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How Grow-And-Switch Gravitropism Generates Root Coiling and Root Waving Growth Responses in Medicago Truncatula

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How Grow-And-Switch Gravitropism Generates Root Coiling and Root Waving Growth Responses in Medicago Truncatula How grow-and-switch gravitropism generates root coiling and root waving growth responses in Medicago truncatula Tzer Han Tana,1, Jesse L. Silverbergb, Daniela S. Flossc, Maria J. Harrisonc, Christopher L. Henleyb,2, and Itai Cohenb aDepartment of Applied and Engineering Physics, Cornell University, Ithaca, NY 14853; bDepartment of Physics, Cornell University, Ithaca, NY 14853; and cBoyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY 14853 Edited by William Bialek, Princeton University, Princeton, NJ, and approved September 1, 2015 (received for review May 21, 2015) Experimental studies show that plant root morphologies can vary experimental work accounted for the waving morphology as a widely from straight gravity-aligned primary roots to fractal-like combination of positive gravitropism and a thigmotropic (growth root architectures. However, the opaqueness of soil makes it dif- response to touch) effect (25). This interpretation relied on the ficult to observe how environmental factors modulate these pat- barrier to simultaneously prevent gravity-aligned growth and acti- terns. Here, we combine a transparent hydrogel growth medium vate a thigmotropic twisting of the root tip; however, later experi- with a custom built 3D laser scanner to directly image the mor- ments demonstrated a role for friction as an additional contributing phology of Medicago truncatula primary roots. In our experi- factor (28). Although Arabidopsis mutants have been used to ex- ments, root growth is obstructed by an inclined plane in the plore the underlying genetic regulatory pathways of root waving, the detailed mechanism coupling gravity sensing and the growth envi- growth medium. As the tilt of this rigid barrier is varied, we find ronment’s mechanical properties is still open to debate (27, 29, 30). Medicago transitions between randomly directed root coiling, si- While these initial studies have proposed different mecha- nusoidal root waving, and normal gravity-aligned morphologies. nisms for root waving, it remains unknown whether the phe- Although these root phenotypes appear morphologically distinct, nomenon is species-specific or a generic root growth strategy. our analysis demonstrates the divisions are less well defined, and Here, we perform experiments on Medicago truncatula, a model instead, can be viewed as a 2D biased random walk that seeks the legume, and find growth patterns similar to root waving. This path of steepest decent along the inclined plane. Features of this plant is larger than Arabidopsis and fast-growing, which makes it growth response are remarkably similar to the widely known run- convenient for study. Our experiments combine 3D imaging with and-tumble chemotactic behavior of Escherichia coli bacteria, a controlled mechanical growth environment that interpolates where biased random walks are used as optimal strategies for between a horizontal physical barrier and normal unobstructed nutrient uptake. growth. This approach allows us to nondestructively examine the in situ root development and quantify the resulting morphology plant biomechanics | root morphology | root waving | root coiling | with a variety of geometric and statistical metrics. Whereas pattern formation previous studies have focused on temporal dynamics and genetic components of root waving, we turn our attention to the growth barrier’s tilt angle and subsequently probe different aspects of lants are able to sense a wide variety of external stimuli, the phenomenon. Ultimately, our analysis reveals a mechanism Pgiving rise to actively controlled responses driven by gradi- that produces root waving as a byproduct of gravitropic reori- ents in light, gravity, touch, nutrient resources, and water. These entation on the mechanical barrier, and the root’s measurement responses, which include phototropism, gravitropism, thigmotro- tolerance for the direction of gravity. pism, chemotropism, and hydrotropism, take input from the local environment and modulate phenotype development in a manner Experimental Procedures essential for survival (1–5). A number of plant growth responses, Medicago seedlings were germinated and transferred to transparent such as the popping of chiral seed pods (6) and the overwinded chambers containing growth media with Gelrite, which provided both morphology of cucumber tendrils (7), are dominated by the me- moderate mechanical impedance to root growth and an abundant source of chanical properties of plant tissues and their passive response to nutrients (see SI Appendix, SI Materials and Methods; also see ref. 31). In physical forces. However, these special cases aside, growth pat- terns are more typically modulated by a combination of actively Significance regulated biological processes and passive mechanical response. The snapping of a Venus fly trap (8–11) is a classic example, where Root waving, a growth response previously discussed pre- cell turgor pressure and thin shell mechanics work in tandem to dominantly in Arabidopsis, is reported in Medicago truncatula. determine the plant’s phenotype. Continued studies of de- Analogous to bacterial chemotaxis where Escherichia coli uses velopmental morphology at the interface between mechanical and a “run-and-tumble” strategy to find sources of food, our ex- biological regulation play an essential role in bridging phenotypic periments reveal a “grow-and-switch” gravitropic response in and biomolecular points of view (12, 13), while offering a more these root systems. This finding offers valuable insights into complete understanding of plant biomechanics. the strategies used for plants as they navigate heterogeneous In the context of roots, the mechanical properties of the growth environments in search of water and nutrient resources. medium play a critical role in modulating root morphology, as evidenced by a variety of studies examining the role of soil im- Author contributions: T.H.T., J.L.S., D.S.F., M.J.H., C.L.H., and I.C. designed research; T.H.T. pedance (14–19), granularity (20), the presence of cracks (21), and and D.S.F. performed research; T.H.T. contributed new reagents/analytic tools; T.H.T., J.L.S., mechanical barriers (22–24). For example, experiments with Ara- C.L.H., and I.C. analyzed data; and T.H.T., J.L.S., D.S.F., M.J.H., C.L.H., and I.C. wrote the paper. bidopsis thaliana primary roots show that normal gravity-aligned The authors declare no conflict of interest. morphologies interrupted by a horizontal barrier lead to an in- This article is a PNAS Direct Submission. plane coiling of the root. As the barrier is tilted, a combination of 1To whom correspondence should be addressed. Email: [email protected]. active and passive growth responses drive root waving (25–30). In 2Deceased June 29, 2015. these conditions, the primary root exhibits sinusoidal growth that This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. deviates from a strict downward direction along the plane. Early 1073/pnas.1509942112/-/DCSupplemental. 12938–12943 | PNAS | October 20, 2015 | vol. 112 | no. 42 www.pnas.org/cgi/doi/10.1073/pnas.1509942112 Downloaded by guest on September 29, 2021 total, 92 plants were germinated, with each growth chamber containing one 2 ° 2 ° ° plant; 87 samples were analyzed in this work, whereas the remaining ABθ=0 θ=10 ±1 5 exhibited atypical stunted growth and were excluded from our analysis. To 1 1 systematically study root waving, we introduced a physical barrier in the growth medium tilted at an angle θ, measured from the horizontal (Fig. 1A). 0 0 Initially, the primary root of each newly transferred seedling was ∼1cmin length, and it grew vertically downward until encountering the physical -1 -1 Position, y (cm) barrier. It then grew almost exclusively on the surface of the barrier plane Position, y (cm) for 10–14 d. We used a translating stage moving perpendicular to a laser -2 -2 sheet to illuminate successive cross sections of the root and captured the ° ° ° ° CD1 θ=25 ±1 1 θ=50 ±1 resulting images with a digital camera (Fig. 1A) (24). The resulting image stack was then analyzed in MATLAB, and the 3D root morphology was 0 0 reconstructed (Fig. 1B). Undulations of the root perpendicular to the barrier surface were generally not observed but, when they did occur, were 1 mm or -1 -1 Pos., y (cm) less. Thus, we projected the 3D root path onto the 2D plane of the growth Pos., y (cm) 0312245031 45 barrier and used this digitized trajectory in our analysis. Position, x (cm) Position, x (cm) Results and Discussion Fig. 2. Overlays of several Medicago root centerlines grown on planes tilted at various angles. As the tilt θ increases, the root morphologies transition Coiling, Waving, and Skewing Morphologies. The morphology of from (A) a random, meandering root path at θ = 0° to (B and C) a sinusoidal Medicago exhibits distinct regimes as the tilt angle of the me- θ = θ pattern around 10° (B) to 25° (C) and, ultimately, (D) a skewed trajectory chanical barrier is increased from 0° to 50°. When the plane is with small undulations at θ = 50°. In each panel, there are multiple root paths horizontal, the primary root meanders on the surface, with seg- shown in different colors, and the point where each root makes first contact ments of alternating chirality that make incomplete planar coils with the tilted plane is marked with a black square. For clarity, A has the before reversing their direction (Fig. 2A). As expected, these re- black squares spread out, and B−D have the squares starting at x = 0 cm with versals exhibit no in-plane directional preference, which is con- growth generally proceeding toward the right. sistent with the uniform gravitational signal across the horizontal growth plane. Owing to the random coils that dominate the morphology and similarity to growth response observed in Arabi- sinusoidal wave and, finally, to a relatively straight skewed path. dopsis, this regime is referred to as “root coiling” (29, 30). This observation suggests that the distinct morphologies have When a nonzero tilt angle is introduced to the mechanical common underlying causal mechanisms and thus can be viewed in barrier (θ > 0°), the gravitational signal along the growth plane is a unified fashion.
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