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      Ethylene promotes root hair growth through coordinated EIN3/EIL1 and RHD6/RSL1 activity in Arabidopsis

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          Significance

          Root hairs are unicellular extensions of root epidermal cells that help plants increase water and nutrient uptake and improve soil anchorage, both of which are crucial for the globally recognized goal of yield improvement with reduced fertilizer use. Previous studies have implicated numerous genes and phytohormones in the control of root hair development. This work uncovers the molecular mechanism of ethylene (ET)-promoted root hair growth and identifies a transcriptional complex consisting of EIN3/EIL1 and RHD6/RSL1 as the key regulator of root hair initiation and elongation. As ET mediates the effects of various root hair stimuli, this work also elucidates a convergent signaling network that integrates diverse environmental cues and intrinsic signals to modulate plant organ development.

          Abstract

          Root hairs are an extensive structure of root epidermal cells and are critical for nutrient acquisition, soil anchorage, and environmental interactions in sessile plants. The phytohormone ethylene (ET) promotes root hair growth and also mediates the effects of different signals that stimulate hair cell development. However, the molecular basis of ET-induced root hair growth remains poorly understood. Here, we show that ET-activated transcription factor ETHYLENE-INSENSITIVE 3 (EIN3) physically interacts with ROOT HAIR DEFECTIVE 6 (RHD6), a well-documented positive regulator of hair cells, and that the two factors directly coactivate the hair length-determining gene RHD6-LIKE 4 ( RSL4) to promote root hair elongation. Transcriptome analysis further revealed the parallel roles of the regulator pairs EIN3/EIL1 (EIN3-LIKE 1) and RHD6/RSL1 (RHD6-LIKE 1). EIN3/EIL1 and RHD6/RSL1 coordinately enhance root hair initiation by selectively regulating a subset of core root hair genes. Thus, our work reveals a key transcriptional complex consisting of EIN3/EIL1 and RHD6/RSL1 in the control of root hair initiation and elongation, and provides a molecular framework for the integration of environmental signals and intrinsic regulators in modulating plant organ development.

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          A high-resolution root spatiotemporal map reveals dominant expression patterns.

          Siobhan Brady, David Orlando, Ji-Young Lee … (2007)
          Transcriptional programs that regulate development are exquisitely controlled in space and time. Elucidating these programs that underlie development is essential to understanding the acquisition of cell and tissue identity. We present microarray expression profiles of a high-resolution set of developmental time points within a single Arabidopsis root and a comprehensive map of nearly all root cell types. These cell type-specific transcriptional signatures often predict previously unknown cellular functions. A computational pipeline identified dominant expression patterns that demonstrate transcriptional similarity between disparate cell types. Dominant expression patterns along the root's longitudinal axis do not strictly correlate with previously defined developmental zones, and in many cases, we observed expression fluctuation along this axis. Both robust co-regulation of gene expression and potential phasing of gene expression were identified between individual roots. Methods that combine these profiles demonstrate transcriptionally rich and complex programs that define Arabidopsis root development in both space and time.
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            TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.

            Anna N Stepanova, Joyce Robertson-Hoyt, Jeonga Yun … (2008)
            Plants have evolved a tremendous ability to respond to environmental changes by adapting their growth and development. The interaction between hormonal and developmental signals is a critical mechanism in the generation of this enormous plasticity. A good example is the response to the hormone ethylene that depends on tissue type, developmental stage, and environmental conditions. By characterizing the Arabidopsis wei8 mutant, we have found that a small family of genes mediates tissue-specific responses to ethylene. Biochemical studies revealed that WEI8 encodes a long-anticipated tryptophan aminotransferase, TAA1, in the essential, yet genetically uncharacterized, indole-3-pyruvic acid (IPA) branch of the auxin biosynthetic pathway. Analysis of TAA1 and its paralogues revealed a link between local auxin production, tissue-specific ethylene effects, and organ development. Thus, the IPA route of auxin production is key to generating robust auxin gradients in response to environmental and developmental cues.
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              Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis.

              Ziqiang Zhu, Fengying An, Ying Feng … (2011)
              Jasmonate (JA) and ethylene (ET) are two major plant hormones that synergistically regulate plant development and tolerance to necrotrophic fungi. Both JA and ET induce the expression of several pathogenesis-related genes, while blocking either signaling pathway abolishes the induction of these genes by JA and ET alone or in combination. However, the molecular basis of JA/ET coaction and signaling interdependency is largely unknown. Here, we report that two Arabidopsis ET-stabilized transcription factors (EIN3 and EIL1) integrate ET and JA signaling in the regulation of gene expression, root development, and necrotrophic pathogen defense. Further studies reveal that JA enhances the transcriptional activity of EIN3/EIL1 by removal of JA-Zim domain (JAZ) proteins, which physically interact with and repress EIN3/EIL1. In addition, we find that JAZ proteins recruit an RPD3-type histone deacetylase (HDA6) as a corepressor that modulates histone acetylation, represses EIN3/EIL1-dependent transcription, and inhibits JA signaling. Our studies identify EIN3/EIL1 as a key integration node whose activation requires both JA and ET signaling, and illustrate transcriptional derepression as a common mechanism to integrate diverse signaling pathways in the regulation of plant development and defense.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Proc Natl Acad Sci U S A
                Journal ID (iso-abbrev): Proc. Natl. Acad. Sci. U.S.A
                Journal ID (hwp): pnas
                Journal ID (pmc): pnas
                Journal ID (publisher-id): PNAS
                Title: Proceedings of the National Academy of Sciences of the United States of America
                Publisher: National Academy of Sciences
                ISSN (Print): 0027-8424
                ISSN (Electronic): 1091-6490
                Publication date (Print): 26 December 2017
                Publication date (Electronic): 12 December 2017
                Volume: 114
                Issue: 52
                Pages: 13834-13839
                Affiliations
                [1] aInstitute of Plant and Food Science, Department of Biology, Southern University of Science and Technology , Shenzhen, Guangdong 518055, China;
                [2] bThe State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University , Beijing 100871, China;
                [3] cCollege of Life Sciences, Nanjing Normal University , Nanjing 210023, China;
                [4] d Peking-Tsinghua Center of Life Sciences , Beijing 100871, China
                Author notes
                1To whom correspondence may be addressed. Email: wangyc@ 123456sustc.edu.cn or guohw@ 123456sustc.edu.cn .

                Edited by José M. Alonso, North Carolina State University, Raleigh, NC, and accepted by Editorial Board Member Joseph R. Ecker November 14, 2017 (received for review July 7, 2017)

                Author contributions: Y.F., Z.Z., and H.G. designed research; Y.F., P.X., P.L., X.W., Y.G., Y.X., and Y.W. performed research; X.W., F.A., and Y.W. contributed new reagents/analytic tools; Y.F. and B.L. analyzed data; and Y.F. and H.G. wrote the paper.

                Article
                Accession ID: PMC5748182 Pmcid ID: PMC5748182 Pmc-uid ID: 5748182 Publisher ID: 201711723
                DOI: 10.1073/pnas.1711723115
                PMC ID: 5748182
                PubMed ID: 29233944
                SO-VID: 2f463cf4-9f72-4e79-a8d8-60bf5f405222
                Copyright statement: Copyright @ 2017
                License:

                Published under the PNAS license.

                History
                Page count
                Pages: 6
                Categories
                Subject: Biological Sciences
                Subject: Plant Biology

                Keywords: ethylene,root hair,EIN3,RHD6,RSL4
                Data availability:
                Keywords: ethylene, root hair, EIN3, RHD6, RSL4

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