Constitutive basis of root system architecture: uncovering a promising trait for breeding nutrient- and drought-resilient crops

Abstract

Root system architecture (RSA) plays a pivotal role in efficient uptake of essential nutrients, such as phosphorous (P), nitrogen (N), and water. In soils with heterogeneous nutrient distribution, root plasticity can optimize acquisition and plant growth. Here, we present evidence that a constitutive RSA can confer benefits for sorghum grown under both sufficient and limiting growth conditions. Our studies, using P efficient SC103 and inefficient BTx635 sorghum cultivars, identified significant differences in root traits, with SC103 developing a larger root system with more and longer lateral roots, and enhanced shoot biomass, under both nutrient sufficient and deficient conditions. In addition to this constitutive attribute, under P deficiency, both cultivars exhibited an initial increase in lateral root development; however, SC103 still maintained the larger root biomass. Although N deficiency and drought stress inhibited both root and shoot growth, for both sorghum cultivars, SC103 again maintained the better performance. These findings reveal that SC103, a P efficient sorghum cultivar, also exhibited enhanced growth performance under N deficiency and drought. Our results provide evidence that this constitutive nature of RSA can provide an avenue for breeding nutrient- and drought-resilient crops.

Supplementary information: The online version contains supplementary material available at 10.1007/s42994-023-00112-w.

Keywords: Abiotic stress; Constitutive root system architecture; Drought resilience; Nutrient efficiency; Plant breeding.

Fig. 1

Schematic representation of root system architectures representing topsoil based and deep rooting systems. A Plants that develop a shallow root system localized within the topsoil (broken rectangle). B Plants that develop an extended, deeper, root system (broken inverted triangle). CR crown root, LR lateral root, PR primary root

Fig. 2

Response of sorghum root systems (lines SC103 and BTx635) grown under 200 μM Pi (sufficient P), and 10, 2.5 and 0 μM Pi (low P), for 7, 9 and 12 days after transplanting (Dat). A hydroponic pouch system was employed for these assays, and representative images are shown

Fig. 3

Root system architecture of sorghum lines SC103 and BTx635, grown in a hydroponic pouch system, under the indicated phosphate (Pi) concentrations. Panels represent shoot dry weight (A), root:shoot ratio (B), total root system length (C), root system width (D), total root system surface area (E), and primary root length (F), analyzed at 7, 9 and 12 Dat. Data shown are means ± SE (n = 6). Asterisks indicate significant differences between the genotypes, under the same Pi concentrations, as determined by the Student’s t test. For these assays, significance differences are indicated as follows: *P < 0.05; **P < 0.01; ***P < 0.001. Different lowercase letters indicate significant differences (P < 0.05) among the four Pi concentrations, in the same genotype, as determined by Tukey’s HSD tests

Fig. 4

Root system architecture profiles for SC103 and BTx635 grown in a hydroponic pouch system, under sufficient Pi (200 μM) and deficient Pi (0 μM) conditions, for 7, 10 and 14 Dat. A Root systems were divided into three equal regions, R1, R2 and R3, based on the root system depth. B Total root system length in each region. C Percentage of total root system length in each of the three regions. Asterisks indicate significant differences between the various Pi concentrations, in the same cultivar, in the same region, as determined by Student’s t test: for these assays, significance differences are indicated as follows: *P < 0.05; **P < 0.01; ***P < 0.001. CR crown root, PR primary root, LR lateral root. Red dotted lines represent the locations where root sections were excised for cross-sectional analyses (see Figs. 5A, E, 6A, E, and Supplementary Fig. 2)

Fig. 5

Primary root anatomy of sorghum cultivars SC103 and BTx635 grown for 10 days in hydroponics under sufficient Pi (SP, 200 μM) and low Pi (LP, 2.5 μM) conditions. Representative transverse images of primary root cross sections, collected 5 cm below the stem-root junction (A), and ~ 5 cm from the primary root tip (E) (see Fig. 4A). Histograms represent root cross-sectional area, total root cortical aerenchyma area (AA), and proportion of root cross section occupied by aerenchyma, near the stem root junction (B–D) and ~ 5 cm from the root tip (F–H) of the SC103 (green) and BTx635 (orange) primary root, respectively. Data shown are means ± SE (n = 6). Asterisks indicate significant differences between the cultivars, under the same condition, as determined by Student’s t test: for these assays, significance differences are indicated as follows: *P < 0.05; **P < 0.01; ***P < 0.001. Different lowercase letters indicate significant differences (P < 0.05) between the two Pi concentrations, in the same genotype, as determined by Tukey’s HSD tests. CSA cross section area (mm²), AA total root cortical aerenchyma area, (mm²). Scale bar applies to all images

Fig. 6

Lateral root anatomy of sorghum cultivars SC103 and BTx635 grown for 10 days in hydroponics under sufficient Pi (SP, 200 μM) and low Pi (LP, 2.5 μM) conditions. Representative transverse images of lateral root cross sections, collected 5 cm below the primary-lateral root junction (A), and ~ 5 cm from the lateral root tip (E) (see Fig. 4A). Histograms represent root cross-sectional area, total root cortical aerenchyma area (AA), and proportion of root cross section occupied by aerenchyma, near the primary-lateral root junction (B–D) and ~ 5 cm from the root tip (F–H) of the SC103 (green) and BTx635 (orange) lateral root, respectively. Data shown are means ± SE (n = 6). Asterisks indicate significant differences between the cultivars, under the same condition, as determined by Student’s t test: for these assays, significance differences are indicated as follows: *P < 0.05; **P < 0.01; ***P < 0.001. Different lowercase letters indicate significant differences (P < 0.05) between the two Pi concentrations, in the same genotype, as determined by Tukey’s HSD tests. CSA cross section area (mm²); AA total root cortical aerenchyma area (mm²). Scale bar applies to all images

Fig. 7

Root system architecture of sorghum cultivars, SC103 and BTx635, grown under sufficient N (SN, 4000 µM) and low N (LN, 400 µM) stress conditions. Plants were grown in a hydroponic pouch system and harvested at 10 Dat. A Representative root images of SC103 and BTx635, under SN and LN conditions. B Radar charts comparing the RSA traits of SC103 (green) and BTx635 (orange) under SN conditions. C Radar charts comparing the root system architecture traits of SC103 (green) and BTx635 (orange) under LN conditions. Asterisks indicate significant differences between the cultivars, under the same condition, as determined by Student’s t test: for these assays, significance differences are indicated as follows: *P < 0.05; **P < 0.01; ***P < 0.001. SDW shoot dry weight, RDW root dry weight, R/S root:shoot ratio

Fig. 8

Phenotypic differences for sorghum cultivars SC103 and BTx635 grown under control (CK), low Pi (LP, 75 μM), and low N (LN, 600 µM) stress conditions. A Representative images of SC103 and BTx635, under CK, LP and LN stress conditions. Images were taken 28 Dat. B Radar plots quantifying the RSA traits of SC103 and BTx635, under CK conditions. C Radar plots quantifying the RSA traits of SC103 and BTx635, under LP conditions. D Radar plots quantifying the RSA traits of SC103 and BTx635, under LN conditions. Asterisks indicate significant differences between the cultivars under CK, LP and LN conditions, as determined by Student’s t test: for these assays, significance differences are indicated as follows: *P < 0.05; **P < 0.01; ***P < 0.001. SDW shoot dry weight, RDW root dry weight, R/S root:shoot ratio

Fig. 9

Phenotypic differences for sorghum cultivars SC103 and BTx635 in response to water stress. Plants were grown in potting mix for 28 Dat. At the 14-day timepoint, plants were separated into two groups; a control group was well-watered (WW), whereas water was withheld from the water stress (WS) group. A Representative images of SC103 and BTx635, grown under WW and WS conditions. B Radar plots quantifying the RSA traits of SC103 and BTx635, under WW treatment. C Radar plots quantifying the RSA traits of SC103 and BTx635, under WS treatment. D Radar plots quantifying the RSA traits of SC103 under WW and WS treatment. E Radar plots quantifying the RSA traits of BTx635 under WW and WS treatment. Asterisks indicate the significant differences between the cultivars and treatments, as determined by Student’s t test: for these assays, significance differences are indicated as follows: *P < 0.05; **P < 0.01; ***P < 0.001. SDW shoot dry weight, RDW root dry weight, R/S root:shoot ratio