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The TOR–Auxin Connection Upstream of Root Hair Growth

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The TOR–Auxin Connection Upstream of Root Hair Growth plants Review The TOR–Auxin Connection Upstream of Root Hair Growth Katarzyna Retzer 1,* and Wolfram Weckwerth 2,3 1 Laboratory of Hormonal Regulations in Plants, Institute of Experimental Botany, Czech Academy of Sciences, 165 02 Prague, Czech Republic 2 Molecular Systems Biology (MOSYS), Department of Functional and Evolutionary Ecology, University of Vienna, 1010 Vienna, Austria; [email protected] 3 Vienna Metabolomics Center (VIME), University of Vienna, 1010 Vienna, Austria * Correspondence: [email protected] Abstract: Plant growth and productivity are orchestrated by a network of signaling cascades involved in balancing responses to perceived environmental changes with resource availability. Vascular plants are divided into the shoot, an aboveground organ where sugar is synthesized, and the underground located root. Continuous growth requires the generation of energy in the form of carbohydrates in the leaves upon photosynthesis and uptake of nutrients and water through root hairs. Root hair outgrowth depends on the overall condition of the plant and its energy level must be high enough to maintain root growth. TARGET OF RAPAMYCIN (TOR)-mediated signaling cascades serve as a hub to evaluate which resources are needed to respond to external stimuli and which are available to maintain proper plant adaptation. Root hair growth further requires appropriate distribution of the phytohormone auxin, which primes root hair cell fate and triggers root hair elongation. Auxin is transported in an active, directed manner by a plasma membrane located carrier. The auxin efflux carrier PIN-FORMED 2 is necessary to transport auxin to root hair cells, followed by subcellular rearrangements involved in root hair outgrowth. This review presents an overview of events upstream and downstream of PIN2 action, which are involved in root hair growth control. Keywords: TOR signaling; auxin; PIN-FORMED 2; root hair growth; polar cell elongation; ROP2; ROS; root growth; plant adaptation Citation: Retzer, K.; Weckwerth, W. The TOR–Auxin Connection Upstream of Root Hair Growth. Plants 2021, 10, 150. https://doi.org/ 1. Introduction 10.3390/plants10010150 Plant growth, and, more critically, its adaptation to ever-changing environmental conditions, is maintained by the ability of plants to perceive exogenous signals, to evaluate Received: 13 December 2020 the availability of resources, and to initiate signaling cascades orchestrating changes in Accepted: 11 January 2021 growth rate and direction [1–3]. The most crucial aspect of plant fitness is to keep the Published: 13 January 2021 potential of balancing the amount of cell division in meristematic regions and elongation processes and differentiation to mature cells, which depends on environmental conditions Publisher’s Note: MDPI stays neu- and available resources [2,4]. Efficient growth requires the generation of energy in form of tral with regard to jurisdictional clai- ms in published maps and institutio- sugars in the leaves of the plant upon photosynthesis, which is followed by the biosynthesis nal affiliations. of the phytohormone and growth regulator auxin [2,5,6]. Furthermore, the plant needs to regulate nutrient and water uptake through the root from the soil [7,8]. To enhance uptake efficiency, the root has the ability to grow tubular structures from specialized epidermis cells, the root hairs [7,8]. Root hair cell priming and outgrowth are highly dependent on Copyright: © 2021 by the authors. Li- proper auxin distribution and abundance, whereby both are dependent on environmental censee MDPI, Basel, Switzerland. conditions and the overall condition of the plant [2,8–11]. Distribution of the phytohormone This article is an open access article auxin through the plant creates auxin gradients, which orchestrate the activity of meristems, distributed under the terms and con- adaptational growth via cell expansion, and differentiation of specialized cells [12–15]. ditions of the Creative Commons At- PIN-FORMED (PIN) proteins, auxin efflux carriers, ensure on-point and polar distribution tribution (CC BY) license (https:// of the phytohormone, whereby auxin signaling underpins the fine-tuning of various creativecommons.org/licenses/by/ cellular processes involved in plant growth adaptation under changing environmental 4.0/). Plants 2021, 10, 150. https://doi.org/10.3390/plants10010150 https://www.mdpi.com/journal/plants Plants 2021, 10, 150 2 of 16 Plants 2021, 10, 150 2 of 15 environmental conditions [3,16–18]. The role of the root-specific PIN family member PIN2 duringconditions root hair [3,16 growth–18]. The adapta roletion of the in root-specificresponse to PINenvironmental family member conditions PIN2 during will be root dis- hair cussedgrowth in particular adaptation in in the response scope of to environmentalthis review. The conditions establishment will be of discussed auxin gradients in particular is crucialin the for scope plant of growth this review. from Thethe establishmentfirst asymmetr ofic auxincell division gradients of isthe crucial zygote for [19,20] plant growthand tissuefrom organization the first asymmetric [21] through cell fine-tuning division of cell the zygoteproliferation [19,20 ]and and cell tissue elongation organization [10,22– [21] 25],through which in fine-tuning the end ensures cell proliferation that the shoot and will cell grow elongation above [the10,22 soil,–25 ],whereas which the in theroot end anchorsensures the thatplant the in the shoot soil will [1]. growShoot abovegrowth the is primarily soil, whereas oriented the roottowards anchors the light the plant(pos- in itivethe phototropic, soil [1]. Shoot negative growth gravitropic) is primarily to ensu orientedre the towards most efficient the light exposure (positive to the phototropic, sun to harvestnegative energy, gravitropic) which is converted to ensure theto sugar most an efficientd powers exposure plant growth to the [1,2,26]. sun to harvest In contrast, energy, thewhich root grows is converted along the to sugargravity and vector powers (positiv plante gravitropic, growth [1,2 ,negative26]. In contrast, phototropic) the root to growsan- choralong it in the soil, gravity where vector it absorbs (positive nutrients gravitropic, and water negative [2,3]. Auxin phototropic) biosynthesis to anchor correlates it in the withsoil, the where sugar itlevels absorbs produced nutrients depending and water on light [2,3]. quality Auxin and biosynthesis quantity perceived correlates by with the the leavessugar and levels transported produced to depending the roots on[1,27,28]. light quality The available and quantity auxin perceived orchestrates by the the leaves estab- and lishmenttransported of root to system the roots architecture [1,27,28]. The includin availableg, among auxin orchestratesothers, the length the establishment of the primary of root root,system the number architecture of lateral including, roots, among and the others, outgrowth the length of root of the hairs primary [3,10,28–30]. root, the Auxin number is of activelylateral transported roots, and towards the outgrowth the root of merist root hairsem, where [3,10,28 it –modulates30]. Auxin root is actively growth transported depend- ingtowards on the therequirements root meristem, in a wherebalance it modulatesbetween environmental root growth depending stimuli and on the available requirements re- sources,in a balance such as between carbohydrates, environmental minerals, stimuli and andwater available [2,31]. The resources, information such as about carbohydrates, the en- ergyminerals, status and and available water [2, 31resources]. The information of the plant about are sensed the energy by the status TARGET and available OF RAPAMY- resources CINof (TOR) the plant complex, are sensed which by then the activates TARGET cellular OF RAPAMYCIN responses upstream (TOR) complex, of root hair which out- then growthactivates [2] (Figure cellular 1). responses upstream of root hair outgrowth [2] (Figure1). FigureFigure 1. Energy 1. Energy status status and resource and resource uptake uptake are orches aretrated orchestrated by an interplay by an interplay of TARGET of TARGETOF RA- OF PAMYCINRAPAMYCIN (TOR) (TOR)and SNF1-RELATED and SNF1-RELATED KINASE KINASE 1 (SnRK1) 1 (SnRK1) complexes, complexes, which antagonistically which antagonistically modulate root and root hair growth. High energy status results from sugar synthesis derived from modulate root and root hair growth. High energy status results from sugar synthesis derived from photosynthesis in the leaves, which is followed by elevated auxin biosynthesis. Auxin signaling photosynthesis in the leaves, which is followed by elevated auxin biosynthesis. Auxin signaling enhances RHO-RELATED PROTEIN FROM PLANTS 2 (ROP2) activity, and ROP2 binds TOR and promotesenhances its phosphorylation. RHO-RELATED PROTEINThis results FROM in the PLANTS activation 2 (ROP2)of the TOR activity, complex, and ROP2which binds further TOR and consistspromotes of the its substrate-pr phosphorylation.esenting Thissubunit results REGULATORY in the activation-ASSOCIATED of the TOR PROTEIN complex, OF which TOR further (RAPTOR)consists and of the the substrate-presenting complex stabilizer LETHAL subunit REGULATORY-ASSOCIATED WITH SEC THIRTEEN 8 (LST8), PROTEIN described OF TORin Sec- (RAP- tionTOR) 2.1. TOR and thesignaling complex positively stabilizer correlates LETHAL with WITH root SEC meristem THIRTEEN activity 8 (LST8), and therefore described with in Sectionroot 2.1. length.TOR TOR signaling stabilizes
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