The euAP1 Protein MPF3 Represses MPF2 to Specify Floral Calyx Identity and Displays Crucial Roles in Chinese Lantern Development in Physalis

Abstract

ORCID IDs: 0000-0001-6984-228X (J.Z.); 0000-0002-2550-0170 (C.H.).The Chinese lantern phenotype or inflated calyx syndrome (ICS) is a postfloral morphological novelty in Physalis. Its origin is associated with the heterotopic expression of the MADS box gene 2 from Physalis floridana (MPF2) in floral organs, yet the process underlying its identity remains elusive. Here, we show that MPF3, which is expressed specifically in floral tissues, encodes a core eudicot APETALA1-like (euAP1) MADS-domain protein. MPF3 was primarily localized to the nucleus, and it interacted with MPF2 and some floral MADS-domain proteins to selectively bind the CC-A-rich-GG (CArG) boxes in the MPF2 promoter. Downregulating MPF3 resulted in a dramatic elevation in MPF2 in the calyces and androecium, leading to enlarged and leaf-like floral calyces; however, the postfloral lantern was smaller and deformed. Starch accumulation in pollen was blocked. MPF3 MPF2 double knockdowns showed normal floral calyces and more mature pollen than those found in plants in which either MPF3 or MPF2 was downregulated. Therefore, MPF3 specifies calyx identity and regulates ICS formation and male fertility through interactions with MPF2/MPF2. Furthermore, both genes were found to activate Physalis floridana invertase gene 4 homolog, which encodes an invertase cleaving Suc, a putative key gene in sugar partitioning. The novel role of the MPF3-MPF2 regulatory circuit in male fertility is integral to the origin of ICS. Our results shed light on the evolution and development of ICS in Physalis and on the functional evolution of euAP1s in angiosperms.

Deciphering the Physalis floridana Double-Layered-Lantern1 Mutant Provides Insights into Functional Divergence of the GLOBOSA Duplicates within the Solanaceae

“…Nonetheless, in these evolutionary processes, it is assumed that processes such as gene expression, protein-protein interactions, and regulation targets of the orthologous genes or the duplicated genes can be altered. These dynamic processes lead to subfunctionalization, neofunctionalization, or loss of genes, thus bringing about morphological innovation (Irish and Litt, 2005;Zhao et al, 2013). The "Chinese lantern," also called inflated calyx syndrome (ICS) in Physalis spp., is a morphological novelty within the Solanaceae ( Fig.…”

“…The trait is triggered by fertilization and is controlled by action of hormones Saedler, 2005, 2007). Furthermore, the molecular genetic basis underlying the origin of this novel trait has started to be empirically deciphered Saedler, 2005, 2007;Zhao et al, 2013). The MADS-box gene2 from Physalis floridana (MPF2) belongs to a small subfamily of the MADS-box genes (He and Saedler, 2005).…”

“…Heterotopic expression of MPF2 is key to the origin of ICS; the gene mainly controls ICS size Saedler, 2005, 2007). The second functionally characterized MADS-box protein associated with the development of ICS was MPF3 (encoded by MPF3, the MADS-box gene3 from Physalis floridana), the euAP1 ortholog of APETALA1 (AP1) in Arabidopsis (Arabidopsis thaliana), and SQUAMOSA (SQUA) in Antirrhinum majus Mandel et al, 1992;Zhao et al, 2013). MPF3 exerts its role in the development of ICS through the MPF3-MPF2/MPF2 interaction and regulatory circuit Zhao et al, 2013).…”

“…The second functionally characterized MADS-box protein associated with the development of ICS was MPF3 (encoded by MPF3, the MADS-box gene3 from Physalis floridana), the euAP1 ortholog of APETALA1 (AP1) in Arabidopsis (Arabidopsis thaliana), and SQUAMOSA (SQUA) in Antirrhinum majus Mandel et al, 1992;Zhao et al, 2013). MPF3 exerts its role in the development of ICS through the MPF3-MPF2/MPF2 interaction and regulatory circuit Zhao et al, 2013). Both MPF2 and MPF3 secure their new roles in male fertility through the evolution of novel genetic and physical interactions with the key components for male functionality, for example, the GLOBOSA (GLO) proteins (He and Saedler, 2005;Zhao et al, 2013).…”

Regulatory change at Physalis Organ Size 1 correlates to natural variation in tomatillo reproductive organ size

“…The genus Physalis features a fruiting calyx shaped like a Chinese lantern, also called the inflated calyx syndrome (ICS), a novelty of the floral calyx formed after fertilization that is controlled by several MADS-box transcription factors 19,21,22 . Unlike Solanum and Capsicum species, Physalis has distinguished fruit morphology owing to the accessory ICS trait.…”