Storage Cotyledons Research Articles

Seed functional traits as predictors of seedling establishment success in Brazilian tropical forest restoration

AbstractSeveral ecological filters in deforested and degraded areas reduce seedling emergence and establishment and hinder ecological restoration by direct seeding. Understanding whether functional traits are related to a species' capacity to overcome these filters and predict their field performance might improve the success of direct seeding techniques for ecological restoration. We assessed eight seed functional traits of tropical tree species, seeking those that best explained their establishment success in direct seeding restoration projects. We analyzed a dataset from 52 studies that tested direct seeding techniques with tree species in Brazil. From each study, we collected the mean establishment percentage for all tree species. Seed mass, cotyledon function, and germination speed were the only functional traits that significantly affected the species establishment percentage in direct seeding restoration projects. Species with larger seeds, storage cotyledons, and faster germination had higher establishment percentages. Choosing species with these functional traits for seed mixes will provide higher establishment percentages and, consequently, improve restoration success by direct seeding techniques.

Functional traits of young seedlings predict trade‐offs in seedling performance in three neotropical forests

Abstract Understanding the mechanisms that promote the coexistence of hundreds of species over small areas in tropical forest remains a challenge. Many tropical tree species are presumed to be functionally equivalent shade tolerant species but exist on a continuum of performance trade‐offs between survival in shade and the ability to quickly grow in sunlight. These trade‐offs can promote coexistence by reducing fitness differences. Variation in plant functional traits related to resource acquisition is thought to predict variation in performance among species, perhaps explaining community assembly across habitats with gradients in resource availability. Many studies have found low predictive power, however, when linking trait measurements to species demographic rates. Seedlings face different challenges recruiting on the forest floor and may exhibit different traits and/or performance trade‐offs than older individuals face in the eventual adult niche. Seed mass is the typical proxy for seedling success, but species also differ in cotyledon strategy (reserve vs. photosynthetic) or other leaf, stem and root traits. These can cause species with the same average seed mass to have divergent performance in the same habitat. We combined long‐term studies of seedling dynamics with functional trait data collected at a standard life‐history stage in three diverse neotropical forests to ask whether variation in coordinated suites of traits predicts variation among species in demographic performance. Across hundreds of species in Ecuador, Panama and Puerto Rico, we found seedlings displayed correlated suites of leaf, stem, and root traits, which strongly correlated with seed mass and cotyledon strategy. Variation among species in seedling functional traits, seed mass, and cotyledon strategy were strong predictors of trade‐offs in seedling growth and survival. These results underscore the importance of matching the ontogenetic stage of the trait measurement to the stage of demographic dynamics. Our findings highlight the importance of cotyledon strategy in addition to seed mass as a key component of seed and seedling biology in tropical forests because of the contribution of carbon reserves in storage cotyledons to reducing mortality rates and explaining the growth‐survival trade‐off among species. Synthesis: With strikingly consistent patterns across three tropical forests, we find strong evidence for the promise of functional traits to provide mechanistic links between seedling form and demographic performance.

Germinative behaviour of ten tree species in white-water floodplain forests in central Amazonia

Amazonian floodplain forests (known as varzea) are classified into high or low varzea depending on the spatial position on the plains. This topographic feature exposes the terrain over different time periods of inundation, causing a major limiting factor for tree seedling establishment. We hypothesize that, strategically, most of the seeds produced by trees in low varzea forests germinate faster and in synchrony (temporally concentrated germination), and that their seedlings tend to have cotyledons without reserve or foliaceous cotyledons (PEF). By contrast, seeds produced by high-varzea specialist trees exhibit slower and temporally scattered germination, and their seedlings tend to have reserve storage cotyledons (CHR). Generalist species may show no clear pattern or may be related to high-varzea species. To test this hypothesis, diaspores of 10 tree species were collected: five of low-varzea specialist trees, three of high-varzea specialist trees and two of generalist species. Seedling emergence and morphology were monitored daily in a nursery for a period of 150 days of being subjected to non-flooded (sown directly in varzea soil) and flooded conditions (15 days in water before sowing in the same soil). The seedling emergence of low-varzea species showed an increase of 37% in germinability whereas high-varzea and generalist species exhibited a decrease of 38% and 35% of germinability, respectively. Foliaceous cotyledons were preferentially found in seedlings of low-varzea species, and storage cotyledons were more common in those of high-varzea species, indicating how cotyledon morphology may determine the amount and use of resources available to a seedling during the first stages of establishment and growth. Conservation plans aiming for the maintenance of ecosystem services must consider these strategies.

Ecologia morfofuncional de plântulas de 15 espécies da Floresta Atlântica Sergipana

Em Sergipe a Floresta Atlântica encontra-se hoje fragmentada e reduzida a apenas 9% da sua cobertura original. O estudo da ecologia morfofuncional de plântulas nesse ecossistema é importante para a taxonomia, silvicultura e ecologia, possibilitando a identificação das plântulas no campo, requisito necessário para o entendimento da regeneração e sucessão vegetal. Neste estudo, foram descritas a germinação e a morfologia de plântulas de 15 espécies de um remanescente florestal sergipano, sendo também analisadas as relações entre biometria das sementes, morfologia das plântulas e outros atributos ecológicos. Do total de espécies analisadas 40% foram classificadas como fanero-epígeo-foliáceas, 26,7%, como cripto-hipógeo-armazenadoras, 26,7% como fanero-epígeo-armazenadoras e 6,6% como fanero-hipógeo-armazenadoras. A existência de relações entre a biometria da semente, o tipo morfofuncional de plântula e os atributos ecológicos das espécies analisadas corroborou os resultados obtidos em outras florestas tropicais, indicando que a morfologia da plântula é fortemente direcionada pelas características do nicho de regeneração.

Morfologia de plântulas de Martiodendron excelsum e sua relevância sistemática em Dialiinae (Leguminosae, "Caesalpinioideae”)

Martiodendron Gleason é um gênero sul-americano com cinco espécies arbóreas, subordinado à Dialiinae (tribo Cassieae). Dialiinae apresenta 17 gêneros, que formam um clado cujas relações genéricas permanecem em grande parte não definidas. Este trabalho descreve e ilustra o desenvolvimento e a morfologia de plântulas de Martiodendron excelsum e avalia, por meio de uma revisão, a relevância sistemática dos atributos de plântulas em nível de gênero em Dialiinae. Sementes de M. excelsum foram coletadas de populações em áreas de mata ciliar no Estado de Roraima, Brasil. Martiodendron excelsum tem plântulas fanero-epígeo-armazenadoras, eofilos estipulados e 1-foliolados nos três primeiros nós. Os dados sobre morfologia de plântulas são potencialmente úteis para diagnosticar gêneros em Dialiinae, visto que Martiodendron e todos os demais gêneros podem ser distintos entre si pela a variação no grupo morfológico de plântulas, na filotaxia e número de folíolos no primeiro e segundo eofilos, nas relações entre o comprimento e largura dos cotilédones e entre o comprimento do hipocótilo e epicótilo e no alongamento do primeiro entrenó eofilar. Por fim, em Leguminosae, a predominância de eofilos 1-foliolados na maior parte dos gêneros de Dialiinae é somente comparável à encontrada entre as plântulas de táxons de Papilionoideae.

Genome-wide analysis reveals divergent patterns of gene expression during zygotic and somatic embryo maturation of Theobroma cacao L., the chocolate tree.

BackgroundTheobroma cacao L. is a tropical fruit tree, the seeds of which are used to create chocolate. In vitro somatic embryogenesis (SE) of cacao is a propagation system useful for rapid mass-multiplication to accelerate breeding programs and to provide plants directly to farmers. Two major limitations of cacao SE remain: the efficiency of embryo production is highly genotype dependent and the lack of full cotyledon development results in low embryo to plant conversion rates. With the goal to better understand SE development and to improve the efficiency of SE conversion we examined gene expression differences between zygotic and somatic embryos using a whole genome microarray.ResultsThe expression of 28,752 genes was determined at 4 developmental time points during zygotic embryogenesis (ZE) and 2 time points during cacao somatic embryogenesis (SE). Within the ZE time course, 10,288 differentially expressed genes were enriched for functions related to responses to abiotic and biotic stimulus, metabolic and cellular processes. A comparison ZE and SE expression profiles identified 10,175 differentially expressed genes. Many TF genes, putatively involved in ethylene metabolism and response, were more strongly expressed in SEs as compared to ZEs. Expression levels of genes involved in fatty acid metabolism, flavonoid biosynthesis and seed storage protein genes were also differentially expressed in the two types of embryos.ConclusionsLarge numbers of genes were differentially regulated during various stages of both ZE and SE development in cacao. The relatively higher expression of ethylene and flavonoid related genes during SE suggests that the developing tissues may be experiencing high levels of stress during SE maturation caused by the in vitro environment. The expression of genes involved in the synthesis of auxin, polyunsaturated fatty acids and secondary metabolites was higher in SEs relative to ZEs despite lack of lipid and metabolite accumulation. These differences in gene transcript levels associated with critical processes during seed development are consistent with the fact that somatic embryos do not fully develop the large storage cotyledons found in zygotic embryos. These results provide insight towards design of improved protocols for cacao somatic embryogenesis.

Size, structure and nitrogen content of seeds of Fabaceae in relation to nodulation

Seed weight in Fabaceae ranges over seven orders of magnitude from 0.1 mg to 334 g. The frequency distribution is strongly right skewed with a single modal peak at 18 mg. The two sets of morphological characters, the presence or absence of endosperm and the anatomical form of the cotyledons, interact to define eight structurally and functionally distinct seed types. The predominant seed type is endospermic with foliar cotyledons. The other seed types have evidently arisen from it by transfer of storage function from endosperm to cotyledons, culminating in exendospermic seeds with storage cotyledons. This has probably happened repeatedly in disparate tribes and genera throughout the family. There is a highly significant allometric relationship between the logarithms of the weight of nitrogen in the seed and the total seed weight, with the datasets for nodulating and non-nodulating species yielding significantly different regression equations. The rate of increase in weight of nitrogen is lower than the rate of increase in total seed weight, and this discrepancy is greater in non-nodulating than in nodulating species. A consequence of the discrepancy is an overall inverse relationship between seed weight and nitrogen concentration. Seeds of the same type are significantly larger and have a higher absolute nitrogen content, but a lower nitrogen concentration in non-nodulating than in nodulating species.

Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest

SummaryTo survive in forest understoreys, seedlings must depend on carbohydrate reserves when they experience negative carbon balance imposed by occasional light reduction and tissue loss to herbivores and diseases. We present the first experimental evidence in support of this hypothesis, using seven woody neotropical species.We transplanted seedlings that had recently expanded their first photosynthetic cotyledon or leaf to the forest understorey (1% of full sun) and quantified initial biomass and total non‐structural carbohydrate (TNC) in stems, roots and storage cotyledons. We then randomly assigned seedlings to control and two stress treatments: light reduction (0.08% of full sun for 8 weeks) and complete defoliation.First‐year survival of control seedlings, a comparative measure of shade tolerance, differed widely among species. The two stress treatments reduced survival and relative growth rates (RGR) of all species. Shade‐tolerant species were little impacted by the stress treatments, whereas the two least shade‐tolerant species experienced 100% mortality.In all treatments, 8‐week and first‐year survival was positively correlated with initial TNC pool size in stems and roots. By contrast, survival was generally not correlated with initial TNC concentration in any organ, TNC pools in cotyledons, seed mass or seedling biomass.TNC in stems and roots, but not in cotyledons, decreased in response to light reduction and defoliation over 8 weeks. Leaf area recovery of defoliated seedlings was positively correlated with initial TNC pools in stems and roots.First‐year survival in each treatment was negatively correlated with 0–8 week RGR of control seedlings, suggesting higher stress tolerance of species with inherently slow growth rates in shade. RGR of control seedlings from 0 to 8 weeks was negatively correlated with initial TNC pools, but not concentrations, in stems and roots. After 8 weeks, RGR was positive for all species, without clear relationships with survival or TNC.We conclude that carbohydrate storage in stems and roots enhances long‐term survival in shade by enabling seedlings to cope with periods of biotic and abiotic stress. Carbohydrate storage is a key functional trait that can explain species differences in growth and survival that lead to species coexistence through niche assembly processes and life‐history trade‐offs.

The potential for predation induced somatic embryogenesis in storage cotyledons

Using seven tropical rainforest species of north Queensland, Australia, we simulated partial predation and compared the development of intact embryos and embryos from which various proportions had been removed, including in some cases the original root–shoot axis. Embryos of all species contained storage reserve cotyledons and germinate in a hypogeal manner. Species mean embryo masses ranged from 0.4–48.1 g. Partial embryo predation treatments were: ½ embryo treatment; embryos separated into component cotyledons, and ¼ embryo treatment; cotyledons separated as above and subsequently cut in half. Germination was scored as production of roots and shoots, or roots or shoots only. Embryos from all species produced seedlings in all treatments, even after the removal of up to 75 percent of the cotyledonary reserve. Moreover, the proportion germinating were not different between intact embryos and i) separated cotyledons, ii) cotyledon halves that maintained or were adjacent to the embryonic axis (except for the largest seeded species), and iii) cotyledon halves that did not include the root–shoot axis (four species). Thus, production of roots and shoots, or roots or shoots only was largely independent of the presence of the embryonic root–shoot axis – implying that somatic cells in storage cotyledons are capable of differentiating into the full range of cell types typical of shoots and roots in the absence of the root–shoot axis. The generality of this response across all seven species suggests somatic embryogenesis in storage cotyledons may be a more widespread phenomenon in tropical floras than currently considered.

Evolutionary and ecological correlates of early seedling morphology in East African trees and shrubs

Seed size and cotyledon morphology are two key juvenile traits that have evolved in response to changes in plant species life-history strategies and habitat associations. Correlations of these traits with each other and with other juvenile traits were examined for 70 species of trees and shrubs in Kibale National Park, Uganda. Although species with photosynthetic cotyledons were more abundant than in other tropical floras, both univariate and multivariate analyses supported trait associations expected from the literature. Trait values varied continuously across species, yet mean trait values differed significantly among habitat association types. Species with large seeds, large seedlings, thick storage cotyledons, slow germination, large-stature adults, and dispersal by large animals were common in forest and gap habitats. An opposite suite of traits was common in open habitats (grassland and edge). Analyses incorporating phylogeny (independent contrasts and omnibus tests) confirmed that these suites of traits showed correlated evolution. Cotyledon functional morphology yielded a strong phylogenetic signal, while seed mass was labile. Nevertheless, contingent change tests found that evolutionary change from photosynthetic to reserve cotyledons was more likely when disperser and perhaps seed size of ancestral species were already large, suggesting a strong interdependency among these traits.

The Role of the Storage Carbon of Cotyledons in the Establishment of Seedlings of Hymenaea courbaril Under Different Light Conditions

Hymenaea courbaril (Leguminosae-Caesalpinioideae) is a tree species with wide distribution through all of the Neotropics. It has large seeds (approx. 5 g) with non-photosynthetic storage cotyledons rich (40 %) in a cell wall polysaccharide (xyloglucan) as a carbon reserve. Because it is found in the understorey of tropical forests, it has been considered as a shade-tolerant, late-secondary species. However, the physiological mechanisms involved in seedling establishment, especially regarding the interplay between storage and light intensity, are not understood. In this work, the ecophysiological role of this carbon cotyledon reserve (xyloglucan) is characterized, emphasizing its effects on seedling growth and development during the transition from heterotrophy to autotrophy under different light conditions. Seedlings of H. courbaril were grown in environments with different light intensities, and with or without cotyledons detached before xyloglucan mobilization. Development, growth, photosynthesis and carbon partitioning (dry mass and [14C]sucrose) were analysed in each treatment. The detachment of cotyledons was not important for seedling survival, but resulted in a strong restriction (50 % less) of shoot growth, which was the main sink for the cotyledon carbon reserves. Carbon restriction promoted an early maturation of the photosynthetic apparatus without changes in the net CO2 fixation per unit area. The reduced surface area of the first leaves in seedlings without cotyledons was evidence of limited growth and development of seedlings in low light conditions (22 micromol m(-2) s(-1) photon flux). There is an increase in the importance of storage xyloglucan in cotyledons for H. courbaril seedling development as light intensity decreases, confirming that this polymer plays a key role in the adaptation of this species to establish successfully in the shadowed understorey of the forest.

Seed mass, seedling herbivory and the reserve effect in tropical rainforest seedlings

Summary The seedlings of larger‐seeded species typically perform better than those of smaller‐seeded species in the face of a variety of hazards. One mechanism that might explain this general pattern is the reserve effect, where larger‐seeded species commit a smaller proportion of their initial seed reserves to seedling construction, keeping a greater proportion in reserve to sustain seedlings during times of resource deficit or imposed hazards. This study tested two hypotheses: (1) that seedlings of larger‐seeded rainforest species can resprout more often, following simulated herbivory, than those of smaller‐seeded species; and (2) that any such correlation is consistent with the reserve effect. To test these hypotheses we grew the seedlings of 15 rainforest species with hypogeal storage cotyledons in a shade house, excised the initial shoot, and sequentially clipped each resprout. Previous work had demonstrated a reserve effect among these species. The first hypothesis was proved true: seedlings of larger‐seeded species resprouted significantly more often than those of smaller‐seeded species. The second hypothesis was proved false: although large‐seeded species resprouted more often, the total mass invested in resprouts scaled isometrically with seed mass across species. The reserve effect predicted that total resprout mass should have scaled more than proportionately with seed mass. This study adds to a growing body of work demonstrating that the seedlings of larger‐seeded species often perform better than those of their smaller‐seeded counterparts. However, the results presented here are at odds with the view that the reserve effect might be a common mechanism explaining this pattern.

Seed–seedling allometry in tropical rain forest trees: seed mass‐related patterns of resource allocation and the ‘reserve effect’

Summary The seedlings of larger seeded species generally perform better than those of smaller seeded species under a variety of hazards. The reserve effect proposes that larger seeded species retain a greater proportion of their initial seed resources and their seedlings are therefore better provisioned to cope with post‐deployment resource deficits. This hypothesis was tested with a suite of 32 Australian rain forest species with storage cotyledons, and seed reserve mass ranging from 36 mg to 25 g. Seedlings germinated in dim light were harvested as their first set of leaves became fully expanded, dissected into shoot, root and left‐over cotyledons, dried and weighed. In cross‐species, allometric analyses, the mean mass of the shoot‐plus‐root scaled less than proportionately (slope c. 0.8), and mean cotyledon mass more than proportionately (slope c. 1.1) with either initial seed mass or seedling mass. These slopes were significantly different from each other. Both conditions for a reserve effect were therefore fulfilled. Cotyledons ranged from 45% of total seedling mass in the smallest species, to 92% in the largest. Solid evidence for a reserve effect was detected within two of four families tested (Lauraceae and Myrtaceae), but only in 7 of the 22 species for which there were sufficient data. Even if the reserve effect has present day utility for enhanced seedling performance in larger seeded species, it may have evolved in response to selection for a greater relative retention of initial seed mass during seedling deployment in larger seeded species, combined with selection for greater deployment of seed reserves to the initial shoot and root of smaller seeded species.

Do shade‐tolerant tropical tree seedlings depend longer on seed reserves? Functional growth analysis of three Bignoniaceae species

Summary 1. A functional growth analysis was used to determine the duration of strict dependency on seed reserves for energy and nitrogen in three woody Bignoniaceae species (Tabebuia rosea DC., Challichlamys latifolia K. Schum. and Pithecoctenium crucigerum A. Gentry) which differed in cotyledon function (photosynthetic, semi‐photosynthetic and storage) and shade tolerance (probability of seedling establishment and survival in the understorey). 2. Seedlings were raised from seeds in sand culture under combinations of three nitrogen levels (daily supply of nutrient solution containing 100, 10 and 0% of 2·6 mm N) and two irradiances (27 and 1% full sun). Time course of biomass, non‐cotyledonous biomass and leaf area for 40 days post‐germination were compared to identify when the external availability of nitrogen or light began to affect seedling growth. 3. Seedlings of all species became dependent on external energy supply earlier than they did on nitrogen supply. In all species seed nitrogen was sufficient to support positive seedling growth for 40 days in shade, but not in sun. 4. Tabebuia rosea with photosynthetic cotyledons responded to light availability earlier than more shade‐tolerant species with storage cotyledons. Challichlamys latifolia, the most shade‐tolerant species, had the highest nitrogen concentration in seeds and was the last to respond to external nitrogen availability. Thus seedlings of the most shade‐tolerant species depended on seed reserves for the longest period for both energy and nitrogen. 5. Relative growth rate after seedlings initiated autotrophic growth was in a trade‐off relationship with seedling survivorship in the understorey across the three species. Tabebuia rosea, the least shade‐tolerant species, had the highest positive net carbon balance in sun and shade. 6. Functional morphology of cotyledons and concentration of seed nitrogen deserve as much attention as seed size as correlates of contrasting seedling regeneration strategies.

Seedling morphology in identification of some Indian species of Bauhinia L. (Caesalpiniaceae)

AbstractSeedling morphology was studied in nine Indian species of Bauhinia L. Four seedling types were recognized on the basis of germination pattern: (a) crypto‐hypogeal; (b) semicrypto‐geal; (c) phanero‐epigeal and (d) phanero‐geal. The seedling types, foliar and storage cotyledons, forms and length of hypocotyl, presence or absence of cataphylls, phyllotaxy and depth of lobing of first two leaves provide essential characters for the identification of the investigated taxa of the genus.

Untersuchungen an Samenglobulinen von Leguminosen. 3. Mitt. Über Samenglobuline der Ackerbohne (Vicia faba L.)

The seed globulins from Vicia faba predominantly consist of two components, vicilin and legumin, which are exclusively deposited within the protein bodies of the storage cotyledons. The globulin biosynthesis commences with high intensity within a distinct phase during seed development as a consequence of reactivated genetic information. Isolation and purification of vicilin and legumin were achieved by a combination of zone precipitation, ion exchange chromatography, and gel filtration. Purity was controlled by disc electrophoresis on polyacrylamide e gels at pH 4.3 and by two dimensional immunoelectrophoresis, respectively. Vicilin prepared by zone precipitation and ion exchange chromatography consists of several serologically different proteins. One of them occupies the legumin position on polyacrylamide gels, although not identic with legumin, as revealed by tandem immunoelectrophoresis. The serological nonrelationship of vicilin and legumin was confirmed. Vicilin is characterized by micro heterogeneity which seems to indicate a molecular polymorphism.