Regulation Of Lateral Root Development Research Articles

Trichoderma-secreted anthranilic acid promotes lateral root development via auxin signaling and RBOHF-induced endodermal cell wall remodeling

Trichoderma spp. have evolved the capacity to communicate with plants by producing various secondary metabolites (SMs). Nonhormonal SMs play important roles in plant root development, while specific SMs from rhizosphere microbes and their underlying mechanisms to control plant root branching are still largely unknown. In this study, a compound, anthranilic acid (2-AA), is identified from T.guizhouense NJAU4742 to promote lateral root development. Further studies demonstrate that 2-AA positively regulates auxin signaling and transport in the canonical auxin pathway. 2-AA also partly rescues the lateral root numbers of CASP1pro:shy2-2, which regulates endodermal cell wall remodeling via an RBOHF-induced reactive oxygen species burst. In addition, our work reports another role for microbial 2-AA in the regulation of lateral root development, which is different from its better-known role in plant indole-3-acetic acid biosynthesis. In summary, this study identifies 2-AA from T.guizhouense NJAU4742, which plays versatile roles in regulating plant root development.

Comparative transcriptome analysis reveals the regulatory effects of exogenous auxin on lateral root development and tanshinone accumulation in Salvia miltiorrhiza.

The physiological and transcriptome analysis revealed that auxin was a positive regulator of lateral root development and tanshinone accumulation in Salvia miltiorrhiza. Roots of S. miltiorrhiza are widely used as medicinal materials in China, and the root morphology and content of bioactive compounds [such as phenolic acids and diterpenoid quinones (tanshinones)] are the main factors to determine the quality of this herb. Auxin regulates root development and secondary metabolism in many plant species, but little is known about its function in S. miltiorrhiza. In this study, S. miltiorrhiza seedlings were treated (exogenous application) with the auxin indole-3-acetic acid (IAA) and the polar auxin transport inhibitor N-1-naphthylphthalamic acid (NPA) to investigate the regulatory roles of auxin in S. miltiorrhiza. The results indicated that exogenous IAA promoted both lateral root development and tanshinones biosynthesis in S. miltiorrhiza. The NPA application suppressed the lateral root development but showed no obvious effects on tanshinones accumulation. Based on the RNA-seq analysis, expressions of genes related to auxin biosynthesis and signaling transduction were altered in both treated groups. Coincidental with the enhanced content of tanshinones, transcripts of several key enzyme genes in the tanshinones biosynthetic pathway were stimulated after the exogenous IAA application. The expression profiles of seven common transcription factor domain-containing gene families were analyzed, and the results implied that some AP2/ERF genes were probably responsible for the auxin-induced lateral root development in S. miltiorrhiza. These findings shed new light on the regulatory roles of auxin on root development and bioactive compounds biosynthesis in S. miltiorrhiza, and lay the groundwork for future research into the detailed molecular mechanism underlying these biological functions.

Composite plants of cucumber and buckwheat as a tool to study auxin distribution and transport in the root system

Genetic transformation of most dicotyledonous plants by Rhizobium rhizogenes (also known as Agrobacterium rhizogenes) results in production of composite plants plants consisting of wild-type shoot and transgenic root system. Composite plants are the suitable model for investigation of hormonal mechanisms related to development of the root system as regulatory links between the root system and the shoot maintains in such plants.
 In most plants initiation of lateral root primordia occurs above the elongation zone [1]. However, in cucurbits and some other species, including important cereal crop buckwheat (Fagopyrum esculentum Moench), lateral root primordia initiation and development occurs in the apical meristem of the parental root [2, 3].
 The phytohormone auxin is a key regulator of lateral root development. Fusions of auxin-responsive promoters and reporter genes can be used to study the role of auxin in the development of root system of non-model plants such as cucumber (Cucumis sativus L.) and buckwheat [4].
 The agrobacterium mediated transformation technique of cucurbits [5] has been adapted for buckwheat. R. rhizogenes strain R1000 was used in all transformations. Set of binary vectors based on pKGW-RR-MGW or pKGW-MGW was developed to study auxin response maxima (DR5::mNeonGreen) or auxin transport (fusions of genes encoding auxin efflux proteins PIN and mNeonGreen).
 Pattern of auxin response maxima was similar in both species and included quiescent center and initial cells, columella, xylem cell files and lateral root primordia on all stages of development. Members of CsPIN1 (CsPINb and CsSoPIN1) group contributed unequally in generation of auxin maximum required for lateral root primordium initiation.
 The research was supported by the RFBR grant 20-016-00233-a.

Theanine, a tea-plant-specific non-proteinogenic amino acid, is involved in the regulation of lateral root development in response to nitrogen status.

Glutamine synthetase type I (GSI)-like proteins are proposed to mediate nitrogen signaling and developmental fate by synthesizing yet unidentified metabolites. Theanine, the most abundant non-proteinogenic amino acid in tea plants, is the first identified metabolite synthesized by a GSI-like protein (CsTSI) in a living system. However, the roles of theanine in nitrogen signaling and development are little understood. In this study we found that nitrogen deficiency significantly reduced theanine accumulation and increased lateral root development in tea plant seedlings. Exogenous theanine feeding significantly repressed lateral root development of seedlings of tea plants and the model plant Arabidopsis. The transcriptomic analysis revealed that the differentially expressed genes in the roots under theanine feeding were enriched in the apoplastic pathway and H2O2 metabolism. Consistently, theanine feeding reduced H2O2 levels in the roots. Importantly, when co-treated with H2O2, theanine abolished the promoting effect of H2O2 on lateral root development in both tea plant and Arabidopsis seedlings. The results of histochemical assays confirmed that theanine inhibited reactive oxygen species accumulation in the roots. Further transcriptomic analyses suggested the expression of genes encoding enzymes involved in H2O2 generation and scavenging was down- and upregulated by theanine, respectively. Moreover, the expression of genes involved in auxin metabolism and signaling, cell division, and cell expansion was also regulated by theanine. Collectively, these results suggested that CsTSI-synthesized theanine is likely involved in the regulation of lateral root development, via modulating H2O2 accumulation, in response to nitrogen levels in tea plants. This study also implied that the module consisting of GSI-like protein and theanine-like metabolite is probably conserved in regulating development in response to nitrogen status in plant species.

Lateral root formation and nutrients: nitrogen in the spotlight.

Lateral roots are important to forage for nutrients due to their ability to increase the uptake area of a root system. Hence, it comes as no surprise that lateral root formation is affected by nutrients or nutrient starvation, and as such contributes to the root system plasticity. Understanding the molecular mechanisms regulating root adaptation dynamics toward nutrient availability is useful to optimize plant nutrient use efficiency. There is at present a profound, though still evolving, knowledge on lateral root pathways. Here, we aimed to review the intersection with nutrient signaling pathways to give an update on the regulation of lateral root development by nutrients, with a particular focus on nitrogen. Remarkably, it is for most nutrients not clear how lateral root formation is controlled. Only for nitrogen, one of the most dominant nutrients in the control of lateral root formation, the crosstalk with multiple key signals determining lateral root development is clearly shown. In this update, we first present a general overview of the current knowledge of how nutrients affect lateral root formation, followed by a deeper discussion on how nitrogen signaling pathways act on different lateral root-mediating mechanisms for which multiple recent studies yield insights.

Gibberellins regulate lateral root development that is associated with auxin and cell wall metabolisms in cucumber

Cucumber is an economically important crop cultivated worldwide. Gibberellins (GAs) play important roles in the development of lateral roots (LRs), which are critical for plant stress tolerance and productivity. Therefore, it is of great importance for cucumber production to study the role of GAs in LR development. Here, the results showed that GAs regulated cucumber LR development in a concentration-dependent manner. Treatment with 1, 10, 50 and 100 μM GA3 significantly increased secondary root length, tertiary root number and length. Of these, 50 μM GA3 treatment had strong effects on increasing root dry weight and the root/shoot dry weight ratio. Pairwise comparisons identified 417 down-regulated genes enriched for GA metabolism-related processes and 447 up-regulated genes enriched for cell wall metabolism-related processes in GA3-treated roots. A total of 3523 non-redundant DEGs were identified in our RNA-Seq data through pairwise comparisons and linear factorial modeling. Of these, most of the genes involved in auxin and cell wall metabolisms were up-regulated in GA3-treated roots. Our findings not only shed light on LR regulation mediated by GA but also offer an important resource for functional studies of candidate genes putatively involved in the regulation of LR development in cucumber and other crops.

Lateral Root Initiation and the Analysis of Gene Function Using Genome Editing with CRISPR in Arabidopsis

Lateral root initiation is a post-embryonic process that requires the specification of a subset of pericycle cells adjacent to the xylem pole in the primary root into lateral root founder cells. The first visible event of lateral root initiation in Arabidopsis is the simultaneous migration of nuclei in neighbouring founder cells. Coinciding cell cycle activation is essential for founder cells in the pericycle to undergo formative divisions, resulting in the development of a lateral root primordium (LRP). The plant signalling molecule, auxin, is a major regulator of lateral root development; the understanding of the molecular mechanisms controlling lateral root initiation has progressed tremendously by the use of the Arabidopsis model and a continual improvement of molecular methodologies. Here, we provide an overview of the visible events, cell cycle regulators, and auxin signalling cascades related to the initiation of a new LRP. Furthermore, we highlight the potential of genome editing technology to analyse gene function in lateral root initiation, which provides an excellent model to answer fundamental developmental questions such as coordinated cell division, growth axis establishment as well as the specification of cell fate and cell polarity.

Regulation of Lateral Root Development by Shoot-Sensed Far-Red Light via HY5 Is Nitrate-Dependent and Involves the NRT2.1 Nitrate Transporter.

Plants are very effective in responding to environmental changes during competition for light and nutrients. Low Red:Far-Red (low R:FR)-mediated neighbor detection allows plants to compete successfully with other plants for available light. This above-ground signal can also reduce lateral root growth by inhibiting lateral root emergence, a process that might help the plant invest resources in shoot growth. Nitrate is an essential nutrient for plant growth and Arabidopsis thaliana responds to low nitrate conditions by enhancing nutrient uptake and reducing lateral and main root growth. There are indications that low R:FR signaling and low nitrate signaling can affect each other. It is unknown which response is prioritized when low R:FR light- and low nitrate signaling co-occur. We investigated the effect of low nitrate conditions on the low R:FR response of the A. thaliana root system in agar plate media, combined with the application of supplemental Far-Red (FR) light to the shoot. We observed that under low nitrate conditions main and lateral root growth was reduced, but more importantly, that the response of the root system to low R:FR was not present. Consistently, a loss-of-function mutant of a nitrate transporter gene NRT2.1 lacked low R:FR-induced lateral root reduction and its root growth was hypersensitive to low nitrate. ELONGATED HYPOCOTYL5 (HY5) plays an important role in the root response to low R:FR and we found that it was less sensitive to low nitrate conditions with regards to lateral root growth. In addition, we found that low R:FR increases NRT2.1 expression and that low nitrate enhances HY5 expression. HY5 also affects NRT2.1 expression, however, it depended on the presence of ammonium in which direction this effect was. Replacing part of the nitrogen source with ammonium also removed the effect of low R:FR on the root system, showing that changes in nitrogen sources can be crucial for root plasticity. Together our results show that nitrate signaling can repress low R:FR responses and that this involves signaling via HY5 and NRT2.1.

Melatonin-ROS signal module regulates plant lateral root development

ABSTRACT Lateral root (LR) branches from primary root. LR is vital for plants acquiring water and nutrients from soil, especially under stress conditions. LR development involves the complicated signaling network, which has not yet been fully understood. Melatonin, a novel endogenous plant regulator, plays a role in the regulation of LR development. However, we still have limited knowledge about melatonin-modulated signaling during LR development. Our recent study identifies that reactive oxygen species (ROS) acts as downstream signaling of melatonin to facilitate LR development. The recently identified receptor of melatonin in plants controls a signaling module involving G protein, ROS, and Ca2+. Based on these findings, we propose a novel signaling network for LR development controlled by melatonin.

Novel Regulators of Sugar-Mediated Lateral Root Development in Arabidopsis thaliana.

Lateral root development is a complex process regulated by numerous factors. An important role for sugar in lateral root development has been known for a while, but the underlying molecular basis still remains unclear. In this study, we first showed that WOX7, a sugar-inducible negative regulator of lateral root development, acts downstream of the glucose sensor HXK1. Using a transgenic line homozygous for a transgene expressing GFP under the control of the WOX7 promoter, we next performed a genetic screen to identify additional genes in this development pathway. A number of mutants with altered level of WOX7 expression were recovered, and two with increased WOX7 expression, named ewe-1 and ewe-2 (for Enhanced WOX7 Expression), were further characterized. Both mutants manifest delayed lateral root development, and genetic analysis indicates that single recessive mutations are responsible for the observed phenotypes. The mutations were then located to similar regions on chromosome 2 by marker-assisted analyses, and candidate genes were identified through whole genome sequencing. The significance and limitations of this work are discussed.

A Co-opted Regulator of Lateral Root Development Controls Nodule Organogenesis in Lotus.

Legumes, a subset of flowering plants, form root nodules in symbiosis with nitrogen-fixing bacteria. The regulatory network controlling nodule formation has remained mysterious. In a recent issue of Science, Soyano etal. (2019) demonstrate that co-option of an existing lateral root developmental program is used in Lotus for nodule organogenesis.

A new tool for discovering transcriptional regulators of co-expressed genes predicts gene regulatory networks that mediate ethylene-controlled root development

Abstract Gene regulatory networks (GRNs) are defined by a cascade of transcriptional events by which signals, such as hormones or environmental cues, change development. To understand these networks, it is necessary to link specific transcription factors (TFs) to the downstream gene targets whose expression they regulate. Although multiple methods provide information on the targets of a single TF, moving from groups of co-expressed genes to the TF that controls them is more difficult. To facilitate this bottom-up approach, we have developed a web application named TF DEACoN. This application uses a publicly available Arabidopsis thaliana DNA Affinity Purification (DAP-Seq) data set to search for TFs that show enriched binding to groups of co-regulated genes. We used TF DEACoN to examine groups of transcripts regulated by treatment with the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC), using a transcriptional data set performed with high temporal resolution. We demonstrate the utility of this application when co-regulated genes are divided by timing of response or cell-type-specific information, which provides more information on TF/target relationships than when less defined and larger groups of co-regulated genes are used. This approach predicted TFs that may participate in ethylene-modulated root development including the TF NAM (NO APICAL MERISTEM). We used a genetic approach to show that a mutation in NAM reduces the negative regulation of lateral root development by ACC. The combination of filtering and TF DEACoN used here can be applied to any group of co-regulated genes to predict GRNs that control coordinated transcriptional responses.

The Control of Zealactone Biosynthesis and Exudation is Involved in the Response to Nitrogen in Maize Root.

Nitrate acts as a signal in regulating plant development in response to environment. In particular nitric oxide, auxin and strigolactones (SLs) were supposed to cooperate to regulate the maize root response to this anion. In this study, a combined approach based on liquid chromatography-quadrupole/time-of-flight tandem mass spectrometry and on physiological and molecular analyses was adopted to specify the involvement of SLs in the maize response to N. Our results showed that N deficiency strongly induces SL exudation, likely through stimulating their biosynthesis. Nitrate provision early counteracts and also ammonium lowers SL exudation, but less markedly. Exudates obtained from N-starved and ammonium-provided seedlings stimulated Phelipanche germination, whereas when seeds were treated with exudates harvested from nitrate-provided plants no germination was observed. Furthermore, our findings support the idea that the inhibition of SL production observed in response to nitrate and ammonium would contribute to the regulation of lateral root development. Moreover, the transcriptional regulation of a gene encoding a putative maize WBC transporter, in response to various nitrogen supplies, together with its mRNA tissue localization, supported its role in SL allocation. Our results highlight the dual role of SLs as molecules able to signal outwards a nutritional need and as endogenous regulators of root architecture adjustments to N, thus synchronizing plant growth with nitrogen acquisition.

Sequence and functional characterization of MIRNA164 promoters from Brassica shows copy number dependent regulatory diversification among homeologs.

The impact of polyploidy on functional diversification of cis-regulatory elements is poorly understood. This is primarily on account of lack of well-defined structure of cis-elements and a universal regulatory code. To the best of our knowledge, this is the first report on characterization of sequence and functional diversification of paralogous and homeologous promoter elements associated with MIR164 from Brassica. The availability of whole genome sequence allowed us to identify and isolate a total of 42 homologous copies of MIR164 from diploid species-Brassica rapa (A-genome), Brassica nigra (B-genome), Brassica oleracea (C-genome), and allopolyploids-Brassica juncea (AB-genome), Brassica carinata (BC-genome) and Brassica napus (AC-genome). Additionally, we retrieved homologous sequences based on comparative genomics from Arabidopsis lyrata, Capsella rubella, and Thellungiella halophila, spanning ca. 45 million years of evolutionary history of Brassicaceae. Sequence comparison across Brassicaceae revealed lineage-, karyotype, species-, and sub-genome specific changes providing a snapshot of evolutionary dynamics of miRNA promoters in polyploids. Tree topology of cis-elements associated with MIR164 was found to re-capitulate the species and family evolutionary history. Phylogenetic shadowing identified transcription factor binding sites (TFBS) conserved across Brassicaceae, of which, some are already known as regulators of MIR164 expression. Some of the TFBS were found to be distributed in a sub-genome specific (e.g., SOX specific to promoter of MIR164c from MF2 sub-genome), lineage-specific (YABBY binding motif, specific to C. rubella in MIR164b), or species-specific (e.g., VOZ in A. thaliana MIR164a) manner which might contribute towards genetic and adaptive variation. Reporter activity driven by promoters associated with MIR164 paralogs and homeologs was majorly in agreement with known role of miR164 in leaf shaping, regulation of lateral root development and senescence, and one previously un-described novel role in trichome. The impact of polyploidy was most profound when reporter activity across three MIR164c homeologs were compared that revealed negligible overlap, whereas reporter activity among two homeologs of MIR164a displays significant overlap. A copy number dependent cis-regulatory divergence thus exists in MIR164 genes in Brassica juncea. The full extent of regulatory diversification towards adaptive strategies will only be known when future endeavors analyze the promoter function under duress of stress and hormonal regimes.

Chrysanthemum MADS-box transcription factor CmANR1 modulates lateral root development via homo-/heterodimerization to influence auxin accumulation in Arabidopsis

Root system architecture is an important agronomic trait by which plants both acquire water and nutrients from the soil and adapt to survive in a complex environment. The adaptation of plant root systems to environmental constraints largely depends on the growth and development of lateral roots (LRs). MADS-box transcription factors (TFs) are important known regulators of plant growth, development, and response to environmental stimuli. However, the potential mechanisms by which they regulate LRs development remain poorly understood. Here, we identified a MADS-box chrysanthemum gene CmANR1, homologous to the Arabidopsis gene AtANR1, which plays a key role in the regulation of LR development. qRT-PCR assays indicated that CmANR1 was primarily expressed in chrysanthemum roots and was rapidly induced by exposure to high nitrate concentrations. Ectopic expression of CmANR1 in Arabidopsis significantly increased the number and length of emerged LRs compared to the wild-type (col) control, but had no obvious affect on primary root (PR) development. We also found that CmANR1 positively influenced auxin accumulation in LRs at least partly by improving auxin biosynthesis and transport, thereby promoting LR development. Furthermore, we found that ANR1 formed homo- and heterodimers through interactions with itself and AGL21 at its C-terminal domain. Overall, our findings provide considerable new information about the mechanisms by which the chrysanthemum MADS-box TF CmANR1 mediates LR development by directly altering auxin accumulation.

Changes in Gene Expression in Space and Time Orchestrate Environmentally Mediated Shaping of Root Architecture.

Shaping of root architecture is a quintessential developmental response that involves the concerted action of many different cell types, is highly dynamic, and underpins root plasticity. To determine to what extent the environmental regulation of lateral root development is a product of cell-type preferential activities, we tracked transcriptomic responses to two different treatments that both change root development in Arabidopsis thaliana at an unprecedented level of temporal detail. We found that individual transcripts are expressed with a very high degree of temporal and spatial specificity, yet biological processes are commonly regulated, in a mechanism we term response nonredundancy. Using causative gene network inference to compare the genes regulated in different cell types and during responses to nitrogen and a biotic interaction, we found that common transcriptional modules often regulate the same gene families but control different individual members of these families, specific to response and cell type. This reinforces that the activity of a gene cannot be defined simply as molecular function; rather, it is a consequence of spatial location, expression timing, and environmental responsiveness.

Nitrate: A Crucial Signal during Lateral Roots Development.

Root plasticity is an important trait for plants to forage nutrient and adapt to survival in a complicated environment. Lateral roots (LRs) are generally more sensitive than primary roots in response to changing environmental conditions. As the main source of nitrogen for most higher plants, nitrate acting as a signal has received great attention in the regulation of LR development. In general, there are dual effects including stimulatory and inhibitory of low nitrate on LR development; while high nitrate supply has an inhibitory effect on LR development; nitrate heterogeneity also has a stimulatory effect on LR development in - rich zone. Here, we focus on recent progresses in the role of a nitrate signal in the regulation of the LRs development.

CLE peptide signaling and nitrogen interactions in plant root development.

The CLAVATA signaling pathway is essential for the regulation of meristem activities in plants. This signaling pathway consists of small signaling peptides of the CLE family interacting with CLAVATA1 and leucine-rich repeat receptor-like kinases (LRR-RLKs). The peptide-receptor relationships determine the specificities of CLE-dependent signals controlling stem cell fate and differentiation that are critical for the establishment and maintenance of shoot and root apical meristems. Plants root systems are highly organized into three-dimensional structures for successful anchoring and uptake of water and mineral nutrients from the soil environment. Recent studies have provided evidence that CLE peptides and CLAVATA signaling pathways play pivotal roles in the regulation of lateral root development and systemic autoregulation of nodulation (AON) integrated with nitrogen (N) signaling mechanisms. Integrations of CLE and N signaling pathways through shoot-root vascular connections suggest that N demand modulates morphological control mechanisms and optimize N uptake as well as symbiotic N fixation in roots.

Interaction between glucose and brassinosteroid during the regulation of lateral root development in Arabidopsis.

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.

A proposed role for selective autophagy in regulating auxin-dependent lateral root development under phosphate starvation in Arabidopsis

Plants respond to limited soil nutrient availability by inducing more lateral roots (LR) to increase the root surface area. At the cellular level, nutrient starvation triggers the process of autophagy through which bulk degradation of cellular materials is achieved to facilitate nutrient mobilization. Whether there is any link between the cellular autophagy and induction of LR had remained unknown. We recently showed that the S-Domain receptor Kinase (ARK2) and U Box/Armadillo Repeat-Containing E3 ligase (PUB9) module is required for lateral root formation under phosphate starvation in Arabidopsis thaliana.1 We also showed that PUB9 localized to autophagic bodies following either activation by ARK2 or under phosphate starvation and ark2–1/pub9–1 plants displayed lateral root defects with inability to accumulate auxin in the root tips under phosphate starvation.1 Supplementing exogenous auxin was sufficient to rescue the LR defects in ark2–1/pub9–1 mutant. Blocking of autophagic responses in wild-type Arabidopsis also resulted in inhibition of both lateral roots and auxin accumulation in the root tips indicating the importance of autophagy in mediating auxin accumulation under phosphate starved conditions.1 Here, we propose a model for ARK2/AtPUB9 module in regulation of lateral root development via selective autophagy.