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1.  Complex Combination of Seed Dormancy and Seedling Development Determine Emergence of Viburnum tinus (Caprifoliaceae) 
Annals of Botany  2004;95(2):323-330.
• Background and Aims The shrub Viburnum tinus is widely distributed in mattoral vegetation of the Mediterranean basin. The purpose of the present study was to classify the seed dormancy type and examine the requirements for embryo growth, root protrusion and shoot emergence.
• Methods Overwintered fruits were collected in western Spain in April 2001 and prepared in three ways: entire pericarp was removed, exocarp and mesocarp were removed or fruits were left intact. Fruits treated in these three ways were subjected to artificial annual temperature cycles or to constant temperature regimes for 1·5 years.
• Key Results Removal of exocarp and mesocarp was necessary for embryo growth and germination. High temperature favoured dormancy alleviation and embryo growth, intermediate to low temperatures favoured root protrusion, and intermediate temperature shoot emergence. There was substantial germination at constant temperature regimes, indicating an overlap between temperature intervals suitable for the different stages of embryo and seedling development. Functionally, V. tinus has the same root and shoot emergence pattern that is described for other Viburnum species considered to have epicotyl dormancy. However, the requirement for high and low temperatures for radicle protrusion and epicotyl emergence, respectively, was missing in V. tinus; these characters are the foundation for the epicotyl dormancy classification.
• Conclusions It is concluded that V. tinus does not have epicotyl dormancy. Instead, there is a combination of a weak morphophysiological dormancy and a slow germination process, where different temperatures during an annual cycle favour different development stages. The present study suggests that the first complete seedlings would emerge in the field 1·5 years after fruit maturation in October, i.e. seed dispersal during winter, embryo growth during the first summer, root protrusion and establishment during the second autumn and winter, and cotyledon emergence during the second spring.
doi:10.1093/aob/mci029
PMCID: PMC4246832  PMID: 15546926
Adoxaceae; Caprifoliaceae; epicotyl dormancy; mattoral; morphophysiological dormancy; pericarp; persistent fruits; ruminant endosperm; seedling emergence; shrub; Viburnaceae; Viburnum tinus
2.  A Comparative Study of Germination Ecology of Four Papaver Taxa 
Annals of Botany  2007;99(5):935-946.
Background and Aims
Comparative studies of closely related taxa can increase understanding of adaptations and changes in seed dormancy and germination preferences in an evolutionary perspective. For such studies, a method to describe and compare the performance of taxa in a general way is needed. The germination ecology of four Papaver taxa was studied with the aim of describing and comparing their responses to different seasonal temperature regimes.
Methods
Germination of Papaver argemone, P. rhoeas, P. dubium ssp. dubium and P. dubium ssp. lecoqii was investigated in three different artificial climates over 2·5 years. Seeds were collected in southern Sweden, and samples from different populations were used as replicates of taxa.
Key Results
Despite substantial intra-taxa variation, there were clear taxon-specific responses. Most germination occurred in the warmest climate. In general, the warmer the climate the more germination occurred in autumn instead of spring. Papaver argemone, phylogenetically most distant from the other taxa, was, in contrast to the others, restricted to germinating only at lower temperatures.
Conclusions
Seed dormancy and germination may be described by dormancy pattern, germination preferences and dormancy strength. The general dormancy pattern was a common feature for these taxa and therefore probably an evolutionary conservative character. Germination preferences varied between taxa, resulting in different temperature optima and intervals for germination, and dormancy strength was to some extent taxon-specific, but highly variable. The dormancy pattern explained how the taxa can perform as winter annuals in warmer climates, but mainly as summer annuals in colder climates. Hence, there is no need to interpret the within-taxon temporal differences in seedling emergence as local adaptations. In the field, an entire seed cohort will not germinate during a single season. Instead, emergence will be distributed over several seasons, regardless of local climate, weather and soil cultivation methods.
doi:10.1093/aob/mcm045
PMCID: PMC2802914  PMID: 17452382
Annual weed; germination ecology; morphophysiological dormancy; Papaver argemone; Papaver dubium; Papaver rhoeas; Papaveraceae; poppy; seed dormancy; Sweden; summer annual; winter annual
3.  Seedling Responses to Water Pulses in Shrubs with Contrasting Histories of Grassland Encroachment 
PLoS ONE  2014;9(1):e87278.
Woody plant encroachment into grasslands has occurred worldwide, but it is unclear why some tree and shrub species have been markedly more successful than others. For example, Prosopis velutina has proliferated in many grasslands of the Sonoran Desert in North America over the past century, while other shrub species with similar growth form and life history, such as Acacia greggii, have not. We conducted a glasshouse experiment to assess whether differences in early seedling development could help explain why one species and not the other came to dominate many Sonoran Desert grasslands. We established eight watering treatments mimicking a range of natural precipitation patterns and harvested seedlings 16 or 17 days after germination. A. greggii had nearly 7 times more seed mass than P. velutina, but P. velutina emerged earlier (by 3.0±0.3 d) and grew faster (by 8.7±0.5 mg d−1). Shoot mass at harvest was higher in A. greggii (99±6 mg seedling−1) than in P. velutina (74±2 mg seedling−1), but there was no significant difference in root mass (54±3 and 49±2 mg seedling−1, respectively). Taproot elongation was differentially sensitive to water supply: under the highest initial watering pulse, taproots were 52±19 mm longer in P. velutina than in A. greggii. Enhanced taproot elongation under favorable rainfall conditions could give nascent P. velutina seedlings growth and survivorship advantages by helping reduce competition with grasses and maintain contact with soil water during drought. Conversely, A. greggii's greater investment in mass per seed appeared to provide little return in early seedling growth. We suggest that such differences in recruitment traits and their sensitivities to environmental conditions may help explain ecological differences between species that are highly similar as adults and help identify pivotal drivers of shrub encroachment into grasslands.
doi:10.1371/journal.pone.0087278
PMCID: PMC3903637  PMID: 24475263
4.  Effect of Canopy Position on Germination and Seedling Survival of Epiphytic Bromeliads in a Mexican Humid Montane Forest 
Annals of Botany  2005;95(6):1039-1047.
• Background and Aims Seeds of epiphytes must land on branches with suitable substrates and microclimates to germinate and for the resulting seedlings to survive. It is important to understand the fate of seeds and seedlings in order to model populations, but this is often neglected when only established plants are included in analyses.
• Methods The seeds of five bromeliad species were exposed to different canopy positions in a Mexican montane forest, and germination and early seedling survival were recorded. Additionally, the survival of naturally dispersed seedlings was monitored in a census over 2·5 years. Survival analysis, a procedure rarely used in plant ecology, was used to study the influence of branch characteristics and light on germination and seedling survival in natural and experimental populations.
• Key Results Experimental germination percentages ranged from 7·2 % in Tillandsia deppeana to 33·7 % in T. juncea, but the seeds of T. multicaulis largely failed to germinate. Twenty months after exposure between 3·5 and 9·4 % of the seedlings were still alive. There was no evidence that canopy position affected the probability of germination, but time to germination was shorter in less exposed canopy positions indicating that higher humidity accelerates germination. More experimental seedlings survived when canopy openness was high, whereas survival in census-seedlings was influenced by moss cover. While mortality decreased steadily with age in juveniles of the atmospheric Tillandsia, in the more mesomorphic Catopsis sessiliflora mortality increased dramatically in the dry season.
• Conclusions Seedling mortality, rather than the failure to germinate, accounts for the differential distribution of epiphytes within the canopy studied. With few safe sites to germinate and high seedling mortality, changes of local climate may affect epiphyte populations primarily through their seedling stage.
doi:10.1093/aob/mci115
PMCID: PMC4246762  PMID: 15767270
Bromeliaceae; Catopsis; epiphytes; germination; habitat heterogeneity; Mexico; seedling establishment; survival analysis; Tillandsia
5.  Seed reserve composition in 19 tree species of a tropical deciduous forest in Mexico and its relationship to seed germination and seedling growth 
Annals of Botany  2011;107(6):939-951.
Background and Aims
The size and composition of seed reserves may reflect the ecological strategy and evolutionary history of a species and also temporal variation in resource availability. The seed mass and composition of seed reserves of 19 co-existing tree species were studied, and we examined how they varied among species in relation to germination and seedling growth rates, as well as between two years with contrasting precipitation (652 and 384 mm).
Methods
Seeds were collected from a tropical deciduous forest in the northwest of Mexico (Chamela Biological Station). The seed dry mass, with and without the seed coat, and the concentrations of lipids, nitrogen and non-structural carbohydrates for the seed minus seed coat were determined. The anatomical localization of these reserves was examined using histochemical analysis. The germination capacity, rate and lag time were determined. The correlations among these variables, and their relationship to previously reported seedling relative growth rates, were evaluated with and without phylogenetic consideration.
Key Results
There were interannual differences in seed mass and reserve composition. Seed was significantly heavier after the drier year in five species. Nitrogen concentration was positively correlated with seed coat fraction, and was significantly higher after the drier year in 12 species. The rate and lag time of germination were negatively correlated with each other. These trait correlations were also supported for phylogenetic independent contrasts. Principal component analysis supported these correlations, and indicated a negative association of seedling relative growth rate with seed size, and a positive association of germination rate with nitrogen and lipid concentrations.
Conclusions
Nitrogen concentration tended to be higher after the drier year and, while interannual variations in seed size and reserve composition were not sufficient to affect interspecific correlations among seed and seedling traits, some of the reserves were related to germination variables and seedling relative growth rate.
doi:10.1093/aob/mcr041
PMCID: PMC3080624  PMID: 21385781
Germination; seed reserves; seedling growth; tropical deciduous forest
6.  Northern Hemisphere Plant Disjunctions: A Window on Tertiary Land Bridges and Climate Change? 
Annals of Botany  2006;98(3):465-472.
• Aims This botanical briefing examines how molecular systematics has contributed to progress in understanding the history of Tertiary relict genera, i.e. those that that now occur disjunctly in parts of Eurasia and N America, and how progress in understanding Southern Hemisphere biogeography paradoxically makes unravelling Northern Hemisphere biogeography more complex.
• Scope Tertiary relict floras comprise genera of warm wet climates that were once circumboreal in distribution but are now confined to E Asia, south-eastern and western N America, and SW Eurasia. The intercontinental disjunctions among these genera have long been believed to result from land connections between Eurasia and N America, across Beringia and the N Atlantic. This view is reassessed in the light of new evidence for long dispersal of propagules across oceans being responsible for many plant disjunctions involving southern continents. The impact of molecular dating, which has been very different in Southern and Northern Hemisphere biogeography, is discussed.
• Conclusions For N America–Eurasia disjunctions involving Tertiary relict floras, land connections remain the more likely cause of disjunctions but data from fossils or infraspecific variation will be required to exclude long-dispersal explanations for disjunctions in any individual genus. Molecular dating of divergence between disjunctly distributed Tertiary relict floras can tell us which palaeoclimatic or palaeogeographic events impacted on them, and how, but only if migration over land and vicariance can be proved and molecular dating is sufficiently accurate.
doi:10.1093/aob/mcl148
PMCID: PMC2803576  PMID: 16845136
Tertiary relict floras; plant disjunctions; biogeography; Bering land bridge; dispersal; vicariance; molecular dating; Northern Hemisphere; paleoclimate
7.  Oviposition strategy as a means of local adaptation to plant defence in native and invasive populations of the viburnum leaf beetle 
Herbivores have been hypothesized to adapt locally to variation in plant defences and such adaptation could facilitate novel associations in the context of biological invasions. Here, we show that in the native range of the viburnum leaf beetle (VLB, Pyrrhalta viburni), two populations of geographically isolated hosts—Viburnum opulus and Viburnum tinus—have divergent defences against VLB oviposition: negative versus positive density-dependent egg-crushing wound responses, respectively. Populations of beetles coexisting with each host show an adaptive behavioural response: aggregative versus non-aggregative oviposition on V. opulus and V. tinus, respectively. In parallel, we show that in North America, where VLB is invasive, defences of three novel hosts are negatively density-dependent, and beetles' oviposition behaviour is aggregative. Thus, local adaptation to plant defences has the potential to facilitate the invasion of herbivores onto novel hosts.
doi:10.1098/rspb.2011.1294
PMCID: PMC3259924  PMID: 21849322
insect oviposition strategy; invasion ecology; adaptive deme hypothesis; Chrysomelidae; plant–insect interactions; plant defence theory
8.  Extreme Reproduction and Survival of a True Cliffhanger: The Endangered Plant Borderea chouardii (Dioscoreaceae) 
PLoS ONE  2012;7(9):e44657.
Cliff sides are extreme habitats, often sheltering a rich and unique flora. One example is the dioecious herb Borderea chouardii (Dioscoreaceae), which is a Tertiary, tropical relict, occurring only on two adjacent vertical cliffs in the world. We studied its reproductive biology, which in some aspects is extreme, especially the unusual double mutualistic role of ants as both pollinators and dispersers. We made a 2-year pollination census and four years of seed-dispersal experiments, recording flower visitors and dispersal rates. Fruit and seed set, self-sowing of seeds, seedling recruitment, and fate of seedlings from seeds sowed by different agents were scored over a period of 17 years. The ants Lasius grandis and L. cinereus were the main pollinators, whereas another ant Pheidole pallidula dispersed seeds. Thus ants functioned as double mutualists. Two thirds of all new seedlings came from self-sown seeds, and 1/3 was dispersed by ants, which gathered the seeds with their oil-rich elaiosome. Gravity played a minor role to dispersal. Both ant dispersal and self-sowing resulted in the same survival rate of seedlings. A double mutualism is a risky reproductive strategy, but B. chouardii buffers that by an unusual long–term demographic stability (some individuals exceed 300 years in lifespan) and its presence in a climatically very stable habitat, inaccessible to large herbivores. Such a combination of traits and habitat properties may explain the persistence of this relict species.
doi:10.1371/journal.pone.0044657
PMCID: PMC3440335  PMID: 22984539
9.  Ecology of Achene Dimorphism in Leontodon saxatilis 
Annals of Botany  2007;100(6):1189-1197.
Backround and Aims
Leontodon saxatilis produces two morphologically distinct achenes (morphs) in a single capitulum: one row of dark brown achenes without a pappus lies at the edge (‘peripheral achenes’; 0·74 ± 0·18 mg) while the inner ones are light brown with a pappus (‘central achenes’; 0·38 ± 0·07 mg). The hypothesis that achene heteromorphism in L. saxatilis widens its ecological amplitude was tested.
Key Results
Achenes of both morphs germinated over the same range of temperatures (6–33 °C) but the central achenes showed significantly higher germination percentages, and the two also differed significantly in their annual dormancy cycle, with the peripheral achenes showing greater dormancy for part of the year. Seedlings from the two morphs did not differ significantly in total biomass after 2 and 4 weeks of growth, neither did they differ significantly in root and shoot weight and root:shoot ratio. Plants from both morphs growing at different regimes of soil moisture, nutrients and competition did not differ significantly in their number of achenes per capitulum. While the number of central achenes varied, that of peripheral achenes remained constant at approx. 13. Drier soil led to an increase in the number of central achenes in plants from both morphs.
Conclusions
The peripheral achenes can replace the mother plant in the following growing season, whereas the central achenes are well adapted for wind dispersal and thus for colonization of new sites. However, the extent of variation in germination characteristics was similar to that found in seed populations of homomorphic plants, which suggests that germination percentage and other growth characteristics do not contribute to widening the ecological amplitude. The habitat of most heteromorphic species, the morphs of which differ greatly in germination and/or growth characteristic, are deserts or highly disturbed areas where such differences are highly advantageous, but in the moderate habitat of L. saxatilis the differences may prove a disadvantage.
doi:10.1093/aob/mcm214
PMCID: PMC2759255  PMID: 17901060
Achene morphology; Asteraceae; dormancy cycle; germination; Leontodon saxatilis; seed heteromorphism; seedling growth
10.  The response of forest plant regeneration to temperature variation along a latitudinal gradient 
Annals of Botany  2012;109(5):1037-1046.
Background and Aims
The response of forest herb regeneration from seed to temperature variations across latitudes was experimentally assessed in order to forecast the likely response of understorey community dynamics to climate warming.
Methods
Seeds of two characteristic forest plants (Anemone nemorosa and Milium effusum) were collected in natural populations along a latitudinal gradient from northern France to northern Sweden and exposed to three temperature regimes in growth chambers (first experiment). To test the importance of local adaptation, reciprocal transplants were also made of adult individuals that originated from the same populations in three common gardens located in southern, central and northern sites along the same gradient, and the resulting seeds were germinated (second experiment). Seedling establishment was quantified by measuring the timing and percentage of seedling emergence, and seedling biomass in both experiments.
Key Results
Spring warming increased emergence rates and seedling growth in the early-flowering forb A. nemorosa. Seedlings of the summer-flowering grass M. effusum originating from northern populations responded more strongly in terms of biomass growth to temperature than southern populations. The above-ground biomass of the seedlings of both species decreased with increasing latitude of origin, irrespective of whether seeds were collected from natural populations or from the common gardens. The emergence percentage decreased with increasing home-away distance in seeds from the transplant experiment, suggesting that the maternal plants were locally adapted.
Conclusions
Decreasing seedling emergence and growth were found from the centre to the northern edge of the distribution range for both species. Stronger responses to temperature variation in seedling growth of the grass M. effusum in the north may offer a way to cope with environmental change. The results further suggest that climate warming might differentially affect seedling establishment of understorey plants across their distribution range and thus alter future understorey plant dynamics.
doi:10.1093/aob/mcs015
PMCID: PMC3310497  PMID: 22345113
Anemone nemorosa; climate change; common garden; growth chambers; latitudinal gradient; local adaptation; Milium effusum; plant regeneration; range edges; recruitment; seedling establishment; temperature
11.  Ecological significance of seed desiccation sensitivity in Quercus ilex 
Annals of Botany  2013;111(4):693-701.
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.
doi:10.1093/aob/mct025
PMCID: PMC3605958  PMID: 23388882
Quercus ilex; acorn; desiccation sensitivity; holm oak; drought; ecological filtering; germination; Mediterranean climate; recalcitrance; winter rainfall
12.  Exploring the Natural Variation for Seedling Traits and Their Link with Seed Dimensions in Tomato 
PLoS ONE  2012;7(8):e43991.
The success of germination, growth and final yield of every crop depends to a large extent on the quality of the seeds used to grow the crop. Seed quality is defined as the viability and vigor attribute of a seed that enables the emergence and establishment of normal seedlings under a wide range of environments. We attempt to dissect the mechanisms involved in the acquisition of seed quality, through a combined approach of physiology and genetics. To achieve this goal we explored the genetic variation found in a RIL population of Solanum lycopersicum (cv. Moneymaker) x Solanum pimpinellifolium through extensive phenotyping of seed and seedling traits under both normal and nutrient stress conditions and root system architecture (RSA) traits under optimal conditions. We have identified 62 major QTLs on 21 different positions for seed, seedling and RSA traits in this population. We identified QTLs that were common across both conditions, as well as specific to stress conditions. Most of the QTLs identified for seedling traits co-located with seed size and seed weight QTLs and the positive alleles were mostly contributed by the S. lycopersicum parent. Co-location of QTLs for different traits might suggest that the same locus has pleiotropic effects on multiple traits due to a common mechanistic basis. We show that seed weight has a strong effect on seedling vigor and these results are of great importance for the isolation of the corresponding genes and elucidation of the underlying mechanisms.
doi:10.1371/journal.pone.0043991
PMCID: PMC3431394  PMID: 22952841
13.  Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa) 
Annals of Botany  2008;103(2):197-209.
Background and Aims
Flooding slows seed germination, imposes fatalities and delays seedling establishment in direct-seeded rice. This study describes responses of contrasting rice genotypes subjected to flooding or low oxygen stress during germination and discusses the basis of tolerance shown by certain cultivars.
Methods
In one set of experiments, dry seeds were sown in soil and either watered normally or flooded with 10 cm of water. Seedling survival and shoot and root growth were assessed and seed portions of germinating seedlings were assayed for soluble sugars and starch concentrations. The whole germinating seedlings were assayed for amylase and peroxidase activities and for ethylene production. Activities of enzymes associated with anaerobic respiration were examined and gene expression was analysed separately with seeds germinating under different amounts of dissolved oxygen in dilute agar.
Key Results
Flooding during germination reduced survival but to a lesser extent in tolerant genotypes. Starch concentration in germinating seeds decreased while sugar concentration increased under flooding, but more so in tolerant genotypes. Amylase activity correlated positively with elongation (r = 0·85 for shoot and 0·83 for root length) and with plant survival (r = 0·92). Tolerant genotypes had higher amylase activity and higher RAmy3D gene expression. Ethylene was not detected in seeds within 2 d after sowing, but increased thereafter, with a greater increase in tolerant genotypes starting 3 d after sowing. Peroxidase activity was higher in germinating seeds of sensitive genotypes and correlated negatively with survival.
Conclusions
Under low oxygen stress, tolerant genotypes germinate, grow faster and more seedlings survive. They maintain their ability to use stored starch reserves through higher amylase activity and anaerobic respiration, have higher rates of ethylene production and lower peroxidase activity as germinating seeds and as seedlings. Relevance of these traits to tolerance of flooding during germination and early growth is discussed.
doi:10.1093/aob/mcn211
PMCID: PMC2707318  PMID: 19001425
Amylase; anoxia; crop establishment; direct-seeded rice; ethylene; flooding; germination; hypoxia; Oryza sativa
14.  Influence of Environmental Factors on the Germination of Urena lobata L. and Its Response to Herbicides 
PLoS ONE  2014;9(3):e90305.
Urena lobata is becoming a noxious and invasive weed in rangelands, pastures, and undisturbed areas in the Philippines. This study determined the effects of seed scarification, light, salt and water stress, amount of rice residue, and seed burial depth on seed germination and emergence of U. lobata; and evaluated the weed's response to post-emergence herbicides. Germination was stimulated by both mechanical and chemical seed scarifications. The combination of the two scarification methods provided maximum (99%) seed germination. Germination was slightly stimulated when seeds were placed in light (65%) compared with when seeds were kept in the dark (46%). Sodium chloride concentrations ranging from 0 to 200 mM and osmotic potential ranging from 0 to −1.6 MPa affected the germination of U. lobata seeds significantly. The osmotic potential required for 50% inhibition of the maximum germination was −0.1 MPa; however, some seeds germinated at −0.8 MPa, but none germinated at −1.6 MPa. Seedling emergence and biomass increased with increase in rice residue amount up to 4 t ha−1, but declined beyond this amount. Soil surface placement of weed seeds resulted in the highest seedling emergence (84%), which declined with increase in burial depth. The burial depth required for 50% inhibition of maximum emergence was 2 cm; emergence was greatly reduced (93%) at burial depth of 4 cm or more. Weed seedling biomass also decreased with increase in burial depth. Bispyribac-sodium, a commonly used herbicide in rice, sprayed at the 4-leaf stage of the weed, provided 100% control, which did not differ much with 2,4-D (98%), glyphosate (97%), and thiobencarb + 2,4-D (98%). These herbicides reduced shoot and root biomass by 99–100%.
doi:10.1371/journal.pone.0090305
PMCID: PMC3962347  PMID: 24658143
15.  Identification of QTLs associated with seedling root traits and their correlation with plant height in wheat 
Journal of Experimental Botany  2013;64(6):1745-1753.
Genetic relationships between plant height and root morphology were investigated in a diverse set of wheat germplasm [199 double-haploid progeny derived from a cross between Avalon and Cadenza (Triticum aestivum L.), Rht near-isogenic lines (NILs), and accessions from the Watkins Collection] to investigate whether Rht genes controlling shoot height also control seedling root growth. A germination paper screen was developed to measure seedling root length (distinguishing seminal axes from seminal lateral roots), surface area, volume, and dry weight, and these were compared with shoot dry weight and the root to shoot ratio. Field experiments were conducted to measure mature plant height (PH) and grain characteristics for the mapping population. Forty-three quantitative trait loci (QTLs) for PH, root and seed traits were identified. Some QTLs for roots and either height or seed characteristics were coincident: chromosome 2D had co-locating root and PH QTLs; chromosomes 4D had co-locating root, PH, and seed QTLs; chromosome 5A and 6A had co-locating root and seed QTLs; and other non-co-locating root and PH QTLs were found on chromosomes 3A and 3B. Rht NILs illustrated that some known dwarfing genes reduce both PH and root proliferation. However, analysis of 25 short and 23 tall lines from the Watkins wheat germplasm collection indicated that PH and root proliferation are not simply related.
doi:10.1093/jxb/ert041
PMCID: PMC3617839  PMID: 23564959
Doubled-haploid population; plant height; QTLs; Rht; roots; wheat.
16.  Wind-dispersed Seed Deposition Patterns and Seedling Recruitment of Artemisia halodendron in a Moving Sandy Land 
Annals of Botany  2005;96(1):69-80.
• Background and Aims Artemisia halodendron is a native sub-shrub that occurs mainly in moving and semi-fixed sandy lands in Inner Mongolia, China. Information on the spatial patterns of wind-dispersed seed deposition and seedling recruitment of A. halodendron inhabiting moving sandy lands is very limited. The aim of this study was to examine wind-dispersed seed deposition patterns and post-dispersal recruitment of A. halodendron seedlings.
•Methods The spatial patterns of wind-dispersed seed deposition and seedling recruitment of A. halodendron were examined by investigating the numbers of deposited seeds, emerged and surviving seedlings using sampling points at a range of distances from the parent plant in eight compass directions for two consecutive growing seasons.
•Key Results Wind-dispersed seed deposition showed considerable variation between directions and years. Wind transported A. halodendron seeds only a few meters away from the parent plant in all eight directions. Seedling emergence and establishment also showed between-direction and between-year variability, but the spatial pattern of seedling distribution differed from that of seed deposition. Only a very small fraction (<1 %) of the deposited seeds emerged in the field and survived for long enough to be included in our seedling censuses at the end of the growing season.
•Conclusions The spatial variation in wind speed and frequency strongly affects the pattern of seed deposition, although the variation in seed deposition does not determine the spatial pattern of seedling recruitment. Seeds of A. halodendron are not dispersed very well by wind. The low probability of recruitment success for A. halodendron seedlings suggests that this species does not rely on seedling recruitment for its persistence and maintenance of population.
doi:10.1093/aob/mci150
PMCID: PMC4246809  PMID: 15857850
Artemisia halodendron; Horqin Sandy Land; moving sand dunes; population dynamics; post-dispersal recruitment; recruitment success; sand-stabilizing plant; seed deposition; seedling emergence; seedling survival; wind dispersal
17.  Effects of Increased Nitrogen Deposition and Precipitation on Seed and Seedling Production of Potentilla tanacetifolia in a Temperate Steppe Ecosystem 
PLoS ONE  2011;6(12):e28601.
Background
The responses of plant seeds and seedlings to changing atmospheric nitrogen (N) deposition and precipitation regimes determine plant population dynamics and community composition under global change.
Methodology/Principal Findings
In a temperate steppe in northern China, seeds of P. tanacetifolia were collected from a field-based experiment with N addition and increased precipitation to measure changes in their traits (production, mass, germination). Seedlings germinated from those seeds were grown in a greenhouse to examine the effects of improved N and water availability in maternal and offspring environments on seedling growth. Maternal N-addition stimulated seed production, but it suppressed seed mass, germination rate and seedling biomass of P. tanacetifolia. Maternal N-addition also enhanced responses of seedlings to N and water addition in the offspring environment. Maternal increased-precipitation stimulated seed production, but it had no effect on seed mass and germination rate. Maternal increased-precipitation enhanced seedling growth when grown under similar conditions, whereas seedling responses to offspring N- and water-addition were suppressed by maternal increased-precipitation. Both offspring N-addition and increased-precipitation stimulated growth of seedlings germinated from seeds collected from the maternal control environment without either N or water addition. Our observations indicate that both maternal and offspring environments can influence seedling growth of P. tanacetifolia with consequent impacts on the future population dynamics of this species in the study area.
Conclusion/Significance
The findings highlight the importance of the maternal effects on seed and seedling production as well as responses of offspring to changing environmental drivers in mechanistic understanding and projecting of plant population dynamics under global change.
doi:10.1371/journal.pone.0028601
PMCID: PMC3237472  PMID: 22194863
18.  Intraspecific Variations in Seedling Emergence and Survival of Potentilla matsumurae (Rosaceae) between Alpine Fellfield and Snowbed Habitats 
Annals of Botany  2003;91(1):21-29.
Potentilla matsumurae has a wide distribution from wind‐blown fellfields to snowbeds in alpine regions of Japan. The environmental factors influencing seedling establishment differ between the fellfield and snowbed habitats; plants growing in each habitat may therefore have different germination strategies. Using a reciprocal sowing experiment, patterns of seedling emergence and survivorship were examined in both habitat types in the Taisetsu Mountains, Japan. Seeds derived from a fellfield population germinated earlier than did those derived from a snowbed population at both habitats, and the germination of fellfield seeds continued throughout the growing season. The timing of seedling emergence greatly affected subsequent survival at the fellfield. Seedlings that emerged in the first half of the growing season had low survivorship during the first year because of frost and drought damage, but the remaining seedlings had high survivorship during the winter; seedlings that emerged in the latter half of the growing season showed the opposite trend. At the snowbed, seedling survival was high throughout the growing season. Germination experiments in the laboratory highlighted a difference in the sensitivity of seeds from the fellfield and snowbed populations to fluctuating temperatures. These results indicate that intraspecific variation in emergence and survivorship may occur over a small scale in an alpine environment.
doi:10.1093/aob/mcg002
PMCID: PMC4240347  PMID: 12495916
Potentilla matsumurae Th. Wolf; fellfield; snowbed; germination pattern; seedling survivorship; temperature fluctuation; intraspecific variation
19.  Understanding the germination of bulbils from an ecological perspective: a case study on Chinese yam (Dioscorea polystachya) 
Annals of Botany  2010;106(6):945-955.
Background and Aims
Bulbils serve as a means of vegetative reproduction and of dispersal for many plants; this latter aspect making them analogous to seeds. However, germination of bulbils may differ considerably from seeds due to dissimilar anatomical structures and perhaps environmental cue perception. The few laboratory studies done on bulbils suggest that their germination is similar to that of seeds in the same habitats and to vegetative buds of winter-dormant plants. The present study is the first to examine how bulbil germination is controlled in nature in relation to dispersal (before vs. after winter of the same cohort) and to ambient temperatures.
Methods
Under laboratory conditions, temperature and light requirements for root and shoot emergences from bulbils of Dioscorea polystachya collected in September, 2005, February, 2006 (produced in 2005) and July, 2006 were determined. Effects of cold stratification and dry storage for releasing dormancy were tested on September and July bulbils. The phenology of dormancy release and of root and shoot emergences and the persistence of bulbils in soil were followed over time under field conditions.
Key Results
Although a low percentage of bulbils collected in July or in September produced roots, but no shoots, in the laboratory and field, these roots died within approx. 1 month. Regardless of collection date, cold stratification markedly increased root and shoot emergences. Bulbils sown outdoors in October produced roots and shoots the following March and April, respectively. The soil bulbil bank is short lived.
Conclusions
Bulbils of D. polystachya are similar to seeds of many temperate plants being mostly dormant when dispersed in summer or autumn and overcoming dormancy with cold stratification during winter. Adaptively, bulbil germination primarily occurs in spring at the beginning of a favourable period for survivorship and growth.
doi:10.1093/aob/mcq189
PMCID: PMC2990661  PMID: 20880931
Aerial tubers; bulbils; Dioscorea polystachya; Dioscoreaceae; dormancy; germination ecology; soil bulbil bank
20.  Highly local environmental variability promotes intrapopulation divergence of quantitative traits: an example from tropical rain forest trees 
Annals of Botany  2013;112(6):1169-1179.
Background and Aims
In habitat mosaics, plant populations face environmental heterogeneity over short geographical distances. Such steep environmental gradients can induce ecological divergence. Lowland rainforests of the Guiana Shield are characterized by sharp, short-distance environmental variations related to topography and soil characteristics (from waterlogged bottomlands on hydromorphic soils to well-drained terra firme on ferralitic soils). Continuous plant populations distributed along such gradients are an interesting system to study intrapopulation divergence at highly local scales. This study tested (1) whether conspecific populations growing in different habitats diverge at functional traits, and (2) whether they diverge in the same way as congeneric species having different habitat preferences.
Methods
Phenotypic differentiation was studied within continuous populations occupying different habitats for two congeneric, sympatric, and ecologically divergent tree species (Eperua falcata and E. grandiflora, Fabaceae). Over 3000 seeds collected from three habitats were germinated and grown in a common garden experiment, and 23 morphological, biomass, resource allocation and physiological traits were measured.
Key Results
In both species, seedling populations native of different habitats displayed phenotypic divergence for several traits (including seedling growth, biomass allocation, leaf chemistry, photosynthesis and carbon isotope composition). This may occur through heritable genetic variation or other maternally inherited effects. For a sub-set of traits, the intraspecific divergence associated with environmental variation coincided with interspecific divergence.
Conclusions
The results indicate that mother trees from different habitats transmit divergent trait values to their progeny, and suggest that local environmental variation selects for different trait optima even at a very local spatial scale. Traits for which differentiation within species follows the same pattern as differentiation between species indicate that the same ecological processes underlie intra- and interspecific variation.
doi:10.1093/aob/mct176
PMCID: PMC3783240  PMID: 24023042
Eperua falcata; E. grandiflora; habitat mosaics; intrapopulation divergence; maternal family inheritance; common garden experiment; ecological traits
21.  The role of carbohydrates in seed germination and seedling establishment of Himatanthus sucuuba, an Amazonian tree with populations adapted to flooded and non-flooded conditions 
Annals of Botany  2009;104(6):1111-1119.
Background and Aims
In the Amazonian floodplains plants withstand annual periods of flooding which can last 7 months. Under these conditions seedlings remain submerged in the dark for long periods since light penetration in the water is limited. Himatanthus sucuuba is a tree species found in the ‘várzea’ (VZ) floodplains and adjacent non-flooded ‘terra-firme’ (TF) forests. Biochemical traits which enhance flood tolerance and colonization success of H. sucuuba in periodically flooded environments were investigated.
Methods
Storage carbohydrates of seeds of VZ and TF populations were extracted and analysed by HPAEC/PAD. Starch was analysed by enzyme (glucoamylase) degradation followed by quantification of glucose oxidase. Carbohydrate composition of roots of VZ and TF seedlings was studied after experimental exposure to a 15-d period of submersion in light versus darkness.
Key Results
The endosperm contains a large proportion of the seed reserves, raffinose being the main non-structural carbohydrate. Around 93 % of the cell wall storage polysaccharides (percentage dry weight basis) in the endosperm of VZ seeds was composed of mannose, while soluble sugars accounted for 2·5%. In contrast, 74 % of the endosperm in TF seeds was composed of galactomannans, while 22 % of the endosperm was soluble sugars. This suggested a larger carbohydrate allocation to germination in TF populations whereas VZ populations allocate comparatively more to carbohydrates mobilized during seedling development. The concentration of root non-structural carbohydrates in non-flooded seedlings strongly decreased after a 15-d period of darkness, whereas flooded seedlings were less affected. These effects were more pronounced in TF seedlings, which showed significantly lower root non-structural carbohydrate concentrations.
Conclusions
There seem to be metabolic adjustments in VZ but not TF seedlings that lead to adaptation to the combined stresses of darkness and flooding. This seems to be important for the survival of the species in these contrasting environments, leading these populations to different directions during evolution.
doi:10.1093/aob/mcp212
PMCID: PMC2766203  PMID: 19770164
Carbohydrate reserves; Himatanthus sucuuba; submergence tolerance; floodplains; galactomannans; raffinose; population differentiation; Amazon; storage
22.  Temperature Requirements for Seed Germination and Seedling Development Determine Timing of Seedling Emergence of Three Monocotyledonous Temperate Forest Spring Geophytes 
Annals of Botany  2008;102(5):865-875.
Background and Aims
The optimal period for seedling emergence depends on factors such as habitat preference, life cycle and geographical distribution. This research was performed to clarify the role of temperature in regulating processes leading to seedling emergence of the European continental Scilla bifolia and the Atlantic Narcissus pseudonarcissus and Hyacinthoides non-scripta.
Methods
Experiments in natural conditions were performed to examine the phenology of embryo growth, seed germination in the soil and seedling emergence. Effects of temperature conditions on embryo growth, seed germination, seedling growth and leaf formation were studied in temperature-controlled incubators.
Key Results
In nature, embryo growth of all three species was initiated from the moment the seeds were dispersed in spring and continued during summer. A sequence of high temperature followed by a lower temperature was required to complete embryo growth and initiate germination. Seeds of H. non-scripta and N. pseudonarcissus germinated in autumn once they attained the critical E:S ratio, while seeds of S. bifolia started germinating when temperatures were low in winter. Seedlings developed normally, but slowly, only when placed in low temperature conditions (5 or 10 °C), resulting in a time lag between the moment of radicle protrusion and seedling emergence in the field.
Conclusions
A continuous development of the embryo and seedlings of the three species was observed from the moment the seeds were dispersed until seedlings emerged. A sequence of high summer temperatures followed by decreasing autumn and winter temperatures was required for all developmental processes to be completed. Although a time lag occurs between radicle protrusion and seedling emergence, the term ‘epicotyl dormancy’ does not apply here, due to the absence of a period of developmental arrest. Timing of first seedling emergence differed between the three species and could be related to differences in geographical distribution.
doi:10.1093/aob/mcn165
PMCID: PMC2712388  PMID: 18757880
Hyacinthoides non-scripta; Scilla bifolia; Narcissus pseudonarcissus; germination; E:S ratio; epicotyl dormancy; seedling development; monocotyledon; geophytes
23.  Comparison of QTL Controlling Seedling Vigour under Different Temperature Conditions Using Recombinant Inbred Lines in Rice (Oryza sativa) 
Annals of Botany  2004;95(3):423-429.
• Background and Aims Seedling vigour is one of the major determinants for stable stand establishment in rice (Oryza sativa), especially in a direct seeding cropping system. The objectives of this study were to identify superior alleles with consistent effects on seedling vigour across different temperature conditions and to investigate genotype × environmental temperature interactions for seedling vigour QTL.
• Methods A set of 282 F13 recombinant inbred lines (RILs) derived from a rice cross were assessed for four seedling vigour traits at three temperatures (25 °C, 20 °C and 15 °C). Using a linkage map with 198 marker loci, the main-effect QTL for the traits were mapped by composite interval mapping.
• Key Results A total of 34 QTL for the four seedling vigour traits were identified. Of these QTL, the majority (82 %) were clustered within five genomic regions, designated as QTL qSV-3-1, qSV-3-2, qSV-5, qSV-8-1 and qSV-8-2. All of these five QTL had small individual effects on the traits, explaining 3·1–15·8 % of the phenotypic variation with a mean of 7·3 %. QTL qSV-3-1, qSV-3-2 and qSV-8-1 showed almost consistent effects on the traits across all three temperatures while qSV-5 and qSV-8-2 had effects mainly at the ‘normal’ temperatures of 20 °C and 25 °C. Among the five QTL identified, all and four showed additive effects on shoot length and germination rate, respectively. The contributions of these five QTL to shoot length and germination rate were also much larger than those to the other two traits.
• Conclusions A few of genomic regions (or QTL) were identified as showing effects on seedling vigour. For these QTL, significant genotype × environmental temperature interactions were found and these interactions appeared to be QTL-specific. Among the four seedling vigour traits measured, shoot length and germination rate could be used as relatively good indicators to evaluate the level of seedling vigour in rice.
doi:10.1093/aob/mci039
PMCID: PMC4246786  PMID: 15574482
Rice (Oryza sativa L.); recombinant inbred line (RIL); seedling vigour; paper-roll tests; quantitative trait loci (QTL); genotype × environment interaction
24.  Reproductive Characteristics of a Populus euphratica Population and Prospects for Its Restoration in China 
PLoS ONE  2012;7(7):e39121.
Populus euphratica is a dominant tree in riparian ecosystems in arid areas of northwest China, but it fails to regenerate in these systems. This study evaluates causes for the failure of sexual and asexual regeneration of this species in the wild. P. euphratica disperses as many as 85743 seeds/m2 during summer, and the seeds germinate to 92.0% in distilled water and to 60.8% on silt. However, very few seeds (3.6%) can germinate on unflooded soil. The seed-rain season is prolonged by temporal variability in seed dispersal among individuals, which ensures that seedling emergence can occur during favorable conditions (i.e., floods and rainfall). As a result of water shortage and river channeling due to water usage and altered river flows, there are no safe sites on river banks for seed germination, which has led to the failure of P. euphratica to regenerate from seed. Root suckers of P. euphratica were present in 86% of the forest gaps investigated. However, extensive grazing has destroyed many of them and thus has reduced this form of regeneration. This research suggests that human activities are resulting in the failure of P. euphratica to regenerate. Changes in land management such as reduced use of concrete canals in Populus forests and/or reduced sheep grazing in these areas may promote their regeneration.
doi:10.1371/journal.pone.0039121
PMCID: PMC3406061  PMID: 22848351
25.  Bushmeat hunting changes regeneration of African rainforests 
To assess ecological consequences of bushmeat hunting in African lowland rainforests, we compared paired sites, with high and low hunting pressure, in three areas of southeastern Nigeria. In hunted sites, populations of important seed dispersers—both small and large primates (including the Cross River gorilla, Gorilla gorilla diehli)—were drastically reduced. Large rodents were more abundant in hunted sites, even though they are hunted. Hunted and protected sites had similar mature tree communities dominated by primate-dispersed species. In protected sites, seedling communities were similar in composition to the mature trees, but in hunted sites species with other dispersal modes dominated among seedlings. Seedlings emerging 1 year after clearing of all vegetation in experimental plots showed a similar pattern to the standing seedlings. This study thus verifies the transforming effects of bushmeat hunting on plant communities of tropical forests and is one of the first studies to do so for the African continent.
doi:10.1098/rspb.2013.0246
PMCID: PMC3619513  PMID: 23516245
bushmeat hunting; seedling community; seed dispersal

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