Heterotrimeric Gα-subunit functions in flower and fruit development via CLAVATA signaling pathway in cucumber

Abstract

Flowers and fruits are the reproductive organs in plants that play essential role in nature beauty and human diet. CLAVATA signaling has been well characterized to regulate floral organ development through modulating shoot apical meristem (SAM) size, however, the signaling molecules downstream of CLV pathway remain largely unknown in crops. Here, we found that functional disruption of CsCLV3 peptide and its receptor CsCLV1 both resulted in flowers with extra organs and stumpy fruits in cucumber. A heterotrimeric G protein α-subunit (CsGPA1) was identified to interact with CsCLV1. Csgpa1 mutant plants derived from gene-editing displayed significantly increased floral organ numbers, shorter and wider fruits, a phenotype resembling of Csclv mutants in cucumber. Moreover, the SAM size was enlarged, and longitudinal cell size of fruit was decreased in Csgpa1 mutants. The expression of the classical stem cell regulator WUSCHEL (WUS) was elevated in the SAM, while the expression of the fruit length stimulator CRABS CLAW (CRC) was reduced in the fruit of Csgpa1 mutants. Therefore, the Gα-subunit CsGPA1 protein interacts with CsCLV1 to inhibit floral organ numbers but promote fruit elongation, via repressing CsWUS expression and activating CsCRC transcription in cucumber. Our findings identified a new player in the CLV signaling pathway during flower and fruit development in dicot, so that enrich target genes for precise manipulation of fruit shape during crop breeding.