Unravelling the paradox in physically dormant species: elucidating the onset of dormancy after dispersal and dormancy-cycling

Abstract

Background: For species that produce seeds with a water-impermeable coat, i.e. physical dormancy (PY), it has been widely recognized that (1) seeds shed at a permeable state cannot become impermeable after dispersal; and (2) dormancy-cycling, i.e. a permeable ↔ impermeable transition, does not occur. Given a tight relationship between moisture content and onset of seed-coat impermeability, seeds maturing at low relative humidity (RH) and occurring in a high-temperature environment are inferred to produce impermeable coats, and ex situ drying of permeable seeds can lead to the onset of impermeability.

Scope and conclusion: It is proposed here that permeable seeds dispersed at low RH and in high-temperature soils might become impermeable due to continuous drying. Similarly, seeds with shallow PY dormancy (with higher moisture content immediately after becoming impermeable) can cycle back to a permeable state or absolute PY (complete dry state) when RH increases or decreases, respectively. A conceptual model is developed to propose that seeds from several genera of 19 angiosperm families at the time of natural dispersal can be (1) impermeable (dormant), i.e. primary dormancy; (2) impermeable (dormant) and become permeable (non-dormant) and then enter a dormant state in the soil, often referred to as secondary dormancy; (3) permeable (non-dormant) and become impermeable (dormant) in the soil, i.e. enforced dormancy; or (4) dormant or non-dormant, but cycle between permeable and non-permeable states depending on the soil conditions, i.e. dormancy-cycling, which is different from sensitivity-cycling occurring during dormancy break. It is suggested that this phenomenon could influence the dormancy-breaking pattern, but detailed studies of this are lacking.

Keywords: Impermeable seed coat; primary dormancy; secondary dormancy; sensitivity-cycling; shallow and absolute PY.

Fig. 1.

(A) Fully matured seeds of Albizia julibrissin, and (B) seeds in the early maturation stage of Acacia nilotica dispersed permeable and impermeable seeds before summer. The moisture content of both species at the time of dispersal was 12–15 %, but seeds collected from the soil after 2 weeks of dispersal had a moisture content of ~ 7 %, with no seeds able to absorb water.

Fig. 2.

An overview of events occurring in PY species from fertilization to dispersal. Here, three stages are recognized: (1) seed formation, (2) maturation and (3) maturation drying. The duration of each stage varies with species, and the last dotted arrow (on the right-hand end) shows the appropriate time that seeds become impermeable. Under ecological conditions, the mother plant may disperse the seeds before this point; in that case, the seeds can dry to lower the moisture content in the soil.

Fig. 3.

Conceptual model showing PY seeds dispersed at different levels due to the variation in maternal environment drying seeds to different moisture content. Non-dormant (i.e. permeable) seeds can germinate or dry to lower moisture content based on the environmental relative humidity (RH) and soil moisture content, thus enforcing dormancy. The drying level determines the ability of seeds to either enter shallow PY or absolute PY. Seeds with shallow PY can cycle between non-dormant and absolute PY states depending on the increase or decrease in seed moisture or directly undergo dormancy break. Absolute PY species can only become permeable to water when suitable cues open the water gap in seeds; thus, reversibility to any other states is improbable. Dashed lines with arrows indicate the possibility of dormancy reversal, while solid lines indicate step-wise movement of seeds towards germination.