A conserved gene regulatory network controls root epidermal cell patterning in superrosid species

Zhu, Yan; Schiefelbein, John

doi:10.1111/nph.18885

Title: A conserved gene regulatory network controls root epidermal cell patterning in superrosid species

Journal Article · 02 April 2023 · New Phytologist

DOI: https://doi.org/10.1111/nph.18885 · OSTI ID:1968062

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Department of Molecular, Cellular, and Developmental Biology University of Michigan Ann Arbor MI 48109 USA

Summary In superrosid species, root epidermal cells differentiate into root hair cells and nonhair cells. In some superrosids, the root hair cells and nonhair cells are distributed randomly (Type I pattern), and in others, they are arranged in a position‐dependent manner (Type III pattern). The model plant Arabidopsis ( Arabidopsis thaliana ) adopts the Type III pattern, and the gene regulatory network (GRN) that controls this pattern has been defined. However, it is unclear whether the Type III pattern in other species is controlled by a similar GRN as in Arabidopsis, and it is not known how the different patterns evolved. In this study, we analyzed superrosid species Rhodiola rosea , Boehmeria nivea , and Cucumis sativus for their root epidermal cell patterns. Combining phylogenetics, transcriptomics, and cross‐species complementation, we analyzed homologs of the Arabidopsis patterning genes from these species. We identified R. rosea and B. nivea as Type III species and C. sativus as Type I species. We discovered substantial similarities in structure, expression, and function of Arabidopsis patterning gene homologs in R. rosea and B. nivea , and major changes in C. sativus . We propose that in superrosids, diverse Type III species inherited the patterning GRN from a common ancestor, whereas Type I species arose by mutations in multiple lineages.

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Research Organization:: Stanford University, CA (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE

Grant/Contract Number:: SC0020358

OSTI ID:: 1968062

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 6 Vol. 238; ISSN 0028-646X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (72)

A Comparative Study of Developing Epidermal Cells in White Mustard and Tomato Roots Cormack, R. G. H. American Journal of Botany, Vol. 34, Issue 6 https://doi.org/10.1002/j.1537-2197.1947.tb12994.x	journal	June 1947
Trichoblasts in Hydrocharis. i. Origin. Differentiation, Dimensions and Growth Cutter, Elizabeth G.; Feldman, Lewis J. American Journal of Botany, Vol. 57, Issue 2 https://doi.org/10.1002/j.1537-2197.1970.tb09807.x	journal	February 1970
Patterning the primary root inArabidopsis Cederholm, Heidi M.; Iyer-Pascuzzi, Anjali S.; Benfey, Philip N. Wiley Interdisciplinary Reviews: Developmental Biology, Vol. 1, Issue 5 https://doi.org/10.1002/wdev.49	journal	March 2012
Epidermal Patterning in Seedling Roots of Eudicotyledons Pemberton, L. Annals of Botany, Vol. 87, Issue 5 https://doi.org/10.1006/anbo.2001.1385	journal	May 2001
The TTG Gene Is Required to Specify Epidermal Cell Fate and Cell Patterning in the Arabidopsis Root Galway, Moira E.; Masucci, James D.; Lloyd, Alan M. Developmental Biology, Vol. 166, Issue 2 https://doi.org/10.1006/dbio.1994.1352	journal	December 1994
Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology Estelle, Mark A.; Somerville, Chris Molecular and General Genetics MGG, Vol. 206, Issue 2 https://doi.org/10.1007/BF00333575	journal	February 1987
Über die Differenzierungsvorgänge in der Cruciferenwurzel Bünning, Erwin Planta, Vol. 39, Issue 2 https://doi.org/10.1007/BF01910114	journal	May 1951
ENHANCER of TRYand CPC 2(ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis Kirik, Victor; Simon, Marissa; Wester, Katja Plant Molecular Biology, Vol. 55, Issue 3 https://doi.org/10.1007/s11103-004-0893-8	journal	May 2004
WEREWOLF, a MYB-Related Protein in Arabidopsis, Is a Position-Dependent Regulator of Epidermal Cell Patterning Lee, Myeong Min; Schiefelbein, John Cell, Vol. 99, Issue 5 https://doi.org/10.1016/S0092-8674(00)81536-6	journal	November 1999
A Tissue-Mapped Axolotl De Novo Transcriptome Enables Identification of Limb Regeneration Factors Bryant, Donald M.; Johnson, Kimberly; DiTommaso, Tia Cell Reports, Vol. 18, Issue 3 https://doi.org/10.1016/j.celrep.2016.12.063	journal	January 2017
RSL Class I Genes Controlled the Development of Epidermal Structures in the Common Ancestor of Land Plants Proust, Hélène; Honkanen, Suvi; Jones, Victor A. S. Current Biology, Vol. 26, Issue 1 https://doi.org/10.1016/j.cub.2015.11.042	journal	January 2016
Identification of six CPC-like genes and their differential expression in leaves of tea plant, Camellia sinensis Wakamatsu, Juri; Wada, Takuji; Tanaka, Wakana Journal of Plant Physiology, Vol. 263 https://doi.org/10.1016/j.jplph.2021.153465	journal	August 2021
Floral organ identity: 20 years of ABCs Causier, Barry; Schwarz-Sommer, Zsuzsanna; Davies, Brendan Seminars in Cell & Developmental Biology, Vol. 21, Issue 1 https://doi.org/10.1016/j.semcdb.2009.10.005	journal	February 2010
The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis Kirik, Victor; Simon, Marissa; Huelskamp, Martin Developmental Biology, Vol. 268, Issue 2 https://doi.org/10.1016/j.ydbio.2003.12.037	journal	April 2004
The role of the SCRAMBLED receptor-like kinase in patterning the Arabidopsis root epidermis Kwak, Su-Hwan; Schiefelbein, John Developmental Biology, Vol. 302, Issue 1 https://doi.org/10.1016/j.ydbio.2006.09.009	journal	February 2007
Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning Simon, Marissa; Lee, Myeong Min; Lin, Yan Developmental Biology, Vol. 311, Issue 2 https://doi.org/10.1016/j.ydbio.2007.09.001	journal	November 2007
A mini binary vector series for plant transformation Xiang, Chengbin; Han, Peng; Lutziger, Isabelle Plant Molecular Biology, Vol. 40, Issue 4, p. 711-717 https://doi.org/10.1023/A:1006201910593	journal	January 1999
Full-length transcriptome assembly from RNA-Seq data without a reference genome Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran Nature Biotechnology, Vol. 29, Issue 7 https://doi.org/10.1038/nbt.1883	journal	May 2011
A basic helix-loop-helix transcription factor controls cell growth and size in root hairs Yi, Keke; Menand, Benoît; Bell, Elizabeth Nature Genetics, Vol. 42, Issue 3 https://doi.org/10.1038/ng.529	journal	February 2010
A fortunate choice: the history of Arabidopsis as a model plant Somerville, Chris; Koornneef, Maarten Nature Reviews Genetics, Vol. 3, Issue 11 https://doi.org/10.1038/nrg927	journal	November 2002
Site-specific phosphorylation of TRANSPARENT TESTA GLABRA1 mediates carbon partitioning in Arabidopsis seeds Li, Chengxiang; Zhang, Bin; Chen, Bin Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03013-5	journal	February 2018
Structural insights into partner selection for MYB and bHLH transcription factor complexes Wang, Baihui; Luo, Qiang; Li, Yingping Nature Plants, Vol. 8, Issue 9 https://doi.org/10.1038/s41477-022-01223-w	journal	August 2022
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Clough, Steven J.; Bent, Andrew F. The Plant Journal, Vol. 16, Issue 6, p. 735-743 https://doi.org/10.1046/j.1365-313x.1998.00343.x	journal	December 1998
Pattern in root meristem development in angiosperms Clowes, F. A. L. New Phytologist, Vol. 146, Issue 1 https://doi.org/10.1046/j.1469-8137.2000.00614.x	journal	April 2000
Network-based microsynteny analysis identifies major differences and genomic outliers in mammalian and angiosperm genomes Zhao, Tao; Schranz, M. Eric Proceedings of the National Academy of Sciences, Vol. 116, Issue 6 https://doi.org/10.1073/pnas.1801757116	journal	January 2019
Genetic and molecular analysis of trichome development in Arabis alpina Chopra, Divykriti; Mapar, Mona; Stephan, Lisa Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1819440116	journal	May 2019
A Single Amino Acid Substitution in IIIf Subfamily of Basic Helix-Loop-Helix Transcription Factor AtMYC1 Leads to Trichome and Root Hair Patterning Defects by Abolishing Its Interaction with Partner Proteins in Arabidopsis Zhao, Hongtao; Wang, Xiaoxue; Zhu, Dandan Journal of Biological Chemistry, Vol. 287, Issue 17 https://doi.org/10.1074/jbc.M111.280735	journal	April 2012
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference Kozlov, Alexey M.; Darriba, Diego; Flouri, Tomáš Bioinformatics, Vol. 35, Issue 21 https://doi.org/10.1093/bioinformatics/btz305	journal	May 2019
TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis Schellmann, S.; Schnittger, A.; Kirik, V. The EMBO Journal, Vol. 21, Issue 19 https://doi.org/10.1093/emboj/cdf524	journal	October 2002
rnaSPAdes: a de novo transcriptome assembler and its application to RNA-Seq data Bushmanova, Elena; Antipov, Dmitry; Lapidus, Alla GigaScience, Vol. 8, Issue 9 https://doi.org/10.1093/gigascience/giz100	journal	September 2019
Evolution and genetics of root hair stripes in the root epidermis Dolan, L.; Costa, S. Journal of Experimental Botany, Vol. 52, Issue suppl 1 https://doi.org/10.1093/jexbot/52.suppl_1.413	journal	March 2001
The HD-ZIP IV transcription factor GL2-LIKE regulates male flowering time and fertility in cucumber Cai, Yanling; Bartholomew, Ezra S.; Dong, Mingming Journal of Experimental Botany, Vol. 71, Issue 18 https://doi.org/10.1093/jxb/eraa251	journal	June 2020
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Regulation of CAPRICE Transcription by MYB Proteins for Root Epidermis Differentiation in Arabidopsis Koshino-Kimura, Yoshihiro; Wada, Takuji; Tachibana, Tatsuhiko Plant and Cell Physiology, Vol. 46, Issue 6 https://doi.org/10.1093/pcp/pci096	journal	June 2005
The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Rerie, W. G.; Feldmann, K. A.; Marks, M. D. Genes & Development, Vol. 8, Issue 12 https://doi.org/10.1101/gad.8.12.1388	journal	June 1994
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Isolation and Characterization of Mutants Defective in Seed Coat Mucilage Secretory Cell Development in Arabidopsis Western, Tamara L.; Burn, Joanne; Tan, Wei Ling Plant Physiology, Vol. 127, Issue 3 https://doi.org/10.1104/pp.010410	journal	November 2001
The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process Masucci, J. D.; Schiefelbein, J. W. Plant Physiology, Vol. 106, Issue 4 https://doi.org/10.1104/pp.106.4.1335	journal	December 1994
Cell Fate in the Arabidopsis Root Epidermis Is Determined by Competition between WEREWOLF and CAPRICE Song, Sang-Kee; Ryu, Kook Hui; Kang, Yeon Hee Plant Physiology, Vol. 157, Issue 3 https://doi.org/10.1104/pp.111.185785	journal	September 2011
Diversification of Root Hair Development Genes in Vascular Plants Huang, Ling; Shi, Xinhui; Wang, Wenjia Plant Physiology, Vol. 174, Issue 3 https://doi.org/10.1104/pp.17.00374	journal	May 2017
Cell Pattern in the Arabidopsis Root Epidermis Determined by Lateral Inhibition with Feedback Lee, Myeong Min; Schiefelbein, John The Plant Cell, Vol. 14, Issue 3 https://doi.org/10.1105/tpc.010434	journal	March 2002
The Arabidopsis Rab GTPase RabA4b Localizes to the Tips of Growing Root Hair Cells[W] Preuss, Mary L.; Serna, Jannie; Falbel, Tanya G. The Plant Cell, Vol. 16, Issue 6 https://doi.org/10.1105/tpc.021634	journal	June 2004
Functional Analysis of the Epidermal-Specific MYB GenesCAPRICEandWEREWOLFinArabidopsis Tominaga, Rumi; Iwata, Mineko; Okada, Kiyotaka The Plant Cell, Vol. 19, Issue 7 https://doi.org/10.1105/tpc.106.045732	journal	July 2007
Conserved Gene Expression Programs in Developing Roots from Diverse Plants Huang, Ling; Schiefelbein, John The Plant Cell, Vol. 27, Issue 8 https://doi.org/10.1105/tpc.15.00328	journal	August 2015
Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation Zhao, Tao; Holmer, Rens; de Bruijn, Suzanne The Plant Cell, Vol. 29, Issue 6 https://doi.org/10.1105/tpc.17.00312	journal	June 2017
A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants: Fluorescent organelle markers Nelson, Brook K.; Cai, Xue; Nebenführ, Andreas The Plant Journal, Vol. 51, Issue 6 https://doi.org/10.1111/j.1365-313X.2007.03212.x	journal	August 2007
Investigations on the Development of root Hairs Cormack, R. G. H. New Phytologist, Vol. 34, Issue 1 https://doi.org/10.1111/j.1469-8137.1935.tb06826.x	journal	February 1935
Root hair development involves asymmetric cell division in Brachypodium distachyon and symmetric division in Oryza sativa Kim, Chul Min; Dolan, Liam New Phytologist, Vol. 192, Issue 3 https://doi.org/10.1111/j.1469-8137.2011.03839.x	journal	August 2011
A protocol for combining fluorescent proteins with histological stains for diverse cell wall components Ursache, Robertas; Andersen, Tonni Grube; Marhavý, Peter The Plant Journal, Vol. 93, Issue 2 https://doi.org/10.1111/tpj.13784	journal	December 2017
Positional Signaling Mediated by a Receptor-like Kinase in Arabidopsis Kwak, S. -H. Science, Vol. 307, Issue 5712 https://doi.org/10.1126/science.1105373	journal	February 2005
An Ancient Mechanism Controls the Development of Cells with a Rooting Function in Land Plants Menand, B.; Yi, K.; Jouannic, S. Science, Vol. 316, Issue 5830 https://doi.org/10.1126/science.1142618	journal	June 2007
Epidermal Cell Differentiation in Arabidopsis Determined by a Myb Homolog, CPC Wada, Takuji; Tachibana, Tatsuhiko; Shimura, Yoshiro Science, Vol. 277, Issue 5329 https://doi.org/10.1126/science.277.5329.1113	journal	August 1997
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome Li, Bo; Dewey, Colin N. BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-323	journal	August 2011
Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis Wang, Shucai; Hubbard, Leah; Chang, Ying BMC Plant Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2229-8-81	journal	January 2008
Embryogenesis: Pattern Formation from a Single Cell Capron, Arnaud; Chatfield, Steven; Provart, Nicholas The Arabidopsis Book, Vol. 7 https://doi.org/10.1199/tab.0126	journal	January 2009
Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation Wada, T. Development, Vol. 129, Issue 23 https://doi.org/10.1242/dev.00111	journal	December 2002
The bHLH genes GLABRA3 (GL3) andENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root Bernhardt, C. Development, Vol. 130, Issue 26 https://doi.org/10.1242/dev.00880	journal	December 2003
The WEREWOLF MYB protein directly regulatesCAPRICEtranscription during cell fate specification in theArabidopsisroot epidermis Ryu, Kook Hui; Kang, Yeon Hee; Park, Young-hwan Development, Vol. 132, Issue 21 https://doi.org/10.1242/dev.02055	journal	November 2005
Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation Kurata, Tetsuya; Ishida, Tetsuya; Kawabata-Awai, Chie Development, Vol. 132, Issue 24 https://doi.org/10.1242/dev.02139	journal	December 2005
Cellular organisation of the Arabidopsis thaliana root Dolan, L.; Janmaat, K.; Willemsen, V. Development, Vol. 119, Issue 1 https://doi.org/10.1242/dev.119.1.71	journal	September 1993
The homeobox gene GLABRA 2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana Masucci, James D.; Rerie, William G.; Foreman, Daphne R. Development, Vol. 122, Issue 4 https://doi.org/10.1242/dev.122.4.1253	journal	April 1996
ClearSee: a rapid optical clearing reagent for whole-plant fluorescence imaging Kurihara, Daisuke; Mizuta, Yoko; Sato, Yoshikatsu Development https://doi.org/10.1242/dev.127613	journal	January 2015
A Gene Regulatory Network for Root Epidermis Cell Differentiation in Arabidopsis Bruex, Angela; Kainkaryam, Raghunandan M.; Wieckowski, Yana PLoS Genetics, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pgen.1002446	journal	January 2012
ROOT HAIR DEFECTIVE SIX-LIKE Class I Genes Promote Root Hair Development in the Grass Brachypodium distachyon Kim, Chul Min; Dolan, Liam PLOS Genetics, Vol. 12, Issue 8 https://doi.org/10.1371/journal.pgen.1006211	journal	August 2016
High-efficiency thermal asymmetric interlaced PCR for amplification of unknown flanking sequences Liu, Yao-Guang; Chen, Yuanling BioTechniques, Vol. 43, Issue 5 https://doi.org/10.2144/000112601	journal	November 2007
Evolutionary Analysis of MBW Function by Phenotypic Rescue in Arabidopsis thaliana Zhang, Bipei; Hülskamp, Martin Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00375	journal	March 2019
Patterning a Leaf by Establishing Polarities Manuela, Darren; Xu, Mingli Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.568730	journal	October 2020
TRANSPARENT TESTA GLABRA1, a Key Regulator in Plants with Multiple Roles and Multiple Function Mechanisms Tian, Hainan; Wang, Shucai International Journal of Molecular Sciences, Vol. 21, Issue 14 https://doi.org/10.3390/ijms21144881	journal	July 2020
Genes of the pig, Sus scrofa , reconstructed with EvidentialGene Gilbert, Donald G. PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6374	journal	January 2019

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59 BASIC BIOLOGICAL SCIENCES
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evolution
gene regulatory network
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Title: A conserved gene regulatory network controls root epidermal cell patterning in superrosid species

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