Ecological significance of seed desiccation sensitivity in Quercus ilex

Background and Aims

Several widespread tree species of temperate forests, such as species of the genus Quercus, produce recalcitrant (desiccation-sensitive) seeds. However, the ecological significance of seed desiccation sensitivity in temperate regions is largely unknown. Do seeds of such species suffer from drying during the period when they remain on the soil, between shedding in autumn and the return of conditions required for germination in spring?

Methods

To test this hypothesis, the Mediterranean holm oak (Quercus ilex) forest was used as a model system. The relationships between the climate in winter, the characteristics of microhabitats, acorn morphological traits, and the water status and viability of seeds after winter were then investigated in 42 woodlands sampled over the entire French distribution of the species.

Key Results

The percentages of germination and normal seedling development were tightly linked to the water content of seeds after the winter period, revealing that in situ desiccation is a major cause of mortality. The homogeneity of seed response to drying suggests that neither intraspecific genetic variation nor environmental conditions had a significant impact on the level of desiccation sensitivity of seeds. In contrast, the water and viability status of seeds at the time of collection were dramatically influenced by cumulative rainfall and maximum temperatures during winter. A significant effect of shade and of the type of soil cover was also evidenced.

Conclusions

The findings establish that seed desiccation sensitivity is a key functional trait which may influence the success of recruitment in temperate recalcitrant seed species. Considering that most models of climate change predict changes in rainfall and temperature in the Mediterranean basin, the present work could help foresee changes in the distribution of Q. ilex and other oak species, and hence plant community alterations.     

Changes in starch and soluble sugars in relation to the acquisition of desiccation tolerance during maturation of Brassica campestris seed

Abstract. We investigated the onset of desiccation tolerance in developing embryos of Brassica campestris seeds and possible correlated ultrastructural modifications in the radiele cells. Since the acquisition of desiccation tolerance is a long asynchronous process which took 9 d to be achieved, we determined criteria allowing us to separate freshly intact harvested seeds into desiccation intolerant and desication tolerant batches that differed in age by only 2 d. No particular structural modifications were found except a strong depletion of intraplastidial starch (-90%) coincident with the appearance of stachyose and an increase of sucrose (+30%) on the acquisition of desiccation tolerance. As we did not observe an increase of lipid reserves as a consequence, we suggest that these metabolic events can be a key factor towards the acquisition of desiccation tolerance.     

Homoiohydrous (recalcitrant) seeds: Developmental status,desiccation sensitivity and the state of water in axes of Landolphia kirkii Dyer

The desiccation sensitivity in relation to the stage of development was investigated in embryonic axes from the homoiohydrous (recalcitrant) seeds of Landolphia kirkii. Electrolyte leakage, used to assess membrane damage after flash (very rapid) drying, indicated that axes from immature (non-germinable) seeds were the most desiccation-tolerant, followed by those from mature seeds, while axes from seeds germinated for increasing times were progressively more desiccation-sensitive. Differential scanning calorimetry was used to study the relationship between desiccation sensitivity and the properties of water in the tissues. Axes from immature seeds had a lower content of non-freezable water than that of any other developmental stage and a higher enthalpy of melting of freezable water. For mature and immature axes electrolyte leakage increased at the point of loss of freezable water. At other developmental stages the water content at which electrolyte leakage increased markedly correlated with the other properties of the water, such as the change in the shape of the melting endotherm and the onset temperature. Ultrastructural studies of axes at the various developmental stages showed changes in the degree and pattern of vacuolation, the presence and quantities of lipid and starch, and the degree of endomembrane development. The results are discussed in relation to current hypotheses on the basis of desiccation tolerance.Abbreviation DSC differential scanning calorimetry     

Changes in sugars during rice seed desiccation

The correlation between desiccation tolerance and soluble sugars was investigated in seeds of a number of rice cultivars belonging to the Asian rice Oryza sativa L. They were dried or ultradried to various low moisture content and then imbibed for germination testing. Few or no changes on germination percentage and vigor index were found in Indian rice seeds even after their moisture content fell to 3.5%, indicating that Indian rice exhibited a strong desiccation tolerance. On the contrary, Japonica rice seed germination percentage rapidly decreased, after their moisture content fell to 4.5%. The capacity for desiccation tolerance in Japonica (cv. Chunjiang 15) and Indian (cv. Zhongzu 1) developing seeds increased on 23–40 and 15–25 days after pollination, respectively. Though the level of monosaccharides declined, the content of sucrose has increased during desiccation. These results suggest that desiccation tolerance might be associated with the increase in seed viability and the changes in sugar level, and that raffinose could be capable of contributing to the desiccation tolerance to ultradrying. Published in Russian in Fiziologiya Rastenii, 2006, Vol. 53, No. 2, pp. 220–226. The text was submitted by the authors in English.     

Differential desiccation sensitivity of corn and Pennisetum pollen linked to their sucrose contents

Abstract. Two pollen species from the Gramineae family were investigated as to their differential sensitivity to desiccation. Germination in vivo ceased to occur after previous drying to 7–8% moisture content in Zea mays and 3% in Pennisetum typhoides. The reduced vitality coincided with extensive membrane damage, as evidenced by the considerable leakage of fluorescein and K⁺ from the prehumidified grains into liquid media. Further experiments were undertaken to investigate the basis for this interspecific difference: (1) phospholipid analyses revealed little difference in composition and content both before and after drying; (2) free fatty acid contents increased in both species upon drying but levels were generally low; and (3) sucrose was the sole soluble carbohydrate found in both species. Fresh maize pollen contained 5% sucrose, as compared to 14% in Pennisetum pollen. During slow drying (8h) this level went up to 12% and 17%, respectively. Drying corn pollen in the cold (2°C), or at high rate, limited sucrose levels and affected the resistance to drying. The authors conclude that survival of dehydration is correlated with the presence of sucrose. Finally, they tested the ability of sucrose to preserve dry liposomes prepared from phospholipids purified from the two species. When liposomes were dried in the presence of sucrose, fusion and leakage could largely be prevented at mass ratio's of sugar to lipid of > 4. Trehalose was also effective but myo-inositol was not. No species differences were observed. The authors suggest that the presence of sucrose is a key factor in preserving membranes in dry pollen.     

Ecological and evolutionary consequences of desiccation tolerance in tropical fern gametophytes

Ferns have radiated into the same diverse environments as spermatophytes, and have done so with an independent gametophyte that is not protected by the parent plant. The degree and extent of desiccation tolerance (DT) in the gametophytes of tropical fern species was assessed to understand mechanisms that have allowed ferns to radiate into a diversity of habitats. Species from several functional groups were subjected to a series of desiccation events, including varying degrees of intensity and multiple desiccation cycles. Measurements of chlorophyll fluorescence were used to assess recovery ability and compared with species ecology and gametophyte morphology. It is shown that vegetative DT (rare in vascular plants) is widely exhibited in fern gametophytes and the degree of tolerance is linked to species habitat preference. It is proposed that gametophyte morphology influences water-holding capacity, a novel mechanism that may help to explain how ferns have radiated into drought-prone habitats. Fern gametophytes have often been portrayed as extreme mesophytes with little tolerance for desiccation. The discovery of DT in gametophytes holds potential for improving our understanding of both the controls on fern species distribution and their evolution. It also advances a new system with which to study the evolution of DT in vascular plants.     

Membrane phospholipid composition during maturation of seeds of Acer platanoides and Acer pseudoplatanus in relation to desiccation tolerance

Membrane phospholipid composition was investigated in seeds of two species from the genus Acer: Norway maple (Acer platanoides L.) — tolerant to desiccation, and sycamore (Acer pseudoplatanus L.) — intolerant to desiccation, during their maturation, from 1 August to 25 September 1995, at weekly intervals. Seeds of Norway maple acquire tolerance to desiccation at the end of August ie. about 125 days after flowering (DAF). Phospholipid composition during development revealed marked differences between studied seeds. Seeds of Norway maple after acquiring tolerance to desiccation contained much more phosphatidylcholine (PC) and phosphatidylethanolamine (PE), compared to sycamore. The ratio of PC/PE in mature Norway maple seeds was evidently higher than those in sycamore. The level of unsaturated fatty acids in the phospholipid fraction substantially increased in Norway maple seeds during development and the saturation of PC and PE was less than in sycamore. The results suggest that phospholipid composition may be involved in desiccation tolerance of Norway maple seeds.     

拟南芥MT-II过量表达提高抗旱性(英文)

富含巯基的植物II型金属硫蛋白(MT)对植物抵抗重金属胁迫具有重要作用,其中一个可能机制是金属硫蛋白可能猝灭重金属引起的氧化胁迫。利用转MT-II基因和野生型拟南芥(Arabidopsis thaliana)植株来对比研究MT在胁迫过程中通过清除氧自由基,特别是H2O2而对植物抗旱性的影响。研究表明,转基因型拟南芥能有效维持体内氧化—还原势,减少MDA的产生,从而缓解干旱胁迫引起的伤害,提高抗旱性。     

A comparative study of seed morphology in relation to desiccation tolerance and other physiological responses in 71 Eastern Australian rainforest species

Seed characteristics were measured in 71 Eastern Australian rainforest species representing 30 families. Sensitivity to desiccation to low moisture contents (< 10%) occurred in 42% of species. We estimate, based on findings from 100 species from this present study and previously published reports, that 49% of Eastern Australian rainforest species have non‐orthodox seeds. Germination level and time to 50% germination were not significantly different between desiccation sensitive (DS) and desiccation tolerant (DT) seeds. The estimation of seed desiccation sensitivity based on predictors is an important tool underpinning ex situ conservation efforts. Seed characteristics differed significantly between DS and DT seeds; that is, DS seeds had: (i) larger fruits (19 949 mg vs 8322 mg); (ii) larger seeds (1663 mg vs 202 mg); (iii) higher seed moisture contents (49.7% vs 35.5% fresh weight); (iv) lower oil content (7.3% vs 24.8% yield); and (v) less investment in seed coats (0.19 vs 0.48 seed coat ratio). Only 25% of DS seeded species had oily seeds compared with 87% of DT seeded species. Most green embryos were DS. Seed coat ratio was the best predictor of seed DS (80% correctly predicted). Seed moisture content at maturity was also related to germination time. Mean seed size was correlated (?0.657, P = 0.01) with mean seed oil content in 46 species. Further research on seed storage physiology of possible oily and/or DS seeded species is crucial to ensure future long‐term security of this biodiversity, particularly for species currently threatened in situ and/or of socioeconomic importance in Eastern Australian rainforests.     

The effect of abscisic acid on the growth and storage of germinating rape (Brassica napus L.) seed dried following selection on the basis of a newly-emerged radicle

Abscisic acid at 1 × 10^–4M concentration controlled the progress of the emerging radicle from germinating rape seeds and apparently restricted it to the dehydration tolerant phase. ABA treatment during germination followed by washing reduced the deleterious effects of drying the seeds following selection based on a newly-emerged radicle. Furthermore, the longevity of these low-moisture-content germinating seeds at a range of temperatures was improved by the ABA treatment. The viability of the treated seeds stored at –20°C was maintained for up to 100 days.     

Partial desiccation augments plant regeneration from irradiated embryogenic cultures of sugarcane

Partial desiccation treatment was applied to improve plant regeneration response in irradiated in vitro cultures. Embryogenic callus cultures of sugarcane cv. Co-671 were exposed to different doses of gamma radiation (0–80 Gy) and radiation effect was evaluated in terms of post-irradiation callus recovery, growth and regeneration of plants. Proliferative capacity of cultures was inversely correlated with radiation dose as the percentage surviving cultures or white proliferating clumps (WPC) decreased as the radiation dose increased up to 80 Gy. LD50 was found to be around 20–30 Gy and at higher doses, poor regeneration frequency was observed after 4–6 weeks of post-irradiation culture. To stimulate regeneration response, irradiated cultures were subjected to partial desiccation for 6 h and the treatment resulted in enhanced plant regeneration response. The study suggests that partial desiccation treatment can be useful in stimulating regeneration response of irradiated in vitro cultures.     

Seasonal rhythms of seed rain and seedling emergence in two tropical rain forests in southern Brazil

Seasonal tropical forests show rhythms in reproductive activities due to water stress during dry seasons. If both seed dispersal and seed germination occur in the best environmental conditions, mortality will be minimised and forest regeneration will occur. To evaluate whether non-seasonal forests also show rhythms, for 2 years we studied the seed rain and seedling emergence in two sandy coastal forests (flooded and unflooded) in southern Brazil. In each forest, one 100 x 30-m grid was marked and inside it 30 stations comprising two seed traps (0.5 x 0.5 m each) and one plot (2 x 2 m) were established for monthly monitoring of seed rain and a seedling emergence study, respectively. Despite differences in soil moisture and incident light on the understorey, flooded and unflooded forests had similar dispersal and germination patterns. Seed rain was seasonal and bimodal (peaks at the end of the wetter season and in the less wet season) and seedling emergence was seasonal and unimodal (peaking in the wetter season). Approximately 57% of the total species number had seedling emergence 4 or more months after dispersal. Therefore, both seed dormancy and the timing of seed dispersal drive the rhythm of seedling emergence in these forests. The peak in germination occurs in the wetter season, when soil fertility is higher and other phenological events also occur. The strong seasonality in these plant communities, even in this weakly seasonal climate, suggests that factors such as daylength, plant sensitivity to small changes in the environment (e.g. water and nutrient availability) or phylogenetic constraints cause seasonal rhythms in the plants.     

Prediction of desiccation sensitivity in seeds of woody species: a probabilistic model based on two seed traits and 104 species

BACKGROUND AND AIMS: Seed desiccation sensitivity limits the ex situ conservation of up to 47 % of plant species, dependent on habitat. Whilst desirable, empirically determining desiccation tolerance levels in seeds of all species is unrealistic. A probabilistic model for the rapid identification of woody species at high risk of displaying seed desiccation sensitivity is presented. METHODS: The model was developed using binary logistic regression on seed trait data [seed mass, moisture content, seed coat ratio (SCR) and rainfall in the month of seed dispersal] for 104 species from 37 families from a semi-deciduous tropical forest in Panamá. KEY RESULTS: For the Panamanian species, only seed mass and SCR were significantly related to the response to desiccation, with the desiccation-sensitive seeds being large and having a relatively low SCR (i.e. thin 'seed' coats). Application of this model to a further 38 species, of known seed storage behaviour, from two additional continents and differing vegetation types (dryland Africa and temperate Europe) correctly predicted the response to desiccation in all cases, and resolved conflicting published data for two species (Acer pseudoplatanus and Azadirachta indica). CONCLUSIONS: This model may have application as a decision-making tool in the handling of species of unknown seed storage behaviour in species from three disparate habitats.     

Modelling the effects of microclimate on bean seed desiccation rate and seed storage ability

Bean seed storage ability is of major interest for seed firms and depends, at least partially, on the effect of desiccation microclimate and desiccation rate on the mother plant; however, their effects are contradictory and not quantified. Therefore, our aims were (a) to predict seed desiccation rate from microclimatic variables at the pod level and (b) to measure the effects of seed desiccation rate and temperature on seed storage ability. For 4 years, beans (Phaseolus vulgaris) were sown at different dates in the field and once in a greenhouse. Pods having seeds at the beginning of desiccation stage were selected according to their colour and then dried in the field or under controlled conditions. In the field, pods were dried under both natural conditions and conditions modified either by defoliation or by water spraying. Under controlled conditions, pods were dried under a wide range of temperature and relative humidity combinations. Seed water content, temperature and relative humidity were measured throughout the desiccation phase. Storage ability was measured by a standard germination test after either 11 or 15 days of controlled deterioration. Seed desiccation rate was highly correlated to air vapour pressure deficit, which measures the combined effects of temperature and relative humidity on drying. With a logit transformation, deterioration test results showed a linear decrease in storage ability as seed desiccation rate increased for either controlled or field‐dried lots. However, for controlled lots desiccated at temperatures lower than 24°C, the lower the temperature, the lower the storage ability at a given desiccation rate. Moreover, the relationship between the results of the two deterioration periods differed between controlled and field‐dried lots. Finally, the high correlation between seed storage ability, desiccation rate and vapour pressure deficit in the field has given new insights for building a crop decision‐oriented model for optimising harvesting.