Rice Plants (Oryza sativa L.) under Cd Stress in Fe Deficiency Conditions

Abstract

Due to the environment pollution by cadmium (Cd) near industrial metallurgic factories and the widespread use of phosphorus fertilizers, the problem of toxic Cd effect on plants is well discussed by many authors, but the phytotoxicity of Cd under iron (Fe) deficiency stress has not been sufficiently studied. The aim of the work was to study comprehensively the effect of Cd under Fe deficiency conditions on physiological, biochemical, and anatomical parameters of rice varieties, to identify varietal differences in plant response to the effect of double stress. Relative resistance and sensitivity to the joint effect of Cd and Fe deficiency stress rice varieties have been identified. Double stress decreased a linear growth and biomass accumulation of roots and shoots (by 36-50% and 33-46% and 32-56% and 32-48%, accordingly), content of photosynthetic pigments (Chla, Chlb, and carotenoids by 36-51%, 32-47%, and 64-78%, accordingly), and relative water content (by 18-26%). Proline content increased by 28-103% in all rice varieties, but to a lesser extent in sensitive varieties. The thickness of the lower and upper epidermis and the diameter of vascular bundles of leaves decreased by 18-50%, 46-60%, and 13-48%, accordingly. The thickness of the root endodermis and exodermis and diameter of the central cylinder mainly decreased. The thickness of the exodermis increased slightly by 7%, and the diameter of the central cylinder remained at the control level in resistant Madina variety while in sensitive Chapsari variety, these indicators decreased significantly by 50 and 45%, accordingly. Thus, the aggravation of adverse effect of Cd under Fe deficiency conditions and the varietal specificity of plants' response to double stress were shown. It creates the need for further study of these rice varieties using Fe to identify mechanisms for reducing the toxic effect of Cd on plants as well as the study of Fe and Cd transporter genes at the molecular level.

Figure 1

The effect of Cd and Fe deficiency on the biomass accumulation in aboveground organs of 14 d rice seedlings. Control-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p < 0.1, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties are significant at p < 0.001.

Figure 2

The effect of Cd and Fe deficiency on the length of aboveground organs of 14 d rice seedlings. Control-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p < 0.1; ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties are significant at p < 0.001

Figure 3

The effect of Cd and Fe deficiency on root biomass of 14 d rice seedlings. Control-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p < 0.1, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties are significant at p < 0.001.

Figure 4

The effect of Cd and Fe deficiency on the root length of 14 d rice seedlings. Control-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p < 0.1, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties are not significant at p > 0.05.

Figure 5

The effect of Cd and Fe deficiency on the content of chlorophyll a in the leaves of 14 d rice seedlings. Сontrol-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p < 0.1, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties are significant at p < 0.001.

Figure 6

Effect of Cd and Fe deficiency on the content of chlorophyll b in the leaves of 14 d rice seedlings. Сontrol-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p < 0.1, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties are significant at p < 0.001.

Figure 7

The effect of Cd and Fe deficiency on the content of carotenoids in the leaves of 14 d rice seedlings. Сontrol-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p < 0.1, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties are not significant (p > 0.05).

Figure 8

The effect of Cd and Fe deficiency on the relative water content (RWC) in the leaves of 14 d rice seedlings. Сontrol-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p < 0.1, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties are significant (p < 0.001).

Figure 9

The effect of Cd and Fe deficiency on proline content in the leaves of 14 d rice seedlings. Сontrol-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p < 0.1, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties (p < 0.05) are significant

Figure 10

Anatomical structures of 14 d rice seedling leaves: (A) control-Fe norm-Cd—nutrient medium (NM)+100 μМ Fe, (B) Fe norm+Cd—NM+100 μМ Fe+200 μМ Сd, (C) Fe deficiency-Cd—NM+0 μМ Fe, and (D) Fe deficiency+Cd—NM+0 μМ Fe+200 μМ Сd. 1—lower epidermis, 2—upper epidermis, and 3—conducting bundles.

Figure 11

Effect of Cd under different Fe status on the thickness of the lower epidermis of 14 d rice seedlings. Control-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p > 0.05, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties (p < 0.001) are significant.

Figure 12

Effect of Cd under different Fe status on the thickness of the upper epidermis of leaves of rice seedlings. Control-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p > 0.05, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties (p < 0.001) are significant.

Figure 13

Effect of Cd under different Fe status on the diameter of conducting bundles of leaf rice seedlings. Control-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety across treatments: ^∗p > 0.05, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties (p < 0.001) are significant.

Figure 14

Anatomical structures of 14 d rice seedling leaves: (A) control-Fe norm-Cd—nutrient medium (NM)+100 μМ Fe, (B) Fe norm+Cd—NM+100 μМ Fe+200 μМ Сd, (C) Fe deficiency-Cd—NM+0 μМ Fe, and (D) Fe deficiency+Cd—NM+0 μМ Fe+200 μМ Сd. 1—exodermis, 2—endodermis, and 3—central cylinder.

Figure 15

Effect of Cd under different Fe status on the thickness of the exodermis of roots of rice seedlings. Control-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p > 0.05, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties (p < 0.001) are significant.

Figure 16

Effect of Cd under different Fe status on the diameter of the central cylinder of roots of rice seedlings. Control-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ± SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p > 0.05, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties (p < 0.001) are significant.

Figure 17

Effect of Cd under different Fe status on the thickness of the endodermis of roots of rice seedlings. Control-Fe norm-Cd: nutrient medium (NM)+100 μМ Fe; Fe norm+Cd: NM+100 μМ Fe+200 μМ Сd; Fe deficiency-Cd: NM+0 μМ Fe; Fe deficiency+Cd: NM+0 μМ Fe+200 μМ Сd. Vertical bars represent ±SE of three replicates (n = 3); the differences within variety between control and treatments: ^∗p > 0.05, ^∗∗p < 0.05, and ^∗∗∗p < 0.01; the differences across varieties (p < 0.001) are significant.