How Does Seed Vigor Affect Soybean Yield

Published online June 7, 2018 Crop Ecology and Physiology

How Does Seed Vigor Affect Soybean Yield Components? Andréia Caverzan, Rafael Giacomin, Mariele Müller, Cristian Biazus, Nadia Canali Lângaro, and Geraldo Chavarria* Abstract Several factors may limit the germination, growth, development, and productivity of soybean [Glycine max (L.) Merrill]. Thus, seed physiological quality is important for crop establishment and uniformity. Among seed quality characteristics, vigor plays a key role for grain production. The objective of this study was to evaluate how seed vigor affects the population density, plant growth, nitrogen fixation, sugar, and starch content in nodes and these influences on yield components in soybean. Treatments consisted of varying vigor levels of seeds of the DM 5958 RSF IPRO cultivar. Using accelerated ageing test, seeds were exposed to 32°C heat for 0, 120, 192, and 216 h to obtain 90%, 75%, 63%, and 48% vigor levels. A field experiment was conducted in a randomized block design with four replicates at three locations. Root and shoot dry mass, leaf area, population density, plant height, stem diameter, nodulation, total soluble sugar and starch content, and grain yield components were measured. Plants grown from high-vigor seeds had greater shoot and root dry mass, leaf area, population density, stem diameter, plant height, number of nodules, nodule dry mass, and thousand-seed weight values. The numbers of productive and unproductive nodes and total soluble sugar and starch contents did not vary significantly with the treatments. Low vigor seeds resulted in increased production variability among plants while high vigor seeds resulted in higher yields due to a greater plant population density.

Core Ideas • Plants originated from the high-vigor seeds presented more efficiency on nitrogen fixation. • Low vigor levels resulted in higher yield variability among plants. • Plants grown from high vigor seeds exhibited higher yield.

Published in Agron. J. 110:1–10 (2018) doi:10.2134/agronj2017.11.0670 Copyright © 2018 by the American Society of Agronomy 5585 Guilford Road, Madison, WI 53711 USA All rights reserved

S

everal factors may limit the germination, growth, development, and productivity of soybean [Glycine max (L.) Merrill]. Crop uniformity influences yield (Tourino et al., 2002; Maddonni and Otegui, 2006), thus plants distributed unevenly imply in inefficient use of the available resources, including light, water, and nutrients (Tourino et al., 2002). When crop have uniform stand, the occurrence of gaps in sowing rows is decreased, which consequently decreases the number of dominant and dominated plants (Maddonni and Otegui, 2006), contributing to increased production (Egli, 1994; Tourino et al., 2002). Crop uniformity has been directly related to seed vigor (Cantarelli et al., 2015). Seed vigor is the sum of those properties that determine plant development across a wide range of environments (ISTA, 2015). Accordingly, the physiological quality of the seed is represented by higher germination and longevity, lower deterioration of reserves, and higher vigor (Krzyzanowski et al., 2008). Low seed physiological quality decreases plant survival in the field (Cantarelli et al., 2015; Finch-Savage and Bassel, 2016) and increases plant variability (Cantarelli et al., 2015). Furthermore, factors such as sowing time, sowing speed, sowing depth, sowing density, soil water, and nutrient availability (Krzyzanowski et al., 2008) must be considered to maximize yield; favorable climatic conditions also play a role (Board and Kahlon, 2011). Taking into account all the aspects indicated above, some factors should be considered to increment grain yield. Factors such as ones associated with sowing processes (Macholdt and Honermeier, 2017), homogeneous spatial availability of mineral elements in soil (Riedell et al., 2013), and seed phytosanitary protected regarding their physiological quality (Dan et al., 2012). Seeds are one of the most important inputs in agriculture. High-quality seeds produce vigorous and well developed plants that can become established in a wider variety of conditions than non-vigorous seeds (Finch-Savage and Bassel, 2016). Under adverse and stressful conditions, plant establishment can vary due to differences in seed vigor (Finch-Savage and Bassel, 2016). Thus, for grain production, seed vigor plays a key role, A. Caverzan, R. Giacomin, M. Müller, N. C. Lângaro, G. Chavarria, Faculdade de Agronomia e Medicina Veterinária, Programa de Pós-Graduação em Agronomia, Universidade de Passo Fundo, Passo Fundo, RS, Brazil; C. Biazus, Faculdade de Agronomia e Medicina Veterinária, Universidade de Passo Fundo, Passo Fundo, RS, Brazil. Received 23 Nov. 2017. Accepted 2 Apr. 2018. *Corresponding author ([email protected]). Abbreviations: DM, dry mass; LA, leaf area; NDM, nodule dry mass; NN, number of nodules; NP, number of pods; NPN, numbers of productive nodes; NS, number of seeds; NUN, numbers of unproductive nodes; PPD, plant population density; TSW, thousand-seed weight.

A g ro n o my J o u r n a l • Vo l u m e 110 , I s s u e 4 • 2 018

1

as it allows rapid and uniform establishment of seedlings and a suitable population in the field (Krzyzanowski and FrançaNeto, 2001). According to Henning et al. (2010) high vigor seeds, 94% determinate by accelerated aging test, have a better performance for seedlings development. In this way, fields cultivated with vigorous seeds tend to have better productivity index values (Kolchinski et al., 2005). Furthermore, high vigor seeds (94%) showed higher capacity of seed reserve mobilization during germination (Henning et al., 2010); these seeds had higher content of soluble proteins, starch, and soluble sugars. However, limited information exists about the relationship between seed vigor and soybean yield. Thus, the objective of this study was to evaluate how seed vigor affects the population density, plant growth, nitrogen fixation, sugar and starch content in nodes and these influences on yield components in soybean. MATERIALS AND METHODS Experimental Design The treatments consisted of soybean seeds of the DM 5958 RSF IPRO cultivar with vigor variations obtained under controlled conditions. Accelerated aging vigor tests (Krzyzanowski et al., 1999) and germination tests (Brasil Ministério da Agricultura, Pecuária e Abastecimento, 2009) were initially performed to test the physiological quality of the seed. The seed lot presented 94% germination and 90% vigor. To obtain different levels of vigor, the seeds were aged, which were subjected to high temperatures and humidity, aiming to maintain the germination potential above 80%, confirmed by germination test. Whereas, the initial vigor was markedly reduced, which was confirmed by the accelerated aging test (Krzyzanowski et al., 1999) followed by another germination test. To obtain different of vigor levels the seeds were exposed to 32°C heat and 95% humidity for 0, 120, 192, and 216 h, thus obtaining vigor levels of 90% (94% of germination), 75% (91% of germination), 63% (91% of germination), and 48% (85% of germination), respectively. These values were determined in three replicates. In this study, 90% was considered high vigor level; 75%, medium vigor level; 63%, low vigor level; and 48%, very low vigor level. Vigor declines before germination reduction (Krzyzanowski and França-Neto, 2001; Egli et al., 2005), therefore seeds with close germination values may present different levels of vigor (Krzyzanowski and França-Neto, 2001). Procedure The experiment was conducted at three sites: (i) the municipality of Coxilha, Rio Grande do Sul state (RS), Brazil (28°07´ S; 52°17´ W; 721 m altitude); (ii) Tapejara, RS, Brazil (28°04´ S; 52°00´ W; 658 m altitude); and (iii) Passo Fundo, RS, Brazil, (28°12´ S; 52°23´ W; 667 m altitude). All sites are located in a humid subtropical climate region with humic dystrophic Red Latosol soil. The experiment was performed in a no-tillage system, with winter crops. Sowing was accompanied by fertilization with 6 kg ha–1 N, 60 kg ha–1 P2O5, and 60 kg ha–1 K 2O. Seeds were inoculated with Bradyrhizobium japonicum and treated with insecticides (imidacloprid and thiodicarb) and fungicides (carbendazim and thiram) according to recommendations for soybean crops. Phytosanitary management was done to control pests, diseases, and weeds. 2

A randomized block experimental design was used, with four replications and four treatments, a total of 16 experimental units. Plots were 7 m long and consisted of 14 rows with a 0.45-m spacing. For all treatments the same seeding rate was used. Plant Growth and Development For the destructive evaluations, 10 plants along the sowing row were collected from each plot. Root and shoot dry mass (DM) were measured at stage V1 (Fehr and Caviness, 1977). The plants were divided into shoots and roots and placed in a drying oven (60°C) until they reached a constant mass. After drying, shoot DM and root DM were determined per plant (g plant–1). A second evaluation of shoot DM was performed when plants reached stage R1 (Fehr and Caviness, 1977). The area of the first trefoliate leaf was measured at stage V2 (Fehr and Caviness, 1977), and the leaf area (LA) at stage R1. Both analyses were performed destructively using a leaf area meter (LI-3100C, LI-COR Biosciences, Lincoln, NE). The final population density of plants was determined at stage R1 by counting the number of plants within 6 m per plot and converted into number of plants per hectare (plant ha–1). Plant height was measured from the soil surface to the apical meristem of the main stem. The diameter of the stem was measured at ground level with the use of a caliper. Both measurements were performed at stages V3 (Fehr and Caviness, 1977) and R1. Nodulation Nodulation was evaluated destructively in 10 plants per plot sequentially along the sowing row by counting the number of nodules (NN) at stage V3. The nodules were taken to a drying oven (60°C) for dehydration until they reached constant mass. After drying, the nodule dry mass (NDM) per plant was determined (g plant–1). Total Soluble Sugar and Starch Content Total soluble sugar and starch quantities were determined at stage V8 (eighth node–seventh trifoliate leaf fully developed; Fehr and Caviness, 1977). The fourth, seventh, and ninth nodes were collected from 10 plants sequentially along the sowing row. The nodes were stored in an ultrafreezer (500H, SUPEROHM, Piracicaba, São Paulo, Brazil), dried in an oven at 60°C, and ground to obtain a homogeneous dry mass. The total soluble sugar content was then determined by the phenolsulfuric acid method (DuBois et al., 1956). The resulting pellet was treated with perchloric acid, and aliquots of the supernatant were used to determine the starch content (McCready et al., 1950). The experiment was performed in triplicate, and the results are expressed as mmol kg–1 dry mass (mmol kg–1 DM). Spatial Variability of Grain Yield Per Plant To determine the variability in production among the plants, the grain yield was analyzed for 10 plants per plot, sequentially along the sowing row. After determining the yield, the standard deviation for each plot was calculated and then subjected to statistical analysis. The schematic diagram was generated from the grain yield analysis, and the yield in grams was calculated.

Agronomy Journal • Volume 110, Issue 4 • 2018

Grain Yield Components The yield components were evaluated by plant stratification at physiological maturation stage. The numbers of productive nodes (NPN) and unproductive nodes (NUN) on the main stem and the number of pods (NP) and number of seeds (NS) on the whole plant (main stem plus branches) were determined. To NPN and NUN the analysis were based on presence or absence of pods or seeds. Harvesting was completed using a plot harvester (WINTERSTEIGER Classic, AT). The samples were weighed and corrected for 13% moisture, and the grain yield (kg ha–1) and thousand-seed weight (TSW) were defined.

2, whereas the stem diameter was smaller for the highest vigor levels (75% and 90%) at Site 3 (Fig. 2B). At stage V3, the plant height for the 90% vigor level were 2.5, 5.4, and 2.8 cm greater than those of the 48% vigor level at Sites 1, 2, and 3, respectively (Fig. 2C). The differences in plant height (stage R1) between 90% and 48% vigor were 16.3, 16.9, and 24.3 cm at Sites 1, 2, and 3, respectively (Fig. 2D). Positive linear trends were observed for the variables stem diameter at stage V3 and plant height at the different evaluation points. The regression indicated that the increase in vigor decreased stem diameter at stage R1 only at Site 3.

Statistical Analysis

Nodulation

The data were subjected to analysis of variance and means were compared with a Tukey test at 0.05 error probability comparing the vigor levels in each site. In addition, regression and Pearson correlation analyses were performed among the variables at 0.05, 0.01 and 0.001 error probability. RESULTS Plant Growth and Development Seeds with higher vigor levels produced plants with higher shoot DM values at stage V1 (Fig. 1A). Shoot DM was greatest for the 90% vigor level, which was approximately 1.6 times the dry mass for 48% vigor at Sites 1 and 3. For Site 2, the difference was even more pronounced, at 2.4 times. Shoot DM at stage R1 did not present significant differences among vigor levels for Sites 1 and 2 (Fig. 1B). For Site 3, production of dry mass was 1.7 times greater for the 63% vigor level compared with the 90% vigor level. Greater growth of the first trifoliate leaf was observed at site 2 for the 90% vigor seeds, which were 11.8 cm2 larger than the trifoliate leaves from the 48% vigor seeds (Fig. 1C). For Sites 1 and 3, these differences were 4.6 and 9.2 cm2 , respectively. No significant difference was observed in LA at stage R1 at Sites 1 and 2 among the different vigor levels (Fig. 1D). Plants from the 63% vigor seeds presented a LA of 4189 cm2 , which is 2263 cm2 more than the LA for the 90% vigor seeds. Root DM at stage V1 was greater for plants from the 75% and 90% vigor seeds at all sites. Root DM increased with vigor levels (Fig. 1E). The plant population density of the 90% vigor plants was 51, 65, and 44% greater than that of the 48% vigor plants at Sites 1, 2, and 3, respectively (Fig. 1F). The regression equations for the area of the first trifoliate leaf, shoot, and root DM, and population density at the three sites evaluated showed a positive linear trend (Fig. 1). Thus, all of these variables increased with an increase in the level of vigor. The plant population densities for the high-vigor seed (90%) were estimated at approximately 251,000, 242,000, and 247,000 plants ha–1 at Sites 1, 2, and 3, respectively (Fig. 1F). For the lower vigor levels (63%), the number of plants per hectare was estimated at 163,000, 127,000, and 170,000 plant ha–1 at Sites 1, 2, and 3, respectively. At the 90% level of vigor, the differences in the plant population density among sites were not significant, but at 63% vigor, there was a difference of 36,000 plant ha–1 in the population density at Site 2 compared with Site 1. Stem diameter at stage V3 was greater for plants from the 75% and 90% vigor seeds (Fig. 2A). No significant differences were observed in stage R1 among the vigor levels at Sites 1 and

For the 75%, 63%, and 48% vigor levels, the decreases (%) in the number of nodules per plant, compared with the 90% vigor level, were approximately 10, 44, and 35% at Site 1; 5, 50 and 56% at Site 2; and 27, 38, and 42% at Site 3 (Fig. 3A). The highest NDM values were from plants originated from the 75% and 90% vigor seeds. The 90% vigor level plants 58% greater than the 48% vigor level at Site 1 and 2, and 63% greater at Site 3 (Fig. 3B). A 1% increase in vigor level was associated with an average increase of 6.21 in the number of nodules. This increase in number of nodules was 59, 53, and 42% determined by vigor levels at Sites 1, 2, and 3, respectively. Because the NDM increased 100 mg with each percentage point increase in vigor, NDM was 70, 56, and 62% determined by vigor levels at Sites 1, 2, and 3, respectively. Total Soluble Sugar and Starch Content The total soluble sugar content in the different analyzed nodes did not vary with seed vigor level (Fig. 4A-C). Variation in starch content was observed only for the fourth node at Site 2, in which plants from seeds with higher vigor presented greater starch content (Fig. 4D-F). Variability of Grain Yield per Plant The standard deviation of grain yield among the different levels of seed vigor demonstrated the yield variability, and the lowest levels of vigor had great variation in yield among plants (Fig. 5A). This difference was 7.0, 5.1, and 3.8 times greater for the 48% vigor plants as compared with the 90% at Sites 1, 2, and 3, respectively. Figure 5B shows the variation in grain yield in grams for plants grown from seeds with different levels of vigor. Grain Yield Primary and Secondary Components The numbers of productive and unproductive nodes per plant did not vary for the different vigor levels in this experiment (Fig. 6A and 6B). The numbers of pods and seeds were greater in plants from lower-vigor seeds (Fig. 6C and 6D). The results obtained for the TSW show an increase with increased vigor levels (Fig. 6E). Plants grown from the 90% vigor seeds produced 1180, 1376, and 1307 kg ha–1 more grains than plants grown from the 48% vigor seeds at Sites 1, 2, and 3, respectively (Fig. 6F). Regression analysis showed that the increase in vigor decreased the numbers of pods and seeds, but TSW and grain yield tended to increase with vigor.


3

Fig. 1. Shoot dry mass, root dry mass, first trifoliate leaf area, leaf area, and plant population for soybean plants germinated from seeds with four vigor levels (48%, 63%, 75%, and 90%). Shoot dry mass at stage V1 (A), shoot dry mass at stage R1 (B), area of first trifoliate at stage V2 (C), leaf area at stage R1 (D), root dry mass at stage V1 (E), and plant population density (F). Values followed by distinct letters for each site differ from each other based on a Tukey test (P < 0.05). * Indicates values that are significantly different in regression analysis (P < 0.05). S 1, site 1; S 2, site 2; S 3, site 3.

Correlation between Grain Yield and Seed Vigor At three sites where the experiment was conducted, a positive correlation existed between both grain yield and vigor and the number of nodules, nodule dry mass, plant population density, and thousand-seed weight, except at Site 3 for grain yield and thousand-seed weight (Table 1). The numbers of productive and unproductive nodes were not significantly correlated with grain yield, and for all sites, the numbers of pods and seeds were inversely correlated with both grain yield and vigor. A strong direct correlation existed between vigor and grain yield, with higher vigor levels leading to higher grain yield.

4

DISCUSSION Seed Vigor Influences the Plant Population Density, Dry Mass, and Leaf Area Several previous studies demonstrated that seed vigor affects germination, seedling development, and overall yield of agricultural crops (Krzyzanowski and França Neto, 2001; Vanzolini and Carvalho, 2002; Kolchinski et al., 2005; Finch-Savage and Bassel, 2016). In the present study, the initial growth of soybean plants from seeds with higher vigor levels provided better soil coverage. Thus, these plants presented a greater capacity to intercept solar radiation at the beginning of the cycle, causing them to be more competitive for space and natural resources (Weiner, 1990; Müller et al., 2017). Agronomy Journal • Volume 110, Issue 4 • 2018

Fig. 2. Stem diameter and height in soybean plants originated from seeds of four vigor levels (48%, 63%, 75%, and 90%). Stem diameter at stage V3 (A), stem diameter at stage R1 (B), plant height at stage V3 (C), and plant height at stage R1 (D). Values followed by distinct letters for each site differ from each other based on a Tukey test (P < 0.05). * Indicates values that are significantly different in regression analysis (P < 0.05). S 1, site 1; S 2, site 2; S 3, site 3.

Fig. 3. Number of nodules and nodule dry mass in soybean plants originated from seeds of four vigor levels (48%, 63%, 75%, and 90%). Number of nodules at stage V3 (A) and nodule dry mass at stage V3 (B). Values followed by distinct letters for each site differ from each other based on a Tukey test (P < 0.05). * Indicates values that are significantly different in regression analysis (P < 0.05). S 1, site 1; S 2, site 2; S 3, site 3.

The greater accumulation of root and shoot DM, as well as greater LA of the first trifoliate leaf in the V1 and V2 phenological stages of the plants originated from the highest vigorous seeds (90% and 75% vigor level), show the importance and the effects of the seed physiological quality. This can be linked to the reserves available to the healthy embryo and to the enzymatic activity for the metabolism of the germination process. Seeds in these conditions exhibit a greater capacity to

transform the reserves from the storage tissues and incorporate them into the embryonic axis (Dan et al., 1987). Thus, likely resulting in faster and more uniform emergence and in seedlings with a larger initial size (Vanzolini and Carvalho, 2002), and influencing leaf area and accumulation of dry mass, as observed in the present study. Höfs et al. (2004) also demonstrated that seeds with high vigor level had uniform emergence and produced plants with more leaf area and dry mass.


5

Fig. 4. Total soluble sugar and starch contents in nodes of soybean plants originated from seeds of four vigor levels (48%, 63%, 75%, and 90%). Sugar content for the fourth node (A), sugar content for the seventh node (B), sugar content for the ninth node (C), starch content for the fourth node (D), starch content for the seventh node (E), and starch content for the ninth node (F). Values followed by distinct letters for each site differ from each other based on a Tukey test (P < 0.05). NS, not significant; S 1, site 1; S 2, site 2; S 3, site 3.

Plants from low-vigor seeds exhibited more robust growth due to the decreased intraspecific competition from the established plant population. A decrease in plant population density was also observed by Vanzolini and Carvalho (2002) in less vigorous soybean seed plots. Seed Vigor Influences Plant Height, Stem Diameter, and Nodulation Although plant population density is greater with the highestvigor seeds, along with possible changes in the red and red extreme wavelength ratios, the most important difference may be the higher stature of these plants at the beginning of vegetative development. This is related to the physiological quality of the seed. The growth pattern presented by the plants continues until the beginning of the reproductive period. Effects of seed vigor on plant height were also found by Vanzolini and Carvalho (2002), Schuch et al. (2009) and Scheeren et al. (2010). High-vigor seeds showed 11.5% greater height, with a difference in height of 2.5 cm between plants, which continued to be evident until the beginning of the reproductive period (Scheeren et al., 2010). These results are a consequence of the faster emergence rate of seedlings from more vigorous seeds, and the greater competitive ability of these plants to utilize the resources of the environment in production (Vanzolini and Carvalho, 2002). Plants from less vigorous seeds and, consequently, with lower population density and smaller stature presented a more open architecture, i.e., with more horizontal growth compared with 6

the plants originating from seeds of greater vigor (Vanzolini and Carvalho, 2002). Thus, the plants may have a larger stem diameter. However, in our study, at initial development stage V3, the stem diameter of plants from less vigorous seeds was smaller. As the plants continued to develop, only at Site 3 did the plants from low-vigor seeds exhibited larger stem diameters by the reproductive stage. This result could be because competition was lower in this experiment due to the lower population density, which also likely reflected in the smaller plant heights. In this study, a correlation between both grain yield and seed vigor and the number of nodules and nodule dry mass was observed. With the best growth performance in the early stages of the development of plants from higher-vigor seeds, photoassimilates were likely more available to the nitrogen-fixing bacteria, as reflected in the increased number and dry mass of nodules. Smith and Ellis (1980) observed that the efficiency of nodulation promoted by B. japonicum was directly proportional to the germination speed. The first seedlings to emerge produced higher numbers of nodules, suggesting that soybean plant nodulation may be influenced by seedling vigor (Smith and Ellis, 1980). The observed increase in nodulation provides more evidence that seed vigor exerts some direct or indirect role in soybean nodulation; however, additional research is needed. Previous studies have shown that soybean plants transfer approximately 14% of the net assimilated carbon to the symbiotic organisms (Kaschuk et al., 2009), and as a reflection of seed vigor, plants


Fig. 5. Standard deviation of grain yield indices for soybean plants originated from seeds of four vigor levels (48%, 63%, 75%, and 90%). Variation in grain yield per plant (kg ha–1) (A) and schematic representation of plant variability (B). Values followed by distinct letters for each site differ from each other based on a Tukey test (P < 0.05). S 1, site 1; S 2, site 2; S 3, site 3.

with greater primary metabolism activity should show higher rates of symbiotic nitrogen fixation. Spatial Variability in Grain Yield due Seed Vigor The spatial variability in grain yield among plants derived from seeds with low levels of vigor may be due to the lack of uniformity in seedling emergence, resulting in the establishment of “dominant” and “dominated” soybean plants. In addition, the distribution of the germinated seeds did not result in regular row distribution, presenting interspaced gaps. Plants that were next to the gaps received more solar radiation and consequently became dominant plants, which was reflected in their higher production. Dominated plants, in which growth was slower, produced less. Thus, in plants where the interception of solar radiation was compromised by dominant plants, the concentration of assimilates in the grains filling decreased (Ottman and Welch, 1989), decreasing grain yield (Müller et al., 2017). According to Egli (1993), earlier-emerging soybean seedlings have a competitive advantage over those that emerge later in alternate positions in the same row, which translates into greater grain yield per plant. In the present study, great variation was found in the production per plant among those with the same level of vigor (Fig. 5), especially in groups grown from the lowervigor seeds. Thus, the analysis of grain production in grams showed that plants from lower-vigor seed may present higher production indices, but this production is not reflected in the final yield because the plant population density is much lower.

Increased variability among plants with seeds of low physiological quality was also observed in soybean by Cantarelli et al. (2015). For both dominant and dominated plants, grain yield loss tends to be less for soybean than for maize, for example, because soybean plants have a greater ability to compensate through the number of branches, pods, and grains (Lueschen and Hicks, 1977). Seed Vigor Influences Grain Yield Soybean plants have a metameric architecture that provides their leaves reserves nearest to the pods (Larson and Dickson, 1973). In this way, productive of fertility nodes reflects in greater yield (Egli, 2013). Soybean yield components are defined by node fertility, which is reflected in the number of pods, seeds number, and grain mass. Therefore, the production of sugars originating from photosynthesis on nearby leaves is important as a source of energy (Chavarria et al., 2017). However, in the present study, the numbers of productive and unproductive nodes on the main stem did not correlated to greater grain yield from higher-vigor seeds. The results for the productive and unproductive nodes are in accordance with the determinations of the total soluble sugar and starch contents in different nodes, which did not vary significantly among plants from different vigor levels. Soybean stems are the main sites of carbohydrate storage (Ciha and Brun, 1978) that are used as energy sources. Antos and Wiebold (1984) reported that the soluble sugar and starch concentrations in the lower third of the vegetative canopy were less than those in the upper part.


7

Fig. 6. Numbers of productive and unproductive nodes per plant, numbers of pods and seeds per plant, thousand-seed weight, and grain yield of soybean plants originated from seeds of four vigor levels (48%, 63%, 75%, and 90%). Number of productive nodes (A), number of unproductive nodes (B), number of pods (C), number of seeds (D) thousand-seed weight (E), and grain yield (F). Values followed by distinct letters for each site differ from each other based on a Tukey test (P < 0.05). * Indicates values that are significantly different in regression analysis (P < 0.05). S 1, site 1; S 2, site 2; S 3, site 3.

Our results are congruent with their observations, as total soluble sugar and starch contents were lower in the lower nodes. The numbers of pods and seeds per plant were inversely correlated with total grain production because plants grown from lower-vigor seed presented better performance for these variables. However, these were not the plants that presented the highest total grain production, as the higher production per plant did not compensate for the lower population density. The present results emphasize that the seed vigor had a direct effect on plant population and an indirect effect of grain yield. Seeds exposed to 216 h to 32°C and 95% humidity have their vigor reduced considerably, thus demonstrating the fragility 8

of their physiological quality. The data presented here indicate that the reduction of seed vigor affected drastically the population density compromising the grain yield. Our results agree with the results obtained by Kolchinski et al. (2005), Schuch et al. (2009), and Scheeren et al. (2010), who reported higher soybean yields using higher-vigor seeds. Since the use of lower-vigor soybean seeds compromises the adequate population density of the crop and indirectly affects the production of grains.


Table 1. Correlation of grain yield and varying vigor levels with primary and secondary components of soybean yield. Variable

NN† (n°)

NDM (g)

PPD (n°)

NPN (n°)

Yield Vigor

0.69** 0.75***

0.83*** 0.82***

0.93*** 0.96***

0.20ns 0.15ns

Yield Vigor

0.69** 0.68**

0.74*** 0.72**

0.77*** 0.81***

–0.24ns –0.17ns

Yield Vigor

0.60* 0.67**

0.71** 0.79***

0.82*** 0.95***

–0.42ns –0.30ns

NUN (n°) Site 1 0.43ns 0.50* Site 2 0.40ns 0.47ns Site 3 0.23ns 0.35ns

NP (n°)

NS (n°)

TSW (g)

Yield (kg ha–1)

–0.66** –0.79***

–0.66** –0.78***

0.64** 0.77***

0.96***

–0.76*** –0.77***

–0.77*** –0.79***

0.64** 0.61*

0.98***

–0.55* –0.55*

–0.52* –0.52*

0.45ns 0.60*

0.88***

*, **, and *** denote significance at P < 0.05, P < 0.01, and P < 0.001, respectively. NS = nonsignificant. † NN, number of nodules; NDM, nodule dry mass; PPD, plant population density; NPN, number of productive nodes; NUN, number of unproductive nodes; NP, number of pods; NG, number of seeds; and TSW, thousand-seed weight.

Acknowledgments We acknowledge the financial support provided by Sementes e Cabanha Butiá, Associação dos Produtores e Comerciantes de Sementes e Mudas do Rio Grande do Sul (APASSUL) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for PNPD/CAPES scholarship of Andréia Caverzan and Prosup/CAPES scholarship of Rafael Giacomin and Mariele Müller. References Antos, M., and W.J. Wiebold. 1984. Abscission, total soluble sugars, and starch profiles within a soybean canopy. Agron. J. 76:715–719. doi:10.2134/agronj1984.00021962007600050002x Brasil Ministério da Agricultura, Pecuária e Abastecimento. 2009. Regras para análise de sementes. Ministério da Agricultura, Pecuária e Abastecimento. Secretária de Defesa Agropecuária, Brazil. Board, J.E., and C.S. Kahlon. 2011. Soybean yield formation: What controls it and how it can be improved? In: H.A. El-Shemy, editor, Soybean physiology and biochemistry. Intech, Rijeka, Croatia. p. 1–37. Cantarelli, L.D., L.O.B. Schuch, L.C. Tavares, and de A.R. Cassyo. 2015. Variability of soybean plants originated from seeds with different levels of physiological quality. Acta Agron. 64:234–238. Ciha, A.J., and W.A. Brun. 1978. Effect of pod removal on nonstructural carbohydrate concentration in soybean tissue. Crop Sci. 18:773– 776. doi:10.2135/cropsci1978.0011183X001800050020x Chavarria, G., A. Caverzan, M. Müller, and M. Rakocevic. 2017. Soybean architecture plants: From solar interception to crop protection. In: M. Kasai, editor, Soybean: The basis of yield, biomass and productivity, Intech, Rijeka, Croatia. p. 15–33. Dan, E.L., V.D.C. Mello, C.T. Wetzel, F. Popinigis, and E.P. Souza. 1987. Transferência de matéria seca como método de avaliação do vigor de sementes de soja. Rev. Bras. Sementes 9:45–55. Dan, L.G.M., H.A. Dan, A.L. Braccini, A.L.L. Barroso, T.T. Ricci, G.G. Piccinin, and C.A. Scapim. 2012. Insecticide treatment and physiological quality of seeds, insecticides. In: F. Perveen, editor, Advances in integrated pest management, Intech, Rijeka, Croatia. p. 327–342. DuBois, M., K.A. Gilles, J.K. Hamilton, P.A. Rebers, and F. Smith. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28:350–356. doi:10.1021/ac60111a017 Egli, D.B. 1993. Relationship of uniformity of soybean seedling emergence to yield. J. Seed Technol. 17:22–28. Egli, D.B. 1994. Mechanisms responsible for soybean yield response to equidistant planting patterns. Agron. J. 86:1046–1049. doi:10.2134/ agronj1994.00021962008600060021x Egli, D.B., D.M. TeKrony, J.J. Heitholt, and J. Rupe. 2005. Air temperature during seed filling and soybean seed germination and vigor. Crop Sci. 45:1329–1335. doi:10.2135/cropsci2004.0029

Egli, D.B. 2013. The Relationship between the number of nodes and pods in soybean communities. Crop Sci. 53:1668–1676. doi:10.2135/ cropsci2012.11.0663 Fehr, W.R., and C.E. Caviness. 1977. Stages of soybean development. Spec. Rep. 80. Iowa State University of Science and Technology, Ames, IA. Finch-Savage, W.E., and G.W. Bassel. 2016. Seed vigor and crop establishment: Extending performance beyond adaptation. J. Exp. Bot. 67:567–591. doi:10.1093/jxb/erv490 Henning, F.A., L.M. Mertz, E.A. Jacob, Jr., R.D. Machado, G. Fiss, and P.D. Zimmer. 2010. Chemical composition and reserve mobilization in soybean seeds with high and low vigor. Bragantia 69:727–734. doi:10.1590/S0006-87052010000300026 Höfs, A., L.O.B. Schuch, S.T. Peske, and A.C.S.A. Barros. 2004. Emergence and initial growth of rice seedlings according to seed vigor. Rev. Bras. Sementes 26:92–97. ISTA. 2015. International rules for seed testing. International Seed Testing Association, Basserdorf, Switzerland. Kaschuk, G., T.W. Kuyper, P.A. Leffelaar, M. Hungria, and K.E. Giller. 2009. Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol. Biochem. 41:1233–1244. doi:10.1016/j.soilbio.2009.03.005 Krzyzanowski, F.C., R.D. Vieira, and J.B. França-Neto. 1999. Vigor de Sementes: Conceitos e testes. Associação Brasileira de Tecnologia de Sementes-ABRATES, Londrina, Brazil. Krzyzanowski, F.C., and J.B. França-Neto. 2001. Vigor de sementes. Informativo ABRATES 11:81–84. Krzyzanowski, F.C., J.B. França-Neto, A.A. Henning, and N.P. Costa. 2008. A semente de soja como tecnologia e base para altas produtividades- série sementes. Embrapa Soja. Circular Técnica, 55. Embrapa Soja, Londrina, Brazil. Kolchinski, E.M., L.O.B. Schuch, and S.T. Peske. 2005. Seeds vigor and intra-specific competition in soybean. Cienc. Rural 35:1248–1256. doi:10.1590/S0103-84782005000600004 Larson, P., and R. Dickson. 1973. Distribution of imported 14C in developing leaves of eastern cottonwood according to phyllotaxy. Planta 111:95–112. doi:10.1007/BF00386270 Lueschen, W.E., and D.R. Hicks. 1977. Influence of plant population on field performance of three soybean cultivars. Agron. J. 69:390–393. doi:10.2134/agronj1977.00021962006900030015x Macholdt, J., and B. Honermeier. 2017. Impact of highly varying seeding densities on grain yield and yield stability of winter rye cultivars under the influence of delayed sowing under sandy soil conditions. Arch. Agron. Soil Sci. 63:1977–1992. doi:10.1080/03650340.2017 .1319048 Maddonni, G.A., and M.E. Otegui. 2006. Intra-specific competition in maize: Contribution of extreme plant hierarchies to grain yield, grain yield components and kernel composition. Field Crops Res. 97:155–166. doi:10.1016/j.fcr.2005.09.013


9

McCready, R.M., J. Guggolz, V. Silviera, and H.S. Owens. 1950. Determination of starch and amylase in vegetables. Anal. Chem. 22:1156– 1158. doi:10.1021/ac60045a016 Müller, M., M. Rakocevic, A. Caverzan, and G. Chavarria. 2017. Grain yield differences of soybean cultivars due to solar radiation interception. Am. J. Plant Sci. 8:2795–2810. doi:10.4236/ajps.2017.811189 Ottman, M.J., and L.F. Welch. 1989. Planting patterns and radiation interception, plant nutrient concentration, and yield in corn. Agron. J. 81:167–174. doi:10.2134/agronj1989.00021962008100020006x Riedell, W.E., S.L. Osborne, and J.L. Pikul, Jr. 2013. Soil attributes, soybean mineral nutrition, and yield in diverse crop rotations under no-till conditions. Agron. J. 105:1231–1236. doi:10.2134/ agronj2013.0037 Scheeren, B.R., S.T. Peske, L.O.B. Schuch, and A.C.A. Barros. 2010. Physiological quality of soybean seeds and productivity. Rev. Bras. Sementes 32:35–41. doi:10.1590/S0101-31222010000300004

10

Schuch, L.O.B., E.M. Kolchinski, and J.A. Finatto. 2009. Seed physiological quality and individual plants performance in soybean. Rev. Bras. Sementes 31:144–149. doi:10.1590/S0101-31222009000100016 Smith, R.S., and M.A. Ellis. 1980. Soybean nodulation as influenced by seedling vigor. Agron. J. 72:605–608. doi:10.2134/agronj1980.000 21962007200040008x Tourino, M.C.C., P.M. de Rezende, and N. Salvador. 2002. Row spacing, plant density and intrarow plant spacing uniformity effect on soybean yield and agronomic characteristics. Pesqi. Agropecu. Bras. 37:1071–1077. doi:10.1590/S0100-204X2002000800004 Vanzolini, S., and N.M. Carvalho. 2002. Effects of soybean seed vigor on field plant performance. Rev. Bras. Sementes 24:33–41. Weiner, J. 1990. Asymmetric competition in plant populations. Trends Ecol. Evol. 5:360–364. doi:10.1016/0169-5347(90)90095-U
