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Ionic signaling in plant responses to gravity and touch

Touch and gravity are two of the many stimuli that plants must integrate to generate an appropriate growth response. Due to the mechanical nature of both of these signals, shared signal transduction elements could well form the basis of the cross-talk between these two sensory systems. However, touch stimulation must elicit signaling events across the plasma membrane whereas gravity sensing is thought to represent transformation of an internal force, amyloplast sedimentation, to signal transduction events. In addition, factors such as turgor pressure and presence of the cell wall may also place unique constraints on these plant mechanosensory systems. Even so, the candidate signal transduction elements in both plant touch and gravity sensing, changes in Ca2+, pH and membrane potential, do mirror the known ionic basis of signaling in animal mechanosensory cells. Distinct spatial and temporal signatures of Ca2+ ions may encode information about the different mechanosignaling stimuli. Signals such as Ca2+ waves or action potentials may also rapidly transfer information perceived in one cell throughout a tissue or organ leading to the systemic reactions characteristic of plant touch and gravity responses. Longer-term growth responses are likely sustained via changes in gene expression and asymmetries in compounds such as inositol-1,4,5-triphosphate (IP3) and calmodulin. Thus, it seems likely that plant mechanoperception involves both spatial and temporal encoding of information at all levels, from the cell to the whole plant. Defining this patterning will be a critical step towards understanding how plants integrate information from multiple mechanical stimuli to an appropriate growth response.

Review↗

Two distinct regions of response drive differential growth in Vigna root electrotropism

Although exogenous electric fields have been reported to influence the orientation of plant root growth, reports of the ultimate direction of differential growth have been contradictory. Using a high-resolution image analysis approach, the kinetics of electrotropic curvature in Vigna mungo L. roots were investigated. It was found that curvature occurred in the same root toward both the anode and cathode. However, these two responses occurred in two different regions of the root, the central elongation zone (CEZ) and distal elongation zone (DEZ), respectively. These oppositely directed responses could be reproduced individually by a localized electric field application to the region of response. This indicates that both are true responses to the electric field, rather than one being a secondary response to an induced gravitropic stimulation. The individual responses differed in the type of differential growth giving rise to curvature. In the CEZ, curvature was driven by inhibition of elongation, whereas curvature in the DEZ was primarily due to stimulation of elongation. This stimulation of elongation is consistent with the growth response of the DEZ to other environmental stimuli.

Non-NASA Center↗

Collection of gravitropic effectors from mucilage of electrotropically-stimulated roots of Zea mays L

We placed agar blocks adjacent to tips of electrotropically stimulated primary roots of Zea mays. Blocks placed adjacent to the anode-side of the roots for 3 h induced significant curvature when subsequently placed asymmetrically on tips of vertically-oriented roots. Curvature was always toward the side of the root unto which the agar block was placed. Agar blocks not contacting roots and blocks placed adjacent to the cathode-side of electrotropically stimulated roots did not induce significant curvature when placed asymmetrically on tips of vertically-oriented roots. Atomic absorption spectrophotometry indicated that blocks adjacent to the anode-side of electrotropically-stimulated roots contained significantly more calcium than (1) blocks not contacting roots, and (2) blocks contacting the cathode-side of roots. These results demonstrate the presence of a gradient of endogenous Ca in mucilage of electrotropically-stimulated roots (i.e. roots undergoing gravitropic-like curvature).

NASA Discipline Number 40-10↗

Characterization of thermotropism in primary roots of maize: dependence on temperature and temperature gradient, and interaction with gravitropism

Thermotropism in primary roots of Zea mays L. was studied with respect to gradient strength (degrees C cm-1), temperature of exposure within a gradient, pre-treatment temperature, and gravitropic stimulation. The magnitude of the response decreased with gradient strength. Maximum thermotropism was independent of gradient strength and pre-treatment temperature. The range of temperature for positive and negative thermotropism did not change with pre-treatment temperature. However, the exact range of temperatures for positive and negative thermotropism varied with gradient strengths. In general, temperatures of exposure lower than 25 degrees C resulted in positive tropic responses while temperatures of exposure of 39 degrees C or more resulted in negative tropic responses. Thermotropism was shown to modify and reverse the normal gravitropic curvature of a horizontal root when thermal gradients were applied opposite the 1 g vector. It is concluded that root thermotropism is a consequence of thermal sensing and that the curvature of the primary root results from the interaction of the thermal and gravitational sensing systems.

Non-NASA Center↗

Hydrotropism and its interaction with gravitropism in maize roots

We have partially characterized root hydrotropism and its interaction with gravitropism in maize (Zea mays L.). Roots of Golden Cross Bantam 70, which require light for orthogravitropism, showed positive hydrotropism; bending upward when placed horizontally below a hydrostimulant (moist cheesecloth) in 85% relative humidity (RH) and in total darkness. However, the light-exposed roots of Golden Cross Bantam 70 or roots of a normal maize cultivar, Burpee Snow Cross, showed positive gravitropism under the same conditions; bending downward when placed horizontally below the hydrostimulant in 85% RH. Light-exposed roots of Golden Cross Bantam 70 placed at 70 degrees below the horizontal plane responded positively hydrotropically, but gravitropism overcame the hydrotropism when the roots were placed at 45 degrees below the horizontal. Roots placed vertically with the tip down in 85% RH bent to the side toward the hydrostimulant in both cultivars, and light conditions did not affect the response. Such vertical roots did not respond when the humidity was maintained near saturation. These results suggest that hydrotropic and gravitropic responses interact with one another depending on the intensity of one or both factors. Removal of the approximately 1.5 millimeter root tip blocked both hydrotropic and gravitropic responses in the two cultivars. However, removal of visible root tip mucilage did not affect hydrotropism or gravitropism in either cultivar.

NASA Program Space Biology↗

Intensity of hydrostimulation for the induction of root hydrotropism and its sensing by the root cap

Roots of Pisum sativum L. and Zea mays L. were exposed to different moisture gradients established by placing both wet cheesecloth (hydrostimulant) and saturated aqueous solutions of various salts in a closed chamber. Atmospheric conditions with different relative humidity (RH) in a range between 98 and 86% RH were obtained at root level, 2 to 3mm from the water-saturated hydrostimulant. Roots of Silver Queen corn placed vertically with the tips down curved sideways toward the hydrostimulant in response to approximately 94% RH but did not respond positively to RH higher than approximately 95%. The positive hydrotropic response increased linearly as RH was lowered from 95 to 90%. A maximum response was observed at RH between 90 and 86%. However, RH required for the induction of hydrotropism as well as the responsiveness differed among plant species used; gravitropically sensitive roots appeared to require a somewhat greater moisture gradient for the induction of hydrotropism. Decapped roots of corn failed to curve hydrotropically, suggesting the root cap as a major site of hydrosensing.

NASA Discipline Plant Biology↗

Wall to membrane linkers, stretch activated channels, and the detection of tension, voltage, temperature, auxin, and pH

Introduction. The higher plant is a heterogeneous, mechanically prestressed structure continually subject to shifting forces. When a cell grows in a plant at gravitropic equilibrium, it must create localized maxima of shear in walls of neighboring cells. Such mechanical stress and strain are likely detected in a variety of ways. However, tension-sensitive ion channels are of particular interest because it appears that they are elaborately evolved for sensory function. We hypothesize that 1) the patchy patterns of high shear are focused via wall-to-membrane linkers onto the plasma membrane, where 2) they are translated by mechanosensory cation channels into corresponding patterns of high cytosolic Ca2+, which 3) initiate local enhancement of wall expansion. Further, we hypothesize that the local promotion of enhancement is achieved at least in part by local intensification of auxin transport across the plasma membrane. By implication, when an organ is asymmetrically pressed, rubbed, or bent or when it is displaced in the gravitational field, the net asymmetry of shear stress occurring across the organ would lead to asymmetric redistribution of auxin and corrective asymmetric growth. We shall describe a representative mechanosensitive Ca(2+) -selective cation channel (MCaC) with susceptibilities to xenobiotics implicating it as a force transducer in thigmo- and gravitropism. Then, we shall consider whether a putative wall-to-membrane linker (WML) could be a key feature of the molecular architecture permitting the stress distributed in the wall system to be focused on the channels.

NASA Discipline Number 40-50↗

Temperature sensing by primary roots of maize

Zea mays L. seedlings, grown on agar plates at 26 degrees C, reoriented the original vertical direction of their primary root when exposed to a thermal gradient applied perpendicular to the gravity vector. The magnitude and direction of curvature can not be explained simply by either a temperature or a humidity effect on root elongation. It is concluded that primary roots of maize sense temperature gradients in addition to sensing the gravitational force.

NASA Program Space Biology↗

The tropic response of plant roots to oxygen: oxytropism in Pisum sativum L

Plant roots are known to orient growth through the soil by gravitropism, hydrotropism, and thigmotropism. Recent observations of plant roots that developed in a microgravity environment in space suggested that plant roots may also orient their growth toward oxygen (oxytropism). Using garden pea (Pisum sativum L. cv. Weibul's Apollo) and an agravitropic mutant (cv. Ageotropum), root oxytropism was studied in the controlled environment of a microrhizotron. A series of channels in the microrhizotron allowed establishment of an oxygen gradient of 0.8 mmol mol-1 mm-1. Curvature of seedling roots was determined prior to freezing the roots for subsequent spectrophotometric determinations of alcohol dehydrogenase activity. Oxytropic curvature was observed all along the gradient in both cultivars of pea. The normal gravitropic cultivar showed a maximal curvature of 45 degrees after 48 h, while the agravitropic mutant curved to 90 degrees. In each cultivar, the amount of curvature declined as the oxygen concentration decreased, and was linearly related to the root elongation rate. Since oxytropic curvature occurred in roots exposed to oxygen concentrations that were not low enough to induce the hypoxically responsive protein alcohol dehydrogenase, we suspect that the oxygen sensor associated with oxytropism does not control the induction of hypoxic metabolism. Our results indicate that oxygen can play a critical role in determining root orientation as well as impacting root metabolic status. Oxytropism allows roots to avoid oxygen-deprived soil strata and may also be the basis of an auto-avoidance mechanism, decreasing the competition between roots for water and nutrients as well as oxygen.

short duration↗

Oxytropism: a new twist in pollen tube orientation

Chemical gradients and structural features within the pistil have been previously proposed as factors determining the directionality of pollen tube growth. In this study, we examine the behavior of pollen of eight species germinated in a dynamic oxygen gradient. While the germination rates of some species decreased directly with decreasing oxygen tension, other species showed no decrease in germination at oxygen tensions as low as 2 kPa. In one species, germination was consistently greater at decreased oxygen tensions than at ambient atmospheric levels. In three of the eight species tested, the developing pollen tube showed clear directional growth away from the more-oxygenated regions of the growth medium, while in one species growth was towards the more-oxygenated region. The remaining four species showed random tube growth. The pattern of oxytropic responses among the taxa suggests that this tropic behavior is both widespread and phylogenetically unpredictable.

NASA Discipline Plant Biology↗