39. The Hydrotime Concept in Seed Germination andDormancy

K.J. BRADFORDDepartment of Vegetable Crops, University ofCalifornia, Davis, CA 95616-8631, USA

Abstract

The hydrotime concept has been developed to describe the relationship betweenwater potential (Ijf) and seed germination rates. In analogy with thermal time,hydrotime is the accumulated Ijf units (MPa) above a base or threshold value (ljfb)multiplied by the time of imbibition at that Ijf. The germination rate (inverse oftime to radicle emergence) increases linearly as the seed Ijf increases above Ijfb' AsIjfb values vary among individual seeds, the amount by which the Ijf exceeds Ijfb alsovaries among seeds, resulting in the typical right-skewed sigmoid germination timecourses. Factors which influence seed germination kinetics alter the mean Ijfb oftheseed lot, with higher (more positive) values resulting in an inhibition of germina­tion or imposition ofdormancy and lower (more negative) values being associatedwith rapid germination and high vigour. The induction or alleviation ofdormancyinvolves physiological shifts in the Ijfb distribution, allowing a seed population totrack both long-term and short-term environmental conditions to enhanceseedling survival.

Introduction

A key question in germination physiology is how seeds integrate the signalsfrom their environment to determine when to initiate radicle growth andcommit to seedling development. This is a critical 'decision' for seeds, as thelikelihood of seedling survival is dependent upon the subsequent availability ofadequate water, temperature, light and nutrients to support plant growth. Giventhe large numbers of seeds produced bymost species, the selection pressures ofaseasonally predictable but locally chaotic environment, and both genetic andphysiological variation in germination and dormancy characteristics, it is notsurprising that a myriad ofgermination behaviours have evolved that are closelyin tune with their native environments. It may not be possible, therefore, toidentify a single physiological mechanism that can account for all of theexuberant individuality that is expressed in the germination ecology of diversespecies. Nonetheless, it seems likely that water is so essential to successfulseedling establishment that virtually all mesophytic and xerophytic species willhave evolved mechanisms to gauge the water potential or content of theirenvironment and attune their germination physiology to ensure that seedlingsventure forth only if there is a high probability ofadequate water being availablefor their initial establishment.

R.H. Ellis, M. Black, A.I. Murdoch. T.D. Hong (eds.), Basic and Applied Aspects ofSeed Biology, pp. 349-360.© 1997 Kluwer Academic Publishers, Dordrecht.

350 KJ. Bradford

In this paper, the hydrotime concept will be introduced as a unifYing model tounderstand the patterns ofgermination that occur as seed populations enter andleave environmentally induced dormant or inhibited states. As has been pointedout by Gordon (1973), there is a characteristic pattern ofgermination timing asdormancy is lost in a seed population. There is almost always a relationshipbetween the final germination percentage (i.e. the percentage of nondormantseeds) and the time required for radicle emergence to occur in the nondormantfraction. That is, as a dormancy-breaking treatment (afterripening, stratifica­tion, etc.) is extended, not only do additional seeds become capable ofcompleting germination, but seeds which already have this capacity are able tocomplete germination more rapidly. Gordon (1973) proposed that there was a'resistance to germination' that was still present even in 'nondormant' seeds (i.e.seeds that could eventually complete germination) which could be detected byvariation in their germination rates. Thus, one could say that a dormancycontinuum exists on both sides of the germinability divide. Among thenongerminable seeds, this is detectable by the different extents of dormancy­breaking treatments required to allow germination; among the germinableseeds, it is detectable by variation in the time required to complete germination.This paper will focus on describing how the hydrotime model can account forthis general pattern of seed behaviour.

The Hydrotime Concept

The hydrotime concept was first proposed by Gummerson (1986) to account forthe effects of reduced water potential (W) on germination. In analogy withthermal time or degree-days, Gummerson (1986) proposed that the time togermination is related to the magnitude of the difference between the seed orenvironme]:lt wand the water potential threshold for radicle emergence (Wb). Inthermal time, the degrees in excess of a base or threshold temperature (Tb),

multiplied by the time to a developmental event (e.g. radicle emergence) is aconstant. Thus, many biological events can be normalized on a common degree­days time scale once the Tb is determined for the particular process. In the caseof seeds, radicle emergence occurs at different times for different seeds, so thethermal time to germination must be defined for a particular germinationpercentage or fraction in the population (see Bradford, 1995). Interestingly,Gummerson (1986) showed that in the case ofgermination responses to reducedW, the total hydrotime(MPa-days) to radicle emergence was the same for allseeds in the population, but that individual seeds varied in their thresholdWatwhich radicle emergence would be prevented. The following symbolism de­scribes the basis of the hydrotime model (Bradford, 1990):

(1)

where 8H is the hydrotime constant (MPa-days), Wis the actual seed water

The hydrotime concept in seed germination and dormancy 351

Hydrotime =(1/1- I/Ib) x time

= constant MPa-days

Inverse relationship between/ time and water potential (rIJ

,.--... 30(f)>-rou 25............Q)uc

20Q)(J)L-Q)

E 15Q)

Q)

uu 10roL-

a+-J 5Q)

Ef- 0

-1.0 -0.75 -0.50 -0.25 0

Water potential (MPa)Figure 1. Relationship between time to germination and water potential ("'). Assuming a base orthreshold'" ("'b) of-1.0 MPa, the curve shows the inverse relationship between the time to radicleemergenceVg) and'" - "'b. The rectangles illustrate that the same total hydrotime (9H,MPa-days) isrequired for germination in all cases

potential, Wb (g) is the base or threshold water potential defined for a specificgermination fraction g, and tg is the time to radicle emergence of fraction g. IfeH is a constant, then tg must increase proportionately as Wis reduced andapproaches Wb(g). This is illustrated graphically in Figure 1, where the time toradicle emergence (tg) is inversely related to the Wof the seed. According toEquation 1, the rectangles defined by any combination of tg andWenclose equalareas (= eH)' Thus, radicle emergence occurs when a given seed has accumu­lated the hydrotime units characteristic of that seed lot. This will take longer atlowWthan at high W, but the relationship betweenW- Wb (g) and tg conforms tothat shown for all seeds in the population.Equation 1 can be rearranged in the following way to illustrate the relation­ship between germination rates, or the inverse of time to radicle emergence (GRg

=l/tg), and W:

(2)

352 KJ. Bradford

Thus, a plot ofGRg versus Wgives a straight line with a slope of 119H and anintercept on the Waxis equal toWb(g) (Fig. 2A). If this relationship is plotted fordifferent germination percentages (e.g. Gummerson, 1986), a series of parallellines are developed with a common slope (1 19H ) but different intercepts (Wb(g).Experimentally, it has been found that in most cases the Wb(g) values varyamong seeds in the population in a normal or Gaussian distribution (e.g.Gummerson, 1986; Bradford, 1990; Dahal and Bradford, 1990). One cantherefore plot the relative frequency of a given Wb value in the seed populationas a normal bell curve, which can be defined by its mean (Wb(50) and standarddeviation (cr'!Jb) (Fig. 2B). The term Wb(g) represents this distribution ofthresh~

old values within the seed population.How do Wb(g) values relate to the times to radicle emergence? According toEquation 1, W- Wb(g) (referred to as AW(g) multiplied by the time togermination of percentage g (tg) is a constant (9H ). In Figure 3B, AW(g) isindicated by the lengths of the horizontal arrows between the seed W(0 MPa inthis case) and the Wb(g) value of different germination fractions. In Figure lA,the times to germination of different percentages are similarly indicated byhorizontal arrows. The arrows connecting panels A and B in Figure 3 show thatspecific threshold values corresponding to the 10th, 50th, or 90th percentiles aredirectly related to the times of radicle emergence for those same percentages.The products of the lengths of the AW(g) arrows in panel B multiplied by thelengths of the tg arrows in panel A for each value ofg are all identical and equalto 9H . Thus, as the seed Wapproaches the Wb(g) value of a particular seed, thetime to radicle emergence lengthens to maintain a constant total hydrotime.This is illustrated in Figure 3C, where the seedWhas been reduced to -0.25 MPafor a seed population with a Wb(50) of -0.5 MPa. For the median seed, the timeto radicle emergencewill be exactly doubled, since the value of AW(50) has beenreduced by half (Fig. 3A). However, the time to 10% radicle emergence will beless than doubled, while the time to 90% will be more than tripled, since a givenreduction in seed Whas differential effects on AW(g) depending upon the specificthreshold values. As shown in Figure 3C, AW(90) is now quite small, and acorrespondingly long time will be required for radicle emergence of the 90thpercentile ofseeds (Fig. 3A). In addition, the maximum germination percentageattained will be less than 100%, since a portion oftheWb(g) distribution extendsabove -0.25 MPa (hatched area under curve in Fig. 3C). This represents seedswhose germination thresholds are higher than -0.25 MPa, and which thereforewill not ever germinate at that water potential. If the Wwas reduced further, thefinal germination percentage would decrease (more of the threshold distributionwould exceed theWvalue), and the times to germination of the remaining seedswould increase such that the total hydrotime (i.e. AW(g) x tg) remained constant.In this way, the hydrotime model simultaneously accounts for both the timingand the final germination percentages of seed populations in response tochanges in W.An additional advantage of the hydrotime model is that germination timecourses at different Wcan be normalized on a common time scale, just as

The hydrotime concept in seedgermination and dormancy 353

1A

Iflti10) Iflti50) IfIb(90)

~ ~ ~

-1.0 -0.8 -0.6 -0.4 -0.2 0

1fI (MPa)

c 0.50 8 'l'b(50).~

:::J 0.4 +Q.0Q.c 0.3>-uc(J) 0.2:::JCT(J)L..-~

0.1..::;ro(J) 0a: -1 -0.8 -0.6 -0.4 -0.2 0

1fIb (MPa)

Figure 2. A. Germination rates (GRg = l/tg) as a function ofV for different germination fractions(g). Germination rates for a given fraction increase linearly with V above the threshold value(Vb (g)), which varies among seed fractions. The slope, however, is constant for all fractions and isequal to 1I9H . B. A normal distribution of Vb values, characterized by the mean (Vb(50)) andstandard deviation (crljrb). The relative frequency ofoccurrence ofa particular Vb value is indicatedby the bell-shaped curve, which is symbolized by Vb(g)

354 KJ. Bradford

12

A

c

-1 -0.8 -0.6 -0.4 -0.2 0V'b (MPa)

0.1

0.2

0.3

--------- - - - - - - - :--:::.~.------,--- If'--,..-".... \

~~ \,/ \

-.-/ \/'" , \" \, \, \

\

II

I/~

2

tso

B

-1 -0.8 -0.6 -0.4 -0.2 0V'b (MPa)

, 4 6 '", 8 \ 10!h1bibition time (dq.ys) \

" '\,....---4-+--+----=T--. 0.5 .--------"......--r-.,----,, \, \

\\

oo

20

40

60

100

c.Qmc.~

Q)

CJ

Figure 3. A. Germination time courses for a seed population at 0 MPa (solid curve) or at -0.25MPa (dashed curve). The times to germination of 10, 50, and 90% of the seeds are indicated by thehorizontal arrows in each case. B. The 1ftb(g) distribution on which the time course at 0 MPa inpanel A is based. The vertical line at 0 MPa indicates the 1ft of the seed. The horizontal arrowsindicate the values of 1ft - 1ftb(g), symbolized as A1ft(g) for the 10th, 50th and 90th percentiles. Thearrows connecting panels A and B illustrate whim particular seed fractions in the 1ftb(g)distribution would germinate. In each case, the product of A1ft(g) times tg is a constant equal to9H. C. The 1ftb(g) distribution on which the time course at -0.25 MPa in panel A is based. The1ftb(g) distribution is identical to that in panel B, but the vertical line now indicates that the seed 1ftis -0.25 MPa. Other details as for panel B. Note the greater effect on the timing of the last seeds togerminate compared to the effect on the first seeds to germinate, resulting in increased skewness inthe time course curve. The hatched area under the 1ftb(g) distribution curve in panel C representsseeds whose germination thresholds exceed the seed 1ft, and which therefore will not completeradicle emergence at this 1ft. Note that the same effect as occurred when the seed 1ft was reduced by0.25 MPa could be achieved by shifting the 1ftb(g) distribution 0.25 MPa more positive

The hydrotime concept in seed germination and dormancy 355

biological processes at a range of temperatures can be normalized on a commonthermal time scale using degree-days. Using the parameters from the hydrotimemodel, germination time courses at any'" can be normalized to the time coursein water for that seed population. The relationship between the time togermination in water (tg(O) and the time to germination at any other '"(tgN) has been derived previously (Bradford, 1990) as:

(3)

When'" =0MPa, the right side ofEquation 3will equal 1, and tg(O) =tgN),as expected. When'" = "'b(g), then the right side of Equation 3 will equal zero,or tgN) essentially becomes infinite. This is exactly what is meant by "'b: the '"at which germination does not occur (or takes infinitely long). At any'" betweenoMPa and "'b(g) , the time to germination at that'" is increased relative to thatin water by the factor 1 - ('" / "'b(g). Thus, once "'b(g) has been characterizedfor a seed lot (i.e. its mean and standard deviation are known), the germinationtime course at any'" can be calculated relative to the time course in water forthose same seeds. Alternatively, rearranging Equation 1,

(4)

shows that the time to germination at any '" can be corrected back to that inwater by multiplying by the bracketed factor. Conceptually, the ability tonormalize germination time courses on a hydrotime basis indicates that seedsat a reduced '" are progressing toward radicle emergence at the same pace asthose in water, given the amount of hydrotime they are accumulating per unitactual time. Just as germination takes longer at a lower temperature, it also takeslonger as '" approaches the "'b(g) threshold. Referring to Figure 3A, one canvisualize that the curve for -0.25 MPa would result if the time axis for the curveat 0 MPa was simply stretched in inverse proportion to A"'(g). As A"'(g)decreased, the axis-stretching would increase proportionately, and this wouldresult in the germination curve shown. Space does not permit further illustra­tion of this normalizing function here, but a number of examples have beenpublished previously (Bradford, 1990; Dahal and Bradford, 1990; 1994;Bradford and Somasco, 1994). The normalized time courses give a direct visualindication of the degree of fit of· the hydrotime model to the data, and canidentify data that deviate from expectations. The latter often indicates analteration in physiology, as distinct from the delay anticipated simply from thelower rate ofhydrotime accumulation at reduced'" (e.g. Ni and Bradford, 1992;Dahal and Bradford, 1994).

Hydrotime and Dormancy

Seed dormancy is a complex phenomenon, and many factors undoubtedly

356 K.J Bradford

contribute to the germination patterns and environmental responses observedamong diverse plant species (Fenner, 1992; Kigel and Galili, 1995). However, asillustrated above, the hydrotime model can reproduce the types of germinationtime courses that are almost universally encountered as seeds enter or leavedormancy. That is, there is generally an increase in both final germinationpercentage and speed of germination as a seed population loses· dormancy. Inthe hydrotime model, this pattern is an automatic consequence of the variationin threshold values among individual seeds and the relationship of the thresholddistribution to the current seed "'. It is significant to note that as far as the modelis concerned, there is no distinction between a constant threshold distributionand a change in "', or a constant'" with a change in the threshold distribution.For example, in comparing Figures 3B and 3C, exactly the same germinationtime course would result if the mean of the threshold distribution had beenincreased by 0.25 MPa as occurred when the '" was decreased by 0.25 MPa. Themodel is sensitive only to A"'(g), and not to the absolute values of either'" or'"b(g). If we visualize progressively shifting the '"b (g) distribution to highervalues, as the "'b(g) values ofpart of the population exceed 0 MPa, those seedswould no longer be able to complete radicle emergence on water. This is at leasta functional definition ofdormancy, that seeds do not germinate on water whengiven otherwise suitable conditions. In a colloquial sense, we can consider thatwater is not 'wet' enough for those seeds to complete radicle emergence.We cantherefore hypothesize that seed dormancy might be related to "'b(g) valuesexceeding 0 MPa, and that as dormancy is broken by the appropriateenvironmental or hormonal signals, the "'b(g) values of the entire populationmight shift toward progressively lower values. This would result in a series ofgermination time courses that become simultaneously more rapid and morecomplete, as is the case for the vast majority of dormancy data in the literature(Gordon, 1973).This hypothesis has been tested experimentally for only a few cases thus far.Detailed studies of gibberellin- and abscisic acid-deficient tomato genotypesdemonstrated that the effect of these hormones was to shift "'b(g) distributionsto more negative values when germination is promoted (i.e. in the presence ofGA or absence of ABA) and to more positive values when germination isinhibited (in the presence of ABA or absence of GA) (Ni and Bradford, 1993).In the case of lettuce seed thermodormancy (or thermoinhibition), as thetemperature increases toward the upper temperature limit for germination, the"'b(g) distribution shifts progressively to more positive values, eventuallyreducing germination percentages (Bradford and Somasco, 1994). Ethylene isable to increase the upper temperature limit of lettuce seed germination, and itappears to act by maintaining more negative "'b(g) values as temperaturesincrease (Dutta and Bradford, 1994). It is also possible to model on a theoreticalbasis germination time courses for a wide range of seed dormancy situations.Data from Perino and Come (1977) can be used as an illustration of how thehydrotime model can accommodate time courses ofgermination as dormancy isalleviated. Apple seeds germinated poorly if imbibed directly at 30°C, but if first

The hydrotime concept in seed germination and dormancy 357

co

'';=;roc'E....Q)

CJ

100

80

60

40

20

germination 8l30'C after hou's 81 15'C

7248

4

2oA

",,(50)-0.95

-0.55

-0.35

-0.15

o0.15025

co'';=; 0.4ro:::J

§: 0.3asQ)en 0.2'0co 0.1.~

~I.J....

5 10 15 20

Imbibition time (days)25

Figure 4. A. Escape of apple seeds from thermoinhibition at 30°C after increasing durations ofpreimbibition at 15°C. The symbols are the actual data taken from Perino and Come (1977). Thesmooth curves are the time courses predicted by the hydrotime model based upon the I/tb(g}distributions shown in panel B. The I/tb(50) values (MPa) used to generate the predicted curves areindicated to the right of panel A. B. Theoretical I/tb(g} distributions used to generate thegermination time courses in panel A. In each case, only the mean threshold (I/tb(50) was changed,with the hydrotime constant (9n) and the standard deviation (crljlb) of the distribution remainingconstant. The progressive negative shift in the I/tb(g} distribution can account for the entire patternof germination responses, including both the rates and final percentages

358 KJ. Bradford

imbibed at 15°C for increasing durations, they became capable of germinatingmore rapidly and to a higher percentage when transferred to 30°C (Fig. 4A). Thesymbols in Figure 4A are taken from from Perino and Come (1977), but thesolid lines are generated from the hydrotime model under the assumption thatthe effect ofpreincubation at 15°C is to progressively shift the "'b(g) distributionto more negative values (Fig. 4B). That is, it is assumed that the standarddeviation (width) of the "'b(g) distribution is constant, and that the hydrotimeconstant (9n) also does not change. Simply shifting the mean of the "'b(g)distribution to progressively lower values is sufficient to generate the completefamily of time courses which match closely to the original data (Fig. 4A).Similar illustrative examples and additional discussion have been presentedelsewhere (Bradford, 1995; 1996). While such theoretical modelling does notprove that "'b(g) distributions actually change as predicted, the fit to the data iscertainly suggestive, and the hypothesis is readily testable by measuring the '"sensitivity ofgermination of seed populations in various dormancy states.

An Ecological Interpretation of the Hydrotime Model

If the hydrotime model provides an accurate description of germinationresponses to dormancy-inducing and dormancy-breaking factors, what are theimplications for seed ecology? In many environments, seasonal or erraticrainfall is the primary determinant of seedling survival, often associated with adry afterripening requirement or high temperature sensitivity (Kigel, 1995). Inother cases, avoiding low temperatures and the danger of frost may be moreimportant, requiring seeds to delay germination until after experiencing a coldperiod (Fenner, 1995; Egley, 1995; Benech-Arnold and Sanchez, 1995). Accord­ing to the hydrotime model (or its extension to hydrothermal time; Gummerson,1986; Dahal and Bradford, 1994), a major physiological response to theseenvironmental signals is a shift in the "'b(g) distribution of the seed populationto more negative values. This has the effect of increasing the probability that agiven seed will initiate and complete germination while sufficient water isavailable in its immediate environment. The linkage between water potentialthresholds and germination rates is important, since it may be critical for seedsto germinate rapidly in environments where soil surfaces are alternately wet anddry (Allen et a/., 1993). As the "'b(g) distribution shifts to more negative values,, the rates of germination of all the seeds are increased. On the other hand, it hasbeen pointed out that from an ecological perspective, slow germination is aseffective as dormancy in preventing germination at unfavorable times in afluctuating environment (Meyer and Monsen, 1991), as seeds are generallycapable of· tolerating dehydration if radicle emergence has not or has onlyrecently occurred (Finch-Savage and McKee, 1989; Bruggink and van derToorn, this volume). Maintaining a wide distribution of "'b(g) values withinthe seed population assures that while some seeds will capitalize rapidly onfavorable conditions, others will be more conservative, committing to radicle

The hydrotime concept in seedgermination and dormancy 359

emergence only after a much longer period or not at all. Finch-Savage andPhelps (1993) and Allen et al. (this volume) have demonstrated convincinglythat successive flushes ofseedling emergence in the field following rainfall eventscan be described on the basis ofwater potential and temperature thresholds thatallow fractions of the total seed population to germinate within specific timewindows. Similarly, seasonal patterns of dormancy cycling controlled bytemperature result in an increasing or decreasing likelihood that germinationwill be completed within a given hydrothermal period (Bouwmeester andKarssen, 1992; Benech-Amold and Sanchez, 1995).There is an ecological rationality to having various environmental signalsinfluence germination capacity via effects on *b(g). As seasonal and environ­mental requirements are met which indicate to the seed that an opportune timeto germinate is approaching (e.g. afterripening, stratification, light, nutrients,etc.), a negative shift in *b(g) will result in an increase in the fraction of seedscapable ofgermination and in the overall speed ofgermination. However, sincethis increased capability is based upon the water potential thresholds, the seedpopulation will still remain highly sensitive to the current local water avail­ability. Even if the *b(g) distribution shifts to quite low values in a physiologicalsense (-1 to -2MPa), a relatively small decline in soil*can still have a dramaticeffect on germination timing and percentage (c.r. Fig. 3). Thus, seasonal orenvironmental effects on the capacity for germination may act throughphysiological shifts in the *b(g) distribution, with the variation in *b(g)providing differential sensitivity to local conditions to ensure that there are bothopportunistic and conservative individuals within the population. By respond­ing to environmental factors via modification of their sensitivity to *, seedpopulations can achieve both long-term integration of their environmental (andevolutionary) history and regulation of their progress toward germination basedupon current water availability.

References

Allen, P. S., Debaene, S. B. G. and Meyer, S. E. 1993. In: Fourth International Workshop on Seeds:Basic and AppliedAspects ofSeed Biology, vol. 3, pp. 387-392 (eds. D. Come and F. Corbineau).Paris: Association pour la Formation Professionelle de l'Interprofession Semences.

Benech-Arnold, R. L. and Sanchez, R. A. 1995. In' Seed Development and Germination, pp. 545-566 (eds. J. Kigel and G. Galili). New York: Marcel Dekker, Inc.

Bouwmeester,H. J. and Karssen, C. M. 1992. Oecologia 90: 88-94.Bradford, K. J. 1990. Plant Physiology 94: 840-849.Bradford, K. J. 1995. In: Seed Development and Germination, pp. 351-396 (eds. J. Kigel and G.Galili). New York: Marcel Dekker, Inc.

Bradford, K. J. 1996. In: Plant Dormancy: Physiology, Biochemistry and Molecular Biology, in press(ed. G. A. Lang). Wallingford, axon, u. K.: CAB International.

Bradford, K. J. and Somasco, O. A. 1994. Seed Science Research 4: 1-10.Dahal, P. and Bradford, K. J. 1990. Journal ofExperimental Botany 41: 1441-1453.Dahal, P. and Bradford, K. J. 1994. Seed Science Research 4: 71-80.Dutta, S. and Bradford, K. J. 1994. Seed Science Research 4: 11-18.

360 K.J. Bradford

Egley, G. H. 1995. In: Seed Development and Germination, pp. 529~543 (eds. 1. Kigel and G. Galili).New York: Marcel Dekker, Inc.

Fenner, M. 1992. Seeds: The Ecology of Regeneration in Plant Communities. Wallingford, Oxon,UK: CAB International.

Fenner, M. 1995. In: Seed Development and Germination, pp. 507-528 (eds. 1. Kigel and G. Galili).New York: Marcel Dekker, Inc.

Finch-Savage, W. E. and McKee, 1. M. T. 1989. Annals ofApplied Biology 114: 587-595.Finch-Savage, W. E. and Phelps, K. 1993. Journal ofExperimental Botany 44: 407--414.Gordon, A. G. 1973. In: Seed Ecology, pp. 391-409 (ed. W. Heydecker). London: Butterworths.Gummerson, R. J. 1986. Journal ofExperimentalBotany 37: 729-741.Kigel, 1. 1995. In: Seed Development and Germination, pp. 645-699 (eds. 1. Kigel and G. Gali1i).New York: Marcel Dekker, Inc.

Kigel,1. and Galili, G. 1995. Seed Development and Germination. New York: Marcel Dekker, Inc.Meyer, S. E. and Monsen, S. B. 1991. Ecology 72: 739-742.Ni, B.-R. and Bradford, K. J. 1992. Plant Physiology 98: 1057-1068.Ni, B.-R. and Bradford, K. 1. 1993. Plant Physiology 101: 607---617.Perino, C. and Come, D. 1977. Physiologie Vegetale 15: 469--474.