Phosphorus Starvation Tolerance in Rice Through Combined Physiological, Biochemical, and Proteome Analyses

doi:10.1016/j.rsci.2023.04.007

Abstract

Abstract:

Phosphorus (P) deficiency limits the growth, development, and productivity of rice. To better understand the underlying mechanisms in P-deficiency tolerance and the role of Pup1 QTL in enhancing P use efficiency (PUE) for the development of P-efficient rice cultivars, a pair of contrasting rice genotypes (Pusa-44 and NIL-23) was applied to investigate the morpho-physio-biochemical and proteomic variation under P-starvation stress. The rice genotypes were grown hydroponically in a PusaRich medium with adequate P (16 mg/kg, +P) or without P (0 mg/kg, -P) for 30 d. P-starvation manifested a significant reductions in root and shoot biomass, shoot length, leaf area, total chlorophyll, and P, nitrogen and starch contents, as well as protein kinase activity. The stress increased root-to-shoot biomass ratio, root length, sucrose content, and acid phosphatase activity, particularly in the P-tolerant genotype (NIL-23). Comparative proteome analysis revealed several P metabolism-associated proteins (including OsCDPKs, OsMAPKs, OsCPKs, OsLecRK2, and OsSAPks) to be expressed in the shoot of NIL-23, indicating that multiple protein kinases were involved in P-starvation/deficiency tolerance. Moreover, the up-regulated expression of OsrbcL, OsABCG32, OsSUS5, OsPolI-like B, and ClpC2 proteins in the shoot, and OsACA9, OsACA8, OsSPS2F, OsPP2C15, and OsBiP3 in the root of NIL-23, indicated their role in P-starvation stress control through the Pup1 QTL. Thus, our findings indicated that -P stress-responsive proteins, in conjunction with morpho-physio-biochemical modulations, improved PUE and made NIL-23 a P-deficiency tolerant genotype due to the introgression of the Pup1 QTL in the Pusa-44 background.

Key words: phosphorus deficiency, Pup1 QTL, protein kinase, acid phosphatase, proteome analysis, rice

Prathap V, Suresh Kumar, Nand Lal Meena, Chirag Maheshwari, Monika Dalal, Aruna Tyagi. Phosphorus Starvation Tolerance in Rice Through Combined Physiological, Biochemical, and Proteome Analyses[J]. Rice Science, 2023, 30(6): 613-631.

Figures/Tables 7

Fig. 1. Shoot and root morphologies of rice genotypes grown hydroponically under P-starvation stress for 30 d. A, Shoot morphology of Pusa-44 (P-sensitive genotype) and NIL-23 (P-tolerant genotype) grown under contrasting P conditions [16 mg/kg (+P) and 0 mg/kg (-P)]. B and C, Root morphology of Pusa-44 (B) and NIL-23 (C) grown under contrasting P conditions [16 mg/kg (+P) and 0 mg/kg (-P)].

Fig. 2. Modulation in root system architecture of rice genotypes grown hydroponically under P-starvation stress for 30 d. The variations of total root projected area (A), total root surface area (B), the number of root tips (C), and the number of root forks (D) observed in Pusa-44 (P-sensitive genotype) and NIL-23 (P-tolerant genotype) treated with different P concentrations. Data are Mean ± SD (n = 3), and different lowercase letters above the bars show significant differences at P < 0.05.

Table 1. Morpho-physiological variations in rice genotypes [Pusa-44 (P-sensitive genotype) and NIL-23 (P-tolerant genotype)] grown hydroponically under P-starvation stress for 30 d.

Genotype	Growth condition	Total leaf area (cm²)	Total chlorophyll content (mg/g)	Shoot biomass (g)	Root biomass (g)	Root-to-shoot biomass ratio	Shoot length (cm)	Total root length (cm)
Pusa-44	-P (0 mg/kg)	44.96 ± 3.35 c	12 ± 1.25 c	0.45 ± 0.10 d	0.20 ± 0.02 d	0.45 ± 0.02 b	22.1 ± 0.9 b	320.0 ± 14.6 d
Pusa-44	+P (16 mg/kg)	182.43 ± 7.30 a	31 ± 2.65 a	1.49 ± 0.35 b	0.53 ± 0.03 b	0.36 ± 0.03 d	32.9 ± 2.9 a	824.7 ± 36.1 b
NIL-23	-P (0 mg/kg)	45.71 ± 11.40 c	17 ± 3.01 b	0.54 ± 0.20 c	0.43 ± 0.03 c	0.80 ± 0.01 a	24.7 ± 2.3 b	502.0 ± 88.9 c
NIL-23	+P (16 mg/kg)	168.29 ± 5.40 b	34 ± 1.98 a	1.57 ± 0.19 a	0.63 ± 0.02 a	0.40 ± 0.02 c	31.6 ± 1.1 a	1 103.0 ± 12.5 a

Fig. 3. Effects of P-starvation stress on biochemical parameters in rice genotypes grown hydroponically under P-starvation stress. Effect of the stress on starch content (A), sucrose content (B), phosphorus content (C), and nitrogen content (D) observed in Pusa-44 (the P-sensitive genotype) and NIL-23 (the P-tolerant genotype) grown under 16 mg/kg (+P) and 0 mg/kg (-P) conditions. Data are Mean ± SD (n = 3), and different lowercase letters above the bars show significant differences at P < 0.05.

Fig. 4. Effects of P-starvation stress on acid phosphatase (A) and total protein kinase activities (B) in rice genotypes grown hydroponically under P-starvation stress for 30 d. Data are Mean ± SD (n = 3), and different lowercase letters show significant differences at P < 0.05.

Fig. 5. Pearson correlation (PC) analysis depicting correlation coefficient and an association between physiological and biochemical characteristics. PC coefficient varies between -1 to +1, and a positive linear relationship between variables is highlighted in red and a negative correlation is highlighted in blue. RSR, Root to shoot biomass ratio. *, P < 0.05; **, P < 0.01; ***, P < 0.001; ns indicates not significant.

Fig. 6. Comparative analysis of differentially expressed proteins (DEPs) in shoot and root of in rice genotypes [ Pusa-44 (P-sensitive genotype) and NIL-23 (P-tolerant genotype)] under a most contrasting condition [16 mg/kg (+P) and 0 mg/kg (-P)]. A, Number of proteins identified in shoot and root. B, Statistically significant total-, up- (in green) and down-regulated (in red) DEPs. C and D, Four-way Venn diagram showing the significantly up-regulated (C) and down-regulated DEPs (D) in shoot and root.

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