RALFL34 regulates formative cell divisions in Arabidopsis pericycle during lateral root initiation

Murphy, Evan; Vu, Lam Dai; Broeck, Lisa Van den; Lin, Zhefeng; Ramakrishna, Priya; Cotte, Brigitte van de; Gaudinier, Allison; Goh, Tatsuaki; Slane, Daniel; Beeckman, Tom; Inzé, Dirk; Brady, Siobhán M.; Fukaki, Hidehiro; Smet, Ive De

doi:10.1093/jxb/erw281

Cited by 74 publications

(79 citation statements)

References 106 publications

(141 reference statements)

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“…Meanwhile the transcriptional level of GATA23 was significantly down-regulated in arf7 , lbd16 , lbd18 and lbd29 single mutant (S7 Fig). Together, auxin induced PRH1 interacts with GATA23, which has been also reported to be up-regulated by auxin [20].…”

Section: Resultsmentioning

confidence: 99%

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PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development inArabidopsis thaliana

Zhang

Tao

Sun

et al. 2019

Preprint

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18The development of lateral roots in Arabidopsis thaliana is strongly dependent on 19 signaling directed by the AUXIN RESPONSE FACTOR7 (ARF7), which in turn 20 activates LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors 21 (LBD16, 18, 29 and 33). Here, the product of PRH1, a PR-1 homolog annotated 22 previously as encoding a pathogen-responsive protein, was identified as a target of 23 ARF7-mediated auxin signaling and also as participating in the development of lateral 24 roots. PRH1 was shown to be strongly induced by auxin treatment, and plants lacking 25 a functional copy of PRH1 formed fewer lateral roots. The transcription of PRH1 was 26 controlled by the binding of both ARF7 and LBDs to its promoter region. An 27 interaction was detected between PRH1 and GATA23, a protein which regulates cell 28 identity in lateral root founder cells. 29 2 30 31 Author Summary 32 In Arabidopsis thaliana AUXIN RESPONSE FACTOR7 (ARF7)-mediated auxin 33 signaling plays a key role in lateral roots (LRs) development. The LATERAL ORGAN 34 BOUNDARIES DOMAIN (LBD) transcription factors (LBD16, 18, 29 and 33) act 35 downstream of ARF7-mediated auxin signaling to control LRs formation. Here, the 36 PR-1 homolog PRH1 was identified as a novel target of both ARF7 and LBDs 37 (especially the LBD29) during auxin induced LRs formation, as both ARF7 and 38LBDs were able to bind to the PRH1 promoter. More interestingly, PRH1 has a 39 physical interaction with GATA23, which has been also reported to be up-regulated 40 by auxin and influences LR formation through its regulation of LR founder cell 41 identity. Whether the interaction between GATA23 and PRH1 affects the stability 42 and/or the activity of either (or both) of these proteins remains an issue to be explored. 43 This study provides improves new insights about how auxin regulates lateral root 44 development. 3 45 Introduction 46 The architecture of the root system depends on the density of lateral roots (LRs) 47 formed along with the extent of root branching. LRs are initiated from mature 48 pericycle cells lying adjacent to the xylem pole, referred to in Arabidopsis thaliana as 49 the xylem pole pericycle [1, 2]. A subset of these cells, namely the founder cells, 50 undergo a series of highly organized divisions to form an LR primordium, which 51 eventually develops into an LR. The entire process of LR development, from its 52 initiation to its emergence, is regulated by auxin [1, 3, 4]. The accumulation of auxin 53 in protoxylem cells results in the priming of neighboring pericycle cells to gain 54 founder cell identity, forming an LR pre-branch site [5, 6]. This auxin signaling is 55 mediated by the proteins ARF7 and ARF19, which act in the IAA28-dependent 56 pathway [7, 8]. LR initiation depends on the transcriptional activation, through the 57 involvement of the transcription factor LBD16 and LBD18, of either E2Fa or CDK 58 A1;1 and CYC B1;1 [9, 10]. Other downstream targets such as EXP14 and EXP17 and 59 the products of certain cell wall loosening-related genes ...

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Section: Resultsmentioning

confidence: 99%

“…PRH1 acts as a downstream gene of both ARF7 and LBDs by the direct transcriptional regulation [14]. Nuclear localized PRH1 can interact with another transcription factor GATA23, known to act downstream of ARF7 and the LBDs, to mediate LR formation [8, 20].…”

Section: Resultsmentioning

confidence: 99%

PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development inArabidopsis thaliana

Zhang

Tao

Sun

et al. 2019

Preprint

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“…The canonical peptide, RALF1, was found to arrest tomato and Arabidopsis root growth with no activation of defense pathways (Pearce et al, 2001), initially suggesting a developmental role for these peptides. However, subsequent studies have identified a wide variety of roles for members of the RALF family, including cell expansion (Haruta et al, 2014), lateral root development (Murphy et al, 2016), root hair growth (Wu et al, 2007), pollen tube elongation (Covey et al, 2010), as well as stress (Atkinson et al, 2013). The diversity of these roles indicates that RALF peptides are fundamentally important for plant development.…”

Section: Introductionmentioning

confidence: 99%

A Comprehensive Analysis of RALF Proteins in Green Plants Suggests There Are Two Distinct Functional Groups

2017

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Rapid Alkalinization Factors (RALFs) are small, cysteine-rich peptides known to be involved in various aspects of plant development and growth. Although RALF peptides have been identified within many species, a single wide-ranging phylogenetic analysis of the family across the plant kingdom has not yet been undertaken. Here, we identified RALF proteins from 51 plant species that represent a variety of land plant lineages. The inferred evolutionary history of the 795 identified RALFs suggests that the family has diverged into four major clades. We found that much of the variation across the family exists within the mature peptide region, suggesting clade-specific functional diversification. Clades I, II, and III contain the features that have been identified as important for RALF activity, including the RRXL cleavage site and the YISY motif required for receptor binding. In contrast, members of clades IV that represent a third of the total dataset, is highly diverged and lacks these features that are typical of RALFs. Members of clade IV also exhibit distinct expression patterns and physico-chemical properties. These differences suggest a functional divergence of clades and consequently, we propose that the peptides within clade IV are not true RALFs, but are more accurately described as RALF-related peptides. Expansion of this RALF–related clade in the Brassicaceae is responsible for the large number of RALF genes that have been previously described in Arabidopsis thaliana. Future experimental work will help to establish the nature of the relationship between the true RALFs and the RALF-related peptides, and whether they function in a similar manner.

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“…Among them, the members of the rapid alkalinization factor (RALF) family were first identified through their ability to trigger a rapid increase in extracellular pH when added to plant cell suspensions (Pearce et al , ). RALF peptides have been linked to several physiological and developmental processes, including cell expansion (Haruta et al , ), lateral root development (Murphy et al , ), root hair growth (Wu et al , ), pollen tube elongation (Covey et al , ), nodulation in legumes (Djordjevic et al , ) and stress (Atkinson et al , ). In silico analysis of the Arabidopsis thaliana genome identified 37 genes belonging to the RALF family, named RALF1 to RALF37 (Olsen et al , ), and the homologues identified in other species have been named according to their similarities to the members of the A. thaliana family (Campbell and Turner, ).…”

Section: Introductionmentioning

confidence: 99%

Induced expression of the Fragaria × ananassa Rapid alkalinization factor‐33‐like gene decreases anthracnose ontogenic resistance of unripe strawberry fruit stages

Merino

Guidarelli

Negrini

et al. 2019

Molecular Plant Pathology

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Summary Rapid alkalinization factor (RALF) genes encode for ubiquitous small peptides that stimulate apoplastic alkalinization through interaction with malectin‐like receptor kinase. RALF peptides may act as negative regulators of plant immune response, inhibiting the formation of the signal receptor complex for immune activation. Recently RALF homologues were identified in different fungal pathogen genomes contributing to host infection ability. Here, FaRALF‐33‐like gene expression was evaluated in strawberry fruits inoculated with Colletotrichum acutatum, Botrytis cinerea , or Penicillium expansum after 24 and 48 h post‐infection. To investigate the role of FaRALF‐33‐like in strawberry susceptibility, transient transformation was used to overexpress it in white unripe fruits and silence it in red ripe fruits. Agroinfiltrated fruits were inoculated with C. acutatum and expression, and histological analysis of infection were performed. Silencing of FaRALF‐33‐like expression in C. acutatum ‐inoculated red fruits led to a delay in fruit colonization by the fungal pathogen, and infected tissues showed less penetrated infective hyphae than in wild‐type fruits. In contrast, C. acutatum‐ inoculated white unripe fruits overexpressing the FaRALF‐33‐like gene decreased the ontogenic resistance of these fruits, leading to the appearance of disease symptoms and penetrated subcuticular hyphae, normally absent in white unripe fruits. The different response of transfected strawberry fruits to C. acutatum supports the hypothesis that the FaRALF‐33‐like gene plays an important role in the susceptibility of fruits to the fungal pathogen C. acutatum .

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RALFL34 regulates formative cell divisions in Arabidopsis pericycle during lateral root initiation

Abstract: HighlightWe describe the role of RALFL34 during early events in lateral root development, and demonstrate its specific importance in orchestrating formative cell divisions in the pericycle.

Cited by 74 publications

References 106 publications

PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development inArabidopsis thaliana

PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development inArabidopsis thaliana

A Comprehensive Analysis of RALF Proteins in Green Plants Suggests There Are Two Distinct Functional Groups

Induced expression of the Fragaria × ananassa Rapid alkalinization factor‐33‐like gene decreases anthracnose ontogenic resistance of unripe strawberry fruit stages

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