Root Morphology and Anatomy Affect Cadmium Translocation and Accumulation in Rice

doi:10.1016/j.rsci.2021.03.003

Abstract

Abstract:

Paddy fields contaminated with cadmium (Cd) present decreased grain yield and produce Cd-contaminated grains. Screening for low-Cd-accumulating cultivars is a useful method to reduce the amount of Cd in the grains. The present study aimed to examine the roles of the root morphology and anatomy in Cd translocation and accumulation in rice plants. Twenty-two rice cultivars were used in the first experiment, after which two cultivars [Zixiangnuo (ZXN) and Jinyou T36 (JYT36)] were selected and used in subsequent experiments under hydroponic conditions. The results showed that there were significant differences in Cd concentrations in the shoots (ranging from 4 to 100 mg/kg) and the Cd translocation rates (shoot/root) (from 7% to 102%) among the 22 cultivars, and the shoot Cd concentration was significantly correlated with the Cd translocation rate of the 22 cultivars under 0.1 mg/L Cd treatment. Compared with cultivar ZXN, JYT36 had greater root Cd uptake and accumulation but lower shoot Cd accumulation and Cd translocation rate. The number of root tips per surface area of cultivar ZXN was greater than that of JYT36, while the average root diameter was lower than that of JYT36. Compared with ZXN, JYT36 had stronger apoplastic barriers, and the Casparian bands and suberin lamellae in the root endodermis and exodermis were closer to the root apex in both the control and Cd treatments, especially for suberin lamellae in the root exodermis with Cd treatments, with a difference of 25 mm. The results also showed that, compared with ZXN, JYT36 had greater percentages of Cd bound in cell walls and intracellular Cd but lower Cd concentrations in the apoplastic fluid under the Cd treatment. The results suggested that Cd translocation, rather than root Cd uptake, is a key process that determines Cd accumulation in the rice shoots. The root morphological and anatomical characteristics evidently affect Cd accumulation in the shoots by inhibiting Cd translocation, especially via the apoplastic pathway. It was possible to pre-screen low-Cd-accumulating rice cultivars on the basis of their root morphology, anatomical characteristics and Cd translocation rate at the seedling stage.

Key words: apoplastic pathway, Cd stress, Cd translocation, Cd accumulation, rice, root morphology and anatomy

Anwen Xiao, Danting Chen, Wai Chin Li, Zhihong Ye. Root Morphology and Anatomy Affect Cadmium Translocation and Accumulation in Rice[J]. Rice Science, 2021, 28(6): 594-604.

Figures/Tables 14

Fig. S1. Cd tolerance index of 22 rice cultivars grown in solution with treatment of 0.1 mg/L Cd for 3 weeks.LYPJ, Liangyoupeijiu; JYT36, Yinyou T36; SYN, Suyunuo; XN1H, Xinnuo 1; TY2168, Tianyou 2168; NY1H, Nuoyou 1; QXY200, Qianxiangyou 2000; TY122, Tianyou 122; NJ44, Nanjing 44; TY998, Tianyou 998; XWN1H, Xiangwannuo 1; WFY128, Wufengyou 128; TXZ, Texianzhan; ZY808, Zhongyou 808; SY402, Shanyou 402; PZ163, Peiyou 163; TY196, Tianyou 196; HY665, Huayou 665; ZD097, Zhongdao 097; SHN, Suihongnuo; ST1H, Shengtai 1; ZXN, Zixiangnuo.Data are Mean ± SE (n = 4). Different letters above the bars indicate significant difference between cultivars at P < 0.05.

Table S1. Growing parameters of 22 rice cultivars grown in solution with treatments of 0 (control) and 0.1 mg/L Cd for 3 weeks.

Cultivar	Control				0.1 mg/L Cd treatment
Cultivar	Plant height (cm)	Longest root length (cm)	Shoot fresh weight (g)	Root fresh weight (g)	Plant height (cm)	Longest root length (cm)	Shoot fresh weight (g)	Root fresh weight (g)
JYT36	26.43 ± 1.25	9.25 ± 0.32	0.30 ± 0.04	0.23 ± 0.04	28.33 ± 0.88	8.67 ± 1.67	0.37 ± 0.09	0.31 ± 0.08
LYPJ	19.63 ± 2.48	8.00 ± 0.74	0.22 ± 0.03	0.14 ± 0.02	20.50 ± 0.96	10.23 ± 0.65	0.21 ± 0.02	0.15 ± 0.02
NJ44	17.25 ± 0.52	9.55 ± 1.00	0.17 ± 0.01	0.14 ± 0.01	14.50 ± 0.89	5.83 ± 0.20	0.08 ± 0.01	0.10 ± 0.01
NY1H	28.88 ± 0.66	6.00 ± 1.02	0.46± 0.05	0.32 ± 0.05	27.25 ± 2.07	8.38 ± 0.43	0.43 ± 0.09	0.33 ± 0.06
QXY200	23.13 ± 1.05	9.13 ± 0.66	0.17 ± 0.02	0. 11 ± 0.02	24.38 ± 3.02	5.25 ± 0.32	0.22 ± 0.06	0.12± 0.01
SYN	23.38 ± 1.65	8.25 ± 0.43	0.29 ± 0.06	0.17 ± 0.03	23.75 ± 1.44	9.53 ± 1.03	0.34 ± 0.07	0.25 ± 0.04
TY122	24.00 ± 0.68	7.75 ± 0.25	0.23 ±0.01	0.15 ± 0.01	21.83 ± 0.93	7.17 ± 0.33	0.29 ± 0.03	0.20 ± 0.03
TY2168	23.00 ± 0.71	8.75 ± 0.63	0.19 ± 0.02	0.12 ± 0.01	20.83 ± 0.73	7.00 ± 0.58	0.19 ± 0.03	0.12 ± 0.03
YY998	23.25 ± 1.01	9.50 ± 0.65	0.29 ± 0.02	0.17 ± 0.01	22.00 ± 0.71	8.63 ± 1.46	0.24 ± 0.01	0.14 ± 0.01
WFY128	23.88 ± 0.13	10.38 ± 1.30	0.28 ± 0.02	0.14 ± 0.02	22.17 ± 2.62	8.50 ± 0.58	0.30 ± 0.08	0.21 ± 0.06
TXZ	18.63 ± 0.55	10.38 ± 0.80	0.14 ± 0.01	0.09 ± 0.01	16.20 ± 3.00	6.83 ± 0.44	0.16 ± 0.06	0.10 ± 0.01
XWN1H	21.75 ± 1.45	12.25 ± 1.27	0.25 ± 0.03	0.17 ± 0.02	20.17 ± 3.06	10.43 ± 0.64	0.33 ± 0.04	0.18 ± 0.02
XN1H	20.75 ± 1.13	10.00 ± 1.24	0.24 ± 0.02	0.13 ± 0.01	18.50 ± 1.04	12.33 ± 0.93	0.21 ± 0.02	0.13 ± 0.01
ZY808	27.88 ± 0.66	7.88 ± 0.75	0.36 ± 0.04	0.20 ± 0.04	30.50 ± 1.26	8.33 ± 1.86	0.59 ± 0.05	0.33 ± 0.03
HY665	21.14 ± 0.51	7.50 ± 0.87	0.24 ± 0.04	0.15 ± 0.03	24.67 ± 2.32	8.67 ± 1.33	0.33 ± 0.07	0.20 ± 0.06
SHN	16.88 ± 0.75	8.75 ± 0.95	0.13 ± 0.01	0.11 ± 0.01	12.33 ± 0.93	7.17 ± 1.01	0.11 ± 0.01	0.12 ± 0.02
SY402	25.38 ± 1.65	7.40 ± 0.37	0.27 ± 0.04	0.19 ± 0.02	23.17 ± 0.83	9.17 ± 1.01	0.29 ± 0.01	0.20 ± 0.02
ST1H	16.20 ± 0.93	9.60 ± 1.00	0.10 ± 0.01	0.08 ± 0.01	18.17 ± 0.33	6.67 ± 0.93	0.15 ± 0.03	0.13 ± 0.03
TY196	22.75 ± 0.48	8.33 ± 0.58	0.23 ± 0.02	0.17 ± 0.02	25.83 ± 2.09	8.83 ± 0.73	0.36 ± 0.08	0.20 ± 0.04
PZ163	25.50 ± 1.26	9.38 ± 1.01	0.29 ± 0.04	0.17 ± 0.01	22.33 ± 1.64	7.50 ± 0.29	0.23 ± 0.04	0.15 ± 0.01
ZXN	16.75 ± 1.20	9.50 ± 0.74	0.11 ± 0.02	0.11 ± 0.01	15.17 ± 1.36	9.50 ± 0.50	0.10 ± 0.02	0.10 ± 0.02
ZD097	15.75 ± 0.14	2.04 ± 0.36	0.14 ± 0.01	0.12 ± 0.00	15.17 ± 1.42	8.87 ± 0.70	0.11 ± 0.02	0.13 ± 0.02

Table S1. Growing parameters of 22 rice cultivars grown in solution with treatments of 0 (control) and 0.1 mg/L Cd for 3 weeks.

Cultivar	Control				0.1 mg/L Cd treatment
Cultivar	Plant height (cm)	Longest root length (cm)	Shoot fresh weight (g)	Root fresh weight (g)	Plant height (cm)	Longest root length (cm)	Shoot fresh weight (g)	Root fresh weight (g)
JYT36	26.43 ± 1.25	9.25 ± 0.32	0.30 ± 0.04	0.23 ± 0.04	28.33 ± 0.88	8.67 ± 1.67	0.37 ± 0.09	0.31 ± 0.08
LYPJ	19.63 ± 2.48	8.00 ± 0.74	0.22 ± 0.03	0.14 ± 0.02	20.50 ± 0.96	10.23 ± 0.65	0.21 ± 0.02	0.15 ± 0.02
NJ44	17.25 ± 0.52	9.55 ± 1.00	0.17 ± 0.01	0.14 ± 0.01	14.50 ± 0.89	5.83 ± 0.20	0.08 ± 0.01	0.10 ± 0.01
NY1H	28.88 ± 0.66	6.00 ± 1.02	0.46± 0.05	0.32 ± 0.05	27.25 ± 2.07	8.38 ± 0.43	0.43 ± 0.09	0.33 ± 0.06
QXY200	23.13 ± 1.05	9.13 ± 0.66	0.17 ± 0.02	0. 11 ± 0.02	24.38 ± 3.02	5.25 ± 0.32	0.22 ± 0.06	0.12± 0.01
SYN	23.38 ± 1.65	8.25 ± 0.43	0.29 ± 0.06	0.17 ± 0.03	23.75 ± 1.44	9.53 ± 1.03	0.34 ± 0.07	0.25 ± 0.04
TY122	24.00 ± 0.68	7.75 ± 0.25	0.23 ±0.01	0.15 ± 0.01	21.83 ± 0.93	7.17 ± 0.33	0.29 ± 0.03	0.20 ± 0.03
TY2168	23.00 ± 0.71	8.75 ± 0.63	0.19 ± 0.02	0.12 ± 0.01	20.83 ± 0.73	7.00 ± 0.58	0.19 ± 0.03	0.12 ± 0.03
YY998	23.25 ± 1.01	9.50 ± 0.65	0.29 ± 0.02	0.17 ± 0.01	22.00 ± 0.71	8.63 ± 1.46	0.24 ± 0.01	0.14 ± 0.01
WFY128	23.88 ± 0.13	10.38 ± 1.30	0.28 ± 0.02	0.14 ± 0.02	22.17 ± 2.62	8.50 ± 0.58	0.30 ± 0.08	0.21 ± 0.06
TXZ	18.63 ± 0.55	10.38 ± 0.80	0.14 ± 0.01	0.09 ± 0.01	16.20 ± 3.00	6.83 ± 0.44	0.16 ± 0.06	0.10 ± 0.01
XWN1H	21.75 ± 1.45	12.25 ± 1.27	0.25 ± 0.03	0.17 ± 0.02	20.17 ± 3.06	10.43 ± 0.64	0.33 ± 0.04	0.18 ± 0.02
XN1H	20.75 ± 1.13	10.00 ± 1.24	0.24 ± 0.02	0.13 ± 0.01	18.50 ± 1.04	12.33 ± 0.93	0.21 ± 0.02	0.13 ± 0.01
ZY808	27.88 ± 0.66	7.88 ± 0.75	0.36 ± 0.04	0.20 ± 0.04	30.50 ± 1.26	8.33 ± 1.86	0.59 ± 0.05	0.33 ± 0.03
HY665	21.14 ± 0.51	7.50 ± 0.87	0.24 ± 0.04	0.15 ± 0.03	24.67 ± 2.32	8.67 ± 1.33	0.33 ± 0.07	0.20 ± 0.06
SHN	16.88 ± 0.75	8.75 ± 0.95	0.13 ± 0.01	0.11 ± 0.01	12.33 ± 0.93	7.17 ± 1.01	0.11 ± 0.01	0.12 ± 0.02
SY402	25.38 ± 1.65	7.40 ± 0.37	0.27 ± 0.04	0.19 ± 0.02	23.17 ± 0.83	9.17 ± 1.01	0.29 ± 0.01	0.20 ± 0.02
ST1H	16.20 ± 0.93	9.60 ± 1.00	0.10 ± 0.01	0.08 ± 0.01	18.17 ± 0.33	6.67 ± 0.93	0.15 ± 0.03	0.13 ± 0.03
TY196	22.75 ± 0.48	8.33 ± 0.58	0.23 ± 0.02	0.17 ± 0.02	25.83 ± 2.09	8.83 ± 0.73	0.36 ± 0.08	0.20 ± 0.04
PZ163	25.50 ± 1.26	9.38 ± 1.01	0.29 ± 0.04	0.17 ± 0.01	22.33 ± 1.64	7.50 ± 0.29	0.23 ± 0.04	0.15 ± 0.01
ZXN	16.75 ± 1.20	9.50 ± 0.74	0.11 ± 0.02	0.11 ± 0.01	15.17 ± 1.36	9.50 ± 0.50	0.10 ± 0.02	0.10 ± 0.02
ZD097	15.75 ± 0.14	2.04 ± 0.36	0.14 ± 0.01	0.12 ± 0.00	15.17 ± 1.42	8.87 ± 0.70	0.11 ± 0.02	0.13 ± 0.02

Fig. 1. Cd concentrations in shoots (A) and roots (B), Cd translocation rate (shoot/root) (C), and correlation between Cd concentration in shoots and Cd translocation rates (shoot/root) (D) of 22 rice cultivars with 0.1 mg/L Cd treatment for 3 weeks.LYPJ, Liangyoupeijiu; JYT36, Jinyou T36; SYN, Suyunuo; XN1H, Xinnuo 1; TY2168, Tianyou 2168; NY1H, Nuoyou 1; QXY200, Qianxiangyou 2000; TY122, Tianyou 122; NJ44, Nanjing 44; TY998, Tianyou 998; XWN1H, Xiangwannuo 1; WFY128, Wufengyou 128; TXZ, Texianzhan; ZY808, Zhongyou 808; SY402, Shanyou 402; PZ163, Peiyou 163; TY196, Tianyou 196; HY665, Huayou 665; ZD097, Zhongdao 097; SHN, Suihongnuo; ST1H, Shengtai 1; ZXN, Zixiangnuo.Data are Mean ± SE (n = 4). Different lowercase letters indicate significant differences among the cultivars at P < 0.05.

Fig. S2. Correlation between Cd concentration in shoots and roots of 22 rice cultivars with treatment of 0.1 mg/L Cd for 3 weeks.Data are Mean ± SE (n = 4).

Table S2. Effects of Cd stress on growth of two rice cultivars with treatments of 0.5 and 2.5 mg/L Cd for 4 weeks.

Measured parameter	Cd concentration (mg/L)	Cultivar
Measured parameter	Cd concentration (mg/L)	JYT36	ZXN
Root length (cm)	0	16.67 ± 0.44 b	14.63 ± 0.75 b
	0.5	16.17 ± 0.73 b	13.17 ± 0.60 ab
	2.5	9.67 ± 0.67 a	12.50 ± 0.35 a
Shoot height (cm)	0	47.67 ± 0.88 c	21.33 ± 3.11 b
	0.5	38.83 ± 0.93 b	17.67 ± 0.60 ab
	2.5	20.00 ± 1.44 a	12.00 ± 0.58 a

Fig. S3. Cd concentration in roots and shoots of two rice cultivars with 0.5 and 2.5 mg/L Cd treatments for 4 weeks.Data are Mean ± SE (n = 4). * indicate significant difference between cultivars at P < 0.05.

Table S3. Kinetic parameters for Cd influx into rice roots of cultivars ZXN and JYT36.

Cultivar	V_max[nmol/(g∙h)]	K_m(μmol/L)	R²
ZXN	35.12 ± 2.32	0.55 ± 0.03	0.91
JYT36	82.29 ± 5.17	0.98 ± 0.06	0.98

Fig. 2. Concentration-dependent and time-dependent kinetics for Cd uptake by rice roots of cultivars Zixiangnuo (ZXN) and Jinyou T36 (JYT36).A, High-affinity uptake kinetics of Cd in the two cultivars.B, Low-affinity uptake kinetics of Cd in the two cultivars.C, Time-dependent kinetics of Cd in the two cultivars.The 10 d old intact seedlings were treated for 30 min in A and B, and treated with 180 nmol/L Cd in C. Data are Mean ± SE (n = 3). Data with different lowercase letters mean significant differences between the treatments at P < 0.001 (A) and P < 0.05 (B).

Table 1 Parameters of root morphology in rice with treatments of 0.5 and 2.5 mg/L Cd for 4 weeks.

Parameter	Cd concentration (mg/L)	Cultivar		Significant
Parameter	Cd concentration (mg/L)	ZXN	JYT36	Significant
No. of root tips per cm²	0.0	90.14 ± 6.72 c	49.40 ± 5.33 b	***
	0.5	62.67 ± 4.36 b	27.24 ± 2.86 b	***
	2.5	29.51 ± 3.30 a	25.98 ± 3.89 a
Average diameter (mm)	0.0	0.26 ± 0.02 a	0.38 ± 0.02 a	***
	0.5	0.32 ± 0.02 ab	0.41 ± 0.02 b	**
	2.5	0.34 ± 0.02 b	0.30 ± 0.02 a

Fig. 3. Schematic representation of endodermal and exodermal apoplastic barriers of two rice cultivars in control (CK) and Cd (2.5 mg/L) treatments.ZXN, Zixiangnuo; JYT36, Jinyou T36. Casparian bands and suberin lamellae in endodermis are represented by red and green lines, respectively. Casparian bands and suberin lamellae in exodermis are represented by brown and blue lines, respectively. The dotted lines indicate the early and immature deposition of the barriers and solid lines represent the Casparian bands or suberin lamellae which have developed maturely in the zone.

Fig. 4. Comparison of development of Casparian bands at 20 mm distance from rice root tips with treatments of control and 2.5 mg/L Cd for 4 weeks.A to D are endodermis sections, and E to H are exodermis sections; A, C, E and G are cultivar Zixiangnuo, and B, D, F and H are cultivar Jinyou T36; A, B, E and F are in the control treatment, and C, D, G and H are in 2.5 mg/L Cd treatment. Arrow heads refer to the Casparian bands. Scale bars are 20 μm in A, B, E, F and G, and 50 μm in C, D and H.

Fig. 5. Comparison of development of suberin lamellae at 20 mm distance from rice root tips with treatments of control and 2.5 mg/L Cd for 4 weeks.A to D are endodermis sections, and E to H are exodermis sections; A, C, E and G are cultivar Zixiangnuo, and B, D, F and H are cultivar Jinyou T36; A, B, E and F are in control treatment, and C, D, G and H are in 2.5 mg/L Cd treatment. Scale bars are 20 μm in A, B, E and F, and 50 μm in C, D, G and H.

Fig. 6. Distribution of Cd in rice roots with treatments of 0.5 and 2.5 mg/L Cd for 4 weeks.A, Cd bound in cell wall and intracellular Cd.B, Cd concentration in the apoplastic fluid.ZXN, Zixiangnuo; JYT36, Jinyou T36. Data are Mean ± SE (n = 3). * and ** mean significant differences between the cultivars in the same treatment at the 0.05 and 0.01 levels, respectively.

Table S4. Rice cultivars used.

Cultivar	Abbreviation	Subspecies
Liangyoupeijiu	LYPJ	Indica
Huayou 665	HY665	Indica
Shanyou 402	SY402	Indica
Jinyou T36	JYT36	Indica
Tianyou 998	TY998	Indica
Tianyou 196	TY196	Indica
Peiyou 163	PZ163	Indica
Tianyou 2168	TY2168	Indica
Wufengyou 128	WFY128	Indica
Qianxiangyou 2000	QXY200	Indica
Nuoyou 1	NY1H	Indica
Tianyou 122	TY122	Indica
Zhongyou 808	ZY808	Indica
Texianzhan	TXZ	Indica
Suihongnuo	SHN	Indica
Xiangwannuo 1	XWN1H	Indica
Shengtai 1	ST1H	Indica
Zhongdao 097	ZD097	Japonica
Nanjing 44	NJ44	Japonica
Suyunuo	SYN	Japonica
Zixiangnuo	ZXN	Japonica
Xinnuo 1	XN1H	Japonica

References 41

[1]	Armstrong J, Armstrong W. 2005. Rice: Sulfide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Ann Bot, 96(4): 625-638.
[2]	Boominathan R, Doran P M. 2003. Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator, Thlaspi caerulescens. Biotechnol Bioeng, 83(2): 158-167.
[3]	Chi Y, Li F, Tam N F Y, Liu C, Ouyang Y, Qi X, Li W C, Ye Z H. 2018. Variations in grain cadmium and arsenic concentrations and screening for stable low-accumulating rice cultivars from multi-environment trials. Sci Total Environ, 643(1): 1314-1324.
[4]	Chiao W T, Syu C H, Chen B C, Juang K W. 2019. Cadmium in rice grains from a field trial in relation to model parameters of Cd-toxicity and -absorption in rice seedlings. Ecotox Environ Safe, 169: 837-847.
[5]	Chiao W T, Chen B C, Syu C H, Juang K W. 2020. Aspects of cultivar variation in physiological traits related to Cd distribution in rice plants with a short-term stress. Bot Stud, 61: 27.
[6]	Grant C A, Clarke J M, Duguid S, Chaney R L. 2008. Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ, 390: 301-310.
[7]	Hoagland D R, Arnon D I. 1938. The water culture method for growing plants without soil. Calif Agric Exp Stn, 347: 1-39.
[8]	Huang G, Ding C, Guo F, Li X G, Zhou Z G, Zhang T L, Wang X X. 2017. The role of node restriction on cadmium accumulation in the brown rice of 12 Chinese rice (Oryza sativa L.) cultivars. J Agric Food Chem, 65(47): 10157-10164.
[9]	Huang L, Li W C, Tam N F, Ye Z H. 2019. Effects of root morphology and anatomy on cadmium uptake and translocation in rice (Oryza sativa L.). J Environ Sci, 75: 296-306.
[10]	Kotula L, Ranathunge K, Schreiber L, Steudle E. 2009. Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution. J Exp Bot, 60(7): 2155-2167.
[11]	Kreszies T, Schreiber L, Ranathunge K. 2018. Suberized transport barriers in Arabidopsis, barley and rice roots: From the model plant to crop species. J Plant Physiol, 227: 75-83.
[12]	Liu J G, Liang J S, Li K Q, Zhang Z J, Yu B Y, Lu X L, Yang J C, Zhu Q S. 2003. Correlations between cadmium and mineral nutrients in absorption and accumulation in various genotypes of rice under cadmium stress. Chemosphere, 52(9): 1467-1473.
[13]	Liu J G, Qian M, Cai G L, Yang J C, Zhu Q S. 2007. Uptake and translocation of Cd in different rice cultivars and the relation with Cd accumulation in rice grain. J Hazard Mater, 143(1/2): 443-447.
[14]	Loix C, Huybrechts M, Vangronsveld J, Gielen M, Keunen E, Cuypers A. 2017. Reciprocal interactions between cadmium- induced cell wall responses and oxidative stress in plants. Front Plant Sci, 8: 1867.
[15]	Lux A, Sottniková A, Opatrná J, Greger M. 2004. Differences in structure of adventitious roots in Salix clones with contrasting characteristics of cadmium accumulation and sensitivity. Physiol Plant, 120(4): 537-545.
[16]	Lux A, Morita S, Abe J, Ito K. 2005. An improved method for clearing and staining free-hand sections and whole-mount samples. Ann Bot, 96(6): 989-996.
[17]	Lux A, Martinka M, Vaculik M, White P J. 2011. Root responses to cadmium in the rhizosphere: A review. J Exp Bot, 62(1): 21-37.
[18]	Ma F, Peterson C A. 2003. Current insights into the development, structure, and chemistry of the endodermis and exodermis of roots. Can J Bot, 81: 405-421.
[19]	Maksimović I, Kastori R, Krstić L, Luković J. 2007. Steady presence of cadmium and nickel affects root anatomy, accumulation and distribution of essential ions in maize seedlings. Biol Plant, 51(3): 589-592.
[20]	Man Y, Zhao Y Y, Ye R, Lin J X, Jing Y P. 2018. In vivo cytological and chemical analysis of Casparian strips using stimulated Raman scattering microscopy. J Plant Physiol, 220: 136-144.
[21]	Moore C A, Bowen H C, Scrase-Field S, Knight M R, White P J. 2002. The deposition of suberin lamellae determines the magnitude of cytosolic Ca2+ elevations in root endodermal cells subjected to cooling. Plant J, 30(4): 457-466.
[22]	Nordberg G, Jin T Y, Bernard A, Fierens S, Buchet J P, Ye T T, Kong Q H, Wang H F. 2002. Low bone density and renal dysfunction following environmental cadmium exposure in China. Ambio, 31(6): 478-481.
[23]	Parrotta L, Guerriero G, Sergeant K, Cai G, Hausman J F. 2015. Target or barrier? The cell wall of early- and later-diverging plants vs cadmium toxicity: Differences in the response mechanisms. Front Plant Sci, 6: 133.
[24]	Qi X L, Tam N F, Li W C, Ye Z H. 2020. The role of root apoplastic barriers in cadmium translocation and accumulation in cultivars of rice (Oryza sativa L.) with different Cd- accumulating characteristics. Environ Pollut, 264: 114736.
[25]	Redjala T, Zelko I, Sterckeman T, Legué V, Lux A. 2011. Relationship between root structure and root cadmium uptake in maize. Environ Exp Bot, 71(2): 241-248.
[26]	Rodda M S, Li G, Reid R J. 2011. The timing of grain Cd accumulation in rice plants: The relative importance of remobilisation within the plant and root Cd uptake post- flowering. Plant Soil, 347: 105-114.
[27]	Rout G R, Das P. 2002. Rapid hydroponic screening for molybdenum tolerance in rice through morphological and biochemical analysis. Rostl Výroba, 48: 505-512.
[28]	Schreiber L, Hartmann K, Skrabs M, Zeier J. 1999. Apoplastic barriers in roots: Chemical composition of endodermal and hypodermal cell walls. J Exp Bot, 50: 1267-1280.
[29]	Shi Y J, Xu Y F, Ni Z Y, Wang J W, Li D, Zhang M K. 2019. Difference of Cd accumulation in main crops in Hangzhou and its influencing factors. Zhejiang Agric Sci, 60(7): 1230-1233. (in Chinese with English abstract)
[30]	Tao Q, Jupa R, Luo J P, Lux A, Kovac J, Wen Y, Zhou Y M, Jan J, Liang Y C, Li T Q. 2017. The apoplasmic pathway via the root apex and lateral roots contributes to Cd hyperaccumulation in the hyperaccumulator Sedum alfredii. J Exp Bot, 68(3): 739-751.
[31]	Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S. 2009. Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot, 60(9): 2677-2688.
[32]	Uraguchi S, Fujiwara T. 2012. Cadmium transport and tolerance in rice: Perspectives for reducing grain cadmium accumulation. Rice, 5(1): 5.
[33]	Uraguchi S, Fujiwara T. 2013. Rice breaks ground for cadmium- free cereals. Curr Opin Plant Biol, 16(3): 328-334.
[34]	Wang F J, Zhang Y T, Guo Q X, Tan H F, Han J H, Lin H R, Wei H W, Xu G W, Zhu C. 2018. Effects of exogenous 5-aminolevulinic acid and 24-epibrassinolide on Cd accumulation in rice from Cd-contaminated soil. Rice Sci, 25(6): 320-329.
[35]	White P J. 2001. The pathways of calcium movement to the xylem. J Exp Bot, 52: 891-899.
[36]	Wilkins D A. 1987. The measurement of tolerance to edaphic factors by means of root growth. New Phytol, 80: 623-633.
[37]	Williams P N, Lei M, Sun G, Huang Q, Lu Y, Deacon C, Meharg A A, Zhu Y G. 2009. Occurrence and partitioning of cadmium, arsenic and lead in mine impacted paddy rice: Hunan, China. Environ Sci Technol, 43(3): 637-642.
[38]	Wu C, Ye Z H, Shu W S, Zhu Y G, Wong M H. 2011. Arsenic accumulation and speciation in rice are affected by root aeration and variation of genotypes. J Exp Bot, 62(8): 2889-2898.
[39]	Yamaguchi N, Mori S, Baba K, Kaburagi-Yada S, Arao T, Kitajima N, Hokura A, Terada Y. 2011. Cadmium distribution in the root tissues of solanaceous plants with contrasting root-to-shoot Cd translocation efficiencies. Environ Exp Bot, 71(2): 198-206.
[40]	Ye J, Yan C L, Liu J C, Lu H L, Liu T, Song Z F. 2012. Effects of silicon on the distribution of cadmium compartmentation in root tips of Kandelia obovata (S., L.) Yong. Environ Pollut, 162: 369-373.
[41]	Zhuang P, Lu H, Li Z, Zou B, McBride M B. 2014. Multiple exposure and effects assessment of heavy metals in the population near mining area in South China. PLoS One, 9(4): e94484.