An official website of the United States government
Abstract The phytohormone ethylene has numerous effects on plant growth and development. Its immediate precursor, 1-aminocyclopropane-1-carboxylic acid (ACC), is a non-proteinogenic amino acid produced by ACC SYNTHASE (ACS). ACC is often used to induce ethylene responses. Here, we demonstrate that ACC exhibits ethylene-independent signaling inArabidopsis thalianareproduction. By analyzing anacsoctuple mutant with reduced seed set, we find that ACC signaling in ovular sporophytic tissue is involved in pollen tube attraction, and promotes secretion of the pollen tube chemoattractant LURE1.2. ACC activates Ca2+-containing ion currents via GLUTAMATE RECEPTOR-LIKE (GLR) channels in root protoplasts. In COS-7 cells expressing mossPpGLR1, ACC induces the highest cytosolic Ca2+elevation compared to all twenty proteinogenic amino acids. In ovules, ACC stimulates transient Ca2+elevation, and Ca2+influx in octuple mutant ovules rescues LURE1.2 secretion. These findings uncover a novel ACC function and provide insights for unraveling new physiological implications of ACC in plants.
more »
« less
This content will become publicly available on February 11, 2026
Ethylene-independent modulation of root development by ACC via downregulation of WOX5 and group I CLE peptide expression
In seed plants, the canonical role of 1-aminocyclopropane-1-carboxylic acid (ACC) is to serve as the precursor in the biosynthesis of the phytohormone ethylene, and indeed, ACC treatment is often used as a proxy for ethylene treatment. Increasing evidence suggests that ACC can also act independently of ethylene to regulate various aspects of plant growth and development. Here, we explore the effects of ACC onArabidopsis thalianaroot growth and the mechanisms by which it acts. ACC inhibits growth of the primary root inArabidopsisseedlings when ethylene signaling is blocked, which becomes evident after 36 h of treatment with ACC. This reduced root growth is in part the result of suppressed cell proliferation in the root meristem resulting from altered expression of a key regulator of stem cell niche activity, WOX5. ACC also promotes lateral root (LR) development, in contrast to ethylene, which inhibits LR formation. Transcriptomic analysis of roots revealed no significant changes in gene expression after 45 min or 4 h of ACC treatment, but longer treatment times revealed a large number of differentially expressed genes, including the downregulation of the expression of a small group of phylogenetically related CLE peptides. Reduced expression of these group 1 CLEs in response to ACC leads to the activation of a transcription factor, LBD18, which promotes LR development. These results suggest that ACC acts to modulate multiple aspects ofArabidopsisroot growth independently of ethylene via distinct transcriptional effects in the root meristem and LR precursor cells.
more »
« less
- Award ID(s):
- 2427432
- PAR ID:
- 10616741
- Publisher / Repository:
- National Academy of Sciences
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 122
- Issue:
- 6
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Marshall-Colon, Amy (Ed.)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.more » « less
-
ABSTRACT Posttranslational tyrosine sulfation of peptides and proteins is catalysed by tyrosylprotein sulfotransferases (TPSTs). InArabidopsis, tyrosine sulfation is essential for the activities of peptide hormones, such as phytosulfokine (PSK) and root meristem growth factor (RGF). Here, we identified a TPST‐encoding gene,MtTPST, from model legumeMedicago truncatula.MtTPSTexpression was detected in all organs, with the highest level in root nodules. Apromoter:GUSassay revealed thatMtTPSTwas highly expressed in the root apical meristem, nodule primordium and nodule apical meristem. The loss‐of‐function mutantmttpstexhibited a stunted phenotype with short roots and reduced nodule number and size. Application of both of the sulfated peptides PSK and RGF3 partially restored the defective root length ofmttpst. The reduction in symbiotic nodulation inmttpstwas partially recovered by treatment with sulfated PSK peptide. MtTPST‐PSK module functions downstream of the Nod factor signalling to promote nodule initiation via regulating accumulation and/or signalling of cytokinin and auxin. Additionally, the small‐nodule phenotype ofmttpst, which resulted from decreased apical meristematic activity, was partially complemented by sulfated RGF3 treatment. Together, these results demonstrate that MtTPST, through its substrates PSK, RGF3 and other sulfated peptide(s), positively regulates nodule development and root growth.more » « less
-
Abstract Shade-intolerant plants rapidly elongate their stems, branches, and leaf stalks to compete with neighboring vegetation, maximizing sunlight capture for photosynthesis. This rapid growth adaptation, known as the shade-avoidance response (SAR), comes at a cost: reduced biomass, crop yield, and root growth. Significant progress has been made on the mechanistic understanding of hypocotyl elongation during SAR; however, the molecular interpretation of root growth repression is not well understood. Here, we explore the mechanisms by which SAR induced by low red:far-red light restricts primary and lateral root (LR) growth. By analyzing the whole-genome transcriptome, we identified a core set of shade-induced genes in roots of Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum) seedlings grown in the shade. Abiotic and biotic stressors also induce many of these shade-induced genes and are predominantly regulated by WRKY transcription factors. Correspondingly, a majority of WRKY genes were among the shade-induced genes. Functional analysis using transgenics of these shade-induced WRKYs revealed that their role is essentially to restrict primary root and LR growth in the shade; captivatingly, they did not affect hypocotyl elongation. Similarly, we also found that ethylene hormone signaling is necessary for limiting root growth in the shade. We propose that during SAR, shade-induced WRKY26, 45, and 75, and ethylene reprogram gene expression in the root to restrict its growth and development.more » « less
-
Summary In seed plants, 1‐aminocyclopropane‐1‐carboxylic acid (ACC) is the precursor of the plant hormone ethylene but also has ethylene‐independent signaling roles. Nonseed plants produce ACC but do not efficiently convert it to ethylene. InArabidopsis thaliana, ACC is transported by amino acid transporters, LYSINE HISTIDINE TRANSPORTER 1 (LHT1) and LHT2. In nonseed plants,LHThomologs have been uncharacterized.Here, we isolated an ACC‐insensitive mutant (Mpain) that is defective in ACC uptake in the liverwortMarchantia polymorpha. Mpaincontained a frameshift mutation (1 bp deletion) in the MpLHT1coding sequence, and was complemented by expression of a wild‐type MpLHT1transgene. Additionally, ACC insensitivity was re‐created in CRISPR/Cas9‐Mplht1knockout mutants. We found that MpLHT1 can also transportl‐hydroxyproline andl‐histidine.We examined the physiological functions of MpLHT1in vegetative growth and reproduction based on mutant phenotypes. Mpainand Mplht1plants were smaller and developed fewer gemmae cups compared to wild‐type plants. Mplht1mutants also had reduced fertility, and archegoniophores displayed early senescence.These findings reveal that MpLHT1 serves as an ACC and amino acid transporter inM. polymorphaand has diverse physiological functions. We propose that MpLHT1 contributes to homeostasis of ACC and other amino acids inM. polymorphagrowth and reproduction.more » « less
