the common reference. The majority of these genes show a very rapid response to the cold treatment, indicating that their expression is affected by the cold stress and, therefore, these genes are not likely to be involved in the flowering process. Based on hierarchical clustering, one gene could be identified that is down-regulated towards the end of the cold period and, in addition, a few genes have been found that are up-regulated in the last weeks of the cold treatment and, hence, are putative candidates for genes involved in the vernalization response. Three of the up-regulated genes are homologous to members of the MADS box, CONSTANS-like and JUMONJI families of transcription factors, respectively. The latter two are novel genes not connected previously to vernalization-induced flowering. Furthermore, members of the JUMONJI family of transcription factors have been shown to be involved in chromatin remodeling, suggesting that this molecular mechanism, as in Arabidopsis, plays a role in the regulation of the vernalization response in monocots.
Isolation and characterization of an AGAMOUS homologue from cocoa
Chaidamsari, T. ; Sugiarit, H. ; Santoso, D. ; Angenent, G.C. ; Maagd, R.A. de - \ 2006
Plant Science 170 (2006)5. - ISSN 0168-9452 - p. 968 - 975.
mads-box genes - ectopic expression - flower development - transcription factors - arabidopsis - plants - transformation - theobroma - evolution - cacao
We report the cloning of a cDNA from TcAG, an AG (Arabidopsis thaliana MADS-box C-type transcription factor gene AGAMOUS) homologue from cocoa (Theobroma cacao L.). TcAG was in the cocoa flower expressed primarily in stamens and ovaries, comparable to AG in Arabidopsis. Additionally, we found that TcAG is also expressed in the fruit (pod) wall and during its entire development, as well as in the fruit pulp. Ectopic expression of TcAG in transgenic A. thaliana plants resulted in a range of weak to strong apetala2 (ap2) mutant-like phenotypes as well as early flowering and curly leaves, as observed in other studies of plants overexpressing a functional AG homologue. The severity of the phenotypes correlated positively with the TcAG transcript level in the transgenic plants.
Phylogenetic analyses of basal angiosperms based on nine plastid, mitochondrial, and nuclear genes
Qiu, Y.L. ; Dombrovska, O. ; Lee, J. ; Li, L. ; Whitlock, B.A. ; Bernasconi-Quadroni, F. ; Rest, J.S. ; Davis, C.C. ; Borsch, T. ; Hilu, K.W. ; Renner, S.S. ; Soltis, D.E. ; Soltis, P.E. ; Zanis, M.J. ; Cannone, J.J. ; Powell, M. ; Savolainen, V. ; Chatrou, L.W. ; Chase, M.W. - \ 2005
International Journal of Plant Sciences 166 (2005)5. - ISSN 1058-5893 - p. 815 - 842.
inferring complex phylogenies - ribosomal dna-sequences - 3 genomic compartments - group-ii intron - mads-box genes - land plants - flowering plants - chloroplast genome - rdna sequences - molecular-data
DNA sequences of nine genes (plastid: atpB, matK, and rbcL; mitochondrial: atp1, matR, mtSSU, and mtLSU; nuclear: 18S and 26S rDNAs) from 100 species of basal angiosperms and gymnosperms were analyzed using parsimony, Bayesian, and maximum likelihood methods. All of these analyses support the following consensus of relationships among basal angiosperms. First, Amborella, Nymphaeaceae, and Austrobaileyales are strongly supported as a basal grade in the angiosperm phylogeny, with either Amborella or Amborella and Nymphaeales as sister to all other angiosperms. An examination of nucleotide substitution patterns of all nine genes ruled out any possibility of analytical artifacts because of RNA editing and GC-content bias in placing these taxa at the base of the angiosperm phylogeny. Second, Magnoliales are sister to Laurales and Piperales are sister to Canellales. These four orders together constitute the magnoliid clade. Finally, the relationships among Ceratophyllum, Chloranthaceae, monocots, magnoliids, and eudicots are resolved in different ways in various analyses, mostly with low support. Our study indicates caution in total evidence approaches in that some of the genes employed (e.g., mtSSU, mtLSU, and nuclear 26S rDNA) added signal that conflicted with the other genes in resolving certain parts of the phylogenetic tree
Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis
Gomez-Mena, C. ; Folter, S. de; Costa, M.M.R. ; Angenent, G.C. ; Sablowski, R. - \ 2005
Development 132 (2005)3. - ISSN 0950-1991 - p. 429 - 438.
mads-box genes - arabidopsis-thaliana - flower development - organ identity - meristem identity - gibberellin 3-beta-hydroxylase - molecular characterization - expression analysis - stem elongation - target genes
Floral organs, whose identity is determined by specific combinations of homeotic genes, originate from a group of undifferentiated cells called the floral meristem. In Arabidopsis, the homeotic gene AGAMOUS (AG) terminates meristem activity and promotes development of stamens and carpels. To understand the program of gene expression activated by AG, we followed genome-wide expression during early stamen and carpel development. The AG target genes included most genes for which mutant screens revealed a function downstream of AG. Novel targets were validated by in situ hybridisation and binding to AG in vitro and in vivo. Transcription factors formed a large fraction of AG targets, suggesting that during early organogenesis, much of the genetic program is concerned with elaborating gene expression patterns. The results also suggest that AG and other homeotic proteins with which it interacts (SEPALLATA3, APETALA3, PISTILLATA) are coordinately regulated in a positive-feedback loop to maintain their own expression, and that AG activates biosynthesis of gibberellin, which has been proposed to promote the shift from meristem identity to differentiation.
Use of Petunia to unravel plant meristem functioning
Angenent, G.C. ; Stuurman, J. ; Snowden, K.C. ; Koes, R. - \ 2005
Trends in Plant Science 10 (2005)5. - ISSN 1360-1385 - p. 243 - 250.
mads-box genes - shoot apical meristem - floral organ - arabidopsis-thaliana - flower development - inflorescence development - antirrhinum-majus - ovule development - cell fate - identity
In the past decade, enormous progress has been made in our understanding of the molecular and genetic control of meristem growth, maintenance and differentiation into plant organs. Several model plants have contributed to our current knowledge of meristem function. Research using Petunia has had a substantial share in this progress. Integration of information obtained from this species gives clues about the common and diverged pathways underlying the formation and functioning of plant meristems
Effect of the colorless non-ripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening
Eriksson, E.M. ; Bovy, A.G. ; Manning, K. ; Harrison, L. ; Andrews, J. ; Silva, J. De; Tucker, A. ; Seymour, G.B. - \ 2004
Plant Physiology 136 (2004)4. - ISSN 0032-0889 - p. 4184 - 4197.
mads-box genes - sambucus-nigra - cdna clone - proteins - mutant - polygalacturonase - arabidopsis - ethylene - cnr - pectinesterase
The Colorless non-ripening (Cnr) mutation in tomato (Solanum lycopersicum) results in mature fruits with colorless pericarp tissue showing an excessive loss of cell adhesion (A.J. Thompson, M. Tor, C.S. Barry, J. Vrebalov, C. Orfila, M.C. Jarvis, J.J. Giovannoni, D. Grierson, G.B. Seymour  Plant Physiol 120: 383-390). This pleiotropic mutation is an important tool for investigating the biochemical and molecular basis of cell separation during ripening. This study reports on the changes in enzyme activity associated with cell wall disassembly in Cnr and the effect of the mutation on the program of ripening-related gene expression. Real-time PCR and biochemical analysis demonstrated that the expression and activity of a range of cell wall-degrading enzymes was altered in Cnr during both development and ripening. These enzymes included polygalacturonase, pectinesterase (PE), galactanase, and xyloglucan endotransglycosylase. In the case of PE, the protein product of the ripening-related isoform PE2 was not detected in the mutant. In contrast with wild type, Cnr fruits were rich in basic chitinase and peroxidase activity. A microarray and differential screen were used to profile the pattern of gene expression in wild-type and Cnr fruits. They revealed a picture of the gene expression in the mutant that was largely consistent with the real-time PCR and biochemical experiments. Additionally, these experiments demonstrated that the Cnr mutation had a profound effect on many aspects of ripening-related gene expression. This included a severe reduction in the expression of ripening-related genes in mature fruits and indications of premature expression of some of these genes in immature fruits. The program of gene expression in Cnr resembles to some degree that found in dehiscence or abscission zones. We speculate that there is a link between events controlling cell separation in tomato, a fleshy fruit, and those involved in the formation of dehiscence zones in dry fruits
Transcript profiling of transcription factor genes during silique development in Arabidopsis
Folter, S. de; Lange, J. ; Colombo, L. ; Losa, A. ; Angenent, G.C. - \ 2004
Plant Molecular Biology 56 (2004)3. - ISSN 0167-4412 - p. 351 - 366.
mads-box genes - shoot apical meristem - fruit-development - ovule development - seed development - domain protein - zinc-finger - plant - expression - thaliana
Flower development is a key process for all angiosperms and is essential for sexual reproduction. The last phase in flower development is fertilization of the ovules and formation of the fruits, which are both biologically and economically of importance. Here, we report the expression profiles of over 1100 unique Arabidopsis genes coding for known and putative transcription factors (TFs) during silique development using high-density filter array hybridizations. Hierarchical cluster analyses revealed distinct expression profiles for the different silique developmental stages. This allowed a functional classification of these expression profiles in groups, namely pistil development, embryogenesis, seed maturation, fruit maturation, and fruit development. A further focus was made on the MADS-box family, which contains many members that are functionally well-characterized. The expression profiles of these MADS-box genes during silique development give additional clues on their functions and evolutionary relationship.
Ectopic expression of LLAG1, an AGAMOUS homologue from lily (Lilium longiflorum Thunb.) causes floral homeotic modifications in Arabidopsis.
Benedito, V.A. ; Visser, P.B. ; Tuyl, J.M. van; Angenent, G.C. ; Vries, S.C. de; Krens, F.A. - \ 2004
Journal of Experimental Botany 55 (2004)401. - ISSN 0022-0957 - p. 1391 - 1399.
mads-box genes - controlling flower development - protein-protein interactions - transcription factors - organ identity - gerbera-hybrida - plant biology - wild-type - petunia - transformation
The ABC model for floral development was proposed more than 10 years ago and since then many studies have been performed on model species, such as Arabidopsis thaliana, Antirrhinum majus, and many other species in order to confirm this hypothesis. This led to additional information on flower development and to more complex molecular models. AGAMOUS (AG) is the only C type gene in Arabidopsis and it is responsible for stamen and carpel development as well as floral determinacy. LLAG1, an AG homologue from lily (Lilium longiflorum Thunb.) was isolated by screening a cDNA library derived from developing floral buds. The deduced amino acid sequence revealed the MIKC structure and a high homology in the MADS-box among AG and other orthologues. Phylogenetic analysis indicated a close relationship between LLAG1 and AG orthologues from monocot species. Spatial expression data showed LLAG1 transcripts exclusively in stamens and carpels, constituting the C domain of the ABC model. Functional analysis was carried out in Arabidopsis by overexpression of LLAG1 driven by the CaMV35S promoter. Transformed plants showed homeotic changes in the two outer floral whorls with some plants presenting the second whorl completely converted into stamens. Altogether, these data strongly indicated the functional homology between LLAG1 and AG.
Conservation and diversity in flower land
Ferrario, S.I.T. ; Immink, R.G.H. ; Angenent, G.C. - \ 2004
Current Opinion in Plant Biology 7 (2004)1. - ISSN 1369-5266 - p. 84 - 91.
mads-box genes - floral organ identity - protein-protein interactions - transcription factor family - arabidopsis-thaliana - ovule development - homeotic proteins - draft sequence - class-b - petunia
During the past decade, enormous progress has been made in understanding the molecular regulation of flower development. In particular, homeotic genes that determine the identity of the floral organs have been characterised from different flowering plants, revealing considerable conservation among angiosperm species. On the other hand, evolutionary diversification has led to enormous variation in flower morphology. Increasing numbers of reports have described differences in the regulation, redundancy and function of homeotic genes from various species. These fundamentals of floral organ specification are therefore an ideal subject for comparative analyses of flower development, which will lead to a better understanding of plant evolution, plant development and the complexity of molecular mechanisms that control flower development and morphology.