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Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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Structural basis for specific gene regulation by Auxin Response Factors
Freire Rios, Alejandra - \ 2016
Wageningen University. Promotor(en): Dolf Weijers. - Wageningen : Wageningen University - ISBN 9789462579538 - 190
auxins - gene regulation - plant growth regulators - embryonic development - plant embryos - dna - auxinen - genregulatie - plantengroeiregulatoren - embryonale ontwikkeling - plantenembryo's - dna

Auxin is a plant hormone that triggers a broad variety of responses during plant development. These responses range from correct cell division patterns during embryogenesis to formation and growth of different organs. Due to its importance for plant growth and development, many aspects of the biology of auxin have been studied. In Chapter 2, we use Arabidopsis embryogenesis as a stage to describe generalities about its biosynthesis, transport, components of its signaling pathway and transcriptional control of some know target genes.

As most of the players involved in transcriptional regulation in response to auxin have been identified, the question of how the same signal can elicit so many different responses remains open. In this thesis we approach this issue by focusing on the ultimate effectors of the auxin signaling pathway: the ARF family of transcription factors. In Chapter 3 we present the crystal structure of the DNA binding Domain (DBD) of two divergent members of the family: ARF1 and ARF5. Careful observation of the structures, followed by in vitro and in vivo experiments led to the following conclusions: 1) ARF DBDs dimerize through a conserved alpha-helix, and bind cooperatively to an inverted repeat of the canonical TGTCTC AuxRE. Dimerization of this domain is important for high-affinity DNA binding and in vivo activity. 2) Monomeric ARFs have the same binding preference for the DNA sequence TGTCGG (determined by protein binding microarray). 3) DNA-contacting residues are almost completely conserved within the ARF family members. 4) The distance between the AuxREs may play a role for binding of specific ARF dimers as for example, ARF5 can accommodate and bind to different spacing (6-9 bp) compared to ARF1 which is more rigid (7-8 bp).

In Chapter 4 we follow up on the observations made. First we again used structural biology to determine the reason of the high binding affinity to the TGTCGG sequence compared to the previously identified canonical TGTCTC element. We found that in complex with TGTCGG, His137 (ARF1) could rotate and make hydrogen bonds with either G5 or G6, as well as a hydrogen bond with the C opposing to G6. This rotation is not possible when in complex with TGTCTC and there the same histidine can make only one hydrogen bond with the G opposing to C6. We conclude then that this histidine plays a role in determining the strength of binding to TGTCNN elements and that this also reflects in its specific transcriptional activity as mutating the corresponding histidine in ARF5 renders a semi-functional protein in vivo (Chapter 3).

The next observation we followed up in Chapter 4 is the biological meaning of ARF DBDcooperative binding to DNA. We identified AuxRE inverted repeats (IR) in the promoter of the TMO5 gene and mutated them. This brought the expression of the gene to very low levels despite the presence of other multiple single AuxREs. Thus, the single inverted AuxRE repeat in the TMO5 promoter is essential for ARF5 binding and gene regulation. Importantly, mutating only a single AuxRE element within the inverted repeat led to very pronounced loss of activity, consistent with requirement of both AuxRE sites for high-affinity ARF5 binding. We then concluded that IR AuxREs have a significant effect in gene regulation by ARFs. Next we search the genome for bipartite AuxREs that correlated to auxin response and found two main elements: inverted repeat with 8 bases of spacing (IR8) and direct repeat with 5 bases of spacing (DR5). As this kind of bipartite AuxREs are rarer to find than single AuxREs, we tested their presence in promoters as predictors of auxin responsiveness by qPCR. We found that about 75% of the selected genes containing either IR8 or DR5 responded to auxin. The expression study also show that genes containing the DR5 sequence were only up-regulated when regulated. Interestingly, Surface Plasmon Resonance study showed that only class A (activator) ARFs can bind the DR5 sequence cooperatively.

As the structural differences of ARFs DBDs are subtle, we then asked if specific gene targeting is determined by this domain alone. In Chapter 5 we used a DBD swap experiment and conclude that the DBD is necessary for specific gene targeting but not sufficient and the other domains of an ARF also contribute in its specific activity.

In Chapter 5 we expand our focus from the DBD to the other ARF domains, Middle Region (MR) and C-terminal (CT). As ARFs have protein-protein interaction interfaces in all three domains, we expressed the isolated domains of ARF5 and perform immuno-precipitation followed by tandem mass-spectrometry. Although the procedure needs optimization, some interactions expected for each domain could be identified. The DBD showed to interact with the general transcription machinery and the CT could interact with another ARF and 3 Aux/IAA. These interactions seem to be specific as the Aux/IAA recovered are not the most abundant in the sampled tissue.

Finally, in Chapter 6 all the obtained results are put in a broader context and new questions derived from our results are proposed.

Stem cell organization in Arabidopsis : from embryos to roots
Wendrich, J.R. - \ 2016
Wageningen University. Promotor(en): D. Weijers, co-promotor(en): B.P.M. de Rybel. - Wageningen : Wageningen University - ISBN 9789462577350 - 192
arabidopsis - stem cells - roots - plant embryos - morphogenesis - biological development - cellular biology - plant cell biology - arabidopsis - stamcellen - wortels - plantenembryo's - morfogenese - biologische ontwikkeling - celbiologie - plantencelbiologie

Growth of plant tissues and organs depends on continuous production of new cells, by niches of stem cells. Stem cells typically divide to give rise to one differentiating daughter and one non-differentiating daughter. This constant process of self-renewal ensures that the niches of stem cells or meristems stay active throughout plant-life. Specification of stem cells occurs very early during development of the emrbyo and they are maintained during later stages. The Arabidopsis embryo is a highly predictable and relatively simple model to study several developmental processes. Chapter 1 discusses the Arabidopsis embryo as a model for development and morphogenesis and describes the currently known factors involved in these processes.

Molecular cloning is a vital technique of today’s plant biological research. The ability to quickly produce reliable constructs for follow-up analyses can greatly accelerate biological research. In Chapter 2, we describe the optimization of a highly efficient Ligation Independent Cloning method. This method makes use of sticky overhangs that enable in vivo ligation of cloning products. We present a step-by-step protocol that enables generating plant transformation-ready constructs in a semi-high-throughput manner, within two to three days. This method can for example facilitate follow-up analysis of genome-wide approaches.

Proteins regularly function as part of larger protein-complexes and their interaction partners can often be indicative of functionality. Unbiased, in vivo analysis of protein complexes can therefore be very informative for the functional characterization of a protein of interest. In Chapter 3, we describe an optimized method for immunoprecipitation followed by tandem mass-spectrometry. By performing mass-spectrometry measurements on at least three biological replicates, relative abundance of proteins in GFP-tagged sample compared to background controls can be statistically evaluated to identify high-confidence interactors. In this step-by-step protocol we detail the entire procedure from plant material to data analysis and visualization.

The establishment of distinct cellular identities is of critical importance for multicellular organisms. The first step that leads to cell identity is the activation of a unique set of transcripts and this often exploited in order to infer cell identity. In Chapter 4, we have generated 12 gene expression marker lines and describe their expression domain in the Arabidopsis embryo. We divided them into four different categories based on their expression domain: (I) ground tissue; (II) root stem cell; (III) shoot apical meristem; and (IV) post-embryonic. In addition, we used two stem cell markers to show their use as marker lines in genetic studies.

A central player in development of the Arabidopsis root meristem is the AUXIN RESPONSE FACTOR5/MONOPTEROS (MP). Several downstream targets of this transcription factor have been characterized, but the main focus has been on targets that were themselves transcription factors. An open question remains, therefore, how MP can orchestrate cellular responses during development. Chapter 5 describes the in-depth functional and biochemical characterization of a group of IQ-domain proteins. We show that their expression is regulated by the hormone auxin and that they bind microtubules and Calmodulins, in vivo. In addition, we show that the subcellular localization of IQD18 is cell cycle dependent. Loss- and gain-of-function analysis resulted in differential auxin- and calcium-signaling output, suggesting these proteins may form a bridge between these two major signaling pathways. Furthermore, this indicates a mode for how MP may be affecting cellular responses, during root development.

In Chapter 6, we take a step back and re-evaluate the currently prevailing model for stem cell organization in the Arabidopsis (embryonic) root. Using different gene expression markers, we were able to generate non-cell type specific and cell type specific transcriptomic datasets from systematically obtained ontogenetic cell populations in the root meristem. Follow-up analyses give support for an extended model for stem cell organization in the root.

Finally, in Chapter 7, we discuss the novel findings of this thesis and suggestions are made for future research directions.

Microspore embryogenesis: reprogramming cell fate from pollen to embryo development
Hui Li, - \ 2014
Wageningen University. Promotor(en): Gerco Angenent, co-promotor(en): Kim Boutilier. - Wageningen : Wageningen University - ISBN 9789462570702 - 224
stuifmeel - embryogenese - embryonale ontwikkeling - biologische ontwikkeling - plantenontwikkeling - in vitro kweek - plantenembryo's - brassica napus - pollen - embryogenesis - embryonic development - biological development - plant development - in vitro culture - plant embryos - brassica napus

Microspore embryogenesis is an expression of plant cell totipotency that leads to the production of haploid embryos. Besides being a widely exploited plant breeding tool, microspore embryogenesis is also a fascinating system that can be used to obtain a deeper mechanistic understanding of plant totipotency. This thesis aims to provide more insight into the process of microspore embryogenesis, from the formation of embryogenic cells to the outgrowth of differentiated embryos.

In Chapter 1 background information is provided on the various aspects of Brassica napus microspore culture and plant development that intersect with the topics that are studied in this thesis. Emphasis is placed on the basic requirements and limitations for successful microspore embryo culture, as well as on the roles of the plant hormone auxin and epigenetic regulation in the development of plant embryos, during both zygotic and in vitro embryo development.

Chapter 2 reviews the recent advances that have been made in understanding the developmental and molecular changes that take place during microspore embryogenesis in model systems. The commonly reported cellular changes associated with the establishment of embryo cell fate are summarized and evaluated. The subsequent differentiation of the embryo is also discussed, specifically, what is known about the establishment of polarity, with emphasis on the importance of exine rupture as a positional clue, and the processes that influence meristem maintenance during culture. Finally, the studies on the molecular changes during microspore embryo induction are put into context of male gametophytic development. Overall, the current perspective on microspore embryo initiation presents a landscape in which several routes can lead to the same final destination.

Stress treatments are widely applied to induce embryogenic growth in microspore culture. Chapter 3 explores the role of histone acetylation status in stress-induced microspore embryogenesis in Brassica napus. Inhibition of histone deactylases (HDACs) using the HDAC inhibitor trichostatin A (TSA), phenocopies the heat stress treatment that is normally used to induce embryogenic cell proliferation in B. napus microspore culture. Arabidopsis is recalcitrant for haploid embryogenesis, yet treatment with TSA also induced embryogenic cell divisions in this model species. Our observations suggest that the totipotency of the male gametophyte is kept in check by an HDAC-dependent mechanism and that the stress treatments used to induce haploid embryo development in culture impinge on this HDAC-dependent pathway. The repression of HDACs or HDAC-mediated pathways by stress and the accompanying changes in histone acetylation status could provide a single, common regulation point for the induction of haploid embryogenesis.

Chapter 4 builds on the knowledge developed in Chapter 3 on the role of HDAC proteins in plant totipotency. A wide variety of chemically distinct HDAC inhibitors was evaluated and additional inhibitors that enhance embryogenic cell induction and/or embryo yield were identified. One surprising observation was made during the course of this study: the initial donor microspore/pollen stage affects the quality of the embryo that is formed. In control cultures, embryos from progressively older stages of donor microspores/pollen became progressively compromised in their basal (axis region) region, characterized by a shift from normal embryos with apical (cotyledons) and basal (root) polarity to abnormal embryos with a reduced basal pole and ball-shaped embryos. These abnormal phenotypes could be partially complemented by treatment with HDAC inhibitors, which promoted growth of the basal region of the embryo. Progressive enhancement of embryo basal identity was accompanied by enhanced and broadened expression of the DR5 auxin response reporter. The embryo phenotypes observed in control and HDAC inhibitor treated microspore cultures are similar to the phenotypes induced by altered expression of the Arabidopsis TOPLESS (TPL)/HDAC19/BODENLOS (BDL) repressor complex, which acts to restrict expression of the AUXIN RESPONSE FACTOR ARF5/MONOPTEROS (MP) to the basal region of the embryo during zygotic embryo development.

To understand why most embryogenic callus failed to develop further, we examined the transcriptome of globular-shaped embryos that have started to histodifferentiate and compared it with embryogenic callus. The transcriptome analysis showed that the expression of many genes that regulate (auxin-related) embryo patterning were downregulated in embryogenic callus compared to globular stage embryos. This result may simply reflect the lack of patterning in these embryos or might indicate a role of auxin-signalling in embryogenic callus formation.

Chapter 5 examines how embryo identity and patterning is established in two B. napus microspore embryo pathways, a zygotic-like pathway, characterized by suspensor and then embryo proper formation, and a pathway characterized by initially unorganized structures that lack a suspensor. We specifically asked the question: how can embryo patterning be established in the absence of an initial asymmetric division and in the absence of a suspensor, two key events in zygotic embryo development. Analysis of embryo fate (GRP) and auxin (PIN1, PIN7 and DR5) markers showed that embryo fate was established prior to cell division, and independent of subsequent division pattern. The suspensorless embryo program was marked by a transient auxin maximum, followed by establishment of the apical and basal poles at the globular stage, coincident with release of the embryo from the pollen exine. Unlike zygotic embryo development, polar auxin transport (PAT) was not required for embryo initiation or polarity establishment in this system. Suspensor embryos developed in a similar fashion as zygotic embryos, PAT was required for specification of the embryo proper from the suspensor. Haploid embryogenesis therefore follows at least two programs, a PAT-dependent program that requires embryo proper specification from the suspensor, and an alternative PAT-independent program marked by an initial auxin maximum.

In the final chapter, Chapter 6, the work presented in this thesis is put in context of the broader plant development field. The epigenetic regulation of developmental transitions that respond to stress and during pollen development are highlighted. A model is provided that histone acetylation levels mediated by HAT and HDAC regulate pollen fate.

The biochemical basis of plant development
Weijers, D. - \ 2013
Wageningen : Wageningen University - ISBN 9789461736215 - 23
fytochemie - plantenontwikkeling - planten - plantenweefsels - celbiologie - moleculaire biologie - biochemie - plantenembryo's - phytochemistry - plant development - plants - plant tissues - cellular biology - molecular biology - biochemistry - plant embryos
Plants develop highly elaborate structures, ranging from small mosses to large trees. All these structures are made by stem cells and consist of a few basic types of tissue. The field of Biochemistry of Plant Development studies the mechanisms by which regulatory proteins control the formation of stem cells and tissues. The young embryo, developing within the seed, is the simplest model to study these fundamental processes, and to gain understanding of the basis for plant development at cellular, molecular and atomic scale.
Identification of novel MONOPTEROS target genes in embryonic root initiation
Moller, B.K. - \ 2012
Wageningen University. Promotor(en): Sacco de Vries, co-promotor(en): Dolf Weijers. - S.l. : s.n. - ISBN 9789461732392 - 192
plantenembryo's - wortels - plantenontwikkeling - genregulatie - arabidopsis - embryonale stamcellen - auxinen - plant embryos - roots - plant development - gene regulation - arabidopsis - embryonic stem cells - auxins - cum laude
cum laude graduation (with distinction)
The role of auxin in cell specification during arabidopsis embryogenesis
Lokerse, A.S. - \ 2011
Wageningen University. Promotor(en): Sacco de Vries, co-promotor(en): Dolf Weijers. - [S.l.] : S.n. - ISBN 9789461731104 - 191
arabidopsis - embryogenese - auxinen - celdifferentiatie - genexpressie - plantenembryo's - transcriptiefactoren - arabidopsis - embryogenesis - auxins - cell differentiation - gene expression - plant embryos - transcription factors

Auxin is a structurally simple molecule, yet it elicits many different responses in plants. In Chapter 1 we have reviewed how specificity in the output of auxin signaling could be generated by distinct regulation and the unique properties of the members of the Aux/IAA and ARF transcription factor families.

In Chapter 2 we further investigated the generation of specificity in auxin responses by generating a set of sensitive transcriptional reporter lines for all Arabidopsis ARFs. This facilitated a comprehensive identification of the ARF complement within a cell/tissue of interest. Our analysis of ARF expression in the root meristem revealed both ubiquitous and specific ARF expression patterns and ARF subsets that distinguished the actively dividing cells from those undergoing elongation. Moreover, a striking correlation between cell type and ARF expression patterns was revealed in the early Arabidopsis embryo, where each cell type expressed a unique ARF complement.

In Chapter 3 we characterized a novel cell-autonomous auxin response is required for hypophysis specification and root meristem initiation, and identify Aux/IAA and ARF transcription factors that mediate this response. We show that auxin response components in the proembryo and the suspensor are intrinsically different, and their regulated, lineage-specific expression creates a prepattern enabling different developmental auxin responses. Surprisingly, we find that, in addition to mediating hypophysis specification, auxin response also acts to maintain suspensor cell identity. We show that auxin controlled maintenance of suspensor cell identity includes repression of the embryonic program. This finding gave us an experimental system in which to investigate suspensor cell identity and embryonic transformation.

In Chapter 4 the targeted and specific inhibition of auxin response in the suspensor was coupled to new embryo dissection techniques and a microarray based approach was used to generate a unique dataset which was subsequently mined for cell identity regulators. Unexpectedly, inhibition of auxin response induced the misregulation of thousands of genes, prior to gross morphological changes, revealing a high degree of transcriptional plasticity in these cells. This complicated the identification of regulators. Moreover, the dataset also included secondary/indirect changes in embryo expressed genes, which were inevitable given the connectivity and developmental connectedness between the embryo and suspensor.

One of the most striking findings from analysis of the dataset generated in Chapter 4 was the convergent regulation of members of many gene families involved in all facets of auxin homeostasis, as investigated in Chapter 5. It appears that transient auxin response inhibition is sensed as an auxin minimum and in general auxin homeostasis genes were activated or repressed in such a way that would increase cellular auxin levels (and response).

Finally, many bHLH superfamily members were misregulated upon the inhibition of suspensor auxin response and subsequently found to have specific expression patterns in the embryo, the focus of in Chapter 6. Several bHLHs were shown to lose their lineage specific expression patterns upon inhibition of auxin response in the suspensor, validating further research to place these factors into the auxin response pathways controlling cell identity in the embryo.

Structural changes in membranes of developing wheat embryos during the acquisition of desiccation tolerance
Golovina, E.A. ; Hoekstra, F.A. - \ 2003
In: The Biology of Seeds: recent research advances / Nicolás, G., Bradford, K.J., Come, D., Pritchard, H.W., Wallingford : CABI Publishing - ISBN 9780851996530 - p. 337 - 344.
triticum aestivum - plantenembryo's - membranen - verdroging - tolerantie - plant embryos - membranes - desiccation - tolerance
Ovules, megagametophytes and embryos. Ultrastructural studies after cryofixation
Thijssen, M.H. - \ 2003
Wageningen University. Promotor(en): J.L. van Went, co-promotor(en): Anne Mie Emons. - [S.l.] : S.n. - ISBN 9058088820
planten - bedektzadigen - brassica - petunia - onbevruchte eitjes - cryopreservering - plantenembryo's - celultrastructuur - biologische technieken - plants - angiosperms - brassica - petunia - ovules - cryopreservation - plant embryos - cell ultrastructure - biological techniques
Coffee (Coffea arabica cv. Rubi) seed germination: mechanisms and regulation
Silva, E.A.A. da - \ 2002
Wageningen University. Promotor(en): L.H.W. van der Plas; H.W.M. Hilhorst; A.A.M. van Lammeren. - S.l. : S.n. - ISBN 9789058086501 - 105
coffea arabica - koffie - zaden - zaadanatomie - plantenembryo's - endosperm - embryogenese - abscisinezuur - gibberellinezuur - plantenfysiologie - coffea arabica - coffee - seeds - seed anatomy - plant embryos - endosperm - embryogenesis - abscisic acid - gibberellic acid - plant physiology

Coffee seeds display slow and variable germination which severely hampers the production of seedlings for planting in the following growth season. Little work has been done with the aim to understand the behavior of coffee seeds during germination and there is a lack of information concerning the regulation of the germination process. This thesis addresses questions concerning the mechanism and regulation of coffee seed germination.

Initial experiments showed that radicle protrusion in the dark at 30 °C was initiated at around day 5 of imbibition. At day 10, 50% of the seed population displayed radicle protrusion and at day 15 most of the seeds had completed germination. The water uptake by the coffee seeds followed a common triphasic pattern as described for many other species (Chapter 2 and 3). During imbibition the coffee embryo grew inside the endosperm. The cotyledons increased in length by 35% and the axis by 40%, resulting in the appearance of a protuberance in the endosperm cap region. There was an increase in the embryo pressure potential up to day 5 of imbibition followed by a release of turgor thereafter, indicating relaxation of embryonic cell walls (Chapter 3). Light microscopy demonstrated that the cells of the embryonic axis displayed isodiametric growth (swelling) at the beginning of the imbibition process followed by both isodiametric and longitudinal growth later during imbibition. The isodiametric growth coincided with a random orientation of the microtubules whereas longitudinal growth was accompanied by a transversal orientation. Accumulation ofb-tubulin, an increase in the number of 4C nuclei and DNA replication were evident during imbibition. These cell cycle events coincided with the growth of the embryo and the appearance of cell division prior to radicle protrusion. However, cell division was not a pre-requisite for radicle protrusion in coffee seeds (Chapter 5).

The endosperm of the coffee seeds possesses polygonal and rectangular cell types located in different parts of the endosperm. The endosperm cap cells have smaller and thinner cell walls than the rest of the endosperm, suggesting that the region where the radicle will protrude is predestined in coffee seed. Low temperature scanning microscopy revealed that during imbibition cells in the endosperm cap became compressed which was followed by a loss of cell integrity, appearance of a protuberance and occurrence of cell wall porosity (Chapter 3). As in many other species, the hemi-cellulose fraction of endosperm cell walls of coffee seeds consists mainly of mannans and galacto-mannans. These polysaccharides are commonly deposited in the cell walls as food reserve. Upon germination, these galacto-mannans are degraded through the action of hydrolytic enzymes, including endo-b-mannanase,b-mannosidase anda-galactosidase resulting in a weakening of the cell walls. The coffee endosperm cap weakens in two steps: cellulase activity correlated with the first step and endo-b-mannanase activity with the second step. Endo-b-mannanase activity appeared first in the endosperm cap and only later in the rest of the endosperm, and coincided with a decrease in the required puncture force and appearance of cell wall porosity. Different isoforms of endo-b-mannanase were found in the endosperm cap and in the rest of the endosperm. The activity ofb-mannosidase increased predominantly in the endosperm cap. However, low levels of endo-b-mannanase andb-mannosidase activities were also observed in the rest of the endosperm and in the embryo prior to radicle protrusion (Chapter 3 and 6). Two partial length cDNA clones encoding for endo-b-mannanase andb-mannosidase, respectively, were isolated from coffee endosperm caps. The deduced amino acid sequences exhibited high homology with those of other endo-b-mannanases andb-mannosidases from plants (Chapter 6).

Abscisic acid (ABA) inhibited germination of coffee seeds but not their water uptake, isodiametric growth, increase in 4C nuclei and DNA synthesis in the embryo cells. In the endosperm cap ABA inhibited the second step of endosperm cap weakening, presumably by inhibiting the activities of at least two endo-b-mannanase isoforms. However, ABA had no effect on endo-b-mannanase activity in the rest of the endosperm or on cellulase activity. Two peaks of endogenous ABA occurred in the embryo cells during germination. The first peak was observed at day 2 of imbibition and the second (smaller) peak at day 5 of imbibition. The occurrence of these ABA peaks coincided with the increase in the embryo growth potential and the second step of endosperm cap weakening, which makes these processes possible targets of ABA action (Chapter 3).

Exogenous gibberellin (GA 4+7 ) inhibited coffee seed germination. The response to GA 4+7 showed two sensitivity thresholds: a lower one between 0 and 1mM and a higher one between 10 and 100mM. However, it was shown that radicle protrusion of coffee seeds depended on de novo synthesis of GAs. Endogenous GAs were required for embryo cell elongation and the second step of endosperm cap weakening. Incubation of seeds in exogenous GA 4+7 resulted in a loss of embryo viability and the occurrence of dead cells, as observed by low temperature scanning microscopy. We suggest that the inhibition of germination by exogenous GAs is caused by factors that are released from the endosperm cap during or after its weakening. Exogenous GAs greatly accelerated the degradation of the endosperm cap. Factors that are involved in (normal) programmed cell death of the endosperm may reach the embryo during germination, causing cell death in the embryonic axis and, hence, inhibition of radicle protrusion. The results presented in this thesis show that coffee seed germination is controlled both by embryo growth and the second step of endosperm cap weakening (Chapter 4).

Finally, the sequence of events during coffee seed germination and their interrelationships are presented and discussed (Chapter 7). The events occurring in embryo and endosperm all followed a two-phase pattern. The first phase occurred during the first 5 days of imbibition and the second phase thereafter, until radicle protrusion. The results make clear that the germination processes are temporally and spatially coordinated and that disturbance of this coordination, as in the presence of GAs, may severely affect seed behaviour.

Embryo's maken de plant
Vries, S.C. de - \ 1999
Wageningen : Landbouwuniversiteit - 29
plantkunde - plantenembryo's - embryogenese - botany - plant embryos - embryogenesis
Sneep, J. - \ 1975
Wageningen : LH, Plantenveredeling - 54
bevruchting - bestuiving - plantenembryo's - voortplanting - embryozak - bedektzadigen - fertilization - pollination - plant embryos - reproduction - embryo sac - angiosperms
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