The perception of positional information for specification of lateral organ founder cells in the shoot apical meristem of Arabidopsis thaliana
Final Report Abstract
The "Arabidopsis thaliana" shoot apical meristem (SAM) is well characterized in terms of stem cell homeostasis in the central zone. Limited, however, is information how cells at the SAM periphery acquire new fates and dependent on positional information are recruited for new organs. Conceptually, a first step is the specification of lateral organ founder cells (LOFCs), which correlates with directional auxin transport and auxin perception maxima prior to visible organ initiation in the peripheral zone of the inflorescence meristem (IM). Expression of the DORNRÖSCHEN-LIKE (DRNL) transcription factor precedes auxin response maxima in the Arabidopsis inflorescence or floral meristem and the number of DRNL-transcribing cells correlates with established numbers of floral LOFCs. Within the project we aimed to verify DRNL transcription as LOFC-marker and asked for (i) promoter elements that perceives phyllotactic information within the IM peripheral zone, (ii) established differences in the chromatin or transcriptome in DRNL-positive cells using fluorescence assisted cell sorting (FACS), and (iii) analysed the fate of potential LOFCs in lateral organs. In summary, the analyses showed that enhancer 2 (En2) about 3 kb upstream of the DRNL transcription start plays a major role to perceive phyllotactic information in the IM. Its central 100-bp En2 core is highly conserved in Brassicaceae and cis-regulatory sequences including two core Auxin Response Elements (AuxREs) are densely clustered. According to the "Assay for Transposase-Accessible Chromatin using sequencing" (ATAC-seq) En2 resides in a chromatin region that is generally open in IM cells, but En2 gains hypersensitivity when the DRNL promoter is active in LOFCs. Sector analyses showed that DRNL-transcribing LOFCs that are specified in the SAM peripheral zone have a cell fate in distal, apical domains of leaves or floral organs. Complementary, transient expression of the diphtheria toxin A chain behind the DRNL promoter temporally arrests meristem function. The sector analyses and cell ablation experiments unequivocally confirm that DRNL promoter activity in small groups of cells in context of the SAM peripheral zone marks LOFCs; the perceiving cis-regulatory sequences for incoming phyllotactic signals is DRNL enhancer En2, a phylogenetically highly conserved promoter element in the Brassicaceae.
Publications
- (2014) Arabidopsis floral phytomer development: auxin response relative to biphasic modes of organ initiation. J Exp Bot. 65:3097-110
Chandler JW, Werr W
(See online at https://doi.org/10.1093/jxb/eru153) - (2015) Cytokinin-auxin crosstalk in cell type specification. Trends Plant Sci. 20:291-300
Chandler JW, Werr W
(See online at https://doi.org/10.1016/j.tplants.2015.02.003) - (2016) Founder-cell-specific transcription of the DORNRÖSCHEN-LIKE promoter and integration of the auxin response. J Exp Bot. 67:143-55
Comelli P, Glowa D, Chandler JW, Werr W
(See online at https://doi.org/10.1093/jxb/erv442) - (2016) The AP2-type transcription factors DORNRÖSCHEN and DORNRÖSCHEN-LIKE promote G1/S transition. Mol Genet Genomics 291:1835-49
Seeliger I, Frerichs A, Glowa D, Velo L, Comelli P, Chandler JW, Werr W
(See online at https://doi.org/10.1007/s00438-016-1224-x) - (2016) The founder-cell transcriptome in the Arabidopsis apetala1 cauliflower inflorescence meristem. BMC Genomics 17:855
Frerichs A, Thoma R, Abdallah AT, Frommolt P, Werr W, Chandler JW
(See online at https://doi.org/10.1186/s12864-016-3189-x) - (2017) DORNRÖSCHEN, DORNRÖSCHEN-LIKE, and PUCHI redundantly control floral meristem identity and organ initiation in Arabidopsis. J Exp Bot. 68:3457-3472
Chandler JW, Werr W.
(See online at https://doi.org/10.1093/jxb/erx208) - (2018) Spatiotemporal control of axillary meristem formation by interacting transcriptional regulators. Development 145 dev158352
Zhang C, Wang J, Wenkel S, Chandler JW, Werr W, Jiao Y
(See online at https://doi.org/10.1242/dev.158352) - (2019) A phylogenetically conserved APETALA2/ETHYLENE RESPONSE FACTOR, ERF12, regulates Arabidopsis floral development. Plant Mol Biol. 102: 39–54
Chandler JW, Werr W.
(See online at https://doi.org/10.1007/s11103-019-00936-5) - (2019) Specific chromatin changes mark lateral organ founder cells in the Arabidopsis inflorescence meristem. J Exp Bot. 70:3867-3879
Frerichs A, Engelhorn J, Altmüller J, Gutierrez-Marcos J, Werr W
(See online at https://doi.org/10.1093/jxb/erz181) - (2020) Functional dissection of the DORNRÖSCHEN-LIKE enhancer 2 during embryonic and phyllotactic patterning. Planta 251: 90
Comelli P, Glowa D, Frerichs A, Engelhorn J, Chandler JW & Werr W
(See online at https://doi.org/10.1007/s00425-020-03381-7)
