View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector South African Journal of Botany 2003, 69(4): 455–461 Copyright © NISC Pty Ltd Printed in South Africa — All rights reserved SOUTH AFRICAN JOURNAL OF BOTANY EISSN 1727–9321 Minireview Thermoinhibition of seed germination PN Hills and J van Staden* Research Centre for Plant Growth and Development, School of Botany and Zoology, University of Natal Pietermaritzburg, Private Bag X01, Scottsville 3209, South Africa * Corresponding author, e-mail: [email protected] Received 21 August 2003, accepted in revised form 25 August 2003 Thermoinhibition describes the inability of seeds to ger- perature induced changes to the structures enclosing minate at high temperatures, although germination pro- the embryo which prevent radicle emergence, to the ceeds immediately when the temperature is reduced interaction of a number of different factors, and probable below a certain threshold level. This phenomenon is expression of certain genes inhibitory to germination distinct from thermodormancy, where some form of dor- which may be temperature regulated. Thermoinhibition mancy-breaking treatment is required before germina- occurs in a large number of important crop species, so tion can proceed at the favourable temperature. Like that an understanding of this phenomenon is both of seed dormancy, thermoinhibition is manifested in a scientific interest and practical importance. number of different ways, ranging from simple high-tem- Introduction Temperature strongly influences both physiological and bio- Mayber 1975). These temperatures may be considerably chemical processes, including those occurring in germinat- modified by several other factors, such as exposure to light ing seeds. In the field, temperature acts to regulate germi- of different wavelengths or the application of different com- nation in three main ways (Bewley and Black 1986). Firstly, pounds, including phytohormones such as ethylene, it may be involved in the removal of either primary or sec- abscisic acid (ABA) and gibberellins. ondary dormancy. Secondly, temperatures outside of the Within the temperature range of a species, the rate of ger- normal limits for germination may cause the establishment mination usually increases as the temperature rises, of secondary dormancy in a seed when conditions are not although the final percentage germination may decline favourable for seedling establishment. Finally, the tempera- (Heydecker 1977). However, as the temperature approach- ture at which seeds are incubated determines their capacity es the maximum for germination, the germination rate for germination and the rate at which this occurs. begins to slow (Heydecker 1977). Variations in the rates of Each species has a range of temperatures over which ger- germination of different seeds ensure that the seeds in a mination may proceed and within which seedling establish- population germinate at different times, thereby leading to ment is possible (Bradbeer 1988). There are three cardinal the temporal dispersal of germination (Bewley and Black temperatures for germination, namely the maximum, mini- 1986). In wild populations this is a distinct advantage. mum and optimum germination temperatures (Bewley and However, it is disadvantageous in a field crop where unifor- Black 1982). The maximum and minimum temperatures rep- mity is an important consideration. resent the extremes of the range of temperatures over which In the environment, temperatures greater than the maxi- the seed is able to germinate. The optimum germination mum favourable temperature for germination will result in temperature may be defined as that temperature at which the suspension of germination. At these supra-optimal tem- the highest percentage germination may be obtained in the peratures, seeds may enter into a state of either thermodor- shortest possible period of time (Mayer and Poljakoff- mancy or thermoinhibition. It is important that a distinction Mayber 1975). These temperatures vary considerably be made between these two phenomena. In thermodormant between species, but may also vary between cultivars of the seeds, a state of secondary dormancy is induced by expo- same species (Bewley and Black 1982) and are thus deter- sure to the elevated temperature, which must then be mined by the source of the seeds, genetic differences with- released by some form of dormancy-breaking treatment in a species and the age of the seed (Mayer and Poljakoff- before the seeds are able to germinate again at their optimal 456 Hills and Van Staden temperature (Vidaver and Hsiao 1975). Seeds are said to be does exist between these different factors in the various thermoinhibited where they fail to germinate at a high tem- species or genotypes that eventually results in the seed perature, but where germination proceeds immediately upon becoming thermoinhibited, for the purposes of this review, transfer to a temperature suitable for germination of seeds of each potential factor which has been proposed as playing a that species (Horowitz and Taylorson 1983). In both ther- role in thermoinhibition will, as far as possible, be dealt with modormant and thermoinhibited seeds, if the temperature is separately. too high or is maintained for an extended period, thermal death will result (Horowitz and Taylorson 1983). In certain Involvement of the embryo coverings circumstances, however, this distinction is hard to make and terminology has been a problem in the study of thermoinhi- In many species, seed dormancy is imposed by the struc- bition. Many authors, particularly in earlier papers, refer to tures surrounding the embryo, including the endosperm, thermodormant seeds, when the seeds in fact appear to be perisperm, pericarp and testa (Bewley and Black 1982). thermoinhibited. Vidaver and Hsiao (1975) stated: These structures may impose dormancy through a number ‘Secondary dormancy is a distinctly different condition from of mechanisms, including mechanical restraint on embryo so-called thermodormancy in these seeds. The term ther- extension, the establishment of permeability barriers inter- moinhibition should probably be substituted for thermodor- fering with water uptake, gaseous exchange or the outward mancy since seeds which have not yet become dormant will diffusion of endogenous germination inhibitors. Similar germinate merely by lowering the temperature.’ This is a mechanisms may also be associated with thermoinhibition in particular problem in lettuce seed studies. The threshold some species. temperature at which lettuce seeds fail to germinate varies In the legume Lathyrus sativus, supra-optimal tempera- between different cultivars, with some genotypes becoming tures increase hardseededness, preventing seed hydration inhibited at temperatures as low as 25°C (Nascimento et al. and germination (Agrawal et al. 1980). In spinach (Spinacia 2001). When this threshold temperature is exceeded during oleracea) seeds, germination is inhibited at temperatures in imbibition, seeds become thermoinhibited. However, if this excess of 30°C (Leskovar et al. 1999). At this temperature, supra-optimal temperature is maintained for more than the pericarp appears to act as a physical barrier to germina- approximately 72h, the seeds enter into a state of ther- tion as well as a source of inhibitory compounds (Leskovar modormancy, such that these seeds will then fail to germi- et al. 1999). Complete removal of the pericarp was able to nate even when the temperature is reduced below the overcome thermoinhibition at 30°C, however, placing the inhibitory threshold. A similar situation appears to occur in pericarp near the embryos had a slight inhibitory effect, celery seeds, in which seeds that do not germinate at high which was more pronounced if the embryos were re-insert- temperatures will germinate when transferred to a lower ed into the excised pericarps (Leskovar et al. 1999). temperature. The longer the seeds are incubated at the The integuments of apple seeds are rich in phenolic com- supra-optimal temperature, the longer they appear to take to pounds that fix oxygen through oxidation, thereby lowering germinate when the temperature is reduced (Biddington and the levels of oxygen available to the embryo (Côme and Thomas 1978). It is therefore important to examine the actu- Tissaoui 1973). When the seeds are imbibed at high tem- al germination curves of the various seed lots used in the lit- peratures the embryo’s requirement for oxygen is increased erature to determine whether the seeds used were in fact as a result of an increase in the metabolic rate. The amount thermodormant or thermoinhibited. of oxygen available to the embryo is, however, decreased as Observations of temperature effects on the germination of oxidation of phenolics rises and oxygen becomes less solu- seeds of a number of different species have led to the for- ble in the water in the seed coat and germination is conse- mulation of a number of hypotheses concerning the basis of quently inhibited (Côme and Tissaoui 1973). Hypoxic condi- thermoinhibition in those species. An analysis of the avail- tions imposed by the seed coat at supra-optimal tempera- able literature reveals that there appears to be a variety of tures may have a different effect in seeds that require ethyl- possible mechanisms resulting in the arrest of germination. ene for germination. Since the ethylene-forming enzyme The situation is made more confusing by the fact that there (ACC oxidase)