Developmental Genetics of Corolla Tube Formation: Role of the tasiRNA-ARF Pathway and a Conceptual Model

Abstract

Over 80,000 angiosperm species produce flowers with petals fused into a corolla tube. The corolla tube contributes to the tremendous diversity of flower morphology and plays a critical role in plant reproduction, yet it remains one of the least understood plant structures from a developmental genetics perspective. Through mutant analyses and transgenic experiments, we show that the tasiRNA-ARF pathway is required for corolla tube formation in the monkeyflower species Mimulus lewisii. Loss-of-function mutations in the M. lewisii orthologs of ARGONAUTE7 and SUPPRESSOR OF GENE SILENCING3 cause a dramatic decrease in abundance of TAS3-derived small RNAs and a moderate upregulation of AUXIN RESPONSE FACTOR3 (ARF3) and ARF4, which lead to inhibition of lateral expansion of the bases of petal primordia and complete arrest of the upward growth of the interprimordial regions, resulting in unfused corollas. Using the DR5 auxin-responsive promoter, we discovered that auxin signaling is continuous along the petal primordium base and the interprimordial region during the critical stage of corolla tube formation in the wild type, similar to the spatial pattern of MlARF4 expression. Auxin response is much weaker and more restricted in the mutant. Furthermore, exogenous application of a polar auxin transport inhibitor to wild-type floral apices disrupted petal fusion. Together, these results suggest a new conceptual model highlighting the central role of auxin-directed synchronized growth of the petal primordium base and the interprimordial region in corolla tube formation.

Comparative analysis of corolla tube development across three closely related Mimulus species with different pollination syndromes

“…The M. lewisii species complex is emerging as a powerful model system to study the developmental genetics and evodevo of pollinator-associated floral traits (Yuan, 2019), including the formation and elaboration of corolla tubes (Ding et al, 2017(Ding et al, , 2020). Yet, little is known about the developmental dynamics of corolla tube growth in these species.…”

Floral Development Stage-Specific Transcriptomic Analysis Reveals the Formation Mechanism of Different Shapes of Ray Florets in Chrysanthemum

“…In addition, ARFs are the core transcription factors of auxin signal transduction and also affect the development process of petals. In Mimulus lewisii , the up-regulation of MlARF3 and MlARF4 resulted in unfused corollas [ 51 ]. Meanwhile, the study on the Asteraceae plant Matricaria recutita found that auxin affected the initiation of ray florets [ 24 ].…”

CYCLOIDEA paralogs function partially redundantly to specify dorsal flower development in Mimulus lewisii

“…Stable plant transformation tools are available to dissect the function of duplicate HCL‐ CYC2 lineage genes in only a few HCL species— Torenia fournieri (Linderniaceae; Su et al, 2017) and species of Mimulus (Yuan et al, 2013; Ding, Patterson, et al, 2020; Ding, Xia, et al, 2020). While Torenia fournieri appears to have lost the HCL‐ CYC2A paralog (Su et al 2017), HCL‐ CYC2A and HCL‐ CYC2B paralogs are retained in the Mimulus lineage (Preston et al, 2014; Zhong et al, 2017) making Mimulus an excellent system to investigate the fate of duplicated HCL‐ CYC2 lineage paralogs.…”