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This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science
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Plants being sessile can often be judged as passive acceptors of their environment. However, plants are actually even more active in responding to the factors from their surroundings. Plants do not have eyes, ears or vestibular system like animals, still they “know” which way is up and which way is down? This is facilitated by receptor molecules within plant which perceive changes in internal and external conditions such as light, touch, obstacles; and initiate signaling pathways that enable the plant to react. Plant responses that involve a definite and specific movement are called “tropic” responses. Perhaps the best known and studied tropisms are phototropism, i.e., response to light, and geotropism, i.e., response to gravity. A robust root system is vital for plant growth as it can provide physical anchorage to soil as well as absorb water, nutrients and essential minerals from soil efficiently. Gravitropic responses of both primary as well as lateral root thus become critical for plant growth and development. The molecular mechanisms of root gravitropism has been delved intensively, however, the mechanism behind how the potential energy of gravity stimulus converts into a biochemical signal in vascular plants is still unknown, due to which gravity sensing in plants still remains one of the most fascinating questions in molecular biology. Communications within plants occur through phytohormones and other chemical substances produced in plants which have a developmental or physiological effect on growth. Here, we review current knowledge of various intrinsic signaling mechanisms that modulate root gravitropism in order to point out the questions and emerging developments in plant directional growth responses. We are also discussing the roles of sugar signals and their interaction with phytohormone machinery, specifically in context of root directional responses.
The gravitropic response mechanism can be divided into several sequential components, including perception of the change in the gravity vector, transduction, and asymmetrical growth response. Unlike unilateral light, gravity does not form a gradient between the upper and lower sides of an organ. All parts of the plant experience the gravitational stimulus equally. The first step of gravitropism addresses how do plant cells detect gravity? Two hypotheses have been proposed to explain how the direction of gravity is perceived by plants: (1) the gravitational-pressure model and (2) the starch-statolith hypothesis. The latter has been strongly supported by a variety of experimental approaches in various plant species. The second component of the gravitropic response mechanism is transduction, in which the development of hormone asymmetry is obtained. In the third step, a curvature response is established that allows the organ to resume growth at a defined set angle from the gravity vector; the gravitational set point angle (GSA). GSA is defined as the angle with respect to the gravity vector at which an organ is maintained as a result of gravitropism (
Plant roots are simple structure divided into various sections like root cap, meristem, elongation zone and maturation zone (
The root cell types responding to gravity stimulus in
Gravity sensing in columella cells. Roots when grown vertical have been designated time 0 min. Reorientation of seedling by rotating to 90° generates a gravistimulus and initiate gravisensing process. The amyloplasts start to settle towards the new bottom of columella cells immediately post reorientation and within 2–4 min of reorientation, amyloplast settles down completely (
According to the starch-statolith hypothesis (
Apart from the support provided for starch-statolith theory, there are enough clues for the existence of alternate mechanisms of gravity sensing in plants. These secondary mechanisms are supposed to be independent of starch and might also govern gravitropic bending. For example, the
Gravity is the only constant factor, both in direction and magnitude, to which plants definitely need to- and have to- adapt. Post gravity perception, a series of events takes place to transduce the signal within the plant system. With the use of electron tomography, it was found that, in response to gravity stimulus, sedimenting amyloplast can bend, and distort the endoplasmic reticulum (ER) upon contact (
According to the mechano-sensitive ion channel hypothesis of signal transduction, the falling amyloplast create pressure on ER or plasma membrane either directly or via actin filaments. The pressurized ER membrane opens mechano-sensitive ion channels leading to changes in concentration of ions, such as Ca2+ which in turn leads to repolarization of statocytes, relocalization of PINs and subsequent changes in auxin transport (
Post gravistimulation, changes in pH also take place in columella cells. Ca2+ levels cause alterations in cell wall pH which can regulate elongation via acid growth (
Mechano-sensitive channels could also open due to straining of actin filaments caused by amyloplast sedimentation as the amyloplasts are usually surrounded by a network of actin filament in the columella cells (
Possible physical interactions between the sedimenting amyloplast and the ER bound proteins can also be involved in generating gravity signals within cells. The ligand-receptor hypothesis came from the study of single-celled rhizoids of the green algae
Another signaling molecule involved in graviresponse is Inositol 1,4,5-trisphosphate (InsP3). Evidence for the role of InsP3 in gravitropism came from measurement of InsP3 levels during early gravitropic responses. Upon gravistimulation, InsP3 fluxes were found to first fluctuate and then increase at the bottom half of oat pulvinus (
Root growth is governed by the coordinated events of cell division and elongation of the newly formed cells. Plants roots are extremely sensitive to environmental stimulation such as; gravity, mechanical obstacles, light, moisture and nutrient gradients modulating the directional growth of roots to obtain an optimal growth trajectory. The initial work of Darwin represented various plant movements which were defined as a result of circumnutation (
Phytohormones have profound effects on development at vanishingly low concentrations. The emerging concept of cooperative hormone action opens new possibilities for a better understanding of the complex interactions between all phytohormones and their possible synergistic effects on regulation of gravitropism. Even though numerous reports on gravitropism are published, the actual gravity receptor has not been identified yet. Auxin, ethylene, cytokinin and BRs have been the most explored hormones in relation to gravitropism but not much evidence has been accumulated regarding the participation of other phytohormones such as; Gibberellins (GAs), abscisic acid (ABA), jasmonates (JA), and salicylic acid (SA) in gravitropism.
Auxin was the earliest hormone to be identified with an implicated function during gravitropism, and for many years it dominated as the primary hormone regulating graviresponses. Auxin transport and response to auxin is pre-requisite for the development of tropic curvatures. Auxin, which is mainly synthesized in young shoot tissues, uses a cell-to-cell transport system that functions in the tip to base direction in shoots. When auxin reaches the root, it is transported through the central cylinder into root tip, where it adds to a pool of locally synthesized auxin, forming an auxin-maximum center that overlaps with the quiescent center and top layers of the root-cap columella. There, auxin is redistributed laterally to peripheral tissues, then transported basipetally through lateral-cap and epidermal cell files toward the elongation zone, where it inhibits cell elongation (
Auxin redistribution upon a gravity stimulus. Auxin distribution (blue) and direction of flow (depicted by arrows). Auxin from the shoot to the root tip (red arrows) is mediated by AUX1 and PIN2. Auxin flow is further distributed through the vascular tissue to the columella cells (yellow arrows). PIN3 is localized in the columella cells and gravity stimulus induces more PIN3 localization (orange) to the lower side of columella cells redirecting auxin flow to the lower side of the root (
There are three types of transmembrane proteins that mainly transport auxin across the plasma membrane; (i) the transmembrane proteins AUXIN RESISTANT 1/LIKE AUX1 (AUX1/LAX), which operates as influx carriers to enable the transport of protonated auxin (
Analysis of gravitropic response of mutants defective in auxin-signaling provided additional support for the involvement of auxin response pathway during root gravitropism. Upon gravistimulation, many auxin-responsive genes are differentially regulated. Auxin is sensed by members of TRANSPORT INHIBITOR RESPONSE 1/AUXIN-RELATED F-BOX (TIR1/AFB) family of auxin receptors (
Besides auxin, ethylene is another phytohormone that has been widely investigated during regulation of gravitropism. Although ethylene is intimately involved in regulating growth at the cellular level, its influence on graviresponses might not be a direct one. Ethylene activates local auxin signaling pathway and regulates root growth by regulating auxin biosynthesis or by modulating the auxin transport (
Gibberellins are prime regulators of cell elongation (
Abscisic acid exerts mainly inhibitory effects on growth and development. Initial studies on the role of ABA in gravitropism were a little discouraging due to several reasons. Exogenously applied ABA does not inhibit rather promotes root growth, and the inhibitory effect is gained only at concentrations significantly higher than those thought to naturally occur. Also, roots of ABA-deficient plants obtained either by chemically inhibiting ABA synthesis or by specific mutations showed no altered response to gravity (
Cytokinins are hormones that regulate cell division and development and play essential and crucial roles in various aspects of plant growth (
Cytokinin may also interact with auxin machineries to regulate gravitropic response (
Brassinosteroid (BRs) are regarded to be essential substances for growth and development in plants, and their occurrence has been demonstrated in all plant organs. Brassinolide (BL) was found to increase the gravitropic response of roots by increasing their sensitivity to IAA (
Jasmonic acid is mostly studied in regulating plant defense but its function during plant growth and development is also fast emerging. There is very less information available in context of root gravitropism. As modulation of JA homeostasis as well as signal transduction can mimic auxin effects on root development, we assume it to have some effect on root gravitropic responses as well. In rice coleoptiles, the total content of JA is found to be increased upon gravity reorientation (
Light is an essential component for energy production and survival in plants. Light regulates nearly all stages of plant development on the basis of its quantity, quality and directionality. On the other hand, gravity is a constant stimulus providing plants with the critical information about its surroundings and thus guiding plant growth. Evidences have shown that light is required for triggering gravitropism in plants. The roots of
Nutrient availability is a major factor controlling growth in a constantly changing environment. Plants, like other living organisms, need to maintain nutrient and energy homeostasis within cells and tissues for growth. They fulfil their energy requirement by fixing light into a metabolizable form via photosynthesis where carbohydrate (sugar) energy is utilized as fuel for growth and/or stored as reserve. Sugars are the prime carbon and energy source to build and fuel cells, and also acquired important regulatory functions in controlling metabolism, stress resistance, growth and development. Sugars also have an important signaling function and act like hormones in translating nutrient status to regulate growth and floral transition (
Sugar signaling pathway exhibits crosstalk with other response pathways such as those involved in light, phytohormones and stress responses. In plants, sugar and phytohormone signal cross-talks have been shown to modulate critical growth and developmental processes such as embryo establishment, seed germination, and early seedling growth and development (
Plants, being sessile organisms, use the coordinated action of several signaling pathways to grow and develop optimally in response to a changing environment. We know that light is an important factor in determining the directionality of plant growth. But gravity, a force that causes objects to fall and holds the planets in their orbits around the sun, is also critically important. Root directional growth and growth angle determines the area coverage in which it can capture water and nutrients and guides a plant to utilize nutrients that are unevenly distributed in soil. Plants have evolved to respond to different stimuli to help them orient to their best advantage. The growth and development of plants is mainly dependent on the platform set by the integrations of various signals such as light, gravity, nutrient, phytohormones etc. There are numerous examples of synergy, antagonism, and causal relationships among the different signaling pathways under various molecular and physiological processes, such as the control of cell expansion and divisions that define the architecture of vascular plants. Gravitropism is one of the major factors that determine root growth direction. Mechanism and control of gravi-response is a highly complex process which also involves several growth regulators. Recently introduced novel fluorescent pH indicator 8-hydroxypyrene-1,3,6-trisulfonic acid trisodium salt (HPTS) have enabled better understanding of asymmetric apoplast alkalization in gravistimulated roots and subsequent processes (
All authors have made intellectual contribution to the article, and approved it for publication. MS, AG, and AL conceptualized the article. MS and AG wrote the article and did final editing.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors are thankful to Department of Science and Technology, Government of India for financial support (BT/PR3302/AGR/02/814/2011) and research fellowships to MS (DST/INSPIRE/04/2016/000634) and AG (DST/INSPIRE/04/2015/001952).