WORKSHOP Impact of Temperature on Robert L. Geneve1 Department of Horticulture, University of Kentucky, Lexington, KY 40546

Additional index words. , scarification, stratification, embryo, after-ripening, thermodormancy

Seed dormancy is an ecological adaptation mancy, endogenous dormancy, and combina- are disrupted by temperature and become the that allows seasonal timing of germination for tion dormancy. Secondary dormancy includes site of water entry into the seed. For example, in a population. Several environmental thermodormancy and conditional dormancy. Quinlivan (1968) demonstrated that seeds of stimuli can trigger dormancy release, the most These types of dormancy and the require- Lupinus varius L. became permeable to water important being seed moisture content, light ments to overcome them are listed in Table 1. at the lens after exposure to fluctuating tem- and temperature. Of these, temperature is argu- Detailed descriptions of these categories can perature (i.e., 65 °C day temperatures with ably the most important. The objective of this be found elsewhere (Baskin and Baskin, 1998; night temperatures down to 25 °C). brief review is to consider the various ways Geneve, 1998; Hartmann et al., 2002). In this temperature impacts seed dormancy release. It review, I will limit each category to a brief Primary endogenous dormancy will cover general aspects of seed dormancy, description and emphasize dormancy condi- temperature effects on primary dormancy and tions that are affected by temperature. The second major category of primary seed considerations for conducting and interpreting dormancy is endogenous seed dormancy. Seeds seed dormancy research. Primary exogenous dormancy with endogenous dormancy fail to germinate Propagators of cultivated plants have because of factors associated with the embryo. long recognized that germination-delaying In exogenous dormancy, the tissues enclos- There are two types of endogenous dormancy mechanisms exist in seeds. The first recorded ing the embryo impact germination by either —morphological and physiological.

discussion of seed dormancy was written by inhibiting water uptake, modifying gas (O2) Morphological dormancy. Seeds with Theophrastus in §300 B.C. (Evenari, 1981). exchange, or possibly contain germination morphological dormancy have an embryo He recognized that germination of most seeds inhibitors (Bewley and Black, 1994). that is not fully developed at the time of seed declined during storage (seed deterioration), Seeds of species with exogenous physical dissemination. Seeds where the embryo fills while germination in some seeds increased dormancy fail to imbibe water because of less than half of the seed are considered to (dormancy release). properties of the seed coverings. This form of have morphological dormancy (Baskin and One problem with discussing seed dor- seed dormancy only occurs in 15 plant families Baskin, 1998). Enlargement of the embryo mancy is that there is no single recognized ter- (Baskin et al., 2000). Of these, most of the spe- occurs after the seeds have imbibed water, minology to describe the many different types cies displaying physical dormancy are found in but usually before germination begins. The of seed dormancy. Crocker (1916) described the Malvaceae and . The anatomical process of embryo enlargement is influenced seven types of dormancy based on treatments structures preventing water uptake can be the by temperature. Atwater (1980) distinguished used to overcome them. Subsequently, Niko- seedcoat (testa) or endocarp (Baskin et al., three types of morphological dormancy based laeva (1977) defined dormancy based primarily 2000). In most species, there are elongated on the embryo type found in herbaceous flower upon physiological controls. More recently, palisade cells in the outer layer of the seedcoat crops. These are rudimentary, linear, and undif- Lang (1987) proposed the terms eco-, para-, (exotesta) that prevent imbibition. Mechanical ferentiated embryo types. and endo-dormancy to simplify terminology. abrasion or chemical degradation of the seed Rudimentary embryos are little more than a This system is currently utilized in American coverings and submersion of the seed in hot proembryo embedded in a massive . Society for Horticultural Science journals. water are the most common horticultural prac- These are found in seeds of various families, However, this terminology is not sufficient to tices to induce seeds with physical dormancy such as the Ranunculaceae, Papaveraceae, and adequately describe all the types of dormancy to imbibe water. Collectively, these treatments Araliaceae. Germination-inhibiting chemicals found in seeds. Baskin and Baskin (1998) have are termed scarification. However, in nature, may occur in the endosperm and become active developed the most complete set of terms to it appears that temperature is the major factor at high temperatures. Methods for inducing describe seed dormancy. They have extended determining water uptake in seeds with physi- germination include: (a) exposure to tem- the dormancy classifications of Nikolaeva to cal dormancy. peratures of 15 °C or below; (b) exposure to include additional specialty types. In this re- Temperature impacts dormancy release for alternating temperatures; and (c) treatment view, I will use a system based on the work of seeds with exogenous physical dormancy by with chemicals such as potassium nitrate or Nikolaeva, as modified by Baskin and Baskin affecting the seed coverings. For instance, some gibberellic acid. (Hartmann et al., 2002). It is a classification seeds require high temperature or daily fluctua- Seeds with linear embryos are torpedo- system that I feel fits both the ecological and tions (>15 °C change) in temperature to allow shaped and up to one-half the size of the seed. horticultural aspects of seed dormancy and is imbibition. This requirement is postulated as Important families and species in this category accepted by most of the scientists working in a way for seeds to detect whether they are in include the Apiaceae, Ericaceae, Primulaceae, the field of seed (Table 1). open or protected areas (Baskin and Baskin, and Gentianaceae. Conditions such as semiper- 1998). A higher daily temperature extreme, as meability of the inner seedcoats and internal SEED DORMANCY CATEGORIES well as a greater day/night fluctuation would germination inhibitors may be involved. Tem- occur in an open area, indicating less competi- perature >20 °C favors germination, as does Major categories include primary and sec- tion from other plants after germination. The treatment with gibberellic acid. ondary seed dormancy. Primary dormancy is coverings of seeds with physical dormancy may Some tropical species have seeds with small a condition that exists in the seed as it is shed also be cracked by temperature fluctuations, embryos that require an extended period at from the plant. In contrast, secondary dormancy alternate freezing and thawing and in some warm temperatures for germination to take occurs in seeds that were previously non-dor- species by fire. place. For example, seeds of some palm spe- mant, but have become dormant because the For many seeds with physical dormancy, cies require 1 to 3 months at high temperatures environment was unfavorable for germination. a specialized location on the seed coverings ( 35 °C) to complete germination (Nagao et Primary dormancy, includes exogenous dor- § can act as an “environmental sensor.” In the al., 1980). Other examples include Actinidia Received for publication 4 Apr. 2002. Accepted for Fabaceae, it is usually the lens (strophiole) sp. and Annona squamosa L. whose seeds publication 4 Sept. 2002. Univ. of Kentucky Experi- (Manning and van Staden, 1987; Morrison require 2 or 3 months at warm temperatures, ment Station publication #02-11-27. et al., 1998); and in the Malvaceae, it is the respectively, to complete germination (Niko- 1E-mail address: [email protected] chalazal plug (Egley, 1989). These structures laeva, 1977).

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4-workshop, p333-350 336 6/2/03, 4:04:47 PM Table 1. Seed dormancy categories (Hartmann et al., 2002). Dormancy types Causes of dormancy Conditions to break dormancy Representative genera 1. Primary dormancy a. Exogenous dormancy Imposed by factors outside the embryo Physical Impermeable seedcoat Scarification Baptisia, Convolvulus, Gleditsia, Lupinus Chemical Inhibitors in seed coverings Removal of seed coverings (fruits) Beta, Iris Leaching seeds b. Endogenous dormancy Imposed by factors in the embryo Morphological The embryo is not fully developed Warm or cold stratification at the time theseed sheds from the plant Rudimentary Small undifferentiated embryo Cold stratification and potassium nitrate Anemone, Ranunculus Linear Small differentiated embryo <1/2 size of seed Warm stratification and gibberellic acid Daucus, Cyclamen, Viburnum Physiological Factors within embryo inhibits germination Nondeep Positively photodormant (requires light) Red light Lactuca, Primula Negatively photodormant (inhibited by light) Darkness Cyclamen, Nigella After-ripening Short period of dry storage Cucumis, Impatiens Intermediate Embryo germinates if separated from the seedcoat Moderate periods (up to 8 weeks) of Aconitum, Cornus, Pinus Often responds to gibberellic acid cold stratification Deep Embryo does not germinate when removed from Long periods (>8 weeks) of cold Dictamnus, Euonymus, seedcoat or will form a physiological dwarf stratification Prunus, Rhodotypos c. Combinational Combinations of different dormancy conditions that must be satisfied sequentially Morphophysiological Combination of underdeveloped or rudimentary Cycles of warm and cold stratification Asimina, Helleborus, Ilex, embryo and physiological dormancy Magnolia, Mertensia Epicotyl Radicle begins growth when temperature Warm followed by cold stratification Asarum, Paeonia and water permit, but epicotyl is dormant Epicotyl and radicle Radicle and epicotyl require chilling stratification, Cold stratification followed by warm Convallaria, Trillium (double dormancy) but radicle is released during first year and then followed by a second cold stratification Exo-endodormancy Combinations of exogenous and endogenous Sequential combinations of dormancy Cercis, Tilia dormancy conditions. Example: physical (hard releasing treatments. Example: seedcoat) plus intermediate physiological scarification followed by cold dormancy stratification 2. Secondary dormancy a. Thermodormancy After primary dormancy is relieved, high Growth regulators or cold stratification Apium, Lactuca, temperature induces dormancy b. Conditional dormancy Change in ability to germinate related to time Chilling stratification Many species with endo- of the year genous dormancy display conditional dormancy

Orchid seeds have undifferentiated embryos sp.) seeds were thought to require moist chilling after-ripening time and temperature that was when shed from the mother plant. They are not to permit germination. However, nonchilled consistent within a species. He showed that considered dormant in the same sense as others seeds will germinate in light (Vanhatalo et time on a log scale to reach 50% germination in this category because they lack substantial al., 1996). was linear with temperature. seed storage materials. Freshly harvested seeds of some herbaceous Moist chilling stratification can relieve Physiological dormancy. The second type plants display endogenous, nondeep physi- dormancy in species with nondeep, interme- of endogenous dormancy is physiological ological dormancy (Association of Official diate, or deep physiological dormancy (Fig. dormancy. This type of dormancy involves Seed Analysts, 1993; Atwater, 1980; Baskin 1). It is often difficult to differentiate between physiological changes within the embryo allow and Baskin, 1998). This type of dormancy is seeds that display nondeep vs. intermediate the radicle to escape the restraint of the seed often transitory and disappears during dry physiological dormancy. In general, seeds with coverings. Physiological dormancy includes storage (after-ripening). For most cultivated nondeep dormancy require only short periods nondeep, intermediate, and deep categories. cereals, grasses, vegetables, and flower crops, (days or up to several months) of chilling Endogenous, nondeep, physiological nondeep physiological dormancy may last for stratification to relieve dormancy. Seeds with dormancy is the most common form of seed 1 to 6 months and disappears with dry storage intermediate physiological dormancy usually dormancy (Baskin and Baskin, 1998). This during normal handling procedures (Geneve, require at least 2 months of chilling or gib- type of dormancy can be broken by light 1998). berellin application can substitute for chilling. or darkness (photodormancy), short periods Temperature affects the time required to Embryos isolated from their seed coverings of chilling stratification, or “after-ripening” after-ripen seeds. For example, cultivated cu- in nondeep or intermediate physiologically (dry storage). cumber (Cucumis sativus var. sativus L.) has dormant seeds will germinate promptly and Seeds from species with endogenous, been selected over many years of cultivation produce normal seedlings. In contrast, seeds nondeep, physiological dormancy (especially for a short dormancy period. Freshly harvested with deep physiological dormancy require long small seeded species) often require light or seeds lose dormancy in dry storage at room periods (>3 months) of chilling stratification to darkness for germination. Light sensitivity temperature after several weeks (15 to 30 d). relieve dormancy and generally do not respond in seeds is a phytochrome response (Casal The hardwickii cucumber [Cucumis sativus to exogenous gibberellin application. Embryos and Sánchez, 1998). For some seeds, there var. hardwickii (Royle) Alef.] is considered isolated from these seeds either will not ger- is a distinct light × temperature interaction a wild progenitor species of the cultivated minate or will grow into abnormal seedlings regarding dormancy and germination. A light cucumber and seeds can remain dormant for with a dwarf phenotype, termed physiological requirement can be offset by cool temperatures 60 to 270 d (Weston et al., 1992). Dormancy dwarfs (Flemion and Waterbury, 1945). and sometimes, by alternating temperatures. release occurred much earlier in hardwickii In most cases, seeds with endogenous Seeds of some cultivars of lettuce generally seeds held in dry storage at warmer tempera- physiological dormancy respond in a similar require light to germinate; however, they can tures (180 d at 17 °C compared to only 75 d manner with regard to stratification tempera- germinate in darkness at temperatures below 23 at 37 °C). Roberts (1965) showed that there ture. A temperature near 4 °C has maximum °C (Hadnagy, 1972). For years, birch (Betula was a negative linear relationship between effect, while below freezing temperatures or

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