Unique and overlapping functions for the transcriptional regulators KANADI1 and ULTRAPETALA1 in Arabidopsis gynoecium and stamen gene regulation

Authors: HAGELTHORN, LYNNE - University Of California Berkeley; MONFARED, MONA - University Of California Berkeley; TALO, ANTHONY - St Mary’s College; Harmon, Frank; Fletcher, Jennifer

Submitted to: Plant Direct
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/21/2023
Publication Date: 5/8/2023
Citation: Hagelthorn, L., Monfared, M.M., Talo, A., Harmon, F.G., Fletcher, J.C. 2023. Unique and overlapping functions for the transcriptional regulators KANADI1 and ULTRAPETALA1 in Arabidopsis gynoecium and stamen gene regulation. Plant Direct. 7(5). Article 7:e496. https://doi.org/10.1002/pld3.496.
DOI: https://doi.org/10.1002/pld3.496

Interpretive Summary: Unlike animals, plants form their male and female reproductive organs at maturity. The male organs, the stamens, make pollen that fertilizes the female organ, the gynoecium, and this process leads to the formation of fruits, seeds and grains that are the harvest of many crop plants. We previously showed that the ULTRAPETALA1 (ULT1) and KANADI1 (KAN1) factors work together to ensure that the gynoecium forms correctly prior to pollination; however, the genes that act downstream of ULT1 and KAN1 to pattern the gynoecium are largely unknown. Here we uncover several hundred genes in developing flowers that are regulated by ULT1, KAN1 or both factors together. We find that ULT1 and KAN1 regulate a number of genes that are expressed in the developing gynoecium, including a subset that are found only in the apical stigma tissue where the pollen lands. In addition, we show that ULT1 and KAN1 together induce several dozen genes that are expressed in stamens. These results suggest that ULT1 and KAN1 may be important for making stamens as well as gynoecia, providing new insight into the genes that control fruit and seed yield.

Technical Abstract: Plants generate their reproductive organs, the stamens and the carpels, de novo within the flowers that form when the plant reaches maturity. The carpels comprise the female reproductive organ, the gynoecium, a complex organ that develops along several axes of polarity and is crucial for plant reproduction, fruit formation and seed dispersal. The epigenetic trithorax group (trxG) protein ULTRAPETALA1 (ULT1) and the GARP domain transcription factor KANADI1 (KAN1) act cooperatively to regulate Arabidopsis thaliana gynoecium patterning along the apical-basal polarity axis; however, the molecular pathways through which this patterning activity is achieved are largely unknown. In this study we used transcriptomics to identify genome-wide ULT1 and KAN1 target genes during reproductive development. We discovered several hundred genes in developing flowers that are regulated by ULT1, KAN1 or both factors together. Genes involved in developmental and reproductive processes are over-represented among ULT1 and/or KAN1 target genes, along with genes involved in biotic or abiotic stress responses. Consistent with their function in regulating gynoecium patterning, a number of the downstream target genes are expressed in the developing gynoecium, including a unique subset restricted to the stigmatic tissue. Unexpectedly, we also uncovered a number of KAN1- and ULT1-induced genes that are transcribed predominantly or exclusively in developing stamens. These findings reveal a potential cooperative role for ULT1 and KAN1 in male as well as female reproductive development.