Manjul Singh

Glucose and Auxin Signaling Interaction in Controlling Arabidopsis thaliana Seedlings Root Growth and Development

Background Plant root growth and development is highly plastic and can adapt to many environmental conditions. Sugar signaling has been shown to affect root growth and development by interacting with phytohormones such as gibberellins, cytokinin and abscisic acid. Auxin signaling and transport has been earlier shown to be controlling plant root length, number of lateral roots, root hair and root growth direction. Principal Findings Increasing concentration of glucose not only controls root length, root hair and number of lateral roots but can also modulate root growth direction. Since root growth and development is also controlled by auxin, whole genome transcript profiling was done to find out the extent of interaction between glucose and auxin response pathways. Glucose alone could transcriptionally regulate 376 (62%) genes out of 604 genes affected by IAA. Presence of glucose could also modulate the extent of regulation 2 fold or more of almost 63% genes induced or repressed by IAA. Interestingly, glucose could affect induction or repression of IAA affected genes (35%) even if glucose alone had no significant effect on the transcription of these genes itself. Glucose could affect auxin biosynthetic YUCCA genes family members, auxin transporter PIN proteins, receptor TIR1 and members of a number of gene families including AUX/IAA, GH3 and SAUR involved in auxin signaling. Arabidopsis auxin receptor tir1 and response mutants, axr2, axr3 and slr1 not only display a defect in glucose induced change in root length, root hair elongation and lateral root production but also accentuate glucose induced increase in root growth randomization from vertical suggesting glucose effects on plant root growth and development are mediated by auxin signaling components. Conclusion Our findings implicate an important role of the glucose interacting with auxin signaling and transport machinery to control seedling root growth and development in changing nutrient conditions.

Interaction between Glucose and Brassinosteroid during the Regulation of Lateral Root Development in Arabidopsis

Glucose and brassinosteroid signals interact via auxin redistribution and signaling to regulate lateral root emergence during seedling growth and development. Glucose (Glc) plays a fundamental role in regulating lateral root (LR) development as well as LR emergence. In this study, we show that brassinosteroid (BR) signaling works downstream of Glc in controlling LR production/emergence in Arabidopsis (Arabidopsis thaliana) seedlings. Glc and BR can promote LR emergence at lower concentrations, while at higher concentrations, both have an inhibitory effect. The BR biosynthesis and perception mutants showed highly reduced numbers of emerged LRs at all the Glc concentrations tested. BR signaling works downstream of Glc signaling in regulating LR production, as in the glucose insensitive2-1brassinosteroid insensitive1 double mutant, Glc-induced LR production/emergence was severely reduced. Differential auxin distribution via the influx carriers AUXIN RESISTANT1/LIKE AUXIN RESISTANT1-3 and the efflux carrier PIN-FORMED2 plays a central role in controlling LR production in response to Glc and BR. Auxin signaling components AUXIN RESISTANT2,3 and SOLITARY ROOT act downstream of Glc and BR. AUXIN RESPONSE FACTOR7/19 work farther downstream and control LR production by regulating the expression of LATERAL ORGAN BOUNDARIES-DOMAIN29 and EXPANSIN17 genes. Increasing light flux could also mimic the Glc effect on LR production/emergence. However, increased light flux could not affect LR production in those BR and auxin signaling mutants that were defective for Glc-induced LR production. Altogether, our study suggests that, under natural environmental conditions, modulation of endogenous sugar levels can manipulate root architecture for optimized development by altering its nutrient/water uptake as well as its anchorage capacity.

Glucose control of root growth direction in Arabidopsis thaliana

Directional growth of roots is a complex process that is modulated by various environmental signals. This work shows that presence of glucose (Glc) in the medium also extensively modulated seedling root growth direction. Glc modulation of root growth direction was dramatically enhanced by simultaneous brassinosteroid (BR) application. Glc enhanced BR receptor BRASSINOSTEROID INSENSITIVE1 (BRI1) endocytosis from plasma membrane to early endosomes. Glc-induced root deviation was highly enhanced in a PP2A-defective mutant, roots curl in naphthyl phthalamic acid 1-1 (rcn1-1) suggesting that there is a role of phosphatase in Glc-induced root-growth deviation. RCN1, therefore, acted as a link between Glc and the BR-signalling pathway. Polar auxin transport worked further downstream to BR in controlling Glc-induced root deviation response. Glc also affected other root directional responses such as root waving and coiling leading to altered root architecture. High light intensity mimicked the Glc-induced changes in root architecture that were highly reduced in Glc-signalling mutants. Thus, under natural environmental conditions, changing light flux in the environment may lead to enhanced Glc production/response and is a way to manipulate root architecture for optimized development via integrating several extrinsic and intrinsic signalling cues.

Hypocotyl directional growth in Arabidopsis: a complex trait

The growth direction of the Arabidopsis (Arabidopsis thaliana) etiolated-seedling hypocotyl is a complex trait that is controlled by extrinsic signals such as gravity and touch as well as intrinsic signals such as hormones (brassinosteroid [BR], auxin, cytokinin, ethylene) and nutrient status (glucose [Glc], sucrose). We used a genetic approach to identify the signaling elements and their relationship underlying hypocotyl growth direction. BR randomizes etiolated-seedling growth by inhibiting negative gravitropism of the hypocotyls via modulating auxin homeostasis for which we designate as reset, not to be confused with the gravity set point angle. Cytokinin signaling antagonizes this BR reset of gravity sensing and/or tropism by affecting ethylene biosynthesis/signaling. Glc also antagonizes BR reset but acts independently of cytokinin and ethylene signaling pathways via inhibiting BR-regulated gene expression quantitatively and spatially, by altering protein degradation, and by antagonizing BR-induced changes in microtubule organization and cell patterning associated with hypocotyl agravitropism. This BR reset is reduced in the presence of the microtubule organization inhibitor oryzalin, suggesting a central role for cytoskeleton reorganization. A unifying and hierarchical model of Glc and hormone signaling interplay is proposed. The biological significance of BR-mediated changes in hypocotyl graviresponse lies in the fact that BR signaling sensitizes the dark-grown seedling hypocotyl to the presence of obstacles, overriding gravitropism, to enable efficient circumnavigation through soil.

Glucose and phytohormone interplay in controlling root directional growth in Arabidopsis

Sensing and responding toward gravity vector is a complicated and multistep process. Gravity is a constant factor feeding plants with reliable information for the spatial orientation of their organs. Auxin, cytokinin, ethylene and BRs have been the most explored hormones in relation to gravitropism. We have previously shown that glucose (Glc) could promote brassinosteroid (BR) signaling thereby inducing changes in root directional growth. Auxin signaling and polar transport components are also involved in Glc induced changes in root directional growth. Here, we provide evidence for involvement of cytokinin and ethylene signaling components in regulation of root directional growth downstream to Glc and BR. Altogether, Glc mediated change in root direction is an adaptive feature which is a result of a collaborative effort integrating phytohormonal signaling cues.

Multiple Interactions between Glucose and Brassinosteroid Signal Transduction Pathways in Arabidopsis Are Uncovered by Whole-Genome Transcriptional Profiling

Brassinosteroid and glucose signals interact extensively during the development of etiolated seedlings. Brassinosteroid (BR) and glucose (Glc) regulate many common responses in plants. Here, we demonstrate that under etiolated growth conditions, extensive interdependence/overlap occurs between BR- and Glc-regulated gene expression as well as physiological responses. Glc could regulate the transcript level of 72% of BR-regulated genes at the whole-genome level, of which 58% of genes were affected synergistically and 42% of genes were regulated antagonistically. Presence of Glc along with BR in medium could affect BR induction/repression of 85% of BR-regulated genes. Glc could also regulate several genes involved in BR metabolism and signaling. Both BR and Glc coregulate a large number of genes involved in abiotic/biotic stress responses and growth and development. Physiologically, Glc and BR interact to regulate hypocotyl elongation growth of etiolated Arabidopsis (Arabidopsis thaliana) seedlings in a dose-dependent manner. Glc may interact with BR via a HEXOKINASE1 (HXK1)-mediated pathway to regulate etiolated hypocotyl elongation. BRASSINOSTEROID INSENSITIVE1 (BRI1) is epistatic to HXK1, as the Glc insensitive2bri1-6 double mutant displayed severe defects in hypocotyl elongation growth similar to its bri1-6 parent. Analysis of Glc and BR sensitivity in mutants defective in auxin response/signaling further suggested that Glc and BR signals may converge at S-phase kinase-associated protein1-Cullin-F-box-TRANSPORT INHIBITOR RESPONSE1/AUXIN-RELATED F-BOX-AUXIN/INDOLE-3-ACETIC ACID-mediated auxin-signaling machinery to regulate etiolated hypocotyl elongation growth in Arabidopsis.

Striking the Right Chord: Signaling Enigma during Root Gravitropism

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.

Ethylene acts as a negative regulator of glucose induced lateral root emergence in Arabidopsis

Plants, being sessile organisms, are more exposed to the hazards of constantly changing environmental conditions globally. During the lifetime of a plant, the root system encounters various challenges such as obstacles, pathogens, high salinity, water logging, nutrient scarcity etc. The developmental plasticity of the root system provides brilliant adaptability to plants to counter the changes exerted by both external as well as internal cues and achieve an optimized growth status. Phytohormones are one of the major intrinsic factors regulating all aspects of plant growth and development both independently as well as through complex signal integrations at multiple levels. We have previously shown that glucose (Glc) and brassinosteroid (BR) signalings interact extensively to regulate lateral root (LR) development in Arabidopsis.1 Auxin efflux as well as influx and downstream signaling components are also involved in Glc-BR regulation of LR emergence. Here, we provide evidence for involvement of ethylene signaling machinery downstream to Glc and BR in regulation of LR emergence.

Arabidopsis RSS1 Mediates Cross-Talk Between Glucose and Light Signaling During Hypocotyl Elongation Growth

Plants possess exuberant plasticity that facilitates its ability to adapt and survive under challenging environmental conditions. The developmental plasticity largely depends upon cellular elongation which is governed by a complex network of environmental and phytohormonal signals. Here, we report role of glucose (Glc) and Glc-regulated factors in controlling elongation growth and shade response in Arabidopsis. Glc controls shade induced hypocotyl elongation in a dose dependent manner. We have identified a Glc repressed factor REGULATED BY SUGAR AND SHADE1 (RSS1) encoding for an atypical basic helix-loop-helix (bHLH) protein of unknown biological function that is required for normal Glc actions. Phenotype analysis of mutant and overexpression lines suggested RSS1 to be a negative regulator of elongation growth. RSS1 affects overall auxin homeostasis. RSS1 interacts with the elongation growth-promoting proteins HOMOLOG OF BEE2 INTERACTING WITH IBH 1 (HBI1) and BR ENHANCED EXPRESSION2 (BEE2) and negatively affects the transcription of their downstream targets such as YUCs, INDOLE-3-ACETIC ACID INDUCIBLE (IAAs), LONG HYPOCOTYL IN FAR-RED1 (HFR1), HOMEOBOX PROTEIN 2 (ATHB2), XYLOGLUCAN ENDOTRANSGLUCOSYLASE/HYDROLASES (XTHs) and EXPANSINS. We propose, Glc signals might maintain optimal hypocotyl elongation under multiple signals such as light, shade and phytohormones through the central growth regulatory bHLH/HLH module.

Role of glucose in spatial distribution of auxin regulated genes

Plants have the ability to adjust its physiology and metabolism to the changes of nutrient availability in the environment. Since a number of common responses are regulated by sugar and auxin, the obvious question arises is whether sugar and auxin act interdependently to bring about changes in plant morphology. In the February issue of the PloS ONE,1 we presented detailed investigation of glucose and auxin signaling interaction in controlling root growth and development in Arabidopsis thaliana seedlings. Further analysis of tissue specific regulation of glucose auxin signaling interaction may provide some insight as to how these two signaling molecules interact to control the morphogenic changes during seedling development.