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.
The exon junction complex (EJC) plays important developmental roles in animals; however, its role in plants is not well known. Here, we show various aspects of the divergence of each duplicated MAGO NASHI (MAGO) and Y14 gene pair in rice (Oryza sativa) encoding the putative EJC core subunits that form the obligate MAGO-Y14 heterodimers. OsMAGO1, OsMAGO2, and OsY14a were constitutively expressed in all tissues, while OsY14b was predominantly expressed in embryonic tissues. OsMAGO2 and OsY14b were more sensitive to different stresses than OsMAGO1 and OsY14a, and their encoded protein pair shared 93.8% and 46.9% sequence identity, respectively. Single MAGO down-regulation in rice did not lead to any phenotypic variation; however, double gene knockdowns generated short rice plants with abnormal flowers, and the stamens of these flowers showed inhibited degradation and absorption of both endothecium and tapetum, suggesting that OsMAGO1 and OsMAGO2 were functionally redundant. OsY14a knockdowns phenocopied OsMAGO1OsMAGO2 mutants, while down-regulation of OsY14b failed to induce plantlets, suggesting the functional specialization of OsY14b in embryogenesis. OsMAGO1OsMAGO2OsY14a triple down-regulation enhanced the phenotypes of OsMAGO1OsMAGO2 and OsY14a down-regulated mutants, indicating that they exert developmental roles in the MAGO-Y14 heterodimerization mode. Modified gene expression was noted in the altered developmental pathways in these knockdowns, and the transcript splicing of UNDEVELOPED TAPETUM1 (OsUDT1), a key regulator in stamen development, was uniquely abnormal. Concomitantly, MAGO and Y14 selectively bound to the OsUDT1 premessenger RNA, suggesting that rice EJC subunits regulate splicing. Our work provides novel insights into the function of the EJC locus in growth, development, and reproduction in angiosperms and suggests a role for these genes in the adaptive evolution of cereals.
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