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1.  Identification and characterization of ten new water gaps in seeds and fruits with physical dormancy and classification of water-gap complexes 
Annals of Botany  2013;112(1):69-84.
Background and Aims
Physical dormancy (PY) occurs in seeds or fruits of 18 angiosperm families and is caused by a water-impermeable palisade cell layer(s) in seed or fruit coats. Prior to germination, the seed or fruit coat of species with PY must become permeable in order to imbibe water. Breaking of PY involves formation of a small opening(s) (water gap) in a morpho-anatomically specialized area in seeds or fruits known as the water-gap complex. Twelve different water-gap regions in seven families have previously been characterized. However, the water-gap regions had not been characterized in Cucurbitaceae; clade Cladrastis of Fabaceae; subfamilies Bombacoideae, Brownlowioideae and Bythnerioideae of Malvaceae; Nelumbonaceae; subfamily Sapindoideae of Sapindaceae; Rhamnaceae; or Surianaceae. The primary aims of this study were to identify and describe the water gaps of these taxa and to classify all the known water-gap regions based on their morpho-anatomical features.
Methods
Physical dormancy in 15 species was broken by exposing seeds or fruits to wet or dry heat under laboratory conditions. Water-gap regions of fruits and seeds were identified and characterized by use of microtome sectioning, light microscopy, scanning electron microscopy, dye tracking and blocking experiments.
Key Results
Ten new water-gap regions were identified in seven different families, and two previously hypothesized regions were confirmed. Water-gap complexes consist of (1) an opening that forms after PY is broken; (2) a specialized structure that occludes the gap; and (3) associated specialized tissues. In some species, more than one opening is involved in the initial imbibition of water.
Conclusions
Based on morpho-anatomical features, three basic water-gap complexes (Types-I, -II and -III) were identified in species with PY in 16 families. Depending on the number of openings involved in initial imbibition, the water-gap complexes were sub-divided into simple and compound. The proposed classification system enables understanding of the relationships between the water-gap complexes of taxonomically unrelated species with PY.
doi:10.1093/aob/mct094
PMCID: PMC3690985  PMID: 23649182
Chalaza; dye tracking; fruit coat; hilum; micropyle; palisade cells; physical dormancy; PY breaking; seed coat; water-gap complex
2.  Quantitative analysis of the thermal requirements for stepwise physical dormancy-break in seeds of the winter annual Geranium carolinianum (Geraniaceae) 
Annals of Botany  2013;111(5):849-858.
Background and Aims
Physical dormancy (PY)-break in some annual plant species is a two-step process controlled by two different temperature and/or moisture regimes. The thermal time model has been used to quantify PY-break in several species of Fabaceae, but not to describe stepwise PY-break. The primary aims of this study were to quantify the thermal requirement for sensitivity induction by developing a thermal time model and to propose a mechanism for stepwise PY-breaking in the winter annual Geranium carolinianum.
Methods
Seeds of G. carolinianum were stored under dry conditions at different constant and alternating temperatures to induce sensitivity (step I). Sensitivity induction was analysed based on the thermal time approach using the Gompertz function. The effect of temperature on step II was studied by incubating sensitive seeds at low temperatures. Scanning electron microscopy, penetrometer techniques, and different humidity levels and temperatures were used to explain the mechanism of stepwise PY-break.
Key Results
The base temperature (Tb) for sensitivity induction was 17·2 °C and constant for all seed fractions of the population. Thermal time for sensitivity induction during step I in the PY-breaking process agreed with the three-parameter Gompertz model. Step II (PY-break) did not agree with the thermal time concept. Q10 values for the rate of sensitivity induction and PY-break were between 2·0 and 3·5 and between 0·02 and 0·1, respectively. The force required to separate the water gap palisade layer from the sub-palisade layer was significantly reduced after sensitivity induction.
Conclusions
Step I and step II in PY-breaking of G. carolinianum are controlled by chemical and physical processes, respectively. This study indicates the feasibility of applying the developed thermal time model to predict or manipulate sensitivity induction in seeds with two-step PY-breaking processes. The model is the first and most detailed one yet developed for sensitivity induction in PY-break.
doi:10.1093/aob/mct046
PMCID: PMC3631331  PMID: 23456728
Geraniaceae; Geranium carolinianum; physical dormancy-break; PY-breaking mechanism; sensitivity induction; stepwise PY-break; thermal time model; winter annual
3.  The autumn effect: timing of physical dormancy break in seeds of two winter annual species of Geraniaceae by a stepwise process 
Annals of Botany  2012;110(3):637-651.
Background and Aims
The involvement of two steps in the physical dormancy (PY)-breaking process previously has been demonstrated in seeds of Fabaceae and Convolvulaceae. Even though there is a claim for a moisture-controlled stepwise PY-breaking in some species of Geraniaceae, no study has evaluated the role of temperature in the PY-breaking process in this family. The aim of this study was to determine whether a temperature-controlled stepwise PY-breaking process occurs in seeds of the winter annuals Geranium carolinianum and G. dissectum.
Methods
Seeds of G. carolinianum and G. dissectum were stored under different temperature regimes to test the effect of storage temperature on PY-break. The role of temperature and moisture regimes in regulating PY-break was investigated by treatments simulating natural conditions. Greenhouse (non-heated) experiments on seed germination and burial experiments (outdoors) were carried out to determine the PY-breaking behaviour in the natural habitat.
Key Results
Irrespective of moisture conditions, sensitivity to the PY-breaking step in seeds of G. carolinianum was induced at temperatures ≥20 °C, and exposure to temperatures ≤20 °C made the sensitive seeds permeable. Sensitivity of seeds increased with time. In G. dissectum, PY-break occurred at temperatures ≥20 °C in a single step under constant wet or dry conditions and in two steps under alternate wet–dry conditions if seeds were initially kept wet.
Conclusions
Timing of seed germination with the onset of autumn can be explained by PY-breaking processes involving (a) two temperature-dependent steps in G. carolinianum and (b) one or two moisture-dependent step(s) along with the inability to germinate under high temperatures in G. dissectum. Geraniaceae is the third of 18 families with PY in which a two-step PY-breaking process has been demonstrated.
doi:10.1093/aob/mcs122
PMCID: PMC3400450  PMID: 22684684
Geraniaceae; Geranium; physical dormancy; stepwise process; the autumn effect;  timing of PY-break; two-step model; winter annual
4.  Acquisition of physical dormancy and ontogeny of the micropyle–water-gap complex in developing seeds of Geranium carolinianum (Geraniaceae) 
Annals of Botany  2011;108(1):51-64.
Background and Aims
The ‘hinged valve gap’ has been previously identified as the initial site of water entry (i.e. water gap) in physically dormant (PY) seeds of Geranium carolinianum (Geraniaceae). However, neither the ontogeny of the hinged valve gap nor acquisition of PY by seeds of Geraniaceae has been studied previously. The aims of the present study were to investigate the physiological events related to acquisition of PY and the ontogeny of the hinged valve gap and seed coat of G. carolinianum.
Methods
Seeds of G. carolinianum were studied from the ovule stage until dispersal. The developmental stages of acquisition of germinability, physiological maturity and PY were determined by seed measurement, germination and imbibition experiments using intact seeds and isolated embryos of both fresh and slow-dried seeds. Ontogeny of the seed coat and water gap was studied using light microscopy.
Key Results
Developing seeds achieved germinability, physiological maturity and PY on days 9, 14 and 20 after pollination (DAP), respectively. The critical moisture content of seeds on acquisition of PY was 11 %. Slow-drying caused the stage of acquisition of PY to shift from 20 to 13 DAP. Greater extent of cell division and differentiation at the micropyle, water gap and chalaza than at the rest of the seed coat resulted in particular anatomical features. Palisade and subpalisade cells of varying forms developed in these sites. A clear demarcation between the water gap and micropyle is not evident due to their close proximity.
Conclusions
Acquisition of PY in seeds of G. carolinianum occurs after physiological maturity and is triggered by maturation drying. The micropyle and water gap cannot be considered as two separate entities, and thus it is more appropriate to consider them together as a ‘micropyle–water-gap complex’.
doi:10.1093/aob/mcr103
PMCID: PMC3119614  PMID: 21546433
Chalaza; maturation drying; micropyle; ontogeny; palisade cells; physical dormancy; physiological maturity; seed coat; water gap; Geranium carolinianum
5.  Identification and characterization of the water gap in physically dormant seeds of Geraniaceae, with special reference to Geranium carolinianum 
Annals of Botany  2010;105(6):977-990.
Background and Aims
Physical dormancy in seeds of species of Geraniaceae is caused by a water-impermeable palisade layer in the outer integument of the seed coat and a closed chalaza. The chalazal cleft has been reported to be the water gap (i.e. location of initial water entry) in innately permeable seeds of Geraniaceae. The primary aim of this study was to re-evaluate the location of the water gap and to characterize its morphology and anatomy in physically dormant seeds of Geraniaceae, with particular reference to G. carolinianum.
Methods
Length, width, mass, anatomy and germination of two seed types (light brown and dark brown) of G. carolinianum were compared. Location, anatomy and morphology of the water gap were characterized using free-hand and microtome tissue sectioning, light microscopy, scanning electron microscopy, dye tracking, blocking and seed-burial experiments.
Key Results
Treatment with dry heat caused a colour change in the palisade cells adjacent to the micropyle. When placed in water, the ‘hinged valve’ (blister) erupted at the site of the colour change, exposing the water gap. The morphology and anatomy in the water-gap region differs from those of the rest of the seed coat. The morphology of the seed coat of the water-gap region is similar in G. carolinianum, G. columbinum, G. molle and G. pusillum and differs from that of the closely related species Erodium cicutarium.
Conclusions
Dislodgment of swollen ‘hinged valve’ palisade cells adjacent to the micropyle caused the water gap to open in physically dormant seeds of G. carolinianum, and it was clear that initial water uptake takes place through this gap and not via the chalazal opening as previously reported. This water gap (‘hinged valve gap’) differs from water gaps previously described for other families in morphology, anatomy and location in the seed coat.
doi:10.1093/aob/mcq078
PMCID: PMC2876017  PMID: 20400757
Erodium; Geraniaceae; Geranium; physical dormancy; seed-coat anatomy; seed burial; seed germination; water gap
6.  Identification and characterization of the water gap in the physically dormant seeds of Dodonaea petiolaris: a first report for Sapindaceae 
Annals of Botany  2009;104(5):833-844.
Background and Aims
The Sapindaceae is one of 17 plant families in which seed dormancy is caused by a water-impermeable seed or fruit coat (physical dormancy, PY). However, until now the water gap in Sapindaceae had not been identified. The primary aim of this study was to identify the water gap in Dodonaea petiolaris (Sapindaceae) seeds and to describe its basic morphology and anatomy.
Methods
Seed fill, viability, water-uptake (imbibition) and other characteristics were assessed for D. petiolaris seeds. The location and structure of the water gap were investigated using a blocking experiment, time series photography, scanning electron microscopy and light microscopy. Dodonaea petiolaris seeds with PY also were assessed for loss of PY at four ecologically significant temperatures under moist and dry conditions. Seeds of three other species of Sapindaceae were examined for presence of a water gap.
Key Results
The water gap in D. petiolaris seeds was identified as a small plug in the seed coat adjacent to the hilum and opposite the area where the radicle emerges. The plug was dislodged (i.e. water gap opened = dormancy break) by dipping seeds in boiling water for 2·5 min or by incubating seeds on a moist substrate at 20/35 °C for 24 weeks. Layers of cells in the plug, including palisade and subpalisade, are similar to those in the rest of the seed coat. The same kind of water gap was found in three other species of Sapindaceae, Diplopeltis huegelii, Distichostemon hispidulus and Dodonaea aptera.
Conclusions
Following dormancy break (opening of water gap), initial uptake of water by the seed occurs only through the water gap. Thus, the plug must be dislodged before the otherwise intact seed can germinate. The anatomy of the plug is similar to water gaps in some of the other plant families with PY.
doi:10.1093/aob/mcp171
PMCID: PMC2749536  PMID: 19620135
Dodonaea petiolaris; physical dormancy; Sapindaceae; seed ecology; seed germination; water gap
7.  Occurrence of Physical Dormancy in Seeds of Australian Sapindaceae: A Survey of 14 Species in Nine Genera 
Annals of Botany  2008;101(9):1349-1362.
Background and Aims
Sapindaceae is one of 16 angiosperm families whose seeds have physical dormancy (PY). However, the extent and nature of PY within this family is poorly known. The primary aims of this study were: (1) to evaluate seed characteristics and determine presence (or not) of PY within nine genera of Australian Sapindaceae; and (2) to compare the frequency of PY across the phylogenetic tree within Australian Sapindaceae.
Methods
Viability, imbibition and seed characteristics were assessed for 14 taxa from nine genera of Sapindaceae. For five species of Dodonaea, optimal conditions for germination and dormancy break were evaluated. An in situ burial experiment was performed on D. hackettiana seeds to identify the factor(s) responsible for overcoming PY. Classes of dormancy and of non-dormancy for 26 genera of Sapindaceae were mapped onto a phylogenetic tree for the family.
Key Results
Mean seed viability across all taxa was 69·7 %. Embryos were fully developed and folded (seven genera) or bent (two genera); no endosperm was present. Seeds of all five Dodonaea spp. and of Distichostemon hispidulus had PY. Hot-water treatment released PY in these six species. Optimal germination temperature for seeds of the four Dodonaea spp. that germinated was 15–20 °C. Following 5 months burial in soil, 36·4 % of D. hackettiana seeds had lost PY and germinated by the beginning of the winter wet season (May). Laboratory and field data indicate that dormancy was broken by warm, moist temperatures (≥50 °C) during summer.
Conclusions
PY occurs infrequently in genera of Sapindaceae native to Australia. Seeds of Dodonaea and Distichostemon had PY, whereas those of the other seven genera did not. Seeds of these two genera and of Diplopeltis (a previous study) are the only three of the 20 native Australian genera of Sapindaceae for which germination has been studied that have PY; all three belong to subfamily Dodonaeoideae.
doi:10.1093/aob/mcn043
PMCID: PMC2710253  PMID: 18369237
Dodonaea spp.; physical dormancy; Sapindaceae; seed ecology; seed germination
8.  Cycling of Sensitivity to Physical Dormancy-break in Seeds of Ipomoea lacunosa (Convolvulaceae) and Ecological Significance 
Annals of Botany  2007;101(3):341-352.
Background and Aims
Although a claim has been made that dormancy cycling occurs in seeds of Ipomoea lacunosa (Convolvulaceae) with physical dormancy, this would seem to be impossible since the water gap cannot be closed again after it opens (dormancy break). On the other hand, changes in sensitivity (sensitive ↔ non-sensitive) to dormancy-breaking factors have been reported in seeds of Fabaceae with physical dormancy. The primary aim of the present study was to determine if sensitivity cycling also occurs in physically dormant seeds of I. lacunosa.
Methods
Treatments simulating conditions in the natural habitat of I. lacunosa were used to break seed dormancy. Storage of seeds at temperatures simulating those in spring, summer, autumn and winter were tested for their effect on sensitivity change. Seeds made non-dormant were stored dry in different temperature regimes to test for dormancy cycling. In addition, seeds collected on different dates (i.e. matured under different climatic conditions) were used to test for maternal effects on sensitivity to dormancy-breaking factors.
Key Results
Sensitivity was induced by storing seeds under wet conditions and reversed by storing them under dry conditions at low (≤5 °C) or high (≥30 °C) temperatures, demonstrating that seeds of I. lacunosa can cycle between sensitive and insensitive states. Sensitive seeds required ≥2 h at 35 °C on moist sand for release of dormancy. However, there is no evidence to support dormancy cycling per se. Conceptual models are proposed for sensitivity cycling and germination phenology of I. lacunosa in the field.
Conclusions
Seasonal germination behaviour of physically dormant I. lacunosa seeds can be explained by sensitivity cycling but not by dormancy cycling per se. Convolvulaceae is only the second of 16 families known to contain species with physical dormancy for which sensitivity cycling has been demonstrated.
doi:10.1093/aob/mcm285
PMCID: PMC2701819  PMID: 18032427
Convolvulaceae; germination phenology; Ipomoea; physical dormancy; sensitivity cycling
9.  Seed Anatomy and Water Uptake in Relation to Seed Dormancy in Opuntia tomentosa (Cactaceae, Opuntioideae) 
Annals of Botany  2007;99(4):581-592.
Background and Aims
There is considerable confusion in the literature concerning impermeability of seeds with ‘hard’ seed coats, because the ability to take up (imbibe) water has not been tested in most of them. Seeds of Opuntia tomentosa were reported recently to have a water-impermeable seed coat sensu lato (i.e. physical dormancy), in combination with physiological dormancy. However, physical dormancy is not known to occur in Cactaceae. Therefore, the aim of this study was to determine if seeds of O. tomentosa are water-permeable or water-impermeable, i.e. if they have physical dormancy.
Methods
The micromorphology of the seed coat and associated structures were characterized by SEM and light microscopy. Permeability of the seed-covering layers was assessed by an increase in mass of seeds on a wet substrate and by dye-tracking and uptake of tritiated water by intact versus scarified seeds.
Key Results
A germination valve and a water channel are formed in the hilum–micropyle region during dehydration and ageing in seeds of O. tomentosa. The funicular envelope undoubtedly plays a role in germination of Opuntia seeds via restriction of water uptake and mechanical resistance to expansion of the embryo. However, seeds do not exhibit any of three features characteristic of those with physical dormancy. Thus, they do not have a water-impermeable layer(s) of palisade cells (macrosclereids) or a water gap sensu stricto and they imbibe water without the seed coat being disrupted.
Conclusions
Although dormancy in seeds of this species can be broken by scarification, they have physiological dormancy only. Further, based on information in the literature, it is concluded that it is unlikely that any species of Opuntia has physical dormancy. This is the first integrative study of the anatomy, dynamics of water uptake and dormancy in seeds of Cactaceae subfamily Opuntioideae.
doi:10.1093/aob/mcm001
PMCID: PMC2802935  PMID: 17298989
México Valley; Opuntia tomentosa; physical dormancy, physiological dormancy; seed anatomy; seed germination; water uptake by seeds

Results 1-9 (9)