The SEEL motif and members of the MYB-related REVEILLE transcription factor family are important for the expression of LORELEI in the synergid cells of the Arabidopsis female gametophyte

Noble, Jennifer A.; Seddon, Alex; Uygun, Sahra; Bright, Ashley; Smith, Steven E.; Shiu, Shin-han; Palanivelu, Ravishankar

doi:10.1007/s00497-021-00432-1

The SEEL motif and members of the MYB-related REVEILLE transcription factor family are important for the expression of LORELEI in the synergid cells of the Arabidopsis female gametophyte

Journal Article · Fri Oct 29 00:00:00 EDT 2021 · Plant Reproduction

DOI:https://doi.org/10.1007/s00497-021-00432-1· OSTI ID:1845902

Noble, Jennifer A. ^[1]; Seddon, Alex ^[2]; Uygun, Sahra ^[3]; Bright, Ashley ^[4]; Smith, Steven E. ^[4]; Shiu, Shin-han ^[2]; ^[4]

Univ. of Arizona, Tucson, AZ (United States); University of Arizona School of Plant Science
Michigan State Univ., East Lansing, MI (United States)
Agendia, Inc., Irvine, CA (United States)
Univ. of Arizona, Tucson, AZ (United States)

Synergid cells in the micropylar end of the female gametophyte are required for critical cell–cell signaling interactions between the pollen tube and the ovule that precede double fertilization and seed formation in flowering plants. LORELEI (LRE) encodes a putative GPI-anchored protein that is expressed primarily in the synergid cells, and together with FERONIA, a receptor-like kinase, it controls pollen tube reception by the receptive synergid cell. Still, how LRE expression is controlled in synergid cells remains poorly characterized. We identified candidate cis-regulatory elements enriched in LRE and other synergid cell-expressed genes. One of the candidate motifs (‘TAATATCT’) in the LRE promoter was an uncharacterized variant of the Evening Element motif that we named as the Short Evening Element-like (SEEL) motif. Deletion or point mutations in the SEEL motif of the LRE promoter resulted in decreased reporter expression in synergid cells, demonstrating that the SEEL motif is important for expression of LRE in synergid cells. Additionally, we found that LRE expression is decreased in the loss of function mutants of REVEILLE (RVE) transcription factors, which are clock genes known to bind the SEEL and other closely related motifs. Here, we propose that RVE transcription factors regulate LRE expression in synergid cells by binding to the SEEL motif in the LRE promoter. Identification of cis-regulatory elements and transcription factors involved in the expression of LRE will serve as a foundation to characterize the gene regulatory networks in synergid cells.

View Accepted Manuscript (DOE)

Research Organization:: Great Lakes Bioenergy Research Center, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0018409

OSTI ID:: 1845902

Journal Information:: Plant Reproduction, Journal Name: Plant Reproduction Journal Issue: 1 Vol. 35; ISSN 2194-7953

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (58)

A Calcium Dialog Mediated by the FERONIA Signal Transduction Pathway Controls Plant Sperm Delivery Ngo, Quy A.; Vogler, Hannes; Lituiev, Dmytro S. Developmental Cell, Vol. 29, Issue 4 https://doi.org/10.1016/j.devcel.2014.04.008	journal	May 2014
Female Control of Male Gamete Delivery during Fertilization in Arabidopsis thaliana Rotman, Nicolas; Rozier, Frédérique; Boavida, Leonor Current Biology, Vol. 13, Issue 5 https://doi.org/10.1016/s0960-9822(03)00093-9	journal	March 2003
Saccharomyces cerevisiae sec59 cells are deficient in dolichol kinase activity. Heller, L.; Orlean, P.; Adair, W. L. Proceedings of the National Academy of Sciences, Vol. 89, Issue 15 https://doi.org/10.1073/pnas.89.15.7013	journal	August 1992
TAMO: a flexible, object-oriented framework for analyzing transcriptional regulation using DNA-sequence motifs Gordon, D. B.; Nekludova, L.; McCallum, S. Bioinformatics, Vol. 21, Issue 14 https://doi.org/10.1093/bioinformatics/bti481	journal	May 2005
Unraveling Transcriptional Control in Arabidopsis Using cis-Regulatory Elements and Coexpression Networks Vandepoele, Klaas; Quimbaya, Mauricio; Casneuf, Tine Plant Physiology, Vol. 150, Issue 2 https://doi.org/10.1104/pp.109.136028	journal	April 2009
MYB98 Is Required for Pollen Tube Guidance and Synergid Cell Differentiation in Arabidopsis Kasahara, Ryushiro D.; Portereiko, Michael F.; Sandaklie-Nikolova, Linda The Plant Cell, Vol. 17, Issue 11 https://doi.org/10.1105/tpc.105.034603	journal	October 2005
MYB98 Positively Regulates a Battery of Synergid-Expressed Genes Encoding Filiform Apparatus–Localized Proteins Punwani, Jayson A.; Rabiger, David S.; Drews, Gary N. The Plant Cell, Vol. 19, Issue 8 https://doi.org/10.1105/tpc.107.052076	journal	August 2007
Maternal Control of Male-Gamete Delivery in Arabidopsis Involves a Putative GPI-Anchored Protein Encoded by the LORELEI Gene Capron, Arnaud; Gourgues, Mathieu; Neiva, Lissiene S. The Plant Cell, Vol. 20, Issue 11 https://doi.org/10.1105/tpc.108.061713	journal	November 2008
A role for LORELEI, a putative glycosylphosphatidylinositol-anchored protein, in Arabidopsis thaliana double fertilization and early seed development: LORELEI functions in fertilization and seed development Tsukamoto, Tatsuya; Qin, Yuan; Huang, Yiding The Plant Journal, Vol. 62, Issue 4 https://doi.org/10.1111/j.1365-313x.2010.04177.x	journal	February 2010
Tick Tock: Circadian Regulation of Plant Innate Immunity Lu, Hua; McClung, C. Robertson; Zhang, Chong Annual Review of Phytopathology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev-phyto-080516-035451	journal	August 2017
Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development Covington, Michael F.; Maloof, Julin N.; Straume, Marty Genome Biology, Vol. 9, Issue 8 https://doi.org/10.1186/gb-2008-9-8-r130	journal	January 2008
A Species-Specific Cluster of Defensin-Like Genes Encodes Diffusible Pollen Tube Attractants in Arabidopsis Takeuchi, Hidenori; Higashiyama, Tetsuya PLoS Biology, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pbio.1001449	journal	December 2012
Genome-Wide Expression Profiling of the Arabidopsis Female Gametophyte Identifies Families of Small, Secreted Proteins Jones-Rhoades, Matthew W.; Borevitz, Justin O.; Preuss, Daphne PLoS Genetics, Vol. 3, Issue 10 https://doi.org/10.1371/journal.pgen.0030171	journal	October 2007
Defensin-Like ZmES4 Mediates Pollen Tube Burst in Maize via Opening of the Potassium Channel KZM1 Amien, Suseno; Kliwer, Irina; Marton, Mihaela L. San Francisco : Public Library Science https://doi.org/10.15488/300	other	January 2010
Female Control of Male Gamete Delivery during Fertilization in Arabidopsis thaliana Rotman, Nicolas; Rozier, Frédérique; Boavida, Leonor Current Biology, Vol. 13, Issue 5 https://doi.org/10.1016/S0960-9822(03)00093-9	journal	March 2003
LHY and CCA1 Are Partially Redundant Genes Required to Maintain Circadian Rhythms in Arabidopsis Mizoguchi, Tsuyoshi; Wheatley, Kay; Hanzawa, Yoshie Developmental Cell, Vol. 2, Issue 5 https://doi.org/10.1016/S1534-5807(02)00170-3	journal	May 2002
Determination and Inference of Eukaryotic Transcription Factor Sequence Specificity Weirauch, Matthew T.; Yang, Ally; Albu, Mihai Cell, Vol. 158, Issue 6 https://doi.org/10.1016/j.cell.2014.08.009	journal	September 2014
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape O’Malley, Ronan C.; Huang, Shao-shan Carol; Song, Liang Cell, Vol. 166, Issue 6 https://doi.org/10.1016/j.cell.2016.08.063	journal	September 2016
Arabidopsis Female Gametophyte Gene Expression Map Reveals Similarities between Plant and Animal Gametes Wuest, Samuel E.; Vijverberg, Kitty; Schmidt, Anja Current Biology, Vol. 20, Issue 6 https://doi.org/10.1016/j.cub.2010.01.051	journal	March 2010
Maternal ENODLs Are Required for Pollen Tube Reception in Arabidopsis Hou, Yingnan; Guo, Xinyang; Cyprys, Philipp Current Biology, Vol. 26, Issue 17 https://doi.org/10.1016/j.cub.2016.06.053	journal	September 2016
LLG2/3 Are Co-receptors in BUPS/ANX-RALF Signaling to Regulate Arabidopsis Pollen Tube Integrity Ge, Zengxiang; Zhao, Yuling; Liu, Ming-Che Current Biology, Vol. 29, Issue 19 https://doi.org/10.1016/j.cub.2019.08.032	journal	October 2019
LORELEI-LIKE GPI-ANCHORED PROTEINS 2/3 Regulate Pollen Tube Growth as Chaperones and Coreceptors for ANXUR/BUPS Receptor Kinases in Arabidopsis Feng, Hanqian; Liu, Chen; Fu, Rong Molecular Plant, Vol. 12, Issue 12 https://doi.org/10.1016/j.molp.2019.09.004	journal	December 2019
Peptide/receptor-like kinase-mediated signaling involved in male–female interactions Zhong, Sheng; Qu, Li-Jia Current Opinion in Plant Biology, Vol. 51 https://doi.org/10.1016/j.pbi.2019.03.004	journal	October 2019
Wheels within wheels: the plant circadian system Hsu, Polly Yingshan; Harmer, Stacey L. Trends in Plant Science, Vol. 19, Issue 4 https://doi.org/10.1016/j.tplants.2013.11.007	journal	April 2014
Phytochrome B and REVEILLE1/2-mediated signalling controls seed dormancy and germination in Arabidopsis Jiang, Zhimin; Xu, Gang; Jing, Yanjun Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12377	journal	August 2016
Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis Duan, Qiaohong; Kita, Daniel; Johnson, Eric A. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4129	journal	January 2014
A gene expression map of Arabidopsis thaliana development Schmid, Markus; Davison, Timothy S.; Henz, Stefan R. Nature Genetics, Vol. 37, Issue 5 https://doi.org/10.1038/ng1543	journal	April 2005
Mechanisms of RALF peptide perception by a heterotypic receptor complex Xiao, Yu; Stegmann, Martin; Han, Zhifu Nature, Vol. 572, Issue 7768 https://doi.org/10.1038/s41586-019-1409-7	journal	July 2019
REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways Rawat, R.; Schwartz, J.; Jones, M. A. Proceedings of the National Academy of Sciences, Vol. 106, Issue 39 https://doi.org/10.1073/pnas.0813035106	journal	September 2009
Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana Zou, C.; Sun, K.; Mackaluso, J. D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 36 https://doi.org/10.1073/pnas.1103202108	journal	August 2011
DNA-binding specificities of plant transcription factors and their potential to define target genes Franco-Zorrilla, José M.; López-Vidriero, Irene; Carrasco, José L. Proceedings of the National Academy of Sciences, Vol. 111, Issue 6 https://doi.org/10.1073/pnas.1316278111	journal	January 2014
Multiple feedback loops of the Arabidopsis circadian clock provide rhythmic robustness across environmental conditions Shalit-Kaneh, Akiva; Kumimoto, Roderick W.; Filkov, Vladimir Proceedings of the National Academy of Sciences, Vol. 115, Issue 27 https://doi.org/10.1073/pnas.1805524115	journal	June 2018
affy--analysis of Affymetrix GeneChip data at the probe level Gautier, L.; Cope, L.; Bolstad, B. M. Bioinformatics, Vol. 20, Issue 3 https://doi.org/10.1093/bioinformatics/btg405	journal	February 2004
The Development of Protein Microarrays and Their Applications in DNA–Protein and Protein–Protein Interaction Analyses of Arabidopsis Transcription Factors Gong, Wei; He, Kun; Covington, Mike Molecular Plant, Vol. 1, Issue 1 https://doi.org/10.1093/mp/ssm009	journal	January 2008
Comparative Transcriptomics of Arabidopsis Sperm Cells Borges, Filipe; Gomes, Gabriela; Gardner, Rui Plant Physiology, Vol. 148, Issue 2 https://doi.org/10.1104/pp.108.125229	journal	July 2008
Distinct Gene Expression Profiles in Egg and Synergid Cells of Rice as Revealed by Cell Type-Specific Microarrays Ohnishi, Takayuki; Takanashi, Hideki; Mogi, Mirai Plant Physiology, Vol. 155, Issue 2 https://doi.org/10.1104/pp.110.167502	journal	November 2010
The REVEILLE Clock Genes Inhibit Growth of Juvenile and Adult Plants by Control of Cell Size Gray, Jennifer A.; Shalit-Kaneh, Akiva; Chu, Dalena Nhu Plant Physiology, Vol. 173, Issue 4 https://doi.org/10.1104/pp.17.00109	journal	March 2017
Arabidopsis LORELEI , a Maternally Expressed Imprinted Gene, Promotes Early Seed Development Wang, Yanbing; Tsukamoto, Tatsuya; Noble, Jennifer A. Plant Physiology, Vol. 175, Issue 2 https://doi.org/10.1104/pp.17.00427	journal	August 2017
Female Gametophyte Development Yadegari, R. THE PLANT CELL ONLINE, Vol. 16, Issue suppl_1 https://doi.org/10.1105/tpc.018192	journal	March 2004
Positive and Negative Factors Confer Phase-Specific Circadian Regulation of Transcription in Arabidopsis Harmer, Stacey L.; Kay, Steve A. The Plant Cell, Vol. 17, Issue 7 https://doi.org/10.1105/tpc.105.033035	journal	May 2005
Plant Circadian Rhythms McClung, C. Robertson The Plant Cell, Vol. 18, Issue 4 https://doi.org/10.1105/tpc.106.040980	journal	April 2006
The Role of LORELEI in Pollen Tube Reception at the Interface of the Synergid Cell and Pollen Tube Requires the Modified Eight-Cysteine Motif and the Receptor-Like Kinase FERONIA Liu, Xunliang; Castro, Claudia; Wang, Yanbing The Plant Cell, Vol. 28, Issue 5 https://doi.org/10.1105/tpc.15.00703	journal	April 2016
The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access Goda, Hideki; Sasaki, Eriko; Akiyama, Kenji The Plant Journal, Vol. 55, Issue 3 https://doi.org/10.1111/j.1365-313X.2008.03510.x	journal	August 2008
The MYB98 subcircuit of the synergid gene regulatory network includes genes directly and indirectly regulated by MYB98 Punwani, Jayson A.; Rabiger, David S.; Lloyd, Alan The Plant Journal, Vol. 55, Issue 3 https://doi.org/10.1111/j.1365-313X.2008.03514.x	journal	August 2008
A role for LORELEI, a putative glycosylphosphatidylinositol-anchored protein, in Arabidopsis thaliana double fertilization and early seed development: LORELEI functions in fertilization and seed development Tsukamoto, Tatsuya; Qin, Yuan; Huang, Yiding The Plant Journal, Vol. 62, Issue 4 https://doi.org/10.1111/j.1365-313X.2010.04177.x	journal	February 2010
Arabidopsis DOK1 encodes a functional dolichol kinase involved in reproduction Kanehara, Kazue; Cho, Yueh; Lin, Ying-Chen The Plant Journal, Vol. 81, Issue 2 https://doi.org/10.1111/tpj.12727	journal	December 2014
Reciprocal Regulation Between TOC1 and LHY/CCA1 Within the Arabidopsis Circadian Clock Alabadi, D. Science, Vol. 293, Issue 5531 https://doi.org/10.1126/science.1061320	journal	August 2001
The FERONIA Receptor-like Kinase Mediates Male-Female Interactions During Pollen Tube Reception Escobar-Restrepo, J. -M.; Huck, N.; Kessler, S. Science, Vol. 317, Issue 5838 https://doi.org/10.1126/science.1143562	journal	August 2007
Conserved Molecular Components for Pollen Tube Reception and Fungal Invasion Kessler, S. A.; Shimosato-Asano, H.; Keinath, N. F. Science, Vol. 330, Issue 6006 https://doi.org/10.1126/science.1195211	journal	November 2010
Orchestrated Transcription of Key Pathways in Arabidopsis by the Circadian Clock Harmer, S. L.; Hogenesch, J. B.; Straume, M. Science, Vol. 290, Issue 5499 https://doi.org/10.1126/science.290.5499.2110	journal	December 2000
A Fruitful Journey: Pollen Tube Navigation from Germination to Fertilization Johnson, Mark A.; Harper, Jeffrey F.; Palanivelu, Ravishankar Annual Review of Plant Biology, Vol. 70, Issue 1 https://doi.org/10.1146/annurev-arplant-050718-100133	journal	April 2019
Identification of transcription-factor genes expressed in the Arabidopsis female gametophyte Wang, Dongfang; Zhang, Changqing; Hearn, David J. BMC Plant Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2229-10-110	journal	June 2010
The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception Huck, N. Development, Vol. 130, Issue 10 https://doi.org/10.1242/dev.00458	journal	May 2003
TURAN and EVAN Mediate Pollen Tube Reception in Arabidopsis Synergids through Protein Glycosylation Lindner, Heike; Kessler, Sharon A.; Müller, Lena M. PLOS Biology, Vol. 13, Issue 4 https://doi.org/10.1371/journal.pbio.1002139	journal	April 2015
Penetration of the Stigma and Style Elicits a Novel Transcriptome in Pollen Tubes, Pointing to Genes Critical for Growth in a Pistil Qin, Yuan; Leydon, Alexander R.; Manziello, Ann PLoS Genetics, Vol. 5, Issue 8 https://doi.org/10.1371/journal.pgen.1000621	journal	August 2009
REVEILLE8 and PSEUDO-REPONSE REGULATOR5 Form a Negative Feedback Loop within the Arabidopsis Circadian Clock Rawat, Reetika; Takahashi, Nozomu; Hsu, Polly Yingshan PLoS Genetics, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pgen.1001350	journal	March 2011
Accurate timekeeping is controlled by a cycling activator in Arabidopsis Hsu, Polly Yingshan; Devisetty, Upendra K.; Harmer, Stacey L. eLife, Vol. 2 https://doi.org/10.7554/eLife.00473	journal	April 2013
Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis Li, Chao; Yeh, Fang-Ling; Cheung, Alice Y. eLife, Vol. 4 https://doi.org/10.7554/eLife.06587	journal	June 2015

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The SEEL motif and members of the MYB-related REVEILLE transcription factor family are important for the expression of LORELEI in the synergid cells of the Arabidopsis female gametophyte

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