CsSPL functions as an adaptor between HD‐ZIP III and CsWUS transcription factors regulating anther and ovule development in Cucumis sativus (cucumber)

Summary Anther and ovule genesis preconditions crop fertilization and fruit production; however, coordinative regulation of anther and ovule development and underlying molecular pathways remain largely elusive. Here, we found that SPOROCYTELESS ( SPL )/ NOZZLE ( NZZ ) expression was nearly abolished in a Cucumis sativus (cucumber) mutant with severely defective anther and ovule development. Cs SPL was expressed specifically in the developing anthers and ovules. Knock‐down of Cs SPL reduced male and female fertility with malformed pollen and suppressed ovule development. Importantly, Cs SPL directly interacted with Cs WUS ( WUSCHEL ) in the nucellus and YABBY family genes in integuments, and positively regulated Cs WUS expression, meanwhile the HD ‐ ZIP III gene Cs PHB ( PHABULOSA ), expressed specifically in the nucellus, promoted Cs SPL expression by binding to the Cs SPL promoter. Thus, Cs SPL acts as an adaptor to link Cs PHB and Cs WUS functioning, underpinning a previously unidentified regulatory pathway orchestrating sex organ development in planta . In addition, auxin accumulation was reduced in the reproductive organs of Cs SPL knock‐down plants. Biochemical analyses further showed that Cs SPL stimulated the expression of AUXIN RESPONSE FACTOR 3 ( Cs ARF 3 ), and was positively regulated by Cs ARF 13 during reproductive organ development, indicating sequential interactions of Cs SPL with auxin signaling components in orchestrating anther and ovule development.