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      Histone Deacetylase HDA6 Is Functionally Associated with AS1 in Repression of KNOX Genes in Arabidopsis

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          Abstract

          ASYMMETRIC LEAVES 1 (AS1) is a MYB-type transcription repressor that controls leaf development by regulating KNOX gene expression, but the underlying molecular mechanism is still unclear. In this study, we demonstrated that AS1 can interact with the histone deacetylase HDA6 in vitro and in vivo. The KNOX genes were up-regulated and hyperacetylated in the hda6 mutant, axe1-5, indicating that HDA6 may regulate KNOX expression through histone deacetylation. Compared with the single mutants, the as1-1/axe1-5 and as2-1/axe1-5 double mutants displayed more severe serrated leaf and short petiole phenotypes. In addition, the frequencies of leaf lobes and leaflet-like structures were also increased in as1-1/axe1-5 and as2-1/axe1-5 double mutants, suggesting that HDA6 acts together with AS1 and AS2 in regulating leaf development. Chromatin immunoprecipitation assays revealed that HDA6 and AS1 bound directly to KNAT1, KNAT2, and KNATM chromatin. Taken together, these data indicate that HDA6 is a part of the AS1 repressor complex to regulate the KNOX expression in leaf development.

          Author Summary

          AS1 is a MYB-type transcription repressor that controls leaf patterning by repressing class-1 KNOX gene expression. The molecular mechanism by which AS1 represses KNOX gene expression is still unclear. In this study, we found that AS1 interacted with the histone deacetylase HDA6. Furthermore, HDA6 repressed KNOX gene expression by histone deacetylation. hda6 mutants displayed serrated leaf and short petiole phenotypes. Additionally, hda6/as1-1 double-mutant plants showed a more severe phenotype compared to the single mutants, indicating that HDA6 may act together with AS1 in controlling leaf development. Taken together, our data indicated that HDA6 is an important component of the AS1 repressor complex in regulating the KNOX gene expression.

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          Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes.

          John Emery, Sandra K. Floyd, John Alvarez … (2003)
          Shoots of all land plants have a radial pattern that can be considered to have an adaxial (central)-abaxial (peripheral) polarity. In Arabidopsis, gain-of-function alleles of PHAVOLUTA and PHABULOSA, members of the class III HD-ZIP gene family, result in adaxialization of lateral organs. Conversely, loss-of-function alleles of the KANADI genes cause an adaxialization of lateral organs. Thus, the class III HD-ZIP and KANADI genes comprise a genetic system that patterns abaxial-adaxial polarity in lateral organs produced from the apical meristem. We show that gain-of-function alleles of REVOLUTA, another member of the class III HD-ZIP gene family, are characterized by adaxialized lateral organs and alterations in the radial patterning of vascular bundles in the stem. The gain-of-function phenotype can be obtained by changing only the REVOLUTA mRNA sequence and without changing the protein sequence; this finding indicates that this phenotype is likely mediated through an interference with microRNA binding. Loss of KANADI activity results in similar alterations in vascular patterning as compared to REVOLUTA gain-of-function alleles. Simultaneous loss-of-function of PHABULOSA, PHAVOLUTA, and REVOLUTA abaxializes cotyledons, abolishes the formation of the primary apical meristem, and in severe cases, eliminates bilateral symmetry; these phenotypes implicate these three genes in radial patterning of both embryonic and postembryonic growth. Based on complementary vascular and leaf phenotypes of class III HD-ZIP and KANADI mutants, we propose that a common genetic program dependent upon miRNAs governs adaxial-abaxial patterning of leaves and radial patterning of stems in the angiosperm shoot. This finding implies that a common patterning mechanism is shared between apical and vascular meristems.
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            A biochemical framework for RNA silencing in plants.

            Guiliang Tang, Brenda Reinhart, David Bartel … (2003)
            RNA silencing phenomena were first discovered in plants, yet only the RNA interference pathway in animals has been subject to biochemical analysis. Here, we extend biochemical analysis to plant RNA silencing. We find that standard wheat germ extract contains Dicer-like enzymes that convert double-stranded RNA (dsRNA) into two classes of small interfering RNAs, as well as an RNA-dependent RNA polymerase activity that can convert exogenous single-stranded RNA into dsRNA. In this plant embryo extract, an endogenous microRNA (miRNA) that lacks perfect complementarity to its RNA targets nonetheless acts as a small interfering RNA. The miRNA guides an endonuclease to cleave efficiently wild-type Arabidopsis PHAVOLUTA mRNA, but not a dominant mutant previously shown to perturb leaf development. This finding supports the view that plant miRNAs direct RNAi and that miRNA-specified mRNA destruction is important for proper plant development. Thus, endonuclease complexes guided by small RNAs are a common feature of RNA silencing in both animals and plants.
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              Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis.

              M Byrne, R Barley, L Curtis … (2015)
              Meristem function in plants requires both the maintenance of stem cells and the specification of founder cells from which lateral organs arise. Lateral organs are patterned along proximodistal, dorsoventral and mediolateral axes. Here we show that the Arabidopsis mutant asymmetric leaves1 (as1) disrupts this process. AS1 encodes a myb domain protein, closely related to PHANTASTICA in Antirrhinum and ROUGH SHEATH2 in maize, both of which negatively regulate knotted-class homeobox genes. AS1 negatively regulates the homeobox genes KNAT1 and KNAT2 and is, in turn, negatively regulated by the meristematic homeobox gene SHOOT MERISTEMLESS. This genetic pathway defines a mechanism for differentiating between stem cells and organ founder cells within the shoot apical meristem and demonstrates that genes expressed in organ primordia interact with meristematic genes to regulate shoot morphogenesis.
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                Author and article information

                Contributors
                Li-Jia Qu: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS Genet
                Journal ID (iso-abbrev): PLoS Genet
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosgen
                Title: PLoS Genetics
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Print): 1553-7390
                ISSN (Electronic): 1553-7404
                Publication date Collection: December 2012
                Publication date (Print): December 2012
                Publication date (Electronic): 13 December 2012
                Volume: 8
                Issue: 12
                Electronic Location Identifier: e1003114
                Affiliations
                [1 ]Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei, Taiwan
                [2 ]Key Laboratory of Plant Resources, Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China
                [3 ]University of Chinese Academy of Sciences, Chinese Academy of Sciences, Beijing, China
                [4 ]Southern Crop Protection and Food Research Centre, Agriculture and Agri-Food Canada, London, Ontario, Canada
                [5 ]Institute of Biochemistry, National Chung Hsing University, Taichung, Taiwan
                Peking University, China
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: ML C-WY F-FC KW. Performed the experiments: ML C-WY F-FC LZ GT. Analyzed the data: ML C-WY F-FC GT XL YC J-YY KW. Contributed reagents/materials/analysis tools: KW YC J-YY. Wrote the paper: ML C-WY KW.

                Article
                Publisher ID: PGENETICS-D-12-00973
                DOI: 10.1371/journal.pgen.1003114
                PMC ID: 3521718
                PubMed ID: 23271976
                SO-VID: 62412b23-867b-40a9-b184-cc3e948a7545
                Copyright statement: Copyright @ 2012
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 20 April 2012
                Date accepted : 10 October 2012
                Page count
                Pages: 10
                Funding
                This study was funded by grants from the National Science Council of Taiwan (101-2311-B-002-012-MY3 and 101-2923-B-002-005-MY3) and National Taiwan University (101R892005). Research in Guangzhou was supported by the National Basic Research Program of China (973 program number 2012CB910900) and grants from the National Natural Science Foundation of China (number 31200965 and number 31128001). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology
                Subject: Genetics
                Subject: Epigenetics
                Subject: Histone Modification
                Subject: Gene Expression
                Subject: Histone Modification
                Subject: Molecular Genetics
                Subject: Gene Regulation
                Subject: Gene Networks
                Subject: Plant Genetics
                Subject: Molecular Cell Biology
                Subject: Plant Science
                Subject: Plants
                Subject: Leafs
                Subject: Plant Genetics
                Subject: Plant Growth and Development

                ScienceOpen disciplines: Genetics
                Data availability:
                ScienceOpen disciplines: Genetics

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