Response of soybean to soil waterlogging associated with iron excess in the reproductive stage

Abstract

Soil waterlogging is a common problem in some agricultural areas, including regions under soybean (Glycine max) cultivation. In waterlogged soils, soil O₂ depletion occurs due to aerobic microorganisms and plants, affecting the metabolic and physiological processes of plants after suffering anoxia in their root tissue. Another harmful factor in this situation is the exponential increase in the availability of iron (Fe) in the soil, which may result in absorption of excess Fe. The present study sought to evaluate the response mechanisms in soybean leaves 'Agroeste 3680' by physiological and biochemical analyses associating them with the development of pods in non-waterlogged and waterlogged soil, combined with one moderate and two toxic levels of Fe. Gas exchange was strongly affected by soil waterlogging. Excess Fe without soil waterlogging reduced photosynthetic pigments, and potentiated this reduction when associated with soil waterlogging. Starch and ureide accumulation in the first newly expanded trifoliate leaves proved to be response mechanisms induced by soil waterlogging and excess Fe, since plants cultivated under soil non-waterlogged soil at 25 mg dm^-3 Fe showed lower contents when compared to stressed plants. Thus, starch and ureide accumulation could be considered efficient biomarkers of phytotoxicity caused by soil waterlogging and excess Fe in soybean plants. The reproductive development was abruptly interrupted by the imposition of stresses, leading to a loss of pod dry biomass, which was largely due to the substantial decrease in the net photosynthetic rate, as expressed by area (A), the blockage of carbohydrate transport to sink tissues and an increase of malondialdehyde (MDA). The negative effect on reproductive development was more pronounced under waterlogged soil.

Keywords: Anoxia; Ferrous ion; Glycine max; Starch; Ureides.

Fig. 1

Net photosynthetic rate (I), stomatal conductance (II), transpiration rate (III), water use efficiency (IV) and instantaneous carboxylation efficiency (V) of soybean leaves based on the significance of ANOVA by factorial analysis (p ≤ 0.05), comprised of soils with two levels of water (without waterlogging and with waterlogging) and three iron levels (25, 125 and 500 mg dm⁻³). Different letters indicate significant differences according to the Tukey test (p < 0.05). Uppercase letters compare the conditions of waterlogging between different iron levels in the soil, while lowercase letters compare the conditions of soil waterlogging with the same iron levels. Vertical bars represent the standard deviation (n = 6 plants)

Fig. 2

Chlorophyll a (I), chlorophyll b (II), total chlorophyll (III) and carotenoid (IV) contents of soybean leaves based on the significance of ANOVA by factorial analysis (p ≤ 0.05), comprised of soils with two levels of water (without waterlogging and with waterlogging) and three iron levels (25, 125 and 500 mg dm⁻³). Different letters indicate significant differences according to the Tukey test (p < 0.05). Uppercase letters compare the conditions of waterlogging between different iron levels in the soil, while lowercase letters compare the conditions of soil waterlogging with the same iron levels. Vertical bars represent the standard deviation (n = 6 plants)

Fig. 3

Starch (I), total carbohydrate (III) and sucrose (II) contents of soybean leaves based on the significance of ANOVA by factorial analysis (p ≤ 0.05), comprised of soils with two levels of water (without waterlogging and with waterlogging) and three iron levels (25, 125 and 500 mg dm⁻³). Different letters indicate significant differences according to the Tukey test (p < 0.05). Uppercase letters compare the conditions of waterlogging between different iron levels in the soil, while lowercase letters compare the conditions of soil waterlogging with the same iron levels. Vertical bars represent the standard deviation (n = 6 plants)

Fig. 4

Total ureides (I), allantoate (II), allantoin (III), nitrate (IV) and protein (V) contents of soybean leaves based on the significance of ANOVA by factorial analysis (p ≤ 0.05), comprised of soils with two levels of water (without waterlogging and with waterlogging) and three iron levels (25, 125 and 500 mg dm⁻³). Different letters indicate significant differences according to the Tukey test (p < 0.05). Isolated uppercase letters compare the conditions of soil waterlogging regardless of iron levels, while isolated lowercase letters compare iron levels regardless of soil waterlogging. Uppercase letters compare the conditions of waterlogging between different iron levels in the soil, while lowercase letters compare the conditions of soil waterlogging with the same iron levels. Vertical bars represent the standard deviation (n = 6 plants)

Fig. 5

Hydrogen peroxide (a) and malondialdehyde (b) concentrations of soybean leaves based on the significance of ANOVA by factorial analysis (p ≤ 0.05), comprised of soils with two levels of water (without waterlogging and with waterlogging) and three iron levels (25, 125 and 500 mg dm⁻³). Different letters indicate significant differences according to the Tukey test (p < 0.05). Isolated uppercase letters compare the conditions of soil waterlogging regardless of iron levels, while isolated lowercase letters compare iron levels regardless of soil waterlogging. Vertical bars represent the standard deviation (n = 6 plants)

Fig. 6

Shoot dry weight (I), pod dry weight (II), root dry weight (III) and iron accumulation in the shoots (IV) of soybean leaves based on the significance of ANOVA by factorial analysis (p ≤ 0.05), comprised of soils with two levels of water (without waterlogging and with waterlogging) and three iron levels (25, 125 and 500 mg dm⁻³). Different letters indicate significant differences according to the Tukey test (p < 0.05). Uppercase letters compare the conditions of waterlogging between different iron levels in the soil, while lowercase letters compare the conditions of soil waterlogging with the same iron levels. Vertical bars represent the standard deviation (n = 6 plants for FEAS; n = 9 plants for dry weights)

Fig. 7

Pearson’s correlation (p < 0.05) with multiple comparisons at 1% probability between traits. The squares that received the white colour belong to the category of non-significant correlative values. Net photosynthetic rate (A), stomatal conductance (gs), transpiration rate (E), water use efficiency (WUE), instantaneous carboxylation efficiency (EiC), Chlorophyll a (Chl a), chlorophyll b (Chl b), total chlorophyll (Tchl), carotenoids (CAR), hydrogen peroxide (H₂O₂), malondialdehyde (MDA), shoot dry weight (SDW), pod dry weight (PDW), root dry weight (RDW), Fe accumulation in the shoot (FEAS)