The Peptide Hormone Receptor CEPR1 Functions in the Reproductive Tissue to Control Seed Size and Yield1[OPEN]

CEP receptor signaling in maternal tissues controls the delivery of nitrogen to reproductive sinks. The interaction of C-TERMINALLY ENCODED PEPTIDES (CEPs) with CEP RECEPTOR1 (CEPR1) controls root growth and development, as well as nitrate uptake, but has no known role in determining yield. We used physiological, microscopic, molecular, and grafting approaches to demonstrate a reproductive tissue-specific role forCEPR1in controlling yield and seed size. Independent Arabidopsis (Arabidopsis thaliana)cepr1null mutants showed disproportionately large reductions in yield and seed size relative to their decreased vegetative growth. These yield defects correlated with compromised reproductive development predominantly in female tissues, as well as chlorosis, and the accumulation of anthocyanins incepr1reproductive tissues. The thinning of competing reproductive organs to improve source-to-sink ratios incepr1, along with reciprocal bolt-grafting experiments, demonstrated that CEPR1 acts locally in the reproductive bolt to control yield and seed size.CEPR1is expressed throughout the vasculature of reproductive organs, including in the chalazal seed coat, but not in other seed tissues. This expression pattern implies that CEPR1 controls yield and seed size from the maternal tissue. The complementation ofcepr1mutants with transgenicCEPR1rescued the yield and other phenotypes. Transcriptional analyses ofcepr1bolts showed alterations in the expression levels of several genes of the CEP-CEPR1 and nitrogen homeostasis pathways. This transcriptional profile was consistent withcepr1bolts being nitrogen deficient and with a reproductive tissue-specific function for CEP-CEPR1 signaling. The results reveal a local role for CEPR1 in the maternal reproductive tissue in determining seed size and yield, likely via the control of nitrogen delivery to the reproductive sinks.