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Summary The conquest of land by plants was concomitant with, and possibly enabled by, the evolution of three‐dimensional (3D) growth. The moss
Physcomitrium patens provides a model system for elucidating molecular mechanisms in the initiation of 3D growth. Here, we investigate whether the phytohormone ethylene, which is believed to have been a signal before land plant emergence, plays a role in 3D growth regulation inP. patens .We report ethylene controls 3D gametophore formation, based on results from exogenously applied ethylene and genetic manipulation of
PpEIN2 , which is a central component in the ethylene signaling pathway.Overexpression (OE) of
PpEIN2 activates ethylene responses and leads to earlier formation of gametophores with fewer gametophores produced thereafter, phenocopying ethylene‐treated wild‐type. Conversely,Ppein2 knockout mutants, which are ethylene insensitive, show initially delayed gametophore formation with more gametophores produced later. Furthermore, pharmacological and biochemical analyses reveal auxin levels are decreased in the OE lines but increased in the knockout mutants.Our results suggest that evolutionarily, ethylene and auxin molecular networks were recruited to build the plant body plan in ancestral land plants. This might have played a role in enabling ancient plants to acclimate to the continental surfaces of the planet.
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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 in
Arabidopsis thaliana reproduction. By analyzing anacs octuple 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 mossPp GLR1, 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. -
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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. In
Arabidopsis thaliana , ACC is transported by amino acid transporters, LYSINE HISTIDINE TRANSPORTER 1 (LHT1) and LHT2. In nonseed plants,LHT homologs have been uncharacterized.Here, we isolated an ACC‐insensitive mutant (Mp
ain ) that is defective in ACC uptake in the liverwortMarchantia polymorpha . Mpain contained a frameshift mutation (1 bp deletion) in the MpLHT1 coding sequence, and was complemented by expression of a wild‐type MpLHT1 transgene. Additionally, ACC insensitivity was re‐created in CRISPR/Cas9‐Mplht1 knockout mutants. We found that MpLHT1 can also transportl ‐hydroxyproline andl ‐histidine.We examined the physiological functions of Mp
LHT1 in vegetative growth and reproduction based on mutant phenotypes. Mpain and Mplht1 plants were smaller and developed fewer gemmae cups compared to wild‐type plants. Mplht1 mutants also had reduced fertility, and archegoniophores displayed early senescence.These findings reveal that MpLHT1 serves as an ACC and amino acid transporter in
M. polymorpha and has diverse physiological functions. We propose that MpLHT1 contributes to homeostasis of ACC and other amino acids inM. polymorpha growth and reproduction.
