Acta Physiol Plant (2011) 33:1877–1885 DOI 10.1007/s11738-011-0731-y
ORIGINAL PAPER
Morpho-physiology and maize grain yield under periodic soil flooding in successive selection cycles T. Correˆa de Souza • P. Ce´sar Magalha˜es F. Jose´ Pereira • E. Mauro de Castro • S. Netto Parentoni
•
Received: 14 June 2010 / Revised: 8 February 2011 / Accepted: 9 February 2011 / Published online: 1 March 2011 Ó Franciszek Go´rski Institute of Plant Physiology, Polish Academy of Sciences, Krako´w 2011
Abstract This study was carried out to evaluate maize plants of different recurrent selection cycles of the variety (Zea mays L.—Saracura-BRS-4154) regarded to genetic gains, morphophysiology, and grain yield, achieved over the selection cycles under intermittent flooding of the soil. This variety has the capacity to survive and produce in temporarily flooded soils and was developed by the National Maize and Sorghum Research Center (EMBRAPA). The experiment was conducted in greenhouse by using ten alternating selection cycles (Cycle 1–18) and BR 107 a variety known for its susceptibility to flooding. The flooding initiated at six-leaf stage by applying 50 mm of water three times a week. At flowering, the following parameters were evaluated: rate of leaf photosynthesis, stomatal conductance, intercellular CO2 concentration, transpiration rate, photosynthetically active leaf area, root porosity, relative chlorophyll content, grain yield, harvest
Communicated by S. Renault. T. C. de Souza (&) F. J. Pereira E. M. de Castro Departamento de Biologia, Universidade Federal de Lavras, Setor de Fisiologia Vegetal, Campus Universita´rio, Caixa Postal 37, Lavras, MG CEP 37200-000, Brazil e-mail:
[email protected]
index, ear length, and interval between male and female flowering. Yield as a function of root porosity and photosynthesis were also evaluated. An index was created in this study, in order to help the discussion of the characteristics evaluated, it was called ‘‘Relative Tolerance Value— RTV’’, only gaseous exchange measurements was not included in this index. By the way, it was observed throughout the selection cycles an increase in all gaseous exchange parameters, being the cycle 18, the one which presented the greatest averages. RTV for leaf area showed the greatest values for cycles 7 and 18, whereas root porosity, chlorophyll relative content, and harvest index, the greater RTV values were found in cycles 17 and 18. The largest grain yield RTV was observed in cycle 7, followed by cycles 13, 15, and 18. Flooding resulted in longer Anthesis-Silking Interval, especially for the first cycles. At flooding condition, grain yield was strongly related to root porosity (R2 = 0.66). These results showed that the selection cycles of ‘‘Saracura’’ maize improved some morphophysiologic characters, which favor their survival in flooded environments, also resulting in higher productivity. Keywords Gas exchange Hypoxia Zea mays L. Flooding tolerance Yield
F. J. Pereira e-mail:
[email protected] E. M. de Castro e-mail:
[email protected] P. C. Magalha˜es S. N. Parentoni Centro Nacional de Pesquisa de Milho e Sorgo, Caixa Postal 151, Sete Lagoas, MG CEP 35701-970, Brazil e-mail:
[email protected] S. N. Parentoni e-mail:
[email protected]
Introduction The stress imposed by flooding is a major obstacle to growth, distribution, and productivity of plants. Natural factors, such as superabundance in precipitation, marginal water coming from rivers and bad drainage, influences the increment in flooding areas. Excess of water in the soil leads to dramatic consequences in the diffusive process, as
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the gases diffuse faster in air than in water and, therefore, there is a depletion of oxygen availability (hypoxia) both on the ground as in parts of the plant. The decline of oxygen is further accentuated by the presence of aerobic microorganisms that use this same gas in their processes in the rhizosphere, which may lead to extreme eradication of oxygen (anoxia) (Dat et al. 2004). Then the tricarboxylic acid cycle is interrupted by lack of reducing power and anaerobic metabolism is activated (Sairam et al. 2008). Maize is one of the most important cereals cultivated in the world, since it presents high potential for grain production, nutritional value, and chemical composition. The inability of maize plants to endure low oxygen availability in the rhizosphere, caused by root flooding, result in substantial losses in productivity for example in South Asia, 15% of maize acreage is affected by flooding, whereas in India, water excess is already the second major stress, reaching around 8.5 millions hectares (Zaidi et al. 2007a). In Brazil, large agricultural constraints by flooding are found in floodplains areas (alluvial and hydromorphic soils), where temporary flooding restrict most agricultural crops, with the exception of flooded rice (Silva et al. 2007). Positive attempts in search tolerant maize genotypes have been carried out through genetic selection, resulting in the development of plants with high yields and stable in water excess conditions (Zaidi et al. 2007b). Maize genotypes tolerant to intermittent flooding have been reported, in these studies it was found that chlorophyll content, shoot dry weight, root volume, root porosity, grain yield, leaf area, and the interval between male and female flowering are quite contrasting in comparison with control (Lizaso et al. 2001; Zaidi et al. 2003, 2004). Leaves of plants with anaerobic root stress are limited in gas exchange by stomatal closure. The low oxygen availability may affect stomatal conductance (gs), decreasing water loss by transpiration (E), and photosynthetic rate (Pn) (Yordanova and Popova 2007). Plants susceptible to flooding have reduced photosynthesis (Chen et al. 2005) due to non-stomatal factors (biochemical) (Yordanova et al. 2005) and stomatal factors (Liao and Lin 2001). The tolerant plants, however, may be able to maintain its photosynthetic rate greater in addition to greater efficiency in the use of water, even in hypoxia (Li et al. 2004; Islam et al. 2008). Concerned about the damage that flooding causes to maize plant and trying to insert it in idle areas immediately after rice in floodplains, the National Maize and Sorghum Research Center (EMBRAPA) developed by stratified phenotypic recurrent selection, a maize variety called Saracura-BRS-4154, with capacity to survive, produce, and support temporary periods of flooding (Ferreira et al. 2007). The name ‘‘Saracura’’ is a reference to a bird commonly found in wetland. Currently, this variety is in the 18th annual selection cycle. Its ability to tolerate
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intermittent periods of flooding is due to the presence of different physiological and biochemical mechanisms (Vitorino et al. 2001; Ferreira et al. 2008), and also to morphoanatomical changes in root and leaves (Pereira et al. 2008; Souza et al. 2009, 2010). The objectives of this study were to characterize the morphological and physiological changes and to evaluate the attributes of grain production in successive selection cycles of ‘‘Saracura’’ maize under intermittent flooding of the soil.
Materials and methods Plant material and growth conditions The genetic material consisted of intercalated selection cycles of maize cv. Saracura-BRS-4154: C1, C3, C5, C7, C9, C11, C13, C15, C17, and C18 and the variety BR 107 as a control, known for its susceptibility to flooding (Magalha˜es et al. 2007). The development of this cultivar was performed by using the method of phenotypic recurrent selection. Each selection cycle (C1, C3, C5 through C18), was obtained by selecting the 300 best plants from previous cycle. A balanced mixture of seeds was planted in a low land type of soil and submitted to intermittent flooding to obtain every year an each new selection cycle. To produce each cycle, primary characteristics such as chlorophyll content, lodging, ear height, plant height, and diseases susceptibility and others were analyzed. By harvesting time, a new analyze (secondary traits) were performed, by selecting healthy ears. The intermittent flooding treatment, means flooding every other day (three times a week). All selection cycles received the same kind of flooding treatments. The experiment was conducted in January 2009, under greenhouse conditions at the National Maize and Sorghum Research Center (EMBRAPA), Sete Lagoas, Minas Gerais, Brazil (altitude 732 m, latitude South 19° 280 , longitude West 44° 150 ). The average maximum and minimum temperature recorded during the evaluation period were 28.2 and 24.8°C, respectively. The relative humidity ranged from 52 to 78%. We used two plants per pot of 20 l, filled up with soil previously classified as Tb Fluvic Neosol, Typical Eutrophic, clay texture, phase plain relief wetland fields (Santos et al. 2006). The fertilization was performed according to the recommendation of the chemical analysis of the soil, applying at planting the fertilizer formula 5-20-20 ? Zn at the doses of 23 g/ 20 kg of soil. The plants were irrigated regularly, maintaining an optimal soil moisture until the imposition of stress. All of the phytosanitary treatments required by the crop were applied.
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Imposition of stress and experimental design
Yield components
Flooding was initiated at the stage of six leaves (when the growing point of plants is already above the soil surface) (Magalha˜es et al. 2007) throughout physiological maturity, corresponding to 80 days of intermittent flooding. This treatment was accomplished by adding 50 mm of water to each pot, three times a week (every other day). The experimental design was the randomized blocks in factorial with 11 maize genotypes (ten alternating selection cycles and a check variety) and two conditions (non-flooded control and flooded) and four replications. Each replicate (one pot) contained two plants, which were used to evaluate the characteristics.
At harvest the following data were analyzed: grain yield (GY), ear length (EL), harvest index (HI) [grain dry weight/(plant dry weight ? grain dry weight 9 100].
Measurement of leaf gas exchange At flowering stage, gas exchange parameters were measured using a portable photosynthesis system (IRGA, Model LI-6400, Li-Cor, Lincoln, Nebraska, USA). All measurements were performed in the morning between 9:00 and 11:00 AM in a fully expanded leaf (ear leaf). The parameters assessed were the rate of leaf photosynthesis (Pn), stomatal conductance (gs), transpiration rate (E), and intercellular CO2 concentration (Ci). Measurements were made on a leaf area of 6 cm2, airflow in the chamber with a CO2 concentration of 380 mmol mol-1. The air was collected from outside the greenhouse and transported into a buffering gallon and then pumped into the chamber. We used a photon flux density (PPFD) of 1500 mmol m-2 s-1, a red-blue LED light source. Other environmental factors such as humidity and temperature were not controlled allowing a natural variation. Measurements of leaf area, root porosity, relative chlorophyll content, and ASI All four parameters were also evaluated at the flowering stage as the gas exchange measurements. The photosynthetically active leaf area was estimated using a leaf area meter (Model LI-3100, Li-Cor, Lincoln, Nebraska, USA). The relative chlorophyll content in vivo was determined in the ear leaf using a chlorophyll meter (Model SPAD 502, Minolta, Japan). Ten readings were taken per plant and from these data obtained the average. Data were expressed in units of spad. The root porosity was measured by the pycnometer method (Jessen et al. 1969). This method quantifies porosity as the percentage of root volume occupied by air (percentage volume/volume). Anthesissilking interval (ASI) was calculated as the difference between number of days from 50% anthesis to 50% silking. This evaluation was recorded by daily visual observations during the flowering period (Zaidi et al. 2004).
Data analysis To compare the characteristics of gas exchange between flooded and unflooded plants we have used the F Test. The averages and standard deviation for leaf area, root porosity, chlorophyll relative content, and yield components are presented in Tables 1, 2. To express tolerance for each genotype, it was created an index: ‘‘Relative Tolerance Value—RTV’’, where values for each characteristic evaluated, (except gaseous exchange data), at flooding condition were divided by values at no flooding condition. The functional relationship between grain yield with root porosity and photosynthesis was determined by regression analysis, using The Table Curve program, version 5.01.
Results Gas exchange measurements As far as rate of leaf photosynthesis (Pn) is concerned there was an appreciable significant difference between the maize plants flooded and not flooded (Fig. 1a). The values of Pn for selection cycles and the variety BR 107 varied between 18.8 and 27.9 in the flooded condition, and from 37.8 to 42.8 in non-flooded condition. Among the selection cycles in non-flooded condition the control (BR 107) resulted in similar values to the last cycle of selection (C18). In flooded condition, however, there was an increase in the rate of leaf photosynthesis during the selection cycles (Fig. 1a). The highest photosynthetic rate, recorded in cycle 18 (27.9), is 33.33% higher than the control BR 107 and 31.22% higher than the C1. For stomatal conductance (gs), all cycles and the variety BR 107 were also significantly different considering the flooded and unflooded conditions (Fig. 1b). There was a variation from 0.46 to 0.66 in non-flooded condition and from 0.11 to 0.21 in the flooded condition. For selection cycles in non-flooded condition, variety BR107 showed an average (0.66) higher than all other cycles (Fig. 1b). Unlikely, in the flooded cycles, stomatal conductance increased over the selection cycles and the cycle 18 had the highest average (0.21) while the cycle 1 had the lowest (0.11) followed by the variety BR 107 (0.12). The cycle 18 had a 47.62% increase in stomatal conductance compared to C1 and 41.43% compared to BR107.
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0.88
1.75 ± 0.9
2.50 ± 1.0
1.43
It is observed in Fig. 1c, that the intercellular CO2 concentration (Ci) was significant among non-flooded and flooded conditions only for cycles 1, 3, 9, and 18 and variety BR 107. The non-flooded plants had higher averages than the flooded ones. Among cycles subject to flooding, the same trend observed for rate of leaf photosynthesis (Pn) and stomatal conductance (gs) were presented for intercellular CO2 concentration (Ci) where an increase over the selection cycles of ‘‘Saracura’’ maize was observed (Fig. 1c). The lowest, intercellular CO2 concentration was displayed by cycle 1 (73.63) followed by the BR 107 (99.97). The cycle 18 had the highest average of Ci, being 34.86 and 52.02% higher than the first cycle and the variety BR 107, respectively. Figure 1d displays transpiration rates in both conditions. As one can see only cycle 11 did not show significant difference between flooded and no-flooded conditions. Transpiration in flooded plants had a range of 3.4–6.6 whereas in non-flooded plants it ranged from 7.7 to 10.2. At flooded conditions the first cycle had the lowest transpiration rate (E) (3.4), followed by the control (4.3) whereas the highest E was found in C18 (6.6), which was 34.80% higher than the control BR 107 and 48.5% higher than the C1. Measurements of leaf area, root porosity, relative chlorophyll content, and ASI
41.47 ± 8.7 ASI anthesis-silking interval; RTV = (F/NF)
6,502.00 ± 0559 C18
4,539.25 ± 1368
0.70
4.13 ± 3.56
13.43 ± 1.63
3.25
36.42 ± 3.6
0.88
1.14 2.00 ± 0.8
1.75 ± 0.9 2.00 ± 0.5
1.75 ± 0.5 0.98
0.79 31.89 ± 5.4
43.62 ± 2.4
40.12 ± 2.6
44.54 ± 4.4
3.38
2.44 10.50 ± 1.62
10.97 ± 1.49 3.25 ± 2.22
4.30 ± 4.70 0.60
0.52 3,147.75 ± 1629
4,228.75 ± 0811
6,055.50 ± 0668
7,070.75 ± 1774
C15
C17
1.83
0.60 1.50 ± 0.6
2.75 ± 0.9 1.50 ± 0.6
2.50 ± 0.6 0.74
0.64 26.94 ± 4.0
30.91 ± 2.8
42.30 ± 3.9
41.60 ± 3.7
2.50
2.70 9.79 ± 0.37
10.18 ± 1.80 4.07 ± 2.64
3.62 ± 1.75 0.57
0.66 4,088.00 ± 1917
3,307.75 ± 1026
6,192.75 ± 0783
5,814.25 ± 0829
C11
C13
0.86
1.86 3.25 ± 2.0
1.50 ± 0.6 1.75 ± 1.5
1.75 ± 0.9 0.69
0.60 25.87 ± 2.3
28.07 ± 1.5
43.21 ± 3.8
40.85 ± 7.9
0.94
1.27 6.57 ± 3.83
4.62 ± 2.34 4.90 ± 3.13
5.16 ± 5.06 0.39
0.79 4,470.25 ± 1893
2,994.25 ± 1399
5,662.75 ± 3776
7,703.60 ± 0558
C7
C9
1.78 1.25 4.00 ± 0.8 2.50 ± 0.5 2.25 ± 0.9 2.00 ± 0.8 0.73 0.72 36.84 ± 3.7 41.00 ± 8.3 6,754.33 ± 1830 6,996.50 ± 1137 C3 C5
3,245.50 ± 1886 3,012.75 ± 1026
0.48 0.43
2.77 ± 2.40 3.97 ± 3.08
5.38 ± 0.33 5.60 ± 0.43
1.94 1.41
27.05 ± 4.0 29.40 ± 5.5
2.63
1.89 4.25 ± 0.5
5.25 ± 0.8 2.00 ± 2.0
2.25 ± 0.5 0.64
0.53 21.64 ± 5.0
24.80 ± 5.8
41.01 ± 4.0
38.74 ± 5.0
1.07
2.11 5.33 ± 0.43
5.72 ± 0.45 5.35 ± 4.20
2.53 ± 0.19 0.54
0.33 2,146.00 ± 0881
3,802.00 ± 1012
6,490.00 ± 0504
6,980.75 ± 0595
BR107
F
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C1
NF F NF RTV F NF NF
RTV
Root porosity (%) Leaf area (cm2)
Chlorophyll (spad unit)
RTV
ASI (days)
F
RVT
Acta Physiol Plant (2011) 33:1877–1885
Cycles
Table 1 Means and standard deviations (±SD, n = 4) of leaf area, root porosity, relative chlorophyll content, ASI and its respective RTV during the selection cycles (alternated) of ‘‘Saracura’’ and variety, BR 107, tested on two conditions: flooded (F) and non-flooded (NF)
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It was observed different averages between flooded and non-flooded conditions concerned leaf area of selection cycles and control (Table 1). The cycle 7 resulted in the greatest RTV (0.79), followed by cycle 18, with 0.70 and variety BR 107, which presented the lowest value (0.33) (Table 1). For RTV leaf area, there was an increase of 56.96 and 51.43% from cycles 7 and 18, respectively, related to variety BR 107. For root porosity RTV, there was an increase throughout the selection cycles in flooded condition, whereas at nonflooded condition no expressive increment was observed, being these averages lower than flooded conditions (Table 1). The greatest RTV observed were from cycle 15 (3.38) and cycle 17 (3.25) and the lowest RTV came from cycle 7 (0.94), followed by the check variety, BR 107 with 1.07. The cycle 18 showed an increment of 71% for root porosity RTV, when compared to cycle 7 and 67% when compared to BR 107. As far as relative chlorophyll content is concerned, selection cycles and check variety showed higher values on non-flooded condition than flooded (Table 1). The highest RTV was performed by cycle 17 (0.9), followed by cycle 18 (0.88), whereas the lowest RTV was found for BR 107 (0.53) (Table 1). The rise in RTV for relative chlorophyll
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Table 2 Means and standard deviations (±SD, n = 4) of grain yield, harvest index, ear length, and its respective RTV along the selection cycles of ‘‘Saracura’’ and the variety BR 107, tested on two conditions: flooded (F) and non-flooded (NF) Cycles
Grain yield (g plant-1) NF
Harvest index
F
RTV
Ear length (cm)
NF
F
RTV
NF
F
RTV
BR107
91.63 ± 22.70
48.92 ± 7.84
0.53
0.35 ± 0.07
0.24 ± 0.03
0.67
12.75 ± 4.7
9.00 ± 3.1
0.71
C1
90.39 ± 16.17
48.02 ± 9.83
0.53
0.33 ± 0.14
0.24 ± 0.02
0.73
13.75 ± 0.9
11.00 ± 2.8
0.80
C3 C5
83.62 ± 18.34 100.50 ± 20.09
64.56 ± 5.90 62.65 ± 15.70
0.77 0.62
0.34 ± 0.20 0.32 ± 0.13
0.30 ± 0.06 0.27 ± 0.09
0.88 0.84
14.37 ± 4.6 14.75 ± 0.9
13.50 ± 2.4 11.50 ± 4.0
0.94 0.78
C7
60.75 ± 30.47
85.30 ± 31.23
1.40
0.36 ± 0.11
0.27 ± 0.03
0.75
16.50 ± 3.1
13.25 ± 2.6
0.80
C9
84.05 ± 36.93
66.93 ± 40.40
0.80
0.41 ± 0.06
0.28 ± 0.13
0.68
16.00 ± 0.7
12.00 ± 3.5
0.75
C11
110.50 ± 14.63
84.68 ± 14.40
0.77
0.41 ± 0.04
0.38 ± 0.08
0.93
13.12 ± 2.7
15.00 ± 0.9
1.14
C13
92.06 ± 36.00
80.35 ± 13.80
0.87
0.32 ± 0.08
0.26 ± 0.13
0.81
15.87 ± 1.0
11.25 ± 5.0
0.71
C15
109.66 ± 31.44
95.59 ± 3.70
0.87
0.37 ± 0.03
0.34 ± 0.11
0.92
12.12 ± 2.0
14.00 ± 2.5
1.16
C17
135.95 ± 13.96
94.70 ± 2.50
0.70
0.40 ± 0.03
0.38 ± 0.13
0.95
12.75 ± 1.5
12.00 ± 3.0
0.94
C18
120.94 ± 28.26
98.52 ± 1.50
0.81
0.42 ± 0.08
0.39 ± 0.03
0.93
14.25 ± 2.0
13.50 ± 2.4
0.95
RTV = (F/NF) 50
B
0,8 0,7
40
0,6
35
*
25 20
*
*
*
*
*
*
*
0,5
*
30
0,4
*
*
*
**
15
*
*
*
*
*
*
*
0,3
*
0,2 0,1
10
250
gs (mol m-2 s-1)
Pn (mmol CO2 m-2 s-1)
45
0,9
Flooded Non-flooded
A
C
0,0 16
D
14
Ci ( mmol mol-1)
ns
150
ns
10
*
ns ns
*
* 100
ns
ns
*
* *
* *
*
*
*
ns
*
*
* *
8 6
E (mmol m-2 s-1)
12
200
4 2 0
C18
C17
C15
C13
C11
C9
C7
C5
C3
7 C1
BR10
C18
C17
C15
C13
C11
C9
C7
C5
C3
B R1 0 7 C1
50
Selection Cycles
Fig. 1 Characteristics of gas exchange along the selection cycles of ‘‘Saracura’’ maize on two-water conditions. a Rate of leaf photosynthesis (Pn), b stomatal conductance (gs), c intercellular CO2
concentration (Ci), d transpiration rate (E). Means ± SD, n = 4. Asterisk indicates statistical significance at P B 0.01
content, when compared to BR 107 was 45.9% for cycle 17 and 39.77% for cycle 18. Flooded condition caused an increment of days for ASI, compared to non-flooded condition (Table 2). Cycle 13 showed the lowest RTV (0.6), whereas variety BR 107 resulted on the greatest RTV (2.63).
Yield components Concerning grain yield the treatments showed a range from 48.02 to 98.52 g plant-1, for flooded condition whereas no-flooded condition presented a range from 83.62 to 135.95 (Table 2). Unexpectedly, cycle 7 under
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for ear length (Table 2). As a matter of fact, cycle 15 resulted on the greatest RTV (1.16), whereas cycle 5 the lowest (0.7).
flooded condition presented an increment on yield of 28.78% compared to non-flooded condition. The others cycles decreased grain yield when were submitted to flooding (Table 2). The last selection cycles resulted on the largest RTV. The cycle 7 showed the greatest RTV (1.40), followed by cycles 13 (0.87), 15 (0.87), and 18 (0.81). The check variety (BR 107) and cycle 1, resulted on the lowest RTV (0.53), followed by the initial cycle (5) (Table 2). The harvest index averages ranged from 0.24 to 0.39 at flooding and 0.32–0.40 at no-flooding condition. As far as RTV is concerned, cycles 17 with 1.05 and 18 with 0.93 were the ones which presented the largest averages, being, 36.2 and 28%, respectively, greater than BR107 which resulted in a RTV of 0.67 (Table 2). At no flooding, the most selection cycles exhibited greater average value than the ones in flooding condition
Relationship between grain yield and morphophysiological characteristics The Fig. 2a, b show the relationship between grain yield and root porosity at no flooding and flooding conditions, respectively. The regression analysis indicated a strong and significant dependence (R2 = 0.66**) between these two characteristics for flooding and a weak and no significant dependence (R2 = 0.12) for no flooding condition. On the other hand, by analyzing Fig. 3a, b one can see that the relationship between grain yield and photosynthesis was weak and no significant either to no flooding (R2 = 0.11) or flooding (R2 = 0.23). Further regression analyses with
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-1
Grain Yield (g plant )
120
y=a+b/x0,5 R2= 0,66**
A
2
y=a+bx+cx 2
R = 0,12
B
100 80 60 40 20 0
0
2
4
6
8
10
12
14
2
4
6
Root porosity (%)
8
10
12
14
16
Root porosity (%)
Fig. 2 Grain yield averages related to root porosity at no flooding (a) and at flooding (b) conditions throughout the ‘‘Saracura’’ maize selection cycles. Double asterisk indicates statistical significance at P B 0.01
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y=a+bx+cx2 R2= 0,11
Grain Yield (Kg plant -1)
120
A
y=a+bx+cx 0,5 R2=0,23
B
100 80 60 40 20 0 25
30
35
40 -2 -1
Pn (mmol CO2 m s )
45
50 10
15
20
25
30
35
40
-2 -1
Pn (mmol CO2 m s )
Fig. 3 Grain yield averages related to photosynthesis at no flooding (a) and at flooding (b) conditions throughout the ‘‘Saracura’’ maize selection cycles
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other characteristics were held, but with no significant evidences (data not shown).
Discussion Flooding significantly affected all the gas exchange process evaluated in this study. We noted that the flooded condition decreases the rate of leaf photosynthesis (Pn), stomatal conductance (gs), transpiration rate (E), and intercellular CO2 concentration (Ci). These results were also observed in other crops such as barley (Yordanova et al. 2005). In corn, Yordanova and Popova (2007) also observed decrease in photosynthesis, stomatal conductance and transpiration but the internal CO2 concentration did not decreased indicating no effect on non-stomatal photosynthetic process. For ‘‘Saracura’’ maize and the variety BR 107 the stomatal limitation on photosynthetic process seems to prevail, because the flooding has led to a stomatal closure restricting the internal content of CO2. The stratified phenotypic recurrent selection used in the breeding process of ‘‘Saracura’’ maize has led to a lower stomatal limitation on photosynthetic process indicated by the higher rate of photosynthesis and other gas exchange traits evaluated (Fig. 1) along the selection cycles. In anatomical studies with the same control variety and the same selection cycles of maize we also observed morphometric stomatal changes (number and size of stomata) over selection cycles (Souza et al. 2010). These modifications may also be improving gas exchange along the selection cycles of ‘‘Saracura’’ maize in this study. The flooded condition affected the leaf area in both control (BR 107) and the selection cycles compared to nonflooded condition. Zaidi et al. (2003) also observed a severe reduction in leaf area in Indian maize genotypes under flooding. The selection performed on the ‘‘Saracura’’ maize led to a greater leaf area throughout the selection cycles. This fact was confirmed by the largest RTV through the cycles. Likewise data reported in literature for tolerant maize genotypes had a lower reduction in leaf area than susceptible genotypes (Zaidi et al. 2004). Several studies with maize are showing an increase in root porosity under flooding (Grineva and Bragina 1993; Zaidi et al. 2007a; Vodnik et al. 2009). The latest selection cycles of ‘‘Saracura’’ had higher root porosity (C18 and C15). This feature could indicate a greater amount of root aerenchyma in the cortex of these genotypes. This can be confirmed, since recent studies with successive selection cycles of ‘‘Saracura’’ maize, both in greenhouse and field (Pereira et al. 2008; Souza et al. 2009), showed higher amounts of aerenchyma along the cycles. The increased porosity in the last selection cycles of ‘‘Saracura’’, caused mainly by the formation of aerenchyma in the root
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(environment with hypoxia), helps to keep the longitudinal flow of oxygen from shoots to roots (Colmer 2003). Increasing root porosity results in metabolic cost decreases due to the decreased presence of cells in respiration (Lynch and Ho 2005), besides being able to determine root growth under conditions of hypoxia (Lenochova´ et al. 2009). The excess of water in the rhizosphere not only reduces the internal concentration of oxygen in the root, but also can lead to decreased nutrient intake and increased free radicals concentration in the plant causing damage also in the pigments (Yordanova and Popova 2007; Zaidi et al. 2007a). Differences in the relative content of chlorophyll were well evidenced when the selection cycles and variety BR 107 were placed in conditions of flooding. During the selection cycles we observed less degradation of chlorophyll, showing another important feature in the tolerance of these genotypes to flooding stress. In accordance with our data Zaidi et al. (2007a) using a chlorophyll meter observed that more tolerant maize genotypes had lower chlorophyll degradation. Stress caused by excess of water has been widely reported as a major negative effect on maize grain yield. As a matter of fact, differences in yield between flooded and non-flooded conditions were evidenced in this study. The results between selection cycles in soil flooded confirmed an effective gain of the last cycles over the first ones. Ferreira et al. (2007) also showed losses in grain yield when four selection cycles of ‘‘Saracura’’ (C1, C5, C9, and C15) were placed under intermittent flooding. These authors also observed a gain in grain yield over the selection cycles. With regards to ear length these authors’ data corroborate this study, where any significant differences between selection cycles, were found, however, differences between the conditions of stress were reported. One reason that may have led to increased yield in the last selection cycles of ‘‘Saracura’’ maize is a major differential allocation of photo-assimilates to ear during its lifecycle. This was showed by harvest index which increased especially at last selection cycles (C18 and C17) in flooded condition (Table 2). Excess of water may be limiting the adaptability of BR 107 and the initial selection cycles interfering with grain yield that, for it’s in turn, tends to be limited by processes that influence the supply of photo-assimilates to the organ of economic interest or by processes that control the source–sink relationship (Dura˜es et al. 2002). Another reason that may have led to improvements in grain yield in recent selection cycles of ‘‘Saracura’’ is the increase in synchrony of the development of reproductive organs. The flooded condition led to negative impacts on reproductive performance especially in initial cycles and the control because of a delay in silking which resulted in long intervals between male and female flowering (ASI).
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By the way, since the RTV is the division of data from flooded cycles by no-flooded cycles, it worthwhile to mention that a greater index for ASI indicates a lower tolerance. Other authors also concluded that maize genotypes more susceptible to flooding tend to have longer ASI while most tolerant genotypes shorter ASI (Zaidi et al. 2003, 2004, 2007b). Under flooding, the grain yield was strongly related to root porosity in this study (Fig. 2b). In other studies, the same relationship was observed (Zaidi et al. 2004, 2007a). In the case of ‘‘Saracura’’ several root anatomical modifications (Souza et al. 2009) and especially the root porosity may be providing more favorable conditions for increased production at hypoxia conditions. For ‘‘Saracura’’ was not found a significant relationship between grain yield and rate of leaf photosynthesis (Pn) (Fig. 3). In Vigna radiata L. Wilczek grain yield and photosynthesis were closely related in flooded conditions (Islam et al. 2008). Long et al. (2006), in their reviews, report specific work questioning the relationship which photosynthesis increase can make up on a higher yield. Some of these studies report that this relationship does not always happen and that other factors may be influencing grain yield other than photosynthesis. In short, it can be concluded that the flooding has affected significantly the genotypes studied and the selection of ‘‘Saracura’’ maize was effective over time for some morphophysiologic characters which favor their survival in flooded environments, and consequently resulting in higher productivity. Acknowledgments The authors thank Capes for the scholarship, National Maize and Sorghum Research Center for the facilities and support for the accomplishment of this research.
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