Genotypic recognition and spatial responses by rice roots

Abstract

Root system growth and development is highly plastic and is influenced by the surrounding environment. Roots frequently grow in heterogeneous environments that include interactions from neighboring plants and physical impediments in the rhizosphere. To investigate how planting density and physical objects affect root system growth, we grew rice in a transparent gel system in close proximity with another plant or a physical object. Root systems were imaged and reconstructed in three dimensions. Root-root interaction strength was calculated using quantitative metrics that characterize the extent to which the reconstructed root systems overlap each other. Surprisingly, we found the overlap of root systems of the same genotype was significantly higher than that of root systems of different genotypes. Root systems of the same genotype tended to grow toward each other but those of different genotypes appeared to avoid each other. Shoot separation experiments excluded the possibility of aerial interactions, suggesting root communication. Staggered plantings indicated that interactions likely occur at root tips in close proximity. Recognition of obstacles also occurred through root tips, but through physical contact in a size-dependent manner. These results indicate that root systems use two different forms of communication to recognize objects and alter root architecture: root-root recognition, possibly mediated through root exudates, and root-object recognition mediated by physical contact at the root tips. This finding suggests that root tips act as local sensors that integrate rhizosphere information into global root architectural changes.

Fig. 1.

Intragenotype and intergenotype rice root interaction on the seventh DAG. (A–C) Intragenotype exhibiting high frequency of overlap between root systems of the same genotype: (A) Azucena, (B) Caiapo, (C) IR64. (D–F) Intergenotype showing lower frequency of overlap between root systems of different genotypes: (D) Azucena (Left) -Caiapo (Right); (E) Azucena (Left) -IR64 (Right); (F) Caiapo (Left) -IR64 (Right).

Fig. 2.

Three-dimensional reconstruction results of rice root interaction on the seventh DAG. (A and B) Intragenotype, Azucena. (C) IR64 (Left) -Azucena (Right). (D) Caiapo (Left) -Azucena (Right). Coloring represents root depth.

Fig. 3.

Interaction analysis based on 3D voxels of rice root systems on the seventh DAG. (A) Intragenotype vs. intergenotype planting significantly affects rice root interaction (P = 0.0011, t test). (B) Comparison of interaction within intergenotype plantings with shoots not separated and separated (P = 0.71, t test). (C) Comparison of interaction within intragenotype planting with shoots not separated and separated (P = 0.95, t test). Bars represent mean of root system overlap.

Fig. 4.

Seeds planted on different days provide insight into root interaction. (A) IR64 (Left, day n+6)-Azucena (Right, day n), Azucena was planted 6 d after IR64; day 2: 2 d after the younger seedling was planted. (B) IR64 (Left, day n+6)-IR64 (Right, day n), the IR64 seedling on the right was planted 6 d after the IR64 seedling on the left. (C) IR64 grown alone on the 13th DAG. (D) Comparison of the change in the angle of the root of IR64, which is the closest to the other root system from day 3 to day 5 (P = 0.021, t test). Bars represent mean of the change in the angle. (E) The angle between OT and OP is calculated as the angle of the closest root of plant A.

Fig. 5.

Root growth differs with different size obstacles in the medium. (A) Depiction of obstacle experiment where thin plastic pieces of different sizes (1-, 3-, 5-, or 7-cm wide by 8-cm deep) were placed 1-cm away from the seed in the cylinder. (B) Comparison of Azucena root growth on the seventh DAG with obstacles of different sizes. (C–E) Change of root traits when grown with 1-cm wide or 7-cm wide obstacles compared with when grown alone with no obstacle. TRL, total root length; SA, surface area; RSV, root system volume; CA, convex area; Bush, bushiness; SRL, specific root length; MaxR, maximum root number; MedR, median root number. Bars represent mean of 15 replicates with SE.