Di-nitrogen fixation at the early and late growth stages of soybean

Soybean derives a significant portion of the required nitrogen (N) from the symbiosis with rhizobia bacteria. However, information on the available genetic variation for N₂ fixation capacity in different growth stages of soybean is limited. The objective of this study was to investigate the N₂ fixation capacity of 22 soybean lines compared with that of non-nodulating and supernodulating checks at the early and late growth stages and identify the most informative traits for selection. Two cycles of greenhouse experiments were carried out to estimate the percentage of N derived from the atmosphere (%Ndfa) as well as 10 different traits related to N₂ fixation. The results showed that %Ndfa was significantly different among the lines at the early and late growth stages. SPAD readings showed the highest correlation with the early N₂ fixation, whereas shoot dry weight with the late N₂ fixation. Early and late %Ndfa could be used to select superior lines for N₂ fixation and study the underlying physiological and molecular mechanism.

Keywords:
Glycine max; %Ndfa; ¹⁵N dilution technique; nodulation; symbiosis

Authorship

Raphael Lemes Hamawaki ^**Author for correspondence. E-mail:hamawaki@siu.edu

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Ministério da Educação, Setor Bancário Norte, Quadra 2, Bloco L, Lote 06, Asa Norte, 70040-020, Brasília, Distrito Federal, Brazil. Ministério da EducaçãoBrazilBrasília, Distrito Federal, BrazilCoordenação de Aperfeiçoamento de Pessoal de Nível Superior, Ministério da Educação, Setor Bancário Norte, Quadra 2, Bloco L, Lote 06, Asa Norte, 70040-020, Brasília, Distrito Federal, Brazil.

Department of Plant, Soil and Agricultural Systems, Southern Illinois University Carbondale,1205 Lincoln Dr., Carbondale, Illinois, 62901, USA.Southern Illinois UniversityUSACarbondale, Illinois, USADepartment of Plant, Soil and Agricultural Systems, Southern Illinois University Carbondale,1205 Lincoln Dr., Carbondale, Illinois, 62901, USA.

Stella K Kantartzi

*Author for correspondence. E-mail:hamawaki@siu.edu

SCIMAGO INSTITUTIONS RANKINGS

Figures | Tables | Formulas

Figures (3)
Tables (3)
Formulas (1)

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Figure 1
Comparison of %Ndfa at the early growth stage (35 d after emergence) between each of the 22 lines and the supernodulating line, SS2-2, using the Dunnett's multiple comparison test. Different letters indicate significant differences between the line and the check. Error bars indicate one standard error of the mean.

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Figure 2
Comparison of %Ndfa at the late growth stage (R7) between each of the 22 lines and the supernodulating line, SS2-2, using the Dunnett's multiple comparison test. Different letters indicate significant differences between the line and the check. Error bars indicate one standard error of the mean.

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Figure 3
Clustering of 23 soybean lines and the two non-nodulating lines, Nitrasoy and D68-099, based on %Ndfa at the early (35 days after emergence; left) and late (R7; right) growth stages using the Ward's method.

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Table 1
Leaf (LAT%) and pod (PAT%) enrichment of ¹⁵N and least squares means for early and late percentage of nitrogen derived from atmosphere (%Ndfa) for 22 lines, one supernodulating line, and two non-nodulating lines grown under greenhouse conditions for two growing seasons in ¹⁵N-labelled soil.

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Table 2
Comparison of nitrogen fixation-related traits among 22 lines, one supernodulating line, and two non-nodulating lines grown under greenhouse conditions for two growing seasons in ¹⁵N-labelled soil.

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Table 3
Correlation matrix of ¹⁵N enrichment and N fixation related traits for 22 lines, one supernodulating line, and two non-nodulating lines grown under greenhouse conditions for two growing seasons in ¹⁵N-labelled soil.

Thumbnail

Figure 1 Comparison of %Ndfa at the early growth stage (35 d after emergence) between each of the 22 lines and the supernodulating line, SS2-2, using the Dunnett's multiple comparison test. Different letters indicate significant differences between the line and the check. Error bars indicate one standard error of the mean.

Figure 2 Comparison of %Ndfa at the late growth stage (R7) between each of the 22 lines and the supernodulating line, SS2-2, using the Dunnett's multiple comparison test. Different letters indicate significant differences between the line and the check. Error bars indicate one standard error of the mean.

Figure 3 Clustering of 23 soybean lines and the two non-nodulating lines, Nitrasoy and D68-099, based on %Ndfa at the early (35 days after emergence; left) and late (R7; right) growth stages using the Ward's method.

Table 1 Leaf (LAT%) and pod (PAT%) enrichment of ¹⁵N and least squares means for early and late percentage of nitrogen derived from atmosphere (%Ndfa) for 22 lines, one supernodulating line, and two non-nodulating lines grown under greenhouse conditions for two growing seasons in ¹⁵N-labelled soil.

Soybean line	Early (35 DAE) %Ndfa			Late (R7) %Ndfa
Soybean line	LAT%	D68-099	Nitrasoy	PAT%	D68-099	Nitrasoy
JTN-4307	0.1642	20	18	0.0121	85	88
JTN-5203	0.1759	14	12	0.0157	82	85
Osage	0.1469	27	25	0.0207	74	81
Ozark	0.1517	27	24	0.0138	84	87
R05-3239	0.1671	20	18	0.0216	74	79
Jake	0.1727	16	14	0.0149	83	86
Saluki 4910	0.1837	12	9	0.0148	83	85
Bragg	0.1784	14	12	0.0091	90	91
Davis	0.1398	31	29	0.0098	89	91
Enrei	0.1498	26	25	0.0679	20	32
Williams	0.1512	27	25	0.0180	80	82
PI 471938	0.1793	10	9	0.0139	82	86
Clark	0.1771	12	10	0.0118	87	88
Bossier	0.1537	25	24	0.0091	89	91
Centennial	0.1618	22	20	0.0124	85	88
Hardee	0.1546	26	24	0.0109	87	90
Jackson	0.1822	11	9	0.0267	67	73
S.J.2	0.1968	4	2	0.0105	88	90
J-200	0.1724	14	13	0.0161	83	84
R01-416F	0.1529	25	23	0.0128	85	87
PI 96169B	0.1890	7	6	0.1322	0	0
PI 96171	0.1469	27	25	0.0632	26	34
Supernodulating check
SS2-2	0.1255	38	38	0.0129	86	88
Non-nodulating checks
Nitrasoy	0.2023			0.1071
D68-099	0.2080			0.0930
Analysis of variance
Genotype (G)	< 0.0001	< 0.0001	< 0.0001	< 0.0001	< 0.0001	< 0.0001
Evaluation Cycle (EC)	< 0.0001	< 0.0001	< 0.0001	ns	ns	ns
G x EC	< 0.0001	< 0.0001	< 0.0001	< 0.0001	< 0.0001	< 0.0001
Multiple comparison test
Tukey HSD 95%	0.0443	22	21	0.0277	32	27

Table 2 Comparison of nitrogen fixation-related traits among 22 lines, one supernodulating line, and two non-nodulating lines grown under greenhouse conditions for two growing seasons in ¹⁵N-labelled soil.

	SPD	SDW	TSW	TSN	MSW	L%N	P%N	NN	NDW	DTM
		g plant^-1	g plant^-1	number plant^-1	mg seed^-1	%	%	number plant^-1	mg plant^-1	number of days
JTN-4307	28.3	10.3	4.6	48.8	98	2.59	0.99	107.5	192	170
JTN-5203	26.6	7.2	2.8	34.8	76	2.51	1.58	55.8	139	164
Osage	25.5	12.9	3.6	42.4	82	2.86	1.10	89.7	205	176
Ozark	25.1	7.2	2.1	24.3	87	2.21	1.65	54.5	101	166
R05-3239	28.0	7.5	2.4	28.2	85	2.45	1.48	70.3	128	162
Jake	26.6	8.6	3.0	29.2	96	2.46	1.28	60.4	105	163
Saluki 4910	26.2	9.1	3.2	34.6	88	2.60	1.39	103.9	159	171
Bragg	20.1	14.0	2.7	30.8	108	1.88	1.16	136.1	245	180
Davis	24.8	10.9	1.9	20.9	73	2.63	1.64	56.4	100	175
Enrei	34.3	3.6	3.7	14.2	250	2.85	0.61	43.7	190	97
Williams	22.4	7.9	4.6	36.7	125	2.18	0.94	119.0	235	152
PI 471938	23.7	9.8	3.1	31.9	85	2.05	1.51	68.5	107	161
Clark	21.2	9.8	3.8	37.9	96	2.01	1.26	71.7	162	161
Bossier	23.4	15.6	2.6	31.7	77	2.38	1.32	154.0	294	186
Centennial	24.3	12.2	3.4	35.5	90	1.93	1.24	128.0	249	177
Hardee	25.5	12.2	2.1	26.9	68	2.25	1.45	81.4	156	189
Jackson	22.6	13.3	3.2	31.3	95	2.13	0.81	95.1	184	169
S.J.2	23.1	12.7	1.2	17.6	45	2.11	1.31	94.5	213	196
J-200	23.7	14.6	1.3	15.5	70	1.96	1.69	88.6	132	196
R01-416F	26.2	8.0	2.5	27.1	80	2.44	1.84	92.9	167	159
PI 96169B	27.7	3.0	1.6	10.3	163	1.85	0.47	2.9	32	107
PI 96171	30.9	3.5	1.9	16.4	117	2.47	0.85	40.1	139	108
Supernodulating check
SS2-2	31.3	9.8	4.6	48.8	112	3.49	1.58	294.1	541	157
Non-nodulating checks
Nitrasoy	21.7	4.0	0.4	7.3	54	1.58	0.73	0	0	179
D68-099	23.9	2.9	0.5	8.5	50	1.92	0.78	0	0	184
Analysis of variance
Genotype (G)	< 0.0001	< 0.0001	< 0.0001	< 0.0001	< 0.0001	< 0.0001	< 0.0001	< 0.0001	< 0.0001	< 0.0001
Evaluation Cycle (EC)	< 0.0001	< 0.0001	< 0.0001	<0.0002	< 0.0001	ns	< 0.0001	< 0.0001	< 0.0001	< 0.0001
G x EC	< 0.0001	< 0.0001	< 0.0001	< 0.0001	ns	0.0437	< 0.0001	< 0.0001	< 0.0001	< 0.0001

Multiple comparison test
Test mean	25.5	9.2	2.9	28.8	100	2.32	1.19	84.8	168	165
Tukey 95%	5.4	3.2	1.8	18.2	70	0.86	0.60	79.9	151	21

SPD, SPAD readings (mg chlorophyll m^-2); SDW, shoot dry weight (g plant^-1); TSW, total seed weight (g plant^-1); TSN, total seed number per plant; MSW, mean seed weight (mg seed^-1); L%N, leaf % nitrogen; P%N, pod % nitrogen, NN, number of nodules per plant; NDW, nodule dry weight (mg plant^-1); DTM, d to maturity.

Table 3 Correlation matrix of ¹⁵N enrichment and N fixation related traits for 22 lines, one supernodulating line, and two non-nodulating lines grown under greenhouse conditions for two growing seasons in ¹⁵N-labelled soil.

NDW

TSN

TSW

MSW

DTM

SPD

SDW

L%N

P%N

-LAT%

-PAT%

1.00

0.88**

0.33**

0.20**

-0.10**

-0.12**

-0.18**

0.39**

0.07^ns

0.20**

0.07^ns

0.27**

NDW

1.00

0.39**

0.30**

-0.01^ns

-0.16**

-0.11**

0.39**

0.08*

0.11**

0.09*

0.26**

TSN

1.00

0.78**

-0.02^ns

0.06^ns

-0.01^ns

0.31**

0.10*

-0.13**

0.20**

0.34**

TSW

1.00

0.40**

-0.06^ns

0.10*

0.12**

0.09*

-0.29**

0.24**

0.26**

MSW

1.00

-0.31**

0.23**

-0.27**

0.09*

-0.32**

0.08*

-0.18**

DTM

1.00

0.16**

0.26**

0.01^ns

-0.04 ^ns

0.16**

0.35**

SPD

1.00

-0.28**

0.44**

-0.23**

0.43**

-0.10**

SDW

1.00

0.00^ns

0.21**

0.03^ns

0.47**

L%N

1.00

0.10*

0.12**

0.09*

P%N

1.00

-0.18**

0.35**

-LAT%

1.00

0.15**

-PAT%

1.00

*, **. Significance at p < 0.05 and p < 0.01, respectively. NN, number of nodules per plant; NDW, nodule dry weight (mg plant^-1); TSW, total seed weight (g plant^-1); TSN, total seed number per plant; MSW, mean seed weight (mg seed^-1); DTM, d to maturity; SPD, SPAD readings (mg chlorophyll m^-2); SDW, shoot dry weight (g plant^-1); L%N, leaf % nitrogen; P%N, pod % nitrogen; -LAT%, negative leaf atom% ¹⁵N excess; -PAT%, negative pod atom% ¹⁵N excess.

% N d f a = (1 - \frac{{a t o m %}^{15} N e x c e s s N_{2} - f i x i n g p l a n t}{{a t o m %}^{15} N e x c e s s r e f e r e n c e p l a n t}) \times 100

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Di-nitrogen fixation at the early and late growth stages of soybean

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[1] *Author for correspondence. E-mail:hamawaki@siu.edu