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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. 

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. 

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.