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Resolving Rapid Radiations Within Families Using Anchored Phylogenomics

Despite the promise that molecular data would provide a seemingly unlimited source of independent characters, many plant phylogenetic studies are based on only two regions, the plastid genome and nuclear ribosomal DNA (nrDNA). Their popularity can be explained by high copy numbers and universal PCR primers that make their sequences easily amplified and converted into parallel datasets. Unfortunately, their utility is limited by linked loci and limited characters resulting in low confidence in the accuracy of phylogenetic estimates, especially when rapid radiations occur. In another contribution on anchored phylogenomics in angiosperms, we presented flowering plant-specific anchored enrichment probes for hundreds of conserved nuclear genes and demonstrated their use at the level of all angiosperms. In this contribution, we focus on a common problem in phylogenetic reconstructions below the family level: weak or unresolved backbone due to rapid radiations ([≤] 10 million years) followed by long divergence, using the Cariceae-Dulichieae-Scirpeae clade (CDS, Cyperaceae) as a test case. By comparing our nuclear matrix of 461 genes to a typical Sanger-sequence dataset consisting of a few plastid genes (matK, ndhF) and an nrDNA marker (ETS), we demonstrate that our nuclear data is fully compatible with the Sanger dataset and resolves short backbone internodes with high support in both concatenated and coalescence-based analyses. In addition, we show that nuclear gene tree incongruence is inversely proportional to phylogenetic information content, indicating that incongruence is mostly due to gene tree estimation error. This suggests that large numbers of conserved nuclear loci could produce more accurate trees than sampling rapidly evolving regions prone to saturation and long-branch attraction. The robust phylogenetic estimates obtained here, and high congruence with previous morphological and molecular analyses, are strong evidence for a complete tribal revision of CDS. The anchored hybrid enrichment probes used in this study should be similarly effective in other flowering plant groups. [Carex, coalescent based species tree, flowering plants, low-copy nuclear genes, low-level phylogenetics, universal hybrid enrichment probes]

plant biology

Boron Hyperaccumulation Mechanisms in Puccinellia distans as Revealed by Transcriptomic Analysis

Boron is an essential plant micronutrient; but is toxic at high concentrations. Boron toxicity can severely affect crop productivity in arid and semi-arid environments. Puccinellia distans (Jacq.) Par1., common alkali grass, is found throughout the world and can survive under boron concentrations that are lethal for other plant species. In addition, P. distans can accumulate very high levels of this element. Despite these interesting features, very little research has been performed to elucidate the boron tolerance mechanism in this species. In this study, P. distans samples were analyzed by RNA sequencing to identify genes related to boron tolerance and hyperaccumulation. Abundance levels of selected differentially expressed transcripts were validated by real-time PCR. The results indicated that the hyperaccumulation mechanism of P. distans involves many transcriptomic changes including those that lead to: alterations in the malate pathway, changes in cell wall components that allow sequestration of excess boron without toxic effects, and increased expression of at least one putative boron transporter and two putative aquaporins. Elucidation of the boron accumulation mechanism is important to develop approaches for bioremediation of boron contaminated soils.

plant biology

The Sorghum bicolor reference genome: improved assembly and annotations, a transcriptome atlas, and signatures of genome organization

2Sorghum bicolor is a drought tolerant C4 grass used for production of grain, forage, sugar, and lignocellulosic biomass and a genetic model for C4 grasses due to its relatively small genome (~800 Mbp), diploid genetics, diverse germplasm, and colinearity with other C4 grass genomes. In this study, deep sequencing, genetic linkage analysis, and transcriptome data were used to produce and annotate a high quality reference genome sequence. Reference genome sequence order was improved, 29.6 Mbp of additional sequence was incorporated, the number of genes annotated increased 24% to 34,211, average gene length and N50 increased, and error frequency was reduced 10-fold to 1 per 100 kbp. Sub-telomeric repeats with characteristics of Tandem Repeats In Miniature (TRIM) elements were identified at the termini of most chromosomes. Nucleosome occupancy predictions identified nucleosomes positioned immediately downstream of transcription start sites and at different densities across chromosomes. Alignment of the reference genome sequence to 56 resequenced genomes from diverse sorghum genotypes identified ~7.4M SNPs and 1.8M indels. Large scale variant features in euchromatin were identified with periodicities of ~25 kbp. An RNA transcriptome atlas of gene expression was constructed from 47 samples derived from growing and developed tissues of the major plant organs (roots, leaves, stems, panicles, seed) collected during the juvenile, vegetative and reproductive phases. Analysis of the transcriptome data indicated that tissue type and protein kinase expression had large influences on transcriptional profile clustering. The updated assembly, annotation, and transcriptome data represent a resource for C4 grass research and crop improvement.

plant biology

Genetic Architecture and Molecular Networks Underlying Leaf Thickness in Desert-Adapted Tomato Solanum pennellii

Thicker leaves allow plants to grow in water-limited conditions. However, our understanding of the genetic underpinnings of this highly functional leaf shape trait is poor. We used a custom-built confocal profilometer to directly measure leaf thickness in a set of introgression lines (ILs) derived from the desert tomato species Solanum pennellii, and identified quantitative trait loci (QTL). We report evidence of a complex genetic architecture of this trait and roles for both genetic and environmental factors. Several ILs with thick leaves have dramatically elongated palisade mesophyll cells and, in some cases, increased leaf ploidy. We characterized thick ILs 2-5 and 4-3 in detail and found increased mesophyll cell size and leaf ploidy levels, suggesting that endoreduplication underpins leaf thickness in tomato. Next, we queried the transcriptomes and inferred Dynamic Bayesian Networks of gene expression across early leaf ontogeny in these lines to compare the molecular networks that pattern leaf thickness. We show that thick ILs share S. pennellii-like expression profiles for putative regulators of cell shape and meristem determinacy, as well as a general signature of cell cycle related gene expression. However, our network data suggest that leaf thickness in these two lines is patterned by at least partially distinct mechanisms. Consistent with this hypothesis, double homozygote lines combining introgression segments from these two ILs show additive phenotypes including thick leaves, higher ploidy levels and larger palisade mesophyll cells. Collectively, these data establish a framework of genetic, anatomical, and molecular mechanisms that pattern leaf thickness in desert-adapted tomato.

plant biology

The Sequence of 1504 Mutants in the Model Rice Variety Kitaake Facilitates Rapid Functional Genomic Studies

The availability of a whole-genome sequenced mutant population and the cataloging of mutations of each line at a single-nucleotide resolution facilitates functional genomic analysis. To this end, we generated and sequenced a fast-neutron-induced mutant population in the model rice cultivar Kitaake (Oryza sativa L. ssp. japonica), which completes its life cycle in 9 weeks. We sequenced 1,504 mutant lines at 45-fold coverage and identified 91,513 mutations affecting 32,307 genes, 58% of all rice genes. We detected an average of 61 mutations per line. Mutation types include single base substitutions, deletions, insertions, inversions, translocations, and tandem duplications. We observed a high proportion of loss-of-function mutations. Using this mutant population, we identified an inversion affecting a single gene as the causative mutation for the short-grain phenotype in one mutant line with a small segregating population. This result reveals the usefulness of the resource for efficient identification of genes conferring specific phenotypes. To facilitate public access to this genetic resource, we established an open access database called KitBase that provides access to sequence data and seed stocks, enabling rapid functional genomic studies of rice.\n\nOne-sentence summaryWe have sequenced 1,504 mutant lines generated in the short life cycle rice variety Kitaake (9 weeks) and established a publicly available database, enabling rapid functional genomic studies of rice.

plant biology

α-tubulin acetylation and detyrosination correlate with starvation-induced autophagy in tobacco cells

Recent data has enabled discovery of novel functions of microtubules (MTs) in the regulation of autophagy development under physiologic/stressful conditions in yeast and animal cells. MTs participate in maturation and traffic of autophagosomes through their dynamic state changes and post-translational modifications of tubulin, including acetylation. We demonstrated the involvement of tobacco cell MTs in the development of starvation-induced autophagy via tubulin acetylation and denitrotyrosination. Induced metabolic stress caused by prolonged cultivation of BY-2 suspension cells results in glucose depletion in the culture medium and following increased rates of protein hydrolysis and autophagy. Development of autophagy was strongly accompanied by -tubulin acetylation and detyrosination. Both post-translational modifications were caused by changes in the molecular microenvironment of the tobacco cell MTs that was revealed via Co-IP assay. The termination of autophagy led to the development of programmed cell death that was characterised by nucleosomal DNA fragmentation and decreases in -tubulin acetylation and detyrosination. Our data suggest the role of the functional state of MTs in the mediation of plant autophagy via changes in the tubulin microenvironment and in its post-translational modifications.\n\nSUMMARY STATEMENTThe main findings cover a possible impact of plant microtubular cytoskeleton to starvation-induced autophagy development. It can be realized by means of tubulin post-translational modifications, acetylation in the first place.

plant biology

The emerging British Verticillium longisporum population consists of aggressive Brassica pathogens

The impact of diseases depends on the dynamic interplay between host, pathogen and the environment. Newly emerging diseases may be the consequence of novel pathogen introductions that are typically associated with unpredictable outcomes, as their interaction with the host in a novel environment is unprecedented. Alternatively, new diseases may emerge from latent, previously established, pathogen populations that are triggered by changes in environmental factors like weather, agricultural practices and ecosystem management. Verticillium stem striping recently emerged in British oilseed rape (Brassica napus) production from a latent Verticillium longisporum population. V. longisporum is a hybrid fungal pathogen consisting of three lineages, each representing a separate hybridization event. Despite its prevalence, little is known of the pathogenicity of the British V. longisporum population. In this study, the pathogenicity of British isolates was tested on four different cultivars of three different Brassica crop species as well as on the model plant Arabidopsis thaliana and compared with previously characterized V. longisporum strains from other regions of the world, including representatives of all three hybrid lineages. Intriguingly, the British isolates appeared to be amongst the most pathogenic strains on Brassica crops. In conclusion, Verticillium stem striping poses a genuine threat to oilseed rape production as the British V. longisporum population consists of aggressive pathogens that have the potential to significantly impact Brassica crops.

plant biology

Generation And Comparative Analysis Of Full-Length Transcriptomes In Sweetpotato And Its Putative Wild Ancestor I. trifida

Sweetpotato [Ipomoea batatas (L.) Lam.] is one of the most important crops in many developing countries and provides a candidate source of bioenergy. However, neither high-quality reference genome nor large-scale full-length cDNA sequences for this outcrossing hexaploid are still lacking, which in turn impedes progress in research studies in sweetpotato functional genomics and molecular breeding. In this study, we apply a combination of second- and third-generation sequencing technologies to sequence full-length transcriptomes in sweetpotato and its putative ancestor I. trifida. In total, we obtained 53,861/51,184 high-quality transcripts, which includes 34,963/33,637 putative full-length cDNA sequences, from sweetpotato/I. trifida. Amongst, we identified 104,540/94,174 open reading frames, 1476/1475 transcription factors, 25,315/27,090 simple sequence repeats, 417/531 long non-coding RNAs out of the sweetpotato/I. trifida dataset. By utilizing public available genomic contigs, we analyzed the gene features (including exon number, exon size, intron number, intron size, exon-intron structure) of 33,119 and 32,793 full-length transcripts in sweetpotato and I. trifida, respectively. Furthermore, comparative analysis between our transcript datasets and other large-scale cDNA datasets from different plant species enables us assessing the quality of public datasets, estimating the genetic similarity across relative species, and surveyed the evolutionary pattern of genes. Overall, our study provided fundamental resources of large-scale full-length transcripts in sweetpotato and its putative ancestor, for the first time, and would facilitate structural, functional and comparative genomics studies in this important crop.

plant biology

NLR1-V, a CC-NBS-LRR encoding gene, is a potential candidate gene of the wheat powdery mildew resistance gene Pm21

Wheat powdery mildew caused by Blumeria graminisb f. sp. tritici is one of the most destructive diseases all over the world. Pm21, transferred from the wild Haynaldia villosa to wheat, confers broad spectrum resistance throughout the whole stage, and this gene has been widely used in wheat production for more than 20 years. Cloning the candidate gene of Pm21 is the prerequisite for elucidating the resistance mechanism, and is a valuable attempt to clone the target genes from the evolutionarily distant wild species. In this study, an innovative approach, which combined cytogenetic stocks development, mutagenesis, RenSeq and PacBio, was tried successfully to clone an NBS-LRR type gene NLR1-V from the Pm21 locus. Firstly, a powdery mildew resistant cryptic alien introgression line HP33 involved very small 6VS segment was developed, and 6 independent susceptible mutants of T6VS {middle dot} 6AL was identified. Then, the transcriptome of H. villosa was obtained by NGS and the full-length NBS-LRR gene database was constructed by RenSeq-PacBio. In the following study, two expressed NLR genes were located to the Pm21 locus using the HP33 as the mapping material, and only NLR1-V showed polymorphism between the wild T6VS {middle dot} 6AL and its six mutants. The functional analysis indicated that silencing of NLR1-V could compromise the resistance of T6VS {middle dot} 6AL completely, and could also decrease the resistance of T6VS {middle dot} 6DL dramatically. Moreover, NLR1-V could recover the resistance of the susceptible mutant and increase the resistance in the susceptible wheat. The study implied that NLR1-V, a CC-NBS-LRR encoding gene, is a potential candidate gene of the powdery mildew resistance gene Pm21.

plant biology

A DNA demethylase overexpression promotes early apical bud maturation in poplar through the biosynthesis and accumulation of flavonoids

ASBTRACTThe transition from active growth to dormancy is critical for the survival of perennial plants. We identified a DEMETER-like (CsDML) cDNA from a winter-enriched cDNA subtractive library in chestnut (Castanea sativa Mill.), an economically and ecologically important species. Next, we characterized this DNA demethylase and its putative orthologue in the more experimentally tractable hybrid poplar (Populus tremula x alba), under the signals that trigger bud dormancy in trees. We performed phylogenetic and protein sequence analysis, gene expression profiling and 5mC immunodetection studies to evaluate the role of CsDML and its homologue in poplar, PtaDML6. Transgenic hybrid poplars overexpressing CsDML were produced and analyzed. Short days (SD) and cold temperatures induced CsDML and PtaDML6. Overexpression of CsDML accelerated SD-induced bud formation, specifically from stage 1 to 0. Bud acquired a red-brown coloration earlier than wild type (WT) plants, alongside with the upregulation of flavonoid biosynthesis enzymes and accumulation of flavonoids in the SAM and bud scales. Our data shows that the CsDML gene induces bud formation needed for the survival of the apical meristem under the harsh conditions of winter. This study provides in planta evidence implicating chromatin remodeling by DNA demethylation during SD induction of bud maturation through the induction of flavonoids biosynthesis.

plant biology

Spot dynamics in a reaction-diffusion model of plant root hair initiation

We study pattern formation in a 2-D reaction-diffusion (RD) sub-cellular model characterizing the effect of a spatial gradient of a plant hormone distribution on a family of G-proteins associated with root-hair (RH) initiation in the plant cell Arabidopsis thaliana. The activation of these G-proteins, known as the Rho of Plants (ROPs), by the plant hormone auxin, is known to promote certain protuberances on root hair cells, which are crucial for both anchorage and the uptake of nutrients from the soil. Our mathematical model for the activation of ROPs by the auxin gradient is an extension of the model of Payne and Grierson [PLoS ONE, 12(4), (2009)], and consists of a two-component Schnakenberg-type RD system with spatially heterogeneous coefficients on a 2-D domain. The nonlinear kinetics in this RD system model the nonlinear interactions between the active and inactive forms of ROPs. By using a singular perturbation analysis to study 2-D localized spatial patterns of active ROPs, it is shown that the spatial variations in the nonlinear reaction kinetics, due to the auxin gradient, lead to a slow spatial alignment of the localized regions of active ROPs along the longitudinal midline of the plant cell. Numerical bifurcation analysis, together with time-dependent numerical simulations of the RD system are used to illustrate both 2-D localized patterns in the model, and the spatial alignment of localized structures.

plant biology

Managed woodlot revealed a trade-off between edible leaves and timber production in Vitex doniana Sweet (Lamiaceae)

Vitex doniana Sweet is a major wild-harvested tree resource for food in Benin. However, the species is under threats characterised by increasing human pressure on remnant populations. This study represents the first to explore species response to biotic stress. We tested the response of V. doniana to coppicing and fertilization. Two stump heights (20 and 40 cm) in combination with three organic manure rates (0.5; 1 and 1.5 kg per seedling), with eight replicates were tested in a randomised complete block design. We used mixed effect models with pseudoreplication, and the maximum likelihood method to compare effects of fixed factors on sprouting vigour, sprout growth and biomass yield in the short (12 months) and medium (5 years) terms. Results indicated that stump height significantly affected sprouting and all growth parameters, in the short and medium terms. However, there seemed a delayed effect of manure. We found initial seedling growth also an important factor. The hidden effect of stump height on biomass yield is discussed. Findings clearly indicate a trade-off between edible leaves and timber production by managed woodlot. Implications of findings for further investigation of above and below ground biomass dynamics and resources allocation in treated trees are discussed.\n\nHighlightsA clear trade-off between edible leaves and timber production is observed in managed Vitex doniana Sweet woodlot. Coppicing as a biotic stress induced important physiological changes that merit further investigations.

plant biology

Life and death of proteins after protease cleavage: protein degradation by the N-end rule pathway

The activity and abundance of proteins within a cell are controlled precisely to ensure the regulation of cellular and physiological processes. In eukaryotes, this can be achieved by targeting specific proteins for degradation by the ubiquitin-proteasome system. The N-end rule pathway, a subset of the ubiquitin-proteasome system, targets proteins for degradation depending on the identity of a protein N-terminal residue or its post-translational modifications. Here, we discuss the most recent findings on the diversity of N-end rule pathways. We also focus on recently found defensive functions of the N-end rule pathway in plants. We then discuss the current understanding of N-end rule substrate formation by protease cleavage. Finally, we review state-of-the-art proteomics techniques used for N-end rule substrate identification, and discuss their usefulness and limitations for the discovery of the molecular mechanisms underlying the roles of the N-end rule pathway in plants.

plant biology

Water and temperature stress define the optimal flowering period for wheat in south-eastern Australia

Across the Australian wheat belt, the time at which wheat flowers is a critical determinant of yield. In all environments an optimal flowering period (OFP) exists which is defined by decreasing frost risk, and increasing water and heat stress. Despite their critical importance, OFPs have not been comprehensively defined across south eastern Australias (SEA) cropping zone using yield estimates incorporating temperature, radiation and water-stress. In this study, the widely validated cropping systems model APSIM was used to simulate wheat yield and flowering date, with reductions in yield applied for frost and heat damage based on air temperatures during sensitive periods. Simulated crops were sown at weekly intervals from April 1 to July 15 of each year. The relationship between flowering date and grain yield was established for 28 locations using 51-years (1963-2013) of climate records. We defined OFPs as the flowering period which was associated with a mean yield of [≥] 95% of maximum yield from the combination of 51 seasons and 16 sowing dates. OFPs for wheat in SEA varied with site and season and were largely driven by seasonal water supply and demand, with extremes of heat and temperature having a secondary though auto-correlated effect. Quantifying OFPs will be a vital first step to identify suitable genotype x sowing date combinations to maximise yield in different locations, particularly given recent and predicted regional climate shifts including the decline in autumn rainfall.

plant biology

Multiple reference genome sequences of hot pepper reveal the massive evolution of plant disease resistance genes by retroduplication

Transposable elements (TEs) provide major evolutionary forces leading to new genome structure and species diversification. However, the role of TEs in the expansion of disease resistance gene families has been unexplored in plants. Here, we report high-quality de novo genomes for two peppers (Capsicum baccatum and C. chinense) and an improved reference genome (C. annuum). Dynamic genome rearrangements involving translocations among chromosome 3, 5 and 9 were detected in comparison between C. baccatum and the two other peppers. The amplification of athila LTR-retrotransposons, members of the gypsy superfamily, led to genome expansion in C. baccatum. In-depth genome-wide comparison of genes and repeats unveiled that the copy numbers of NLRs were greatly increased by LTR-retrotransposon-mediated retroduplication. Moreover, retroduplicated NLRs exhibited great abundance across the angiosperms, with most cases lineage-specific and thus recent events. Our study revealed that retroduplication has played key roles in the emergence of new disease-resistance genes in plants.

plant biology

Stacks off tracks: A role for the golgin AtCASP in plant endoplasmic reticulum - Golgi apparatus tethering

The plant Golgi apparatus modifies and sorts incoming proteins from the endoplasmic reticulum (ER), and synthesises cell wall matrix material. Plant cells possess numerous motile Golgi bodies, which are connected to the ER by yet to be identified tethering factors. Previous studies indicated a role of cis-Golgi plant golgins (long coiled-coil domains proteins anchored to Golgi membranes) in Golgi biogenesis. Here we show a tethering role for the golgin AtCASP at the ER-Golgi interface. Using live-cell imaging, Golgi body dynamics were compared in Arabidopsis thaliana leaf epidermal cells expressing fluorescently tagged AtCASP, a truncated AtCASP-{Delta}CC lacking the coiled-coil domains, and the Golgi marker STtmd. Golgi body speed and displacement were significantly reduced in AtCASP-{Delta}CC lines. Using a dual-colour optical trapping system and a TIRF-tweezer system, individual Golgi bodies were captured in planta. Golgi bodies in AtCASP-{Delta}CC lines were easier to trap, and the ER-Golgi connection was more easily disrupted. Occasionally, the ER tubule followed a trapped Golgi body with a gap, indicating the presence of other tethering factors. Our work confirms that the intimate ER-Golgi association can be disrupted or weakened by expression of truncated AtCASP-{Delta}CC, and suggests that this connection is most likely maintained by a golgin-mediated tethering complex.\n\nHighlightHere we show that the Golgi-associated Arabidopsis thaliana protein AtCASP may form part of a golgin-mediated tethering complex involved in anchoring plant Golgi stacks to the endoplasmic reticulum (ER).

plant biology

Gene expression polymorphism underpins evasion of host immunity in an asexual lineage of the Irish potato famine pathogen

Outbreaks caused by asexual lineages of fungal and oomycete pathogens are an expanding threat to crops, wild animals and natural ecosystems (Fisher et al. 2012,Kupferschmidt 2012). However, the mechanisms underlying genome evolution and phenotypic plasticity in asexual eukaryotic microbes remain poorly understood (Seidl and Thomma 2014). Ever since the 19th century Irish famine, the oomycete Phytophthora infestans has caused recurrent outbreaks on potato and tomato crops that have been primarily caused by the successive rise and migration of pandemic asexual lineages (Cooke et al. 2012, Yoshida et al. 2013,Yoshida et al. 2014). Here, we reveal patterns of genomic and gene expression variation within a P. infestans asexual lineage by compared sibling strains belonging to the South American EC-1 clone that has dominated Andean populations since the 1990s (Forbes et al. 1997, Oyarzun et al. 1998, Delgado et al. 2013, Yoshida et al. 2013, Yoshida et al. 2014). We detected numerous examples of structural variation, nucleotide polymorphisms and gene conversion within the EC-1 clone. Remarkably, 17 genes are not expressed in one of the two EC-1 isolates despite apparent absence of sequence polymorphisms. Among these, silencing of an effector gene was associated with evasion of disease resistance conferred by a potato immune receptor. These results highlight the exceptional genetic and phenotypic plasticity that underpins host adaptation in a pandemic clonal lineage of a eukaryotic plant pathogen.

plant biology

The Molecular Link Between Auxin And ROS-Mediated Polar Growth

Root hair polar growth is endogenously controlled by auxin and sustained by oscillating levels of reactive oxygen species (ROS). These cells extend several hundred-fold their original size toward signals important for plant survival. Although their final cell size is of fundamental importance, the molecular mechanisms that control it remain largely unknown. Here, we show that ROS production is controlled by the transcription factors RSL4, which in turn is transcriptionally regulated by auxin through several Auxin Responsive Factors (ARFs). In this manner, auxin controls ROS-mediated polar growth by activating RSL4, which then upregulates the expression of genes encoding NADPH oxidases (also known as RBOHs, RESPIRATORY BURST OXIDASE HOMOLOG proteins) and Class-III Peroxidases (PER), which catalyse ROS production. Chemical or genetic interference with the ROS balance or peroxidase activity affect root hair final cell size. Overall, our findings establish a molecular link between auxin regulated ARFs-RSL4 and ROS-mediated polar root hair growth.\n\nSignificance StatementTip-growing root hairs are excellent model systems to decipher the molecular mechanism underlying reactive oxygen species (ROS)-mediated cell elongation. Root hairs are able to expand in response to external signals, increasing several hundred-fold their original size, which is important for survival of the plant. Although their final cell size is of fundamental importance, the molecular mechanisms that control it remain largely unknown. In this study, we propose a molecular mechanism that links the auxin-Auxin Response Factors (ARFs) module to activation of RSL4, which directly targets genes encoding ROS-producing enzymes, such as NADPH oxidases (or RBOHs) and secreted type-III peroxidases (PERs). Activation of these genes impacts apoplastic ROS homeostasis, thereby stimulating root hair cell elongation.

plant biology