Rose Breeding Selects More Total Floral Organs, a Trait Linked to CLAVATA3 Expression

Rose represents the most traded cut flowers worldwide with enormous diversity in floral organs, especially petal number, a target trait during modern rose breeding. With a detailed phenome analysis, we here report the high variation pattern in floral organ number among 132 rose lines, including wild species, traditional Chinese varieties, and modern lines. Seven wild species are single- or five-petaled flowers. Intriguingly, compared to traditional Chinese roses, modern lines feature more floral organs in the inner three whorls simultaneously (about 36% more total floral organs), a pattern that has not been identified previously. More floral organs correlate with the increase of flower meristem size, a pattern tightly controlled by the CLAVATA3 (CLV3) and its related molecular module in known model species. Within the vicinity of a known petal number QTL, in which polymorphism in APETALA2 (AP2) has been hypothesized to regulate the rose double flower trait, we identified the presence of CLV3, whose expression domain conversely correlates with total floral organ numbers in roses. Genetic alteration of CLV3 expression in both rose and Arabidopsis significantly altered the meristem size and the floral organ development and number. Exogenous application of rose CLV3-encoded CLAVATA3/EMBRYO SURROUNDING REGION-related (CLE) peptide led to reduced meristem size, accompanied by reduced root length in both rose and Arabidopsis plants. Collectively, our data suggest that, either alone or working potentially together with the AP2 variation, expression diversity in CLV3 may serve as an important factor regulating floral organ number diversity in roses. These findings thus provide fresh insights into the molecular mechanisms underlying the floral organ number trait in both roses and other ornamental plants.