Isaiah Taylor, Kevin Lehner,  Erin McCaskey, Niba Nirmal,  Yasemin Ozkan-Aydin, Mason Murray-Cooper,  Rashmi Jain,  Elliot W. Hawkes,  Pamela C. Ronald,  Daniel I. Goldman, and Philip N. Benfey

PNAS February 23, 2021 118 (8) e2018940118

Significance

Root growth in soil is complex. With limited sensory input, roots must navigate an environment containing heterogeneities such as rocks and compaction. The ability of roots to penetrate soil is crucial for water and nutrient uptake as well as mechanical anchorage. Here, we describe a molecular framework controlling helical root growth known as circumnutation. Functional characterization of circumnutation is consistent with the hypothesis that it is crucial for exploratory behavior and substrate penetration. This work lays a foundation for an integrated understanding of how roots grow in soil.

Abstract

Early root growth is critical for plant establishment and survival. We have identified a molecular pathway required for helical root tip movement known as circumnutation. Here, we report a multiscale investigation of the regulation and function of this phenomenon. We identify key cell signaling events comprising interaction of the ethylene, cytokinin, and auxin hormone signaling pathways. We identify the gene Oryza sativa histidine kinase-1 (HK1) as well as the auxin influx carrier gene OsAUX1 as essential regulators of this process in rice. Robophysical modeling and growth challenge experiments indicate circumnutation is critical for seedling establishment in rocky soil, consistent with the long-standing hypothesis that root circumnutation facilitates growth past obstacles. Thus, the integration of robotics, physics, and biology has elucidated the functional importance of root circumnutation and uncovered the molecular mechanisms underlying its regulation.

See: https://www.pnas.org/content/118/8/e2018940118

Figure 1:

Phenotypic analysis of the hk1 mutant. (A) Primary root depth 2 d after germination for wild type and the hk1-1 mutant. n = 8 and 18 primary roots for wild type and mutant, respectively. Two-sided Wilcoxon Rank Sum test P value = 7.1 × 10⁻⁵. The horizontal dash indicates mean value. (B) Two-dimensional projected displacement of root tip from central axis of growth every 15 min for 48 h after germination. Red plots represent natural cubic splines fit to the data for visualization. (C) Quantification of average radius of circumnutation in wild type and hk1 between 40 and 48 h after germination. n = 7 primary roots for each genotype. Two-sided Wilcoxon Rank Sum test P value = 0.0005828. The horizontal dash indicates mean value. (D) Example circumnutating wild-type primary root exhibiting higher epidermal cell elongation on the outer bend compared to the inner bend. (E) Quantification of the difference between outer and inner length of the region of 15 epidermal cells flanking the maximal bend in wild type, with n = 9. Two-sided Wilcoxon Signed Rank test P values = 0.003906. The horizontal dash indicates mean value.