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Ancient peptide-redox signalling underlies sperm motility in Marchantia.

Zhang, Y., et al. · 2026 · Nature Plants   research

doi:10.1038/s41477-026-02334-4   PMID:42399668

Linked genes (25)  5 core 20 peripheral

Gene ID Name Evidence / Role Function (this paper)
Mp4g15890 MpFER experimental subject The single Marchantia CrRLK1L receptor kinase, shown here to be the MpRALF1 receptor in spermatozoids. MpFER is enriched in antheridiophores (proMpFER:GUS) and the MpFER-Flag protein localizes to sperm flagella; CRISPR Mpfer knockouts and amiRNA Ri-MpFER lines had reduced sperm ROS and motility that MpRALF1 peptide could no longer rescue. MpFER binds MpRALF1 (pulldown with MBP-MpFERecd, luciferase complementation with MpFER-deltaC) preferentially via the peptide's N-terminal region and forms a complex with MpLLG (CoIP); the MpFER-G282A substitution did not affect MpRALF1 binding, indicating a binding mode distinct from angiosperm RALF23-FER-LLG2 and RALF4-ANX1/BUPS1-LLG3. Gene ID not printed in the paper: resolved from the paper's own MpFER-RT-F/R qPCR primers (Suppl. Table 2), which match Mp4g15890 exactly, in agreement with Mecchia et al. 2022.
Mp4g22100 MpLRE2 experimental subject GPI-anchored LORELEI-like co-receptor, renamed in this paper from MpLRE2 (the MpLRE gene that retains the GPI-anchoring site). MpLLG is enriched in antheridiophores and its Flag/eGFP fusions accumulate in sperm flagella; CRISPR Mpllg and amiRNA Ri-MpLLG lines showed reduced sperm ROS and motility that exogenous MpRALF1 failed to rescue. MpLLG co-immunoprecipitates with MpFERecd, binds MpRALF1 preferentially through the peptide C-terminal 38-aa region, and the MpLLG-N100A and MpLLG-A126Y substitutions disturb that binding, defining an MpRALF1-MpFER-MpLLG module upstream of ROS production. Gene ID not printed in the paper: resolved from the paper's own MpLLG-RT-F/R qPCR primers (Suppl. Table 2), which match Mp4g22100 (= MpLRE2 of Mecchia et al. 2022) exactly.
Mp7g07270
MpRALF3 paper
MpRALF1 nomenclature
experimental subject Sperm-derived RAPID ALKALINIZATION FACTOR peptide, the central subject of this study. Identified in a screen of the top 1,000 antheridia-expressed genes, MpRALF1 is specifically and highly expressed in mature antheridia (RT-qPCR, proMpRALF1:GUS) and the peptide accumulates in spermatozoid flagella. Three CRISPR/Cas9 frameshift knockout lines and amiRNA knockdown (Ri-MpRALF1) reduced male fertility (fewer sporophytes after crossing), lowered sperm ROS levels and impaired sperm kinematics (reduced curvilinear velocity, fewer rapidly progressive and more slow/non-progressive spermatozoids); 10 nM synthetic MpRALF1 peptide rescued both ROS and motility. MpRALF1 is perceived by the MpFER-MpLLG receptor complex (pulldown, CoIP, luciferase complementation), and its N-terminal 18-aa region binds MpFER whereas its C-terminal 38-aa region binds MpLLG. NAMING NOTE: gene ID stated in the paper; Mecchia et al. 2022 (Development, doi:10.1242/dev.200580) calls this same locus MpRALF3 and uses MpRALF1 for Mp1g27120.
Mp7g00270 MpRBOHA experimental subject The second Marchantia NADPH oxidase (RBOH) gene, also highly expressed in antheridiophores and antheridia. amiRNA knockdown (Ri-MpRBOH2) reduced sperm ROS levels and produced the same class of motility defects as Ri-MpRBOH1, supporting RBOH-derived ROS as the effector of MpRALF1-MpFER-MpLLG signalling in spermatozoids. NAMING NOTE: no gene ID is printed in the paper; resolved from the paper's own MpRBOH2-RT-F/R primers (Suppl. Table 2), which match Mp7g00270 (= MpRBOHA / MpNOX2; this locus is MpRBOH1 in Yotsui et al. 2023). Link by ID, never by name.
Mp3g20340 MpRBOHB experimental subject One of the two Marchantia NADPH oxidase (respiratory burst oxidase homologue) genes, both highly expressed in antheridiophores and antheridia. amiRNA knockdown (Ri-MpRBOH1) significantly reduced sperm ROS levels - more strongly than Ri-MpRBOH2 - and impaired sperm kinematics (lower curvilinear velocity, fewer rapidly progressive and more slow-progressive spermatozoids), phenocopied by the NADPH-oxidase inhibitor DPI; this places RBOH-derived ROS downstream of the MpRALF1-MpFER-MpLLG module in sperm motility control. NAMING NOTE: no gene ID is printed in the paper; the locus was resolved from the paper's own MpRBOH1-RT-F/R primers (Suppl. Table 2), which match Mp3g20340 (= MpRBOHB / MpNOX1; MpRBOH1 in Chu et al. 2023 but MpRBOH2 in Yotsui et al. 2023). Link by ID, never by name.
Mp3g23400 MpEF1 experimental tool Housekeeping gene used to normalize all RT-qPCR transcript measurements.
Mp1g03930 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 71 aa; no predicted signal peptide; FPKM 87.6177/104.321 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp1g09940 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 104 aa; signal peptide predicted; FPKM 203.428/188.183 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp2g12030 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 64 aa; no predicted signal peptide; FPKM 201.81/168.769 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp2g18090 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 50 aa; no predicted signal peptide; FPKM 89.157/99.0344 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp3g00220 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 89 aa; no predicted signal peptide; FPKM 88.5917/97.2983 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp3g16180 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 74 aa; no predicted signal peptide; FPKM 143.565/143.739 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp3g21270 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 91 aa; no predicted signal peptide; FPKM 447.429/471.366 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp3g22390 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (annotated as arabinogalactan peptide; 77 aa; signal peptide predicted; FPKM 136.58/154.867 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp4g01930 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 70 aa; signal peptide predicted; FPKM 180.97/183.813 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp4g05540 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 45 aa; no predicted signal peptide; FPKM 153.845/165.333 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp4g05860 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 47 aa; no predicted signal peptide; FPKM 153.012/175.651 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp4g10350 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 64 aa; signal peptide predicted; FPKM 433.106/457.258 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp5g01750 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 84 aa; no predicted signal peptide; FPKM 191.441/95.6325 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp5g03630 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 83 aa; signal peptide predicted; FPKM 99.2707/117.315 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp6g10430 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (no functional annotation; 78 aa; no predicted signal peptide; FPKM 115.709/133.423 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp6g11390 missing experimental background Listed among the 17 putative peptide-encoding genes retrieved by this study's screen of the top 1,000 antheridia-expressed genes (annotated as signalling peptide taximin 2; 78 aa; no predicted signal peptide; FPKM 89.0919/54.7961 in the two antheridia replicates). Not characterized further - MpRALF1 (Mp7g07270) was the candidate pursued.
Mp5g09600 MpLRE1 citation background Cited as the other of the two MpLRE genes; because it lacks the typical GPI-anchoring site (reported by Mecchia et al. 2022) it was not pursued, and the study focused on MpLRE2/MpLLG instead.
Mp1g27120
MpRALF1 paper
MpRALF3 nomenclature
experimental background One of the three Marchantia RALF genes profiled by RT-qPCR (Extended Data Fig. 1a); not antheridia-enriched, so the study focused on MpRALF1. Locus resolved from the paper's MpRALF3-RT-F/R primers (Suppl. Table 2), which match Mp1g27120 - the locus that Mecchia et al. 2022 calls MpRALF1.
Mp2g21670 MpRALF2 experimental background One of the three Marchantia RALF genes whose transcript levels were measured by RT-qPCR across male and female tissues (Extended Data Fig. 1a); unlike MpRALF1 it is not antheridia-enriched. Locus resolved from the paper's MpRALF2-RT-F/R primers (Suppl. Table 2).