Category: Publications

REGULATION OF LEAF MATURATION BY CHROMATIN-MEDIATED MODULATION OF CYTOKININ RESPONSES

Citation:

Efroni, I, Han SK, Kim HJ, Wu MF, Steiner E, Birnbaum KD, Hong JC, Eshed Y, Wagner D.  2013.  Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses, Feb 25. Dev Cell. 24:438-45., Number 4

Abstract:

Plant shoots display indeterminate growth, while their evolutionary decedents, the leaves, are determinate. Determinate leaf growth is conditioned by the CIN-TCP transcription factors, which promote leaf maturation and are negatively regulated by miR319 in leaf primordia. Here we show that CIN-TCPs reduce leaf sensitivity to cytokinin (CK), a phytohormone implicated in inhibition of differentiation in the shoot. We identify the SWI/SNF chromatin remodeling ATPase BRAHMA (BRM) as a genetic mediator of CIN-TCP activities and CK responses. An interactome screen further revealed that SWI/SNF complex components including BRM preferentially interacted with basic-helix-loop-helix (bHLH) transcription factors and the bHLH-related CIN-TCPs. Indeed, TCP4 and BRM interacted in planta. Both TCP4 and BRM bound the promoter of an inhibitor of CK responses, ARR16, and induced its expression. Reconstituting ARR16 levels in leaves with reduced CIN-TCP activity restored normal growth. Thus, CIN-TCP and BRM together promote determinate leaf growth by stage-specific modification of CK responses.

Notes:

Efroni, IdanHan, Soon-KiKim, Hye JinWu, Miin-FengSteiner, EvyatarBirnbaum, Kenneth DHong, Jong ChanEshed, YuvalWagner, DorisDev Cell. 2013 Feb 25;24(4):438-45. doi: 10.1016/j.devcel.2013.01.019.

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THE SWI2/SNF2 CHROMATIN REMODELING ATPASE BRAHMA REPRESSES ABSCISIC ACID RESPONSES IN THE ABSENCE OF THE STRESS STIMULUS IN ARABIDOPSIS

Citation:

Han, SK, Sang Y, Rodrigues A, Wu MF, Rodriguez PL, Wagner D.  2012.  The SWI2/SNF2 chromatin remodeling ATPase BRAHMA represses abscisic acid responses in the absence of the stress stimulus in Arabidopsis, Dec. The Plant cell. 24:4892-906., Number 12

Abstract:

The survival of plants as sessile organisms depends on their ability to cope with environmental challenges. Of key importance in this regard is the phytohormone abscisic acid (ABA). ABA not only promotes seed dormancy but also triggers growth arrest in postgermination embryos that encounter water stress. This is accompanied by increased desiccation tolerance. Postgermination ABA responses in Arabidopsis thaliana are mediated in large part by the ABA-induced basic domain/leucine zipper transcription factor ABA INSENSITIVE5 (ABI5). Here, we show that loss of function of the SWI2/SNF2 chromatin remodeling ATPase BRAHMA (BRM) causes ABA hypersensitivity during postgermination growth arrest. ABI5 expression was derepressed in brm mutants in the absence of exogenous ABA and accumulated to high levels upon ABA sensing. This effect was likely direct; chromatin immunoprecipitation revealed BRM binding to the ABI5 locus. Moreover, loss of BRM activity led to destabilization of a nucleosome likely to repress ABI5 transcription. Finally, the abi5 null mutant was epistatic to BRM in postgermination growth arrest. In addition, vegetative growth defects typical of brm mutants in the absence of ABA treatment could be partially overcome by reduction of ABA responses, and brm mutants displayed increased drought tolerance. We propose a role for BRM in the balance between growth or stress responses.

Notes:

Han, Soon-KiSang, YiRodrigues, AmericoBIOL425 F2010Wu, Miin-FengRodriguez, Pedro LWagner, DorisR01 GM064650/GM/NIGMS NIH HHS/R01 GM64650-01/GM/NIGMS NIH HHS/Plant Cell. 2012 Dec;24(12):4892-906. doi: 10.1105/tpc.112.105114. Epub 2012 Dec 3.

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MUTATIONS IN TWO NON-CANONICAL ARABIDOPSIS SWI2/SNF2 CHROMATIN REMODELING ATPASES CAUSE EMBRYOGENESIS AND STEM CELL MAINTENANCE DEFECTS

Citation:

Sang, Y, Silva-Ortega CO, Wu S, Yamaguchi N, Wu MF, Pfluger J, Gillmor CS, Gallagher KL, Wagner D.  2012.  Mutations in two non-canonical Arabidopsis SWI2/SNF2 chromatin remodeling ATPases cause embryogenesis and stem cell maintenance defects, Oct 13. The Plant journal : for cell and molecular biology.

Abstract:

SWI2/SNF2 chromatin remodeling ATPases play important roles in plant and metazoan development. Whereas metazoans generally encode one or two SWI2/SNF2 ATPase genes, Arabidopsis encodes four such chromatin regulators: the well-studied BRAHMA and SPLAYED ATPases, as well as two closely related non-canonical SWI2/SNF2 ATPases, CHR12 and CHR23. No developmental role has as yet been described for CHR12 and CHR23. Here, we show that although strong single chr12 or chr23 mutants are morphologically indistinguishable from the wild type, chr12 chr23 double mutants cause embryonic lethality. The double mutant embryos fail to initiate root and shoot meristems, and display few and aberrant cell divisions. Weak double mutant embryos give rise to viable seedlings with dramatic defects in the maintenance of both the shoot and the root stem cell populations. Paradoxically, the stem cell defects are correlated with increased expression of the stem cell markers WUSCHEL and WOX5. During subsequent development, the meristem defects are partially overcome to allow for the formation of very small, bushy adult plants. Based on the observed morphological defects, we named the two chromatin remodelers MINUSCULE 1 and 2. Possible links between minu1 minu2 defects and defects in hormone signaling and replication-coupled chromatin assembly are discussed.

Notes:

Sang, YiSilva-Ortega, Claudia OWu, ShuangYamaguchi, NobutoshiWu, Miin-FengPfluger, JenniferGillmor, C StewartGallagher, Kimberly LWagner, DorisPlant J. 2012 Oct 13. doi: 10.1111/tpj.12009.

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READING THE SECOND CODE: MAPPING EPIGENOMES TO UNDERSTAND PLANT GROWTH, DEVELOPMENT, AND ADAPTATION TO THE ENVIRONMENT

Citation:

EPIC, Planning, Committee.  2012.  Reading the Second Code: Mapping Epigenomes to Understand Plant Growth, Development, and Adaptation to the Environment. Plant Cell. 24(6), 2257-2261.

Abstract:

We have entered a new era in agricultural and biomedical science made possible by remarkable advances in DNA sequencing technologies. The complete sequence of an individual’s set of chromosomes (collectively, its genome) provides a primary genetic code for what makes that individual unique, just as the contents of every personal computer reflect the unique attributes of its owner. But a second code, composed of “epigenetic” layers of information, affects the accessibility of the stored information and the execution of specific tasks. Nature’s second code is enigmatic and must be deciphered if we are to fully understand and optimize the genetic potential of crop plants. The goal of the Epigenomics of Plants International Consortium is to crack this second code, and ultimately master its control, to help catalyze a new green revolution.

Notes:

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RNA IN SITU HYBRIDIZATION IN ARABIDOPSIS

Citation:

Wu, MF, Wagner D.  2012.  RNA in situ hybridization in Arabidopsis. Methods in molecular biology. 883:75-86.

Abstract:

RNA in situ hybridization using digoxigenin-labeled riboprobes on tissue sections is a powerful technique for revealing microscopic spatial gene expression. Here, we describe an in situ hybridization method commonly practiced in Arabidopsis research labs. The highly stringent hybridization condition eliminates the usage of Ribonlucease A and gives highly specific signals. This also allows the use of longer probes which enhance signal strength without cross hybridization to closely related genes. In addition, using spin columns in template and riboprobe purification greatly reduces background signals.

Notes:

Wu, Miin-FengWagner, DorisClifton, N.J.Methods Mol Biol. 2012;883:75-86. doi: 10.1007/978-1-61779-839-9_5.

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LEAFY CONTROLS ARABIDOPSIS PEDICEL LENGTH AND ORIENTATION BY AFFECTING ADAXIAL-ABAXIAL CELL FATE

Citation:

Yamaguchi, N, Yamaguchi A, Abe M, Wagner D, Komeda Y.  2012.  LEAFY controls Arabidopsis pedicel length and orientation by affecting adaxial-abaxial cell fate, Mar. The Plant journal : for cell and molecular biology. 69:844-56., Number 5

Abstract:

Pedicel length and orientation (angle) contribute to the diversity of inflorescence architecture, and are important for optimal positioning of the flowers. However, relatively little is known about pedicel development. We previously described the Arabidopsis CORYMBOSA1 (CRM1)/BIG gene, which affects inflorescence architecture by controlling pedicel elongation and orientation. Here, we performed a suppressor screen using the partial loss-of-function allele crm1-13 to identify genes and pathways that affect pedicel development. We identified a hypomorph allele of the meristem identity regulator LEAFY (LFY) as the suppressor. Consistent with this, crm1 pedicels had elevated LFY levels and conditional gain of LFY function produced downward-bending pedicels. Steroid activation of 35S:LFY-GR plants caused a reduction in the cortical cell length in the abaxial domain and additional defects associated with adaxialization. Further analyses of loss of LFY function revealed that LFY is required for reduced cortical cell elongation at the adaxial side of the pedicel base. Defects in conditional LFY gain-of-function pedicels were correlated with decreased BREVIPEDICELLUS (BP) expression, while ASYMMETRIC LEAVES2 (AS2), a transcriptional repressor of BP, and REVOLUTA, a promoter of adaxial cell fate, were highly and ectopically expressed in LFY gain-of-function pedicels. LFY bound to cis-regulatory regions upstream of AS2, and as2 mutations partially suppressed the pedicel length and orientation defects caused by increased LFY activity. These data suggest that LFY activity promotes adaxial cell fate and hence the proper orientation and length of the pedicel partly by directly activating AS2 expression, which suppresses BP expression.

Notes:

Yamaguchi, NobutoshiYamaguchi, AyakoAbe, MitsutomoWagner, DorisKomeda, YoshibumiEnglandPlant J. 2012 Mar;69(5):844-56. doi: 10.1111/j.1365-313X.2011.04836.x. Epub 2011 Dec 16.

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SWI2/SNF2 CHROMATIN REMODELING ATPASES OVERCOME POLYCOMB REPRESSION AND CONTROL FLORAL ORGAN IDENTITY WITH THE LEAFY AND SEPALLATA3 TRANSCRIPTION FACTORS

Citation:

Wu, MF, Sang Y, Bezhani S, Yamaguchi N, Han SK, Li Z, Su Y, Slewinski TL, Wagner D.  2012.  SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors, Feb 28. Proceedings of the National Academy of Sciences of the United States of America. 109:3576-81., Number 9

Abstract:

Patterning of the floral organs is exquisitely controlled and executed by four classes of homeotic regulators. Among these, the class B and class C floral homeotic regulators are of central importance as they specify the male and female reproductive organs. Inappropriate induction of the class B gene APETALA3 (AP3) and the class C gene AGAMOUS (AG) causes reduced reproductive fitness and is prevented by polycomb repression. At the onset of flower patterning, polycomb repression needs to be overcome to allow induction of AP3 and AG and formation of the reproductive organs. We show that the SWI2/SNF2 chromatin-remodeling ATPases SPLAYED (SYD) and BRAHMA (BRM) are redundantly required for flower patterning and for the activation of AP3 and AG. The SWI2/SNF2 ATPases are recruited to the regulatory regions of AP3 and AG during flower development and physically interact with two direct transcriptional activators of class B and class C gene expression, LEAFY (LFY) and SEPALLATA3 (SEP3). SYD and LFY association with the AP3 and AG regulatory loci peaks at the same time during flower patterning, and SYD binding to these loci is compromised in lfy and lfy sep3 mutants. This suggests a mechanism for SWI2/SNF2 ATPase recruitment to these loci at the right stage and in the correct cells. SYD and BRM act as trithorax proteins, and the requirement for SYD and BRM in flower patterning can be overcome by partial loss of polycomb activity in curly leaf (clf) mutants, implicating the SWI2/SNF2 chromatin remodelers in reversal of polycomb repression.

Notes:

Wu, Miin-FengSang, YiBezhani, StaverYamaguchi, NobutoshiHan, Soon-KiLi, ZhentengSu, YanhuiSlewinski, Thomas LWagner, DorisProc Natl Acad Sci U S A. 2012 Feb 28;109(9):3576-81. doi: 10.1073/pnas.1113409109. Epub 2012 Feb 9.

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SWITCHING ON FLOWERS: TRANSIENT LEAFY INDUCTION REVEALS NOVEL ASPECTS OF FLOWER DEVELOPMENT IN ARABIDOPSIS

Citation:

Wagner, D, Meyerowitz E.  2011.  Switching on flowers: transient LEAFY induction reveals novel aspects of flower development in Arabidopsis. Frontiers in Plant Science. 2, Number 80

Abstract:

Developmental fate decisions in cell populations fundamentally depend on at least two parameters: a signal that is perceived by the cell and the intrinsic ability of the cell to respond to the signal. The same regulatory logic holds for phase transitions in the life cycle of an organism, for example the switch to reproductive development in flowering plants. Here we have tested the response of the monocarpic plant species Arabidopsis thaliana to a signal that directs flower formation, the plant-specific transcription factor LEAFY (LFY). Using transient steroid-dependent LEAFY (LFY) activation in lfy null mutant Arabidopsis plants, we show that the plant’s competence to respond to the LFY signal changes during development. Very early in the life cycle, the plant is not competent to respond to the signal. Subsequently, transient LFY activation can direct primordia at the flanks of the shoot apical meristem to adopt a floral fate. Finally, the plants acquire competence to initiate the flower-patterning program in response to transient LFY activation. Similar to a perennial life strategy, we did not observe reprogramming of all primordia after perception of the transient signal, instead only a small number of meristems responded, followed by reversion to the prior developmental program. The ability to initiate flower formation and to direct flower patterning in response to transient LFY upregulation was dependent on the known direct LFY target APETALA1 (AP1). Prolonged LFY or activation could alter the developmental gradient and bypass the requirement for AP1. Prolonged high AP1 levels, in turn, can also alter the plants’ competence. Our findings shed light on how plants can fine-tune important phase transitions and developmental responses.

Keywords: LEAFY, flower development, reproductive competence

Notes:

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LATE MERISTEM IDENTITY2 ACTS TOGETHER WITH LEAFY TO ACTIVATE APETALA1

Citation:

Pastore, JJ, Limpuangthip A, Yamaguchi N, Wu MF, Sang Y, Han SK, Malaspina L, Chavdaroff N, Yamaguchi A, Wagner D.  2011.  LATE MERISTEM IDENTITY2 acts together with LEAFY to activate APETALA1, Aug. Development. 138:3189-98., Number 15

Abstract:

The switch from producing vegetative structures (branches and leaves) to producing reproductive structures (flowers) is a crucial developmental transition that significantly affects the reproductive success of flowering plants. In Arabidopsis, this transition is in large part controlled by the meristem identity regulator LEAFY (LFY). The molecular mechanisms by which LFY orchestrates a precise and robust switch to flower formation is not well understood. Here, we show that the direct LFY target LATE MERISTEM IDENTITY2 (LMI2) has a role in the meristem identity transition. Like LFY, LMI2 activates AP1 directly; moreover, LMI2 and LFY interact physically. LFY, LMI2 and AP1 are connected in a feed-forward and positive feedback loop network. We propose that these intricate regulatory interactions not only direct the precision of this crucial developmental transition in rapidly changing environmental conditions, but also contribute to its robustness and irreversibility.

Notes:

Pastore, Jennifer JLimpuangthip, AndreaYamaguchi, NobutoshiWu, Miin-FengSang, YiHan, Soon-KiMalaspina, LaurenChavdaroff, NatashaYamaguchi, AyakoWagner, Doris5-T32-HD007516/HD/NICHD NIH HHS/EnglandCambridge, EnglandDevelopment. 2011 Aug;138(15):3189-98.