Based on these findings, it was proposed that endosperm derived auxin could be critically important in early embryo patterning in maize. Additionally, there are other novel signaling pathways involved in embryo-endosperm communication, such as sugar, small-interfering RNA siRNA , and polypeptides. Trehalosephosphate T6P , a dominant sugar signal in plants, modulates sucrose metabolism and allocation, thus performing an active role in regulating crop growth and development Griffiths et al.
Mutation in PHS8 causes the phytoglycogen breakdown and sugar accumulation in endosperm, which is accompanied by preharvest sprouting of the matured embryo. This result suggests that sugar in endosperm not only acts as a fundamental energy source but also as a signal mediating embryo development Du et al. Nutrients unloaded from the maternal tissues are first stored in endosperm. Then, they are either utilized by endosperm to synthesize storage compounds like starch and proteins, or transferred to the developing embryo.
In this regard, endosperm dominates nutrient allocation among the compartments within a seed. The direct evidence of the impact of embryo on endosperm development may come from the scanning electron microscopy SEM photos that show the decomposition of starch granules in the endosperm cells facing the scutellum of embryo Figure 4.
In addition, these pits mainly occur at the interfaces between the two compartments, thus it is tempting to assume that the degradation of starch is associated with the urgent demanding for sugars by embryonic development.
Whether signaling of GA from embryo plays a role in decomposing endosperm starch remains unclear. Figure 4. Starch degradation in the endosperm cells facing the scutellum of the embryo. The location of A is nearer to embryo scutellum than that of B. Note that starch granules are smaller at location A than those at B.
The immature starch granules at location A might be the result of nutrient deprivation by the developing embryo. The signal released from embryo regulates endosperm development Figure 3C. Nowack et al. They found that upon exclusive fertilization of the egg cell, the unfertilized endosperm also began to develop, suggesting a positive signal from the fertilized egg cell the embryo to the central cell the endosperm at early stage.
Growing evidence in maize and Arabidopsis suggest that ESR involves in nurturing and defensing the embryo, and also mediate signaling between embryo and endosperm Widiez et al. Recently, a newly interface tissue, named endosperm adjacent to scutellum EAS , was identified by the analysis of genome-wide expression profiles of tissues at the interfaces between embryo and endosperm in maize seed. The EAS appears around 9 DAF and persists for around 11 days, with enrichment transcriptome of genes encoding transporters.
The absence of embryo in an embryo specific mutant can change the expression pattern of the marker genes, suggesting a role of embryo in controlling this specific endosperm tissue Doll et al.
The embryo also regulates nutrient allocation between itself and endosperm. Loss of VP1 function leads to preharvest sprouting in maize, showing a viviparous phenotype. VP1 starts to be expressed in embryo at 5 DAF, particularly in scutellum the nutrient transfer link between embryo and endosperm , possibly functioning as mediator for their interactions Cao et al.
Recent study suggests that VP1 senses the nutritional status of endosperm through endosperm-embryo communication, likely the ABA signaling pathway. It regulates scutellum development, enlarges embryo nutrient-storage capacity, and consequently mediates nutrient remobilization from endosperm to embryo Zheng et al.
One of the evolutive advantages of double fertilization in angiosperms is the coordinating development of endosperm and embryo that minimizes nutrient and energy wastage Ingram, Belmonte et al. They identified strong overlap in embryo and endosperm expression programs, suggesting a substantial coordination of embryo and endosperm in terms of biological processes.
Further, the results were in favor of the embryo-based evolutionary origin of the endosperm, although not excluding the possibility that homology may exist between endosperm and the female gametophyte.
It is strongly expressed in the interfacing tissues between embryo and endosperm. Heterofertilization and transgenic experiments proved that GE performs its function in both embryo and endosperm to acquire a delicate size balance between them, which is associated with the regulation of ROS homeostasis and cell death in endosperm.
Some signals responsible for the size balance may be originated from endosperm to embryo and vice versa. In addition, considering space limitation by the glumes lemma and palea , it is likely that cell death is the solution to embryo-endosperm conflict Nagasawa et al.
A hydrophobic cuticle around the embryo prevents it from catastrophic dehydration at early germinating stage. Doll et al. The TWS1 precursor is produced in embryo and then translocated to endosperm, where it is transformed into an active form.
The active peptide shuttles back into the embryo to act with the receptors of GSO1 and GSO2, thus activating local gap repair. The shuttle of TWS1 continues until all gaps are bridged to form an intact cuticle. Physically and chemically, rice quality refers to the properties of starchy endosperm packed with starch granules and protein bodies.
And most of the studies on quality traits had been centered on endosperm, and concluded that C and N metabolisms and their interaction form the foundation for traits like appearance chalkiness and eating quality Xi et al. However, the role of embryo needs to be thoroughly estimated, due to its substantial impact on endosperm development and storage accumulation, as discussed above. Chalkiness is the opaque tissue feature that usually occurs on the ventral white-belly and central white-core parts of rice endosperm Figure 1.
It is a highly undesirable trait that negatively affects not only appearance quality but also milling, eating, and cooking quality. High occurrence of chalky grains has been a major obstacle for rice producers, especially under the scenario of global warming Jagadish et al. The physiological and molecular mechanisms underlying chalkiness formation remain largely elusive, because of the complex interactions between the regulating genes and the environmental factors. Lin et al.
Using this mutant, they developed a novel comparison system that can clarify the mechanisms underlying grain chalkiness. Notably, the comparison is conducted within the same grain, thus forming a nearly identical genetic background to minimize the compound effects of genetic background and growing environment.
Employing this comparison system, Lin et al. Some novel key pathways were highlighted as being involved in chalky tissue formation, especially the interaction between C and N metabolisms, the downregulation of ribosomal proteins, and the decreased accumulation of 13 kDa prolamin subunit.
More importantly, substantial influence of the embryo on endosperm composition was revealed, with the embryo negatively affecting the storage of total protein, amino acids, and minerals in the chalky endosperm Lin et al.
Further, this was associated with the upregulation of genes responsible for the transporters for metabolites and the signal messengers of hormones in the chalky endosperm, and therefore, embryo may be involved in regulating the nutrient distribution within the seed Lin et al.
Results of Hakata et al. However, it is still unclear whether there exists a similar pathway in developing seed of cereals. In Arabidopsis , endosperm undergoes programmed cell death PCD and is decomposed after completing its nourishment function. In developing rice grain, especially under heat stress, part of the endosperm starch granule decomposes.
However, the signaling pathway responsible for it is largely unknown. Intriguingly, the involvement of GA in regulating starch hydrolysis was excluded. Similarly, Hakata et al. Overall, these results imply divergent hormonal signals modulating starch degradation between developing and germinating stages for cereal grains. Recent advances in Arabidopsis and maize have conformed substantial bidirectional interactions between embryo and endosperm during seed development, indicating that the interplay of the two compartments should be common among plant species.
As a monocotyledon plant, rice seed is structurally different with that of the dicotyledon Arabidopsis. The direct relevance of data from Arabidopsis and maize for rice therefore remains unclear. Several key questions need to be answered. Signaling controlling the developmental transition of the endosperm. The developmental transitions in endosperm like cellularization of the syncytium are dramatic and abrupt, meaning that gene expression patterns are globally and rapidly reprogrammed Sabelli and Larkins, Mechanisms underlying the duration of syncytial phase of endosperm have captured attention of crop scientists, for there exists a positive relation between duration of this phase and grain size and yield Ishimaru et al.
What signals trigger the major endosperm developmental transitions remains unknown. Does this signaling pathway originate from the embryo that undergoes morphogenesis? Hormonal regulation of starch degradation. Much knowledge about starch degradation has been derived from biochemical analyses on germinating cereal grain, especially barley and wheat Triticum aestivum. During germination, GA signaling from embryo triggers the secretion of starch-degrading enzymes from the living aleurone layer and scutellum Zeeman, It is still uncertain whether the hydrolyzation of endosperm starch during grain filling is analogous to that of the germination.
Do these two processes have a mirror-image relationship? What is the role of GA in regulating starch degradation in developing endosperm? What is the relevance of this signaling to chalky tissue formation? And what is the function of aleurone layer in embryo-endosperm interaction? Cellular events at late stage. Accumulating literature indicates that the duration of embryo morphogenesis and endosperm filling would be conserved, with the former ending at 10 DAF while the latter at 30 DAF Itoh et al.
After that, the seed enters the stage of desiccation and maturation, lasting for 20—40 days with no obvious increase in grain weight. There is scarcer information concerning the cellular events at the late stage. If that developmental pattern is common among rice cultivars, is there an embryo-endosperm interaction at the late stage of grain filling?
And what does this mean to preharvest sprouting? All the above questions ultimately relate to the physiological and molecular controls of the intercompartmental coordination between embryo and endosperm, which is largely elusive and should be an important future focus. Currently, there exists a knowledge gap between the fundamental plant sciences and the applied technology of crop breeding and management, as partially reflected by the limited progress in high-yielding and quality breeding in sharp contrast to the quantum leap in rice functional genomics.
This review calls for cooperative endeavors between crop geneticists, breeders, physiologists, and agronomists to address the crucial events implied in the embryo-endosperm interaction, especially revisiting the role of embryo development in grain filling and rethinking the strategies involved in the high yielding and high quality rice crops.
In angiosperms, a double fertilization event initiates the development of two distinct structures, the embryo and endosperm. The endosperm plays an important role in supporting embryonic growth by supplying nutrients, protecting the embryo and controlling embryo growth by acting as a mechanical barrier during seed development and germination.
Its structure and function in the mature dry seed is divergent and specialized among different plant species. Such endospermic proteins have been used to acquire stress tolerance when expressed in a heterologous organism Amara et al.
In cereals, the role of the endosperm in seed germination has been well documented. The scutellum of the embryo synthesizes and secretes gibberellin to the aleurone layer of the endosperm. The embryo utilizes sugars released by starch degradation for its growth. The embryo-less half-seed the dissected aleurone layer and starchy endosperm from the embryo has traditionally been used for examining the function of the endosperm in cereal physiology and biochemistry.
More recently, dissection of the endosperm is now being utilized for the study of the endosperm in other species Muller et al. A major focus in seed biology at the moment is the elucidation of the function of individual cell types or tissues, and the mechanism by which these interact to coordinate a systemic response.
In this regard, identifying the sites i. Current advances in crop functional genomics have produced novel tools, concepts and methodologies, and allowed for the comparison of conserved and divergent functions of each organ. This has promoted the accelerated translation of seed biology knowledge into agricultural and biotechnological uses Martinez-Andujar et al. This review article summarizes the current progress in our understanding of the endosperm, and its function during seed germination.
Cells of the endosperm are triploid 3 n and arise from the fusion of the polar nuclei 2 n with the sperm nucleus n through a double fertilization event. The development of the endosperm is divergent among plant species. Nonetheless, the comparison of endosperm development between cereals and Arabidopsis Arabidopsis thaliana displays some similar features Olsen The development of the endosperm in these plants can be divided into several phases, and includes the formation of the nuclear endosperm or coenocyte-type endosperm , cellularization, differentiation, maturation and cell death.
The development of the nuclear endosperm involves repetitive nuclear divisions without separation of nuclei by the cell wall. This is followed by cellularization which separates sister nuclei by the formation of a periclinal cell wall. There are four main cell types in the cereal endosperm: the starchy endosperm, the aleurone layer, transfer cells and the region surrounding the embryo.
The starchy endosperm is the major tissue for seed reserve accumulation in cereal grains, which serves as a nutrient source for seed germination and seedling establishment. In contrast to cereals, in dicot seeds the endosperm is cellularized and consumed for use as an energy source for embryo growth during seed development Lopes and Larkins The endosperm adjacent to the radicle, the part that protrudes during seed germination, is referred to as the micropylar endosperm ME.
The ME expresses a set of endosperm-specific genes, including those related to cell wall loosening Dekkers et al. ME-specific gene expression has been visualized by several techniques such as tissue print Nonogaki et al.
The structure of the endosperm in the mature seed varies considerably between different species. The tomato Solanum lycopersicum contains a hard and thick endosperm cell layer in the mature seed, which undergoes extensive weakening during germination Fig. In contrast, exalbuminous seeds such as soybean Glycine max and pea Pisum sativum contain very little or no endosperm in the mature seed, as it is fully consumed during seed development Fig.
In Arabidopsis, the endosperm is confined to a peripheral aleurone-like cell layer in the mature seed Fig. Lee et al. It acts as a mechanical barrier to inhibit embryonic growth, and as a nutrient reserve for seed germination and early seedling establishment.
The seed coat undergoes programmed cell death PCD during seed development, and as a consequence is no longer alive in the mature seed. In contrast, cereal seeds have more complex structures with a large starchy endosperm and living aleurone layers. In most cereal grains the aleurone is a single cell layer Fig.
The exception is the barley Hordeum vulgare grain, which contains three cell layers. Structures of the embryo and endosperm. The endospermic and embryonic tissues are labeled with red and blue, respectively.
The region of ME is colored with red A and C. In cereals, starch and proteins are catabolized upon the initiation of germination by hydrolytic enzymes secreted from the aleurone layer. The hydrolyzed starch and proteins act as an energy source, providing carbon and nitrogen for seed germination, and subsequent seedling establishment.
The one cell layer endosperm in Arabidopsis accumulates lipids in the form of triacylglycerols TAGs. TAGs are catabolized into sucrose through gluconeogenesis during and after germination Penfield et al.
Strikingly, lipids found within the Arabidopsis endosperm differ from those found within the embryo not only in composition, but also in how their catabolism is regulated.
Tissue-specific proteomes have been reported for the ME of germinating cress seeds Muller et al. Germinating cress endosperm accumulates proteins involved in energy production, protein folding, protein stability and defense.
Their abundance is associated temporally, hormonally and spatially with ME weakening and rupture. This work supports the view that the ME of cress has a regulatory function for seed germination through the modification of cell walls, and does not act exclusively as a source of nutrition Muller et al.
Modification of the cell wall at the ME is a common strategy to regulate seed germination in dicot seeds that contain living endosperm cells in the mature seeds.
The cell wall forms a complex three-dimensional network composed of cellulose, hemicellulose and pectin. Hemicellulose cross-links cellulose microfibrils, and pectin is embedded in the cell wall matrix.
The endosperm cell wall often contains mannan-rich hemicellulose as a major component in some species such as tomato and tobacco Nicotiana tabacum Rodriguez-Gacio et al. Cell wall remodeling enzymes CWREs are important for synthesizing, loosening and reinforcing the cell walls.
The endosperm cell wall is dynamic, as its structure changes in response to environmental, hormonal and developmental signals, all of which can affect the outcome of germination Leubner-Metzger , Rodriguez-Gacio et al. Both the composition and abundance of CWREs alter the tensile properties of the endosperm to influence the rate of seed germination. The endosperm cell walls have diverse structure and compositions of hemicellulose and pectin monomers.
The architecture of the cell wall for the tobacco endosperm is asymmetrical K. In contrast to tobacco, Arabidopsis and cress display a largely uniform architectural arrangement of the endosperm K. The endosperm of Arabidopsis and cress, while composed of cellulose and xyloglucan like tobacco, additionally contains evenly distributed unesterified galacturonan and arabinan.
Upon imbibition after testa rupture in tobacco, mannans are degraded in the ME to promote endosperm weakening Leubner-Metzger Both CWREs were thus predicted to play a role in endosperm weakening.
MANs contribute to the regulation of seed germination in Arabidopsis. XYL3 is expressed in the endosperm during the early stage in seed development, but is not expressed during the late stage in seed development. It is currently unknown whether delayed germination is due to the defect in endosperm development or to reduced embryonic growth potential. Galacturonans are demethylesterified by PMEs, which are highly expressed in the Arabidopsis endosperm during germination Muller et al.
When PME expression is inhibited, galacturonans remain highly methylesterified in the endosperm cell wall and, as a result, seeds are much larger and germination speed is enhanced. The overall breakdown of the endosperm in seed germination is a complex process that strikes a balance between cell wall strengthening and weakening.
PCD plays an important role in the developmental program of the plant van Doorn et al. It is well documented that PCD occurs during seed germination in cereal aleurone cells in order to promote the mobilization of stored nutrients required to support germination and early seedling growth Young and Gallie The starchy endosperm of cereals is subjected to PCD during seed development, while the outer aleurone layer remains viable in the mature seed Young and Gallie In addition to hormones, this response is mediated by environmental stimuli, such as hypoxia Kuo et al.
By analyzing the effect of okadaic acid OA , Kuo et al. OA is a protein phosphatase inhibitor that impedes gibberellin-induced PCD, but has no effect on the response to hypoxia.
This suggests a possible role for protein phosphatases in gibberellin-induced PCD. PCD also occurs in the aleurone layers of other plant species such as Arabidopsis Bethke et al. PCD occurs via vacuolation, a conserved process by which multiple vacuoles fuse to form a single large lytic vacuole Bethke et al.
This compromises the integrity of the plasma membrane, causing the collapse and subsequent death of the cell Bethke et al. The degradation of DNA begins during this highly vacuolated state Bethke et al. This suggests that vacuolation does not trigger, but rather is a consequence of, germination. Gene expression in the endosperm has been extensively examined in Arabidopsis.
Penfield et al. Though a number of embryo- and endosperm-specific genes were found, it was largely determined that the transcriptomes of the embryo and endosperm were quite similar. Thus, the two tissues express similar genetic programs that are intrinsic to the seed. Despite the distinct causes of endosperm cellularization failure in each mutant, the effect on embryo development is similar, strengthening the idea that endosperm cellularization is essential for embryo development.
Endosperm cellularization causes the central vacuole to decrease in size. As a corollary, incoming sucrose will no longer be predominantly channeled to the central vacuole and can instead be partitioned to the embryo, which will form the major sink in the developing seed Morley-Smith et al.
Failure of endosperm cellularization will cause the central vacuole to remain the major sink in the seed, consistent with high hexose-to-sucrose ratios in fis2 and ede1 mutant seeds. As a consequence, it is possible that sucrose is not sufficiently channeled to the embryo, but remains to be transported to the vacuole and is cleaved into hexoses.
In agreement with this view, delayed endosperm cellularization in the apetala 2 mutant is similarly connected with increased hexose-to-sucrose ratios and to a delay in embryo development Ohto et al. The tissue-specific localization of carbohydrates using the APL3 promoter supports the idea that, as a consequence of endosperm cellularization, sucrose is channeled to the embryo through the surrounding endosperm in wild-type seeds, in agreement with sucrose tracer experiments in oilseed rape Morley-Smith et al.
Consistently, APL3 expression could not be detected in the region surrounding the fis2 embryo, suggesting that owing to the lack of endosperm cellularization in fis2 the incoming sucrose remains to be channeled to the central vacuole and does not reach the embryo.
Alternatively, it is possible that the embryo-surrounding endosperm in fis2 and ede1 mutants fails to appropriately differentiate to deliver incoming sucrose to the embryo.
Together, we hypothesize that reduced provision of the embryo with sucrose is the likely cause for embryo arrest in mutants that fail to undergo endosperm cellularization. In line with this view is the fact that the patterning of heart stage embryos lacking FIS activity is undistinguishable from that of wild-type embryos Leroy et al.
AGL62 is a negative regulator of endosperm cellularization Kang et al. The fis2 phenotype could partially be reversed by maternal loss of AGL62 function. As AGL62 is exclusively expressed in the endosperm Kang et al.
Similarly, triploid seed failure could be suppressed by maternal loss of AGL62 function, in agreement with the view that endosperm cellularization failure is largely responsible for triploid seed failure Scott et al.
Loss of maternal AGL62 function has previously been shown to cause partial rescue of hybrid seeds derived from crosses of Arabidopsis thaliana and Arabidopsis arenosa Walia et al. We thank Sabrina Huber for excellent technical support; Wilhelm Gruissem for sharing laboratory facilities; Samuel Zeeman and Sebastian Streb for sharing materials and intellectual support; Abed Chaudhury and Max Bush for providing fis and ede seeds, respectively; and Lars Hennig and members of the C.
Endosperm cellularization in wild type and fis2 at 7 DAP. Schiff-stained Technovit sections of wild-type left and fis right seeds at 7 DAP. Read more about our commitment to Open Access. Our latest special issue focussing on the role of the immune system in development and regeneration is open. The first articles are online now and we will be adding new articles over the coming months. Development Editor James Wells has invited three speakers to share their research on stem cells and disease models.
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Find out more about the Node Network. Sign In or Create an Account. Advanced Search. User Tools. Sign in. Skip Nav Destination Article Navigation. Close mobile search navigation Article navigation. Volume , Issue Previous Article Next Article. Article contents. Article Navigation. Endosperm cellularization defines an important developmental transition for embryo development Elisabeth Hehenberger , Elisabeth Hehenberger.
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David Kradolfer. Competing interests statement The authors declare no competing financial interests. Accepted: 21 Mar Online Issn: Development 11 : — Article history Accepted:.
Cite Icon Cite. View large Download slide. An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Search ADS. The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. Dynamic analyses of the expression of the histone::YFP fusion protein in Arabidopsis show that syncytial endosperm is divided in mitotic domains. Events during the first four rounds of mitosis establish three developmental domains in the syncytial endosperm of Arabidopsis thaliana.
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