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Crop Science 42:451-457 (2002)
© 2002 Crop Science Society of America

SEED PHYSIOLOGY, PRODUCTION & TECHNOLOGY

Seed Vigor, Soilborne Pathogens, Preemergent Growth, and Soybean Seedling Emergence

Brigitte Hamman*,a, D. B. Eglic and Gwen Koningb

a Dep. of Botany, Univ. of Pretoria, Pretoria, 0002, South Africa
b Forestry and Agricultural Biotechnology Inst., Univ. of Pretoria, Pretoria, 0002, South Africa
c Dep. of Agronomy, Univ. of Kentucky, Lexington, KY 40546-0091

* Corresponding author (bhamman{at}postino.up.ac.za)


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Emergence of soybean [Glycine max (L.) Merr.] seedlings in the field is frequently less than predicted by standard germination, but the causes of this emergence failure are not well understood. This study explored the influence of soil pathogens and seed vigor on soybean seedling preemergent growth and emergence. Seed from six seedlots, representing a range in seed vigor, were planted as pregerminated and as dry seed into sterile and pathogen-infested soil maintained at a constant soil water potential (-0.005 MPa). Final emergence (FE) and emergence rates from two planting depths (25 and 60 mm) were recorded under ambient greenhouse conditions. Once the FE stage had been reached, nonemerged seedlings were exhumed, and classified as stunted, abnormal, or dead. The FE of the high- and medium-vigor seedlots was always higher than the low-vigor seedlots, and the advantage was greatest under stressful conditions (deep planting, nonsterile soil). The FE was always lower in nonsterile than sterile soil. Seedlings emerged more slowly from deep plantings and when pathogens were present, and FE decreased as emergence was delayed in nonsterile soil. This relationship became more pronounced with low vigor seed. Planting pregerminated seeds always resulted in higher FE than dry seeds, but it did not eliminate emergence failure. Abnormal seedlings accounted for most of the emergence failure in sterile soil, but the lack of germination or of growth immediately after germination was also important in nonsterile soil. Lack of germination alone therefore does not account for lack of emergence; postgerminative, preemergent growth may be more important.

Abbreviations: CWT, controlled water table • FE, final emergence • T50, time to 50% emergence


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
SOYBEAN SEEDLING EMERGENCE is the result of two growth phases, namely, seed germination and preemergent seedling growth through the soil. Emergence is influenced by the quality of the seed planted and by the seedbed environment, with soil moisture, pathogens, temperature and impedance being the most important components (Delouche, 1952; Gummerson, 1986; Helms et al., 1996; Ferriss et al., 1987; Wheeler and Ellis, 1992).

There are a number of laboratory tests with which soybean seed quality can be evaluated (Association of Official Seed Analysts, 1983; Loeffler et al., 1988; International Seed Testing Associaton, 1995). However, to date, no single test can claim to accurately relate performance in the field to seed quality when conditions are less than favorable (TeKrony and Egli, 1977; Johnson and Wax, 1978). The predictive ability of seed quality tests appears to be directly related to the condition of the seedbed environment (Egli and TeKrony, 1996). Knowledge of the precise causes of emergence failure and their relative importance is lacking, and would identify those factors in the soil environment which need to be countered or modified if emergence is to be successfully predicted and achieved. Such knowledge may also contribute to the development of improved vigor tests with which to identify seedlots most likely to be tolerant of adverse soil conditions.

Emergence responses to seedbed conditions have previously been examined primarily in prevailing field conditions, as opposed to controlled conditions (Hegarty, 1979; Halmer and Bewley, 1984; Finch-Savage and Pill, 1990). Few attempts have been made to distinguish between the effects of the seedbed environment, seed quality, or soilborne pathogens on germination sensu stricto, and on preemergent growth. In fact, the two terms are often erroneously used interchangeably, yet the two are biochemically distinct phases of growth (Perino and Côme, 1991), with potentially different responses to specific environmental conditions. The purpose of this study, therefore, was to investigate the nature of the relationship between components of the seedbed environment and seed quality, and their effect on soybean seedling emergence. Postgerminative, preemergent seedling growth in particular was examined by comparing the emergence from seeds planted dry or pregerminated. Nonemerged seeds and seedlings were also exhumed for evaluation after FE had been reached.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Greenhouse Experiment
Cultural Conditions
Soybean seed (50 per treatment) was planted into soil-filled trays (50 x 30 x 8 cm) in a greenhouse where temperature was maintained between {approx}20 and 30°C. Soil moisture was maintained at a constant -0.005 MPa with a controlled water table (CWT) irrigation system (Buxton et al., 1994). This is an automatic subirrigation system that consists of a capillary mat placed above a constant water level in a reservoir. The amount of water contained in the mat is determined by the mat's vertical distance above the water table. Because of the nature of the CWT system, water entered the seedling trays from the bottom, and moved up through the soil, thereby eliminating the crusting that may occur when watered from the top. Seedling emergence responses to the treatments applied in this study were also therefore not confounded by fluctuations in the moisture level of the soil. Soil was sampled periodically to verify that the moisture content did indeed remain constant both over time and across treatments [variation was less than ±50 g kg-1 (dry mass basis)]. The trays were partially filled with soil that was allowed to absorb water and reach moisture equilibrium with the mat prior to planting. The seed were planted on the wet soil and covered with dry soil to the desired planting depth.

Treatments
Six seedlots were used, all having commercially acceptable levels (>80%) of standard germination, but exhibiting a range in seed vigor (Table 1). Seed was free of seedborne pathogens, as determined by plating surface sterilized seed onto acidified potato-dextrose agar. The standard germination and vigor tests (accelerated aging, cold test, and conductivity) were performed according to the procedures outlined in the rules for testing seed (International Seed Testing Associaton, 1995; Association of Official Seed Analysts, 1998) and by Loeffler et al. (1988).


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  		Table 1. Seed quality of seedlots used in experiments.

 
Pregerminated and dry seeds were planted. Pregerminated seeds were imbibed in moistened germination towels for 36 h at 25°C and those with radicles 1 mm in length were planted.

Seeds were planted into sterile and nonsterile soil. Nonsterile soil was topsoil (Maury silt loam: fine, mixed, semiactive, mesic Typic Paleudalfs) collected from a field at Spindletop Research Farm at the University of Kentucky, Lexington, KY, where soybean had been grown the previous three growing seasons to provide adequate populations of soilborne pathogens. The soil was assayed by plating a soil dilution series onto media selective for Pythium, Fusarium, Rhizoctonia, and Phytophthora spp. (Dhingra and Sinclair, 1995). The number of fungal propagules isolated were 4000, 98000, 22000, and 5000 colony-forming units g-1 soil, respectively. These levels were well above those suggested as providing a suitable level of disease pressure (P. Vincelli, 1996, personal communication). Greenhouse soil mixed with sand in a 2:1 ratio (v/v) was microwaved according to the instructions of Ferriss (1984) in order to create sterile conditions. The soil was assayed for pathogens as described above after microwaving, to confirm sterility.

Seed was planted at a depth of 25 (shallow) and 60 mm (deep).

Data Collected
Seedlings were considered emerged when cotyledons were free of the soil (Stage VE, Fehr and Caviness, 1977). Emergence counts were taken every 8 h after the first seedlings emerged. Once the FE stage had been reached, seedlings were exhumed from the soil (soil in trays was sifted, and seed and seedlings were removed), and nonemerged seedlings were classified as either stunted (seedlings had stunted hypocotyls but were otherwise normal-looking), abnormal, or dead. It was impossible to distinguish between those seeds which were dead and those which had germinated but grown no further in those treatments involving dry-planted seed, and so they were combined. Pregerminated seeds that had grown no further after planting were included with the abnormal seedlings.

Soil temperatures were monitored with 10 thermocouples positioned at planting depth in randomly selected trays, and the average temperature over 2 h (measured every 5 min) was recorded with a LI-Cor 1000 data logger (Li-Cor Inc., Lincoln, NE). The Gompertz equation (Tipton, 1984; Gan et al., 1996), was used to describe cumulative emergence as a function of thermal time, using 10°C as the base temperature (Enken, 1959). Regression analysis was done, with all r2 > 0.98. Time to 50% emergence (T50) was calculated from the regression equations.

Soil moisture retention curves were obtained for both sterile and nonsterile soils from the Soil Analysis Laboratory in the Agronomy Department, University of Kentucky. Soil moisture concentrations were determined by drying at 130°C for 24 h (dry mass basis).

Statistical Analysis
The experimental design was a split-split-split-plot with main plots arranged in a randomized complete block with two replications. The main plots were soil treatments, subplots were planting depths, sub-subplots were pregerminated vs. dry seed, and sub-sub-subplots were seed vigor levels. Significant differences between treatments were determined using the LSD procedure. Spatial limitations in the greenhouse made it necessary to replicate in time, with the main plots conducted sequentially.

Field Experiment
The field emergence experiment was conducted on Spindletop Research Farm at the University of Kentucky. Nongerminated seed of the same six seedlots used in the greenhouse experiment (Table 1) were sown (50 seed per seedlot) 30 mm deep in a single row, in a seedbed prepared by conventional tillage practices on a Maury silt loam soil. The exact position of each sown seed was marked. There were four replications of each seedlot in a randomized complete block design. Final emergence counts were taken after emergence had stopped, and the nonemerged seed and seedlings were exhumed and categorized as described for the greenhouse experiment.


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
General
Although seed vigor varies along a continuum, for the sake of interpretation, seedlots are often placed into discrete groups of various levels of seed vigor, for example, high-, medium-, and low-vigor groups (Table 1). Vigor classification for this study was based primarily on accelerated aging germination. This test has proven to be a reliable indicator of soybean seed vigor levels (Byrd and Delouche, 1971; TeKrony and Egli, 1977), and is supported by results from the cold and conductivity tests. Seedlots were selected so as to have high standard germination (>80%) and a range in vigor, with the two low-vigor seedlots being of extraordinary low vigor.

The emergence response of seedlots within a vigor group was similar. Consequently, the effects of the various treatments were averaged across seedlots within vigor levels.

The capillary mat system successfully maintained soil moisture content at a constant -0.005 MPa, and there was no crusting.

As anticipated, the analysis of variance indicated that almost all interactions were significant, and therefore comparisons were made among individual treatment means.

Seed Vigor
Under ideal conditions (sterile soil and shallow plantings), FE was high and did not differ significantly among seedlots of different vigor levels (Fig. 1) . The introduction of stress into the seedbed environment (i.e., nonsterile soil or deep plantings) resulted in larger and significant differences among vigor levels. The largest difference was always between the low- and medium- or high-vigor seedlots. The advantage for the high- and medium-vigor lots was significant in the shallow planting in nonsterile soil, and in both the sterile and nonsterile soil in the deep planting for dry and pregerminated seeds. The largest advantage occurred in the most stressful situation—deep planting of dry seeds in nonsterile soil.



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  		Fig. 1. Effects of planting depth, soil pathogens, and seed quality on final emergence of soybean seedlings when pregerminated and dry seed were planted in sterile and nonsterile soil. Data were averaged across seedlots within a vigor level. Soil moisture content was a constant -0.005 MPa. Shallow planting = 25 mm, deep planting = 60 mm. LSD is for the comparison of any two means.

 
These results offer direct support of the concept that vigor provides an advantage only in stressful environments (Burris, 1976; Johnson and Wax, 1978; TeKrony et al., 1987). The value of our study lies in the direct comparisons between well-defined favorable and unfavorable conditions. When favorable conditions were created in this study (i.e., adequate moisture, shallow planting, absence of pathogens, seeds already pregerminated), seedlots of different vigor levels performed equally well in terms of FE. However, as soon as the environment became more stressful [i.e., pathogens present, dry (nongerminated) seeds, deeper plantings], the advantage for high- and medium-vigor levels was clearly apparent. As reported previously (Egli and TeKrony, 1996), under the most stressful conditions (deep planting in nonsterile soil), FE of even the high vigor seed lots was not satisfactory (<80%).

Soilborne Pathogens
Final seedling emergence was always lower in nonsterile soil than in sterile soil (Fig. 1), irrespective of the planting depth, the vigor level of the seedlots, or whether seeds were planted dry or pregerminated. However, FE of the low-vigor seedlot was reduced more by the nonsterile soil than the medium- and high-vigor seedlots, and the effect was larger on dry seed and in deep plantings.

The T50s of the deep plantings were usually larger than those from the shallow plantings (Fig. 2) . The FE in sterile soil was not related to T50 when high- or medium-vigor seed was used, but there was a trend (not significant) for lower emergence at large T50s for low-vigor seedlots. In nonsterile soil however, FE decreased as T50 increased, for all three vigor levels, with the largest effect at the low vigor level.



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  		Fig. 2. Relationship between final seedling emergence and thermal time (base temperature of 10°C) to 50% of final emergence (T50) of pregerminated and dry seed, at two planting depths, for high-, medium-, and low-vigor seedlots in sterile and nonsterile soil. Data points represent individual replicates. Regression analysis for the sterile soil treatments were not significant and the equations are not shown. The symbols *, ** denote significance at P <= 0.05 and 0.01, respectively.

 
The presence of pathogens in the soil clearly had a deleterious effect on FE. The pathogenicity of soilborne fungi such as Pythium, Fusarium, Rhizoctonia and Phytophthora spp. has been implicated in reduced emergence of soybean seedlings (Thomison et al., 1971; Pieczarka and Abawi, 1978; Schlub and Lockwood, 1981; Schlub et al., 1981). In this study, not only did the pathogens reduce FE, they tended to increase the time it took for the seedlings to emerge, which was associated with lower FE.

When pathogens are involved, the rate of emergence is related to two aspects of the system: the period during preemergent growth during which the disease process takes place, and the host activity during this period. Since host response to pathogen challenge is an active process in most systems, it would be expected that conditions which limit the general metabolic activity of the host might also limit its ability to respond to the pathogen (Gleason, 1985). If a seed can be killed by a pathogen only if the attack occurs before a particular stage of preemergent development, then a seed which reaches that stage more quickly should be exposed to attack for a shorter period of time (Ferriss and Baker, 1990). Shortening the period of potential pathogen attack should logically result in a lower probability that the pathogen will kill the seedling. In an environment free of pathogens (sterile soil, Fig. 2), little effect of emergence speed on percentage emergence would be expected, since no pathogen inoculum would be present to impose a developmental finish line (Ferriss and Baker, 1990). This would explain the smaller reductions in FE due to pathogens when high-vigor seed was planted, or when seed was planted shallow (Fig. 1 and 2). Both the deeper planting depth, and low seed vigor imposed a time disadvantage on the developing seedlings, which fell prey to the pathogens present in the nonsterile soil more frequently, compared with their counterparts in sterile soil. A similar response was demonstrated in winter wheat (Triticum aestivum L.) by Lafond and Fowler (1989), who found that increased planting depth increased the time to emergence, resulting in poorer seedling development. Slow emergence in corn (Zea mays L.) was also noticed by Stewart et al. (1990) to predispose the crop to disease and adverse environmental conditions.

Preemergent Seedling Growth
It is entirely possible that a planted seed will germinate, yet still fail to emerge from the soil. Indeed, there are a number of instances involving studies on a range of vegetable crops which assigned the cause of emergence losses to the failure of seedlings to grow under the soil surface, and not to germination failure (Halmer and Bewley, 1984). For example, retrieval experiments covering a range of moisture and soil conditions of calabrese (Brassica oleracea L.), carrot (Daucus carota L.), onion (Allium cepa L.) and sugar beet (Beta vulgaris L.), established that virtually all viable seed sown did germinate (Hegarty, 1979; Durrant, 1980). The question therefore arises as to which is more important when determining causes for poor emergence in soybean: failure to germinate, or failed postgerminative growth?

Each treatment in our emergence study was therefore applied to seeds planted both pregerminated and dry. In those instances where seeds were pregerminated, radicle length at planting was already 1 mm, so it was only the preemergent growth stage that was under investigation. Seeds planted dry on the other hand, had to germinate prior to going through a preemergent growth stage and emerging. Thus, the question of whether lack of emergence is due to failed germination, poor preemergent growth, or a combination of the two, could be directly addressed.

As a group, pregerminated seedlings consistently had higher levels of emergence (Fig. 1), but differences between pregerminated and dry seed were significant only for the low-vigor seedlots in nonsterile soil or in the deep planting in sterile soil. It was to be expected that planting seed pregerminated would result in greater numbers of emergent seedlings, since the dead seeds in the seedlots were obviously eliminated. The low-vigor seedlots had lower germination (Table 1), so the advantage for the pregerminated seeds was larger in those seed lots.

Planting pregerminated seeds in this study however, did not eliminate emergence failure. For example, of the seedlings pregerminated before planting 60 mm deep in nonsterile soil, 19 to 39% failed to emerge (Fig. 1). Even when soil was sterile, up to 13% still did not emerge. Obviously, failure to grow at all after germination, or poor preemergent growth, contributed to reductions in emergence. Most of the exhumed seedlings were either abnormal or failed to grow after planting pregerminated seeds in both the sterile and nonsterile soil and for all vigor levels (Fig. 3) . Formation of stunted seedlings did not seem to play a significant role in emergence failure.



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  		Fig. 3. Effects of soil pathogens and seed quality on the type of nonemerged seedlings formed when soybean seed was planted pregerminated at a depth of 60 mm in the greenhouse. Seed that grew no further after germination are included in the abnormal seedling category. Bars representing total nonemerged seedlings with different letters are statistically different (P <= 0.05).

 
Exhuming nonemerged seeds and seedlings from the dry planted treatments provided another evaluation of the causes of emergence failure. Deficient preemergent growth was also the main cause of emergence failure when dry seed was planted into sterile soil, accounting for 64 to 100% of the nonemerged seedlings (Table 2). In nonsterile soil, fewer than half of the nonemerged seedlings were easily identifiable as abnormal or stunted, but this does not reveal the full extent of deficient preemergent growth since it is impossible to distinguish between dead seeds, and those that germinated with no further growth. Thus, in the presence of pathogens, the lack of germination, or more likely, of growth immediately after germination, was much more important. Similar results were obtained in a field experiment (Table 3), where seeds that were dead or exhibited little growth after germination also made a significant contribution to emergence failure of low vigor seed lots. In an earlier comparison of single seed conductivity levels and the emergence performance of individual soybean seedlings, stunted and abnormal seedlings accounted for nearly half of nonemerged seedlings in some seedlots (Hamman et al., 2001). The failure of pregerminated seeds to grow contributed to emergence failure of high- and medium-vigor seeds planted deep in nonsterile soil (Fig. 3), but these seeds were included in the abnormal category.


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  		Table 2. The proportion of nonemerged seedlings that were stunted or abnormal, for seeds that were planted dry.

 

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  		Table 3. Final emergence of high, medium, and low vigor seeds planted dry in the field, and classification of nonemerged seeds and seedlings after retrieval.

 
The destruction of the seed by pathogens before or immediately after germination was a significant cause of low emergence, especially when low-vigor seed was used. These results are in contrast to reports for vegetable seeds, suggesting that emergence failures were generally associated with growth after germination (Hegarty, 1979; Durrant, 1980). It is possible that these differing responses may be a result of the relatively high pathogen levels in our nonsterile greenhouse soil, which was collected from a field where three successive crops of soybean had been grown. At more moderate pathogen levels, that is, more similar to the sterile soil, growth that failed to produce emergence would probably be a more important source of emergence failure.

Our results clearly demonstrate the advantage for high-vigor seeds in stressful seed bed environments, thus confirming the results of Egli and TeKrony (1996), based on the comparison of a large number of field experiments. The advantage for high-vigor seed seemed to be independent of the source of stress, existing when stress was provided by pathogens or by deep plantings. Stress-induced emergence failure was a result of both a deficiency in preemergent growth, and a lack of germination or growth after germination, which was more important in nonsterile soils. Rapid emergence, whether from high-vigor seed or from shallow plantings, contributed to high levels of emergence in nonsterile field soils. Efforts to improve emergence should probably focus on the initial stages of growth immediately after radicle protrusion, or on the processes that trigger an abnormal preemergent type of growth that prevents emergence.


   ACKNOWLEDGMENTS
 
We thank Dr. Jack W. Buxton, Department of Horticulture, University of Kentucky for his kind assistance with the establishment of the controlled water table irrigation system.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Contribution from the Kentucky Agric. Exp. Stn. no. 01-06-60.

Received for publication April 24, 2001.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 




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