Transcriptional Regulation in Plants

Rhiannon K Macrae, The Salk Institute for Biological Studies, La Jolla, California, USA
Jeffrey A Long, The Salk Institute for Biological Studies, La Jolla, California, USA

Published online: May 2012

DOI: 10.1002/9780470015902.a0023755

Transcriptional regulation encompasses all of the events leading up to a change in gene expression status, either activation or repression. Although many of the mechanisms of transcriptional regulation are shared between plants and animals, plants are distinctly different in that they rely more heavily on subtle environmental cues than animals do because they are sessile, and they continue to develop new organs post‐embryonically. These unusual features require constant refinement at the transcriptional level to implement large‐scale gene expression changes. Many signalling pathways converge at the level of transcription in plants, including hormone‐response pathways and light‐response pathways, forming complex gene regulatory networks and intricate feed‐back loops to control the growth and development of plants. Additionally, alterations to the chromatin such as deoxyribonucleic acid (DNA) methylation and histone modifications can also affect transcriptional regulation and even lead to the formation of epialleles and genomic imprinting.

Key Concepts:

  • Transcriptional regulation in plants relies on many of the same mechanisms as transcriptional regulation in animals but with subtle variations.
  • Plant hormones, such as auxin, play a major instructive role in gene expression.
  • Because plants are sessile organisms, environmental cues (e.g. quality and quantity of light) are critical for regulating transcription and affect the timing of developmental decisions.
  • DNA and histone methylation can alter gene expression and contributes to the formation of heritable epialleles and imprinting.

Keywords: Transcriptional regulation; gene regulatory networks; epigenetics; feed‐back loop; Arabidopsis

Figure 1. Life cycle of Arabidopsis, from embryogenesis to the next generation. (a) Heart‐stage embryo. Green shading indicates developing shoot tissue, blue shading marks root apical meristem. (b) Seedling stage. (c) Adult stage. (d) Developing embryo within the seed (adapted from http://seedgenenetwork.net/).
Figure 2. Auxin gradients instruct apical/basal patterning during embryogenesis. (a) Auxin (pink) flow and maxima are established in the embryo by the PIN efflux proteins. These levels are interpreted by the plant at the level of transcription. (b) Hypothetical model for PLETHORA (PLT1/2) gene activation. PLT1/2, master regulators of root fate, are activated in the root apical meristem (RAM), where auxin levels are high, in an auxin response factor (ARF)‐dependent manner, although direct binding of ARF to the promoter has not been reported. Auxin binds to TIR1, which in turn binds to the ARF binding partner, IAA, and targets IAA for degradation via the 26S proteasome. In the shoot apical meristem (SAM), an area of low auxin concentration, PLT1/2 are repressed through the concerted action of an IAA transcription factor that binds to and prevents the ARF from activating transcription as well as recruits the corepressor TPL.
Figure 3. The shoot apical meristem (SAM) is a stem cell niche regulated by a transcriptional feed‐back circuit that spatially controls CLAVATA1 (CLV1), CLAVATA2 (CLV2) and WUSCHEL (WUS). WUS specifies stem cell fate in the organising centre of the L3 layer. It is repressed in part through the action of CLV1, a leucine‐rich receptor kinase expressed in the L1 and L2 layers but migrates to the L3 layer that binds to the mobile glycopeptide CLV3. Through an indirect mechanism, WUS activates CLV3, leading to a feed‐back loop. Additionally, WUS binds to and represses CLV1. Figure partially adapted from Clark (2001).
Figure 4. Light regulation of CONSTANS (CO), a key regulator of flowering time. Under long day conditions, CO is activated by GIGANTEA (GI) and FLAVIN‐BINDING, KELCH REPEAT, F‐BOX 1 (FKF1), which negatively regulate CYCLING DOF FACTOR1 (CDF1). Under short day conditions, CDF1 can bind to and repress CO. CO is also regulated post‐transcriptionally by light. In the absence of light, the E3 ligase COP1 targets CO for degradation. In the presence of light, the cryptochrome CRY2 interacts with COP1, releasing CO, which then activates FLOWERING LOCUS T (FT). FT is transported from the leaf to the shoot apical meristem where it interacts with FLOWERING LOCUS D (FD). Together, FT and FD activate genes promoting flowering, including the floral identity gene APETALA1 (AP1).
Figure 5. Maternal and paternal genomes make different contributions to the developing embryo. In the endosperm, MEDEA (MEA) is expressed only from the maternal genome, and it is activated by DEMETER (DME), which maintains the chromatin in an open, hypomethylated state. MEA acts as part of a complex that deposits H3K27 dimethylation at the paternal MEA and maternal PHERES1 (PHE) loci.
close
 References
    Aida M, Beis D, Heidstra R et al. (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119: 109–120.
    Barton MK (2010) Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Developmental Biology 341: 95–113.
    Bauer MJ and Fischer RL (2011) Genome demethylation and imprinting in the endosperm. Current Opinion in Plant Biology 14: 162–167.
    Becker C, Hagmann J, Müller J et al. (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480: 245–249.
    Benhamed M, Bertrand C, Servet C and Zhou D‐X (2006) Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light‐responsive gene expression. Plant Cell 18: 2893–2903.
    Brady S, Zhang L and Megraw M (2011) A stele‐enriched gene regulatory network in the Arabidopsis root. Molecular Systems Biology 7: 459.
    Busch W, Miotk A, Ariel FD et al. (2010) Transcriptional control of a plant stem cell niche. Developmental Cell 18: 841–853.
    Chan SWL (2004) RNA silencing genes control de novo DNA methylation. Science 303: 1336–1336.
    Chinnusamy V and Zhu J‐K (2009) Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology 12: 133–139.
    Choi Y, Gehring M, Johnson L and Hannon M (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110(1): 33–42.
    Clark SE (2001) Cell signalling at the shoot meristem. Nature Reviews Molecular Cell Biology 2: 276–284. Available at: http://www.nature.com/nrm/journal/v2/n4/abs/nrm0401_276a.html
    Corbesier L, Vincent C, Jang S et al. (2007) FT protein movement contributes to long‐distance signaling in floral induction of Arabidopsis. Science 316: 1030–1033.
    Cubas P, Vincent C and Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157–161.
    Davidson EH (2010) Emerging properties of animal gene regulatory networks. Nature 468: 911–920.
    Fletcher JC (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283: 1911–1914.
    Galinha C, Hofhuis H, Luijten M et al. (2007) PLETHORA proteins as dose‐dependent master regulators of Arabidopsis root development. Nature 449: 1053–1057.
    Gehring M, Huh J, Hsieh T and Penterman J (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self‐imprinting by allele‐specific demethylation. Cell. 124(3): 495–506.
    Geldner N, Richter S, Vieten A and Marquardt S (2004) Partial loss‐of‐function alleles reveal a role for GNOM in auxin transport‐related, post‐embryonic development of Arabidopsis. Development 131: 389–400.
    Goda H, Sasaki E, Akiyama K et al. (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant Journal 55: 526–542.
    Han P, Li Q and Zhu Y‐X (2008) Mutation of Arabidopsis BARD1 causes meristem defects by failing to confine WUSCHEL expression to the organizing center. Plant Cell 20: 1482–1493.
    Hanano S and Goto K (2011) Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. The Plant Cell Online 23: 3172–3184.
    Heard E (2005) Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Current Opinion in Genetics & Development 15: 482–489.
    Jang S, Marchal V, Panigrahi KCS et al. (2008) Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO Journal 27: 1277–1288.
    Jiao Y, Lau OS and Deng XW (2007) Light‐regulated transcriptional networks in higher plants. Nature Reviews Genetics 8: 217–230.
    Kaufman PD and Rando OJ (2010) Chromatin as a potential carrier of heritable information. Current Opinion in Cell Biology 22: 284–290.
    Kieffer M (2006) Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. The Plant Cell Online 18: 560–573.
    Köhler C, Page D and Gagliardini V (2004) The Arabidopsis thaliana MEDEA polycomb group protein controls expression of PHERES1 by parental imprinting. Nature Genetics 37: 28–30.
    Kwon CS, Chen C and Wagner D (2005) WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis. Genes & Development 19: 992–1003.
    Lang‐Mladek C, Popova O, Kiok K et al. (2010) Transgenerational inheritance and resetting of stress‐induced loss of epigenetic gene silencing in Arabidopsis. Molecular Plant 3: 594–602.
    Laufs P, Grandjean O, Jonak C, Kiêu K and Traas J (1998) Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 10: 1375–1390.
    Laux T, Mayer KF, Berger J and Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122: 87–96.
    Lee J, He K, Stolc V et al. (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19: 731–749.
    Mayer U and Buttner G (1993) Apical‐basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117: 149–162.
    Mosher RA, Melnyk CW, Kelly KA et al. (2009) Uniparental expression of PolIV‐dependent siRNAs in developing endosperm of Arabidopsis. Nature 460: 283–286.
    Ogawa M, Shinohara H, Sakagami Y and Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319: 294.
    Ohyama K, Shinohara H, Ogawa‐Ohnishi M and Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nature Chemical Biology 5: 578–580.
    Palstra R‐J, de Laat W and Grosveld F (2008) Beta‐globin regulation and long‐range interactions. Advances in Genetics 61: 107–142.
    Richards EJ (2006) Inherited epigenetic variation‐‐revisiting soft inheritance. Nature Reviews Genetics 7: 395–401.
    Schmitz RJ, Schultz MD, Lewsey MG et al. (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334: 369–373.
    Smith ZR and Long JA (2010) Control of Arabidopsis apical‐basal embryo polarity by antagonistic transcription factors. Nature 464: 423–426.
    Suárez‐López P, Wheatley K, Robson F et al. (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410: 1116–1120.
    Teale WD, Paponov IA and Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nature Reviews Molecular Cell Biology 7: 847–859.
    Tiwari S, Shen Y, Chang H and Hou Y (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis element. New Phytologist 187(1): 57–66.
    Tóth R, Kevei E, Hall A et al. (2001) Circadian clock‐regulated expression of phytochrome and cryptochrome genes in Arabidopsis. Plant Physiology 127: 1607–1616.
    Valverde F, Mouradov A, Soppe W et al. (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303: 1003–1006.
    Vercruysse S and Kuiper M (2005) Simulating genetic networks made easy: network construction with simple building blocks. Bioinformatics 21: 269–271.
    Wigge PA, Kim MC, Jaeger KE et al. (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056–1059.
    Wolters H, Anders N, Geldner N, Gavidia R and Jurgens G (2010) Coordination of apical and basal embryo development revealed by tissue‐specific GNOM functions. Development 138: 117–126.
    Yadav R, Perales M, Gruel J and Girke T (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes & Development 25: 2025–2030.
    Zhang EE and Kay SA (2010) Clocks not winding down: unravelling circadian networks. Nature Reviews Molecular Cell Biology 11: 764–776.
 Further Reading
    Chapman EJ and Estelle M (2009) Mechanism of auxin‐regulated gene expression in plants. Annual Review of Genetics 43: 265–285.
    Moazed D (2011) Mechanisms for the inheritance of chromatin states. Cell 146: 510–518.
    Srikanth A and Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cellular and Molecular Life Sciences 68: 2013–2037.
    Vanneste S and Friml J (2009) Auxin: a trigger for change in plant development. Cell 136: 1005–1016.
    Zhang X (2008) The epigenetic landscape of plants. Science 320: 489–492.

Related Sub-Topics:

Transcriptional Regulation | Plant Development | Plant Genetics and Molecular Biology
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Transcriptional Regulation in Plants
 
How to Cite close
Macrae, Rhiannon K, and Long, Jeffrey A(May 2012) Transcriptional Regulation in Plants. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023755]