The bHLH transcription factor gene EGL3 accounts for the natural diversity in Arabidopsis fruit trichome pattern and morphology

Abstract

The number and distribution of trichomes, i.e., the trichome pattern, in different plant organs shows a conspicuous inter- and intraspecific diversity across Angiosperms that is presumably involved in adaptation to numerous environmental factors. The genetic and molecular mechanisms accounting for the evolution of trichome patterns have just begun to be elucidated. In this study, we aimed to identify and characterize MALAMBRUNO 1 (MAU1), a locus affecting trichome number in the fruits of Arabidopsis (Arabidopsis thaliana) natural populations. To this end, we developed introgression lines (ILs) from the hairy fruit accession Don-0 in the genetic background of the Ler strain with glabrous fruits. Genetic analyses of ILs showed that MAU1 affects fruit trichome patterns through synergistic epistasis with the MYB genes TRICHOMELESS1 (TCL1), GLABRA1 (GL1), and TRIPTYCHON (TRY). In addition, fine mapping and characterization of transgenic lines demonstrated that MAU1 is the bHLH transcription factor gene EGL3, for which Don-0 carries a gain-of-function semidominant allele. Gene expression analyses did not detect differences between EGL3 alleles, thus supporting that a structural missense mutation is the causal nucleotide polymorphism of Don-0. Further phylogenetic analyses of EGL3 showed that most Arabidopsis populations with hairy fruits belong to three haplogroups, suggesting that additional EGL3 natural alleles account for fruit trichome development. Finally, the characterization of EGL3 pleiotropy indicates that Don-0 hyperfunction also increases stem trichome branching. We conclude that EGL3 interactions in the core gene regulatory network of trichome development explain the Arabidopsis natural diversity for fruit trichome pattern and morphology.