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The unique evolutionary adaptation of legumes for nitrogen-fixing symbiosis leading to nodulation is tightly regulated by the host plant. The autoregulation of nodulation (AON) pathway negatively regulates the number of nodules formed in response to the carbon/nitrogen metabolic status of the shoot and root by long-distance signaling to and from the shoot and root. Central to AON signaling in the shoots ofMedicago truncatulais SUNN, a leucine-rich repeat receptor-like kinase with high sequence similarity with CLAVATA1 (CLV1), part of a class of receptors inArabidopsisinvolved in regulating stem cell populations in the root and shoot. This class of receptors inArabidopsisincludes the BARELY ANY MERISTEM family, which, like CLV1, binds to CLE peptides and interacts with CLV1 to regulate meristem development.M. truncatulacontains five members of theBAMfamily, but onlyMtBAM1andMtBAM2are highly expressed in the nodules 48 hours after inoculation. Plants carry mutations in individualMtBAMs, and several doubleBAMmutant combinations all displayed wild-type nodule number phenotypes. However,Mtbam2suppressed thesunn-5hypernodulation phenotype and partially rescued the short root length phenotype ofsunn-5 when present in asunn-5background. Grafting determined thatbam2suppresses supernodulation from the roots, regardless of theSUNNstatus of the root. Overexpression ofMtBAM2in wild-type plants increases nodule numbers, while overexpression ofMtBAM2in somesunnmutants rescues the hypernodulation phenotype, but not the hypernodulation phenotypes of AON mutantrdn1-2orcrn. Relative expression measurements of the nodule transcription factor MtWOX5 downstream of the putativebam2 sunn-5complex revealed disruption of meristem signaling; while bothbam2andbam2 sunn-5influenceMtWOX5expression, the expression changes are in different directions. We propose a genetic model wherein the specific root interactions of BAM2/SUNN are critical for signaling in nodule meristem cell homeostasis inM. truncatula.
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The rise of CLAVATA: evidence for CLAVATA3 and WOX signaling in the fern gametophyte
SUMMARY CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptides are 12–13 amino acid‐long peptides that serve as positional signals in plants. The core CLE signaling module consists of a CLE peptide and a leucine‐rich repeat receptor‐like kinase, but in flowering plants, WUSCHEL‐RELATED HOMEOBOX (WOX) transcription factors are also incorporated to form negative feedback loops that regulate stem cell maintenance in the shoot and root. It is not known whenWOXgenes were co‐opted into CLE signaling pathways, only that mosses and liverworts do not require WOX for CLE‐regulated stem cell activities. We identified 11 CLE‐encoding genes in the Ceratopteris genome, including one (CrCLV3) most similar to shoot meristem CLE peptide CLAVATA3. We performed the first functional characterization of a fern CLE using techniques including RNAi knockdown and synthetic peptide dosage. We found that CrCLV3 promotes cell proliferation and stem cell identity in the gametophyte meristem. Importantly, we provide evidence for CrCLV3 regulation of theWOXgeneCrWOXAduring the developmental stage when female gametangium formation begins. These discoveries open a new avenue for CLE peptide research in the fern and clarify the evolutionary timeline of CLE‐WOX signaling in land plants.
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- Award ID(s):
- 2423834
- PAR ID:
- 10560110
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- The Plant Journal
- Volume:
- 121
- Issue:
- 2
- ISSN:
- 0960-7412
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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