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The Roles of Microtubules in Tropisms Plant Science Plant Science 175 (2008) 747–755 Contents lists available at ScienceDirect Plant Science journal homepage: www.elsevier.com/locate/plantsci Review The roles of microtubules in tropisms Sherryl R. Bisgrove * Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, B.C., Canada V5A 1 s6 ARTICLE INFO ABSTRACT Article history: Plant tropisms, or growth towards or away from a stimulus, usually involve the bending of shoots or roots Received 11 March 2008 which reorient growth in a new direction. Plant responses to tropic cues, especially gravity and light, have Received in revised form 19 August 2008 been active areas of investigation for many years. Despite all of this attention we still do not understand Accepted 19 August 2008 how these responses are regulated. In this review possible roles for microtubules in tropisms are Available online 7 September 2008 discussed. Tropisms occur in a series of steps; directional cues are perceived and converted into biochemical signals that induce bending in roots and shoots. One model suggests that microtubules Keywords: function late in the response pathway, during organ bending. Microtubules have been linked to organ Microtubule Cytoskeleton bending by virtue of their role in regulating the direction of cell elongation. In elongating cells Cell expansion microtubules appear to function as guides for the deposition of cellulose microfibrils into the cell wall and Cell wall the placement of the microfibrils in the wall is thought to constrain the direction of cell elongation. Tropism According to the model bending occurs when different microtubule/microfibril alignments across the organ cause cells on the outer flank to elongate more than cells on the inner flank. In support of this idea is the observation that tropic signals can induce the appropriate changes in microtubule orientations across a bending organ. However, attempts to validate the hypothesis have produced conflicting results and the idea that microtubule alignment regulates cell expansion during organ bending is controversial. Microtubules have also been linked to organizational events associated with the plasma membrane. Although speculative, one possibility is that microtubules influence tropisms by positioning regulatory proteins and/or complexes in the plasma membrane. Two possible mechanisms by which microtubules could contribute to organizational events associated with the plasma membrane are outlined. In addition to cell expansion, microtubules are postulated to have roles in the perception of touch and gravity signals. Although microtubules are associated with touch sensing in animals, we know very little about the relevant receptors in plants. One way to assess how microtubules function during tropisms is to identify and study proteins that function in concert with microtubules. In particular, the analysis of microtubule- associated proteins whose mutant forms confer defects in tropic responses promises to provide additional insights into the roles of microtubules in tropisms. ß 2008 Elsevier Ireland Ltd. All rights reserved. Contents 1. Introduction . 748 1.1. Signal perception . 748 1.2. Auxin redistribution and differential growth . 748 1.3. Possible roles for microtubules . 749 2. Cortical microtubule organization and cell elongation . 749 2.1. Cellulose deposition . 750 2.2. Microtubule reorientations and tropisms . 750 3. Beyond cellulose deposition: new roles for microtubules? . 751 4. Summary and future directions . 753 Acknowledgements. 753 References...................................................................................................... 753 * Tel.: +1 778 782 5269; fax: +1 778 782 3496. E-mail address: [email protected]. 0168-9452/$ – see front matter ß 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.plantsci.2008.08.009 748 S.R. Bisgrove / Plant Science 175 (2008) 747–755 1. Introduction mechanosensors [7]. However, the physiological relevance of these channels in intact plants is unknown. Plants are sessile and cannot move when conditions become The receptors that mediate gravity perception have not been unfavorable. They can, however, redirect their growth to identified, although two models that describe how gravity is position stems, roots, leaves, and flowers towards the best sensed have been put forward in the literature. The starch-statolith possible locations. Shoots grow towards light, maximizing hypothesis postulates that gravity-sensitive cells detect the falling photosynthetic activity. Roots point down along the gravity of intracellular masses called statoliths (see refs. [18,23] for vector and can be attracted to areas of higher moisture or reviews). The gravitational pressure model proposes that the nutrient content in the soil. When conditions change, plants settling of the protoplast within the cell wall is sensed by receptors respond by redirecting their growth in accordance with the new at the plasma membrane–extracellular matrix junction [18,24]. signals. Tropisms, these changes in the direction of growth in These receptors would be capable of detecting differences in response to stimuli, involve the bending of stems or roots that tension and compression between the plasma membrane and the reorient growth in the most favorable direction. Tropisms extracellular matrix at the top and bottom of the cell. Higher plant include responses to a number of cues including gravity cells that can sense gravity commonly contain starch-filled (gravitropism), light (phototropism), and touch (thigmotrop- amyloplasts that sediment and it is thought that this is the ism), as well as gradients of moisture (hydrotropism), chemicals primary mechanism by which gravity is perceived, although it is (chemotropism), and temperature (thermotropism). Although possible that protoplast settling is also detected [18,23]. How these tropisms have all been documented many have not been amyloplast sedimentation is converted into a biochemical signal is investigated in any further detail [1].Gravitropismand not understood, although it has been proposed that mechan- phototropism have received the most attention, although some osensitive ion channels are involved [11,14,16,25,26]. studies addressing hydrotropism and thigmotropism have been With the exception of hydrotropism, plant responses to most published in recent years [2–10]. other directional cues have been described mainly from a Tropisms can be either positive or negative depending on phenomenological perspective [1]. Recently genetic approaches whether growth occurs towards or away from the stimulus. The have been used in efforts to understand the mechanisms that response occurs through a series of steps. Directional cues are regulate hydrotropism [3–6,27,28]. Screens for mutants that are sensed and converted into biochemical signals. Under normal defective in hydrotropic responses have been done [29] and the conditions, plants receive many cues at once often from different characterization of the corresponding genes promises to yield directions. To cope with all of this information incoming signals insight into the molecular mechanisms that regulate hydrotropism must be integrated and transmitted to the responding cells where [1]. the changes in growth occur (see ref. [11] for a review). Gravity is a constant stimulus and changes in growth occur only when 1.2. Auxin redistribution and differential growth opposing cues out compete or over-ride gravity [11]. Because of the large amount of incoming information and the requirement for Signals controlling tropisms often result in a concentration an integrated growth response, the signaling pathways that gradient of auxin across a responding organ and this auxin gradient underlie tropisms are complex and they are not well understood. is responsible for redirecting growth [17,19,30]. Consider, for However, this is an active area of investigation and it is discussed in example, a seedling that has been placed on its side. Auxin several recent reviews [1,6,11–19]. accumulates to a higher level on the lower flanks of the hypocotyl and root. According to the Cholodony–Went hypothesis [31],an 1.1. Signal perception auxin gradient triggers a differential growth response in which cells on one side of the organ elongate more than cells on the other The receptors responsible for initiating phototropism, the side. Because the cells are held together and cannot move apart phototropins, were the first to be described at the molecular level from one another, differential growth results in the formation of a (see ref. [12] for a review). They are autophosphorylating protein kinases that are activated by blue light [12,17,20]. In addition to phototropins cryptochromes, another class of blue light receptors, and phytochromes, red/far-red reversible photoreceptors, also modulate phototropism [17,19,21]. Once activated, the photo- tropins transfer the light signal to proteins in downstream signaling pathways, but as of yet only a few of these intermediates have been identified [12,17,22]. Little is known about mechanoperception in plants, although studies in bacteria and animals are providing information about how mechanical stimuli are sensed in these organisms. The relevant receptors appear to be mechanosensitive ion channels Fig. 1. Bend formation in the hypocotyl and root of a seedling responding to light [16]. These channels are transmembrane complexes that open in and gravity. In the seedling on the left, the shoot (shaded in green) grows up response to mechanical forces exerted
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